Complement System As a Common Link in the Pathogenesis of Hemolytic Uremic Syndrome
- Авторлар: Blinova M.1, Generalova G.2,3, Emirova K.2,3, Popov E.4, Tsvetaeva N.5, Vasiliev S.5, Avdonin P.1
-
Мекемелер:
- Koltzov Institute of Developmental Biology, Russian Academy of Sciences
- Saint Vladimir Moscow City Children’s Clinical Hospital
- Moscow State University of Medicine and Dentistry named after A.I. Evdokimov
- National Medical Research Centre of Cardiology named after academician E.I. Chazov, Ministry of Health of the Russian Federation
- Hematology Research Center, Ministry of Health of Russian Federation
- Шығарылым: Том 40, № 4 (2023)
- Беттер: 235-258
- Бөлім: ОБЗОРЫ
- URL: https://journals.rcsi.science/0233-4755/article/view/135009
- DOI: https://doi.org/10.31857/S0233475523040047
- EDN: https://elibrary.ru/OJTBPO
- ID: 135009
Дәйексөз келтіру
Аннотация
Hemolytic uremic syndrome (HUS) is the most common cause of acute renal failure in children. The main causes of HUS are infections caused by Shiga toxin-producing bacteria: hemorrhagic Escherichia coli and Shigella dysenteriae type 1. They account for up to 90% of all cases of HUS. The remaining 10% represent a heterogeneous group of diseases collectively referred to as atypical HUS. The pathogenesis of most cases of atypical HUS is based on congenital or acquired disorders in the complement system. Over the past decades, evidence has accumulated that, in addition to E. coli and Sh. dysenteriae type 1, a wide variety of bacterial and viral infections, including the pathogens of pneumonia Streptococcus pneumoniae, immunodeficiency virus, H1N1 influenza, and a new coronavirus infection, can cause the development of HUS. In particular, infectious diseases act as the main cause of recurrence of atypical HUS. This review presents summarized data from recent studies, indicating that in various types of infectious HUS, disturbances in the complement system are a key pathogenetic factor. The links in the complement system are considered, the dysregulation of which in bacterial and viral infections can lead to complement hyperactivation with subsequent damage to the microvascular endothelium and the development of acute renal failure.
Авторлар туралы
M. Blinova
Koltzov Institute of Developmental Biology, Russian Academy of Sciences
Email: ppavdonin@gmail.com
Russia, 119334, Moscow
G. Generalova
Saint Vladimir Moscow City Children’s Clinical Hospital; Moscow State University of Medicine and Dentistry named after A.I. Evdokimov
Email: ppavdonin@gmail.com
Russia, 107014, Moscow; Russia, 127473, Moscow
Kh. Emirova
Saint Vladimir Moscow City Children’s Clinical Hospital; Moscow State University of Medicine and Dentistry named after A.I. Evdokimov
Email: ppavdonin@gmail.com
Russia, 107014, Moscow; Russia, 127473, Moscow
E. Popov
National Medical Research Centre of Cardiology named after academician E.I. Chazov,Ministry of Health of the Russian Federation
Email: ppavdonin@gmail.com
Russia, 121552, Moscow
N. Tsvetaeva
Hematology Research Center, Ministry of Health of Russian Federation
Email: ppavdonin@gmail.com
Russia, 125167, Moscow
S. Vasiliev
Hematology Research Center, Ministry of Health of Russian Federation
Email: ppavdonin@gmail.com
Russia, 125167, Moscow
P. Avdonin
Koltzov Institute of Developmental Biology, Russian Academy of Sciences
Хат алмасуға жауапты Автор.
Email: ppavdonin@gmail.com
Russia, 119334, Moscow
Әдебиет тізімі
- Aigner C., Schmidt A., Gaggl M., Sunder-Plassmann G. 2019. An updated classification of thrombotic microangiopathies and treatment of complement gene variant-mediated thrombotic microangiopathy. Clin. Kidney J. 12, 333–337. https://doi.org/10.1093/ckj/sfz040
- Brocklebank V., Wood K.M., Kavanagh D. 2018. Thrombotic microangiopathy and the kidney. Clin. J. Am. Soc. Nephrol. 13, 300–317. https://doi.org/10.2215/CJN.00620117
- Fakhouri F., Zuber J., Fremeaux-Bacchi V., Loirat C. 2017. Haemolytic uraemic syndrome. Lancet. 390, 681–696. https://doi.org/10.1016/S0140-6736(17)30062-4
- Loirat C., Fakhouri F., Ariceta G., Besbas N., Bitzan M., Bjerre A., Coppo R., Emma F., Johnson S., Karpman D., Landau D., Langman C.B., Lapeyraque A.L., Licht C., Nester C., Pecoraro C., Riedl M., van de Kar N.C., Van de Walle J., Vivarelli M., Fremeaux-Bacchi V., International H.U.S. 2016. An international consensus approach to the management of atypical hemolytic uremic syndrome in children. Pediatr. Nephrol. 31, 15–39. https://doi.org/10.1007/s00467-015-3076-8
- Fakhouri F., Fila M., Hummel A., Ribes D., Sellier-Leclerc A.L., Ville S., Pouteil-Noble C., Coindre J.P., Le Quintrec M., Rondeau E., Boyer O., Provot F., Djeddi D., Hanf W., Delmas Y., Louillet F., Lahoche A., Favre G., Chatelet V., Launay E.A., Presne C., Zaloszyc A., Caillard S., Bally S., Raimbourg Q., Tricot L., Mousson C., Le Thuaut A., Loirat C., Fremeaux-Bacchi V. 2021. Eculizumab discontinuation in children and adults with atypical hemolytic-uremic syndrome: A prospective multicenter study. Blood. 137, 2438–2449. https://doi.org/10.1182/blood.2020009280
- Warwicker P., Goodship T.H., Donne R.L., Pirson Y., Nicholls A., Ward R.M., Turnpenny P., Goodship J.A. 1998. Genetic studies into inherited and sporadic hemolytic uremic syndrome. Kidney Int. 53, 836–844. https://doi.org/10.1111/j.1523-1755.1998.00824.x
- Zipfel P.F., Skerka C. 2009. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 9, 729–740. https://doi.org/10.1038/nri2620
- Cserhalmi M., Papp A., Brandus B., Uzonyi B., Jozsi M. 2019. Regulation of regulators: Role of the complement factor H-related proteins. Semin. Immunol. 45, 101341. https://doi.org/10.1016/j.smim.2019.101341
- Wurzner R., Joysey V.C., Lachmann P.J. 1994. Complement component C7. Assessment of in vivo synthesis after liver transplantation reveals that hepatocytes do not synthesize the majority of human C7. J. Immunol. 152, 4624–4629.
- Carroll M.C. 1998. The role of complement and complement receptors in induction and regulation of immunity. Annu. Rev. Immunol. 16, 545–568. https://doi.org/10.1146/annurev.immunol.16.1.545
- Arbore G., Kemper C., Kolev M. 2017. Intracellular complement – the complosome – in immune cell regulation. Mol. Immunol. 89, 2–9. https://doi.org/10.1016/j.molimm.2017.05.012
- Bhakdi S., Tranum-Jensen J. 1986. C5b-9 assembly: average binding of one C9 molecule to C5b-8 without poly-C9 formation generates a stable transmembrane pore. J. Immunol. 136, 2999–3005.
- Podack E.R., Tschoop J., Muller-Eberhard H.J. 1982. Molecular organization of C9 within the membrane attack complex of complement. Induction of circular C9 polymerization by the C5b-8 assembly. J. Exp. Med. 156, 268–282. https://doi.org/10.1084/jem.156.1.268
- Ward P.A., Newman L.J. 1969. A neutrophil chemotactic factor from human C'5. J. Immunol. 102, 93–99.
- Ogden C.A., Elkon K.B. 2006. Role of complement and other innate immune mechanisms in the removal of apoptotic cells. Curr. Dir. Autoimmun. 9, 120–142. https://doi.org/10.1159/000090776
- Anliker-Ort M., Dingemanse J., van den Anker J., Kaufmann P. 2020. Treatment of rare inflammatory kidney diseases: Drugs targeting the terminal complement pathway. Front. Immunol. 11, 599417. https://doi.org/10.3389/fimmu.2020.599417
- Dempsey P.W., Allison M.E., Akkaraju S., Goodnow C.C., Fearon D.T. 1996. C3d of complement as a molecular adjuvant: Bridging innate and acquired immunity. Science. 271, 348–350. https://doi.org/10.1126/science.271.5247.348
- Chen J.Y., Cortes C., Ferreira V.P. 2018. Properdin: A multifaceted molecule involved in inflammation and diseases. Mol. Immunol. 102, 58–72. https://doi.org/10.1016/j.molimm.2018.05.018
- Mukherjee P., Thomas S., Pasinetti G.M. 2008. Complement anaphylatoxin C5a neuroprotects through regulation of glutamate receptor subunit 2 in vitro and in vivo. J. Neuroinflammation. 5, 5. https://doi.org/10.1186/1742-2094-5-5
- Ling M., Murali M. 2019. Analysis of the complement system in the clinical immunology laboratory. Clin. Lab. Med. 39, 579–590. https://doi.org/10.1016/j.cll.2019.07.006
- Garred P., Genster N., Pilely K., Bayarri-Olmos R., Rosbjerg A., Ma Y.J., Skjoedt M.O. 2016. A journey through the lectin pathway of complement-MBL and beyond. Immunol. Rev. 274, 74–97. https://doi.org/10.1111/imr.12468
- Pouw R.B., Ricklin D. 2021. Tipping the balance: Intricate roles of the complement system in disease and therapy. Semin. Immunopathol. 43, 757–771. https://doi.org/10.1007/s00281-021-00892-7
- Bossi F., Fischetti F., Pellis V., Bulla R., Ferrero E., Mollnes T.E., Regoli D., Tedesco F. 2004. Platelet-activating factor and kinin-dependent vascular leakage as a novel functional activity of the soluble terminal complement complex. J. Immunol. 173, 6921–6927. https://doi.org/10.4049/jimmunol.173.11.6921
- Chen Y., Yang C., Jin N., Xie Z., Tang Y., Fei L., Jia Z., Wu Y. 2007. Terminal complement complex C5b-9-treated human monocyte-derived dendritic cells undergo maturation and induce Th1 polarization. Eur. J. Immunol. 37, 167–176. https://doi.org/10.1002/eji.200636285
- Jozsi M., Barlow P.N., Meri S. 2021. Editorial: Function and dysfunction of complement factor H. Front. Immunol. 12, 831044. https://doi.org/10.3389/fimmu.2021.831044
- Majowicz S.E., Scallan E., Jones-Bitton A., Sargeant J.M., Stapleton J., Angulo F.J., Yeung D.H., Kirk M.D. 2014. Global incidence of human Shiga toxin-producing Escherichia coli infections and deaths: A systematic review and knowledge synthesis. Foodborne Pathog. Dis. 11, 447–455. https://doi.org/10.1089/fpd.2013.1704
- Rivas M., Chinen I., Miliwebsky E., Masana M. 2014. Risk factors for shiga toxin-producing Escherichia coli-associated human diseases. Microbiol. Spectr. 2. https://doi.org/10.1128/microbiolspec.EHEC-0002-2013
- Karpman D., Loos S., Tati R., Arvidsson I. 2017. Haemolytic uraemic syndrome. J Intern. Med. 281, 123–148. https://doi.org/10.1111/joim.12546
- Bowen E.E., Coward R.J. 2018. Advances in our understanding of the pathogenesis of hemolytic uremic syndromes. Am. J. Physiol. Renal Physiol. 314, F454–F461. https://doi.org/10.1152/ajprenal.00376.2017
- Garg A.X., Suri R.S., Barrowman N., Rehman F., Matsell D., Rosas-Arellano M.P., Salvadori M., Haynes R.B., Clark W.F. 2003. Long-term renal prognosis of diarrhea-associated hemolytic uremic syndrome: A systematic review, meta-analysis, and meta-regression. JAMA. 290, 1360–1370. https://doi.org/10.1001/jama.290.10.1360
- Rosales A., Hofer J., Zimmerhackl L.B., Jungraithmayr T.C., Riedl M., Giner T., Strasak A., Orth-Holler D., Wurzner R., Karch H., German-Austrian HUS Study Group. 2012. Need for long-term follow-up in enterohemorrhagic Escherichia coli-associated hemolytic uremic syndrome due to late-emerging sequelae. Clin. Infect. Dis. 54, 1413–1421. https://doi.org/10.1093/cid/cis196
- Frankel G., Phillips A.D. 2008. Attaching effacing Escherichia coli and paradigms of Tir-triggered actin polymerization: Getting off the pedestal. Cell Microbiol. 10, 549– 556. https://doi.org/10.1111/j.1462-5822.2007.01103.x
- Orth D., Ehrlenbach S., Brockmeyer J., Khan A.B., Huber G., Karch H., Sarg B., Lindner H., Wurzner R. 2010. EspP, a serine protease of enterohemorrhagic Escherichia coli, impairs complement activation by cleaving complement factors C3/C3b and C5. Infect. Immun. 78, 4294–4301. https://doi.org/10.1128/IAI.00488-10
- Djafari S., Ebel F., Deibel C., Kramer S., Hudel M., Chakraborty T. 1997. Characterization of an exported protease from Shiga toxin-producing Escherichia coli. Mol. Microbiol. 25, 771–784. https://doi.org/10.1046/j.1365-2958.1997.5141874.x
- Tarr P.I., Gordon C.A., Chandler W.L. 2005. Shiga-toxin-producing Escherichia coli and haemolytic uraemic syndrome. Lancet. 365, 1073–1086. https://doi.org/10.1016/S0140-6736(05)71144-2
- Bauwens A., Betz J., Meisen I., Kemper B., Karch H., Muthing J. 2013. Facing glycosphingolipid-Shiga toxin interaction: Dire straits for endothelial cells of the human vasculature. Cell Mol. Life Sci. 70, 425–457. https://doi.org/10.1007/s00018-012-1060-z
- Rutjes N.W., Binnington B.A., Smith C.R., Maloney M.D., Lingwood C.A. 2002. Differential tissue targeting and pathogenesis of verotoxins 1 and 2 in the mouse animal model. Kidney Int. 62, 832–845. https://doi.org/10.1046/j.1523-1755.2002.00502.x
- Scheutz F., Teel L.D., Beutin L., Pierard D., Buvens G., Karch H., Mellmann A., Caprioli A., Tozzoli R., Morabito S., Strockbine N.A., Melton-Celsa A.R., Sanchez M., Persson S., O’Brien A.D. 2012. Multicenter evaluation of a sequence-based protocol for subtyping Shiga toxins and standardizing Stx nomenclature. J. Clin. Microbiol. 50, 2951–2963. https://doi.org/10.1128/JCM.00860-12
- Gallegos K.M., Conrady D.G., Karve S.S., Gunasekera T.S., Herr A.B., Weiss A.A. 2012. Shiga toxin binding to glycolipids and glycans. PLoS One. 7, e30368. https://doi.org/10.1371/journal.pone.0030368
- Clayton F., Pysher T.J., Lou R., Kohan D.E., Denkers N.D., Tesh V.L., Taylor F.B., Jr., Siegler R.L. 2005. Lipopolysaccharide upregulates renal shiga toxin receptors in a primate model of hemolytic uremic syndrome. Am. J. Nephrol. 25, 536–540. https://doi.org/10.1159/000088523
- Louise C.B., Obrig T.G. 1992. Shiga toxin-associated hemolytic uremic syndrome: Combined cytotoxic effects of shiga toxin and lipopolysaccharide (endotoxin) on human vascular endothelial cells in vitro. Infect. Immun. 60, 1536–1543. https://doi.org/10.1128/iai.60.4.1536-1543.1992
- Ikeda M., Ito S., Honda M. 2004. Hemolytic uremic syndrome induced by lipopolysaccharide and Shiga-like toxin. Pediatr. Nephrol. 19, 485–489. https://doi.org/10.1007/s00467-003-1395-7
- Keepers T.R., Psotka M.A., Gross L.K., Obrig T.G. 2006. A murine model of HUS: Shiga toxin with lipopolysaccharide mimics the renal damage and physiologic response of human disease. J. Am. Soc. Nephrol. 17, 3404–3414. https://doi.org/10.1681/ASN.2006050419
- Zanchi C., Zoja C., Morigi M., Valsecchi F., Liu X.Y., Rottoli D., Locatelli M., Buelli S., Pezzotta A., Mapelli P., Geelen J., Remuzzi G., Hawiger J. 2008. Fractalkine and CX3CR1 mediate leukocyte capture by endothelium in response to Shiga toxin. J. Immunol. 181, 1460–1469.
- O’Brien A.D., Tesh V.L., Donohue-Rolfe A., Jackson M.P., Olsnes S., Sandvig K., Lindberg A.A., Keusch G.T. 1992. Shiga toxin: Biochemistry, genetics, mode of action, and role in pathogenesis. Curr. Top. Microbiol. Immunol. 180, 65–94. https://doi.org/10.1007/978-3-642-77238-2_4
- Lingwood C.A. 1996. Role of verotoxin receptors in pathogenesis. Trends Microbiol. 4, 147– 153. https://doi.org/10.1016/0966-842x(96)10017-2
- Lingwood CA. 2003. Shiga toxin receptor glycolipid binding. Pathology and utility. Methods Mol. Med. 73, 165–86.
- Endo Y., Tsurugi K., Yutsudo T., Takeda Y., Ogasawara T., Igarashi K. 1988. Site of action of a Vero toxin (VT2) from Escherichia coli O157:H7 and of Shiga toxin on eukaryotic ribosomes. RNA N-glycosidase activity of the toxins. Eur. J. Biochem. 171, 45–50. https://doi.org/10.1111/j.1432-1033.1988.tb13756.x
- Lee M.S., Koo S., Jeong D.G., Tesh V.L. 2016. Shiga toxins as multi-functional proteins: Induction of host cellular stress responses, role in pathogenesis and therapeutic applications. Toxins (Basel). 8. https://doi.org/10.3390/toxins8030077
- Petruzziello-Pellegrini T.N., Moslemi-Naeini M., Marsden P.A. 2013. New insights into Shiga toxin-mediated endothelial dysfunction in hemolytic uremic syndrome. Virulence. 4, 556–563. https://doi.org/10.4161/viru.26143
- Tesh V.L. 2012. Activation of cell stress response pathways by Shiga toxins. Cell. Microbiol. 14, 1–9. https://doi.org/10.1111/j.1462-5822.2011.01684.x
- Zoja C., Buelli S., Morigi M. 2010. Shiga toxin-associated hemolytic uremic syndrome: Pathophysiology of endothelial dysfunction. Pediatr. Nephrol. 25, 2231– 2240. https://doi.org/10.1007/s00467-010-1522-1
- Brigotti M., Tazzari P.L., Ravanelli E., Carnicelli D., Rocchi L., Arfilli V., Scavia G., Minelli F., Ricci F., Pagliaro P., Ferretti A.V., Pecoraro C., Paglialonga F., Edefonti A., Procaccino M.A., Tozzi A.E., Caprioli A. 2011. Clinical relevance of shiga toxin concentrations in the blood of patients with hemolytic uremic syndrome. Pediatr Infect. Dis. J. 30, 486–490. https://doi.org/10.1097/INF.0b013e3182074d22
- He X., Ardissino G., Patfield S., Cheng L.W., Silva C.J., Brigotti M. 2018. an improved method for the sensitive detection of Shiga toxin 2 in human serum. Toxins (Basel). 10. https://doi.org/10.3390/toxins10020059
- Obrig T.G., Karpman D. 2012. Shiga toxin pathogenesis: Kidney complications and renal failure. Curr. Top Microbiol. Immunol. 357, 105–136. https://doi.org/10.1007/82_2011_172
- Brigotti M., Carnicelli D., Arfilli V., Tamassia N., Borsetti F., Fabbri E., Tazzari P.L., Ricci F., Pagliaro P., Spisni E., Cassatella M.A. 2013. Identification of TLR4 as the receptor that recognizes Shiga toxins in human neutrophils. J. Immunol. 191, 4748–4758. https://doi.org/10.4049/jimmunol.1300122
- Stahl A.L., Arvidsson I., Johansson K.E., Chromek M., Rebetz J., Loos S., Kristoffersson A.C., Bekassy Z.D., Morgelin M., Karpman D. 2015. A novel mechanism of bacterial toxin transfer within host blood cell-derived microvesicles. PLoS Pathog. 11, e1004619. https://doi.org/10.1371/journal.ppat.1004619
- Villysson A., Tontanahal A., Karpman D. 2017. Microvesicle involvement in Shiga toxin-associated infection. Toxins (Basel). 9. https://doi.org/10.3390/toxins9110376
- Matussek A., Lauber J., Bergau A., Hansen W., Rohde M., Dittmar K.E., Gunzer M., Mengel M., Gatzlaff P., Hartmann M., Buer J., Gunzer F. 2003. Molecular and functional analysis of Shiga toxin-induced response patterns in human vascular endothelial cells. Blood. 102, 1323–1332. https://doi.org/10.1182/blood-2002-10-3301
- Morigi M., Micheletti G., Figliuzzi M., Imberti B., Karmali M.A., Remuzzi A., Remuzzi G., Zoja C. 1995. Verotoxin-1 promotes leukocyte adhesion to cultured endothelial cells under physiologic flow conditions. Blood. 86, 4553–4558.
- Zoja C., Angioletti S., Donadelli R., Zanchi C., Tomasoni S., Binda E., Imberti B., te Loo M., Monnens L., Remuzzi G., Morigi M. 2002. Shiga toxin-2 triggers endothelial leukocyte adhesion and transmigration via NF-kappaB dependent up-regulation of IL-8 and MCP-1. Kidney Int. 62, 846–856. https://doi.org/10.1046/j.1523-1755.2002.00503.x
- Morigi M., Galbusera M., Binda E., Imberti B., Gastoldi S., Remuzzi A., Zoja C., Remuzzi G. 2001. Verotoxin-1-induced up-regulation of adhesive molecules renders microvascular endothelial cells thrombogenic at high shear stress. Blood. 98, 1828–1835.
- Lo N.C., Turner N.A., Cruz M.A., Moake J. 2013. Interaction of Shiga toxin with the A-domains and multimers of von Willebrand Factor. J. Biol. Chem. 288, 33118–33123. https://doi.org/10.1074/jbc.M113.487413
- Dettmar A.K., Binder E., Greiner F.R., Liebau M.C., Kurschat C.E., Jungraithmayr T.C., Saleem M.A., Schmitt C.P., Feifel E., Orth-Holler D., Kemper M.J., Pepys M., Wurzner R., Oh J. 2014. Protection of human podocytes from shiga toxin 2-induced phosphorylation of mitogen-activated protein kinases and apoptosis by human serum amyloid P component. Infect. Immun. 82, 1872–1879. https://doi.org/10.1128/IAI.01591-14
- Ergonul Z., Clayton F., Fogo A.B., Kohan D.E. 2003. Shigatoxin-1 binding and receptor expression in human kidneys do not change with age. Pediatr. Nephrol. 18, 246–253. https://doi.org/10.1007/s00467-002-1025-9
- Hughes A.K., Stricklett P.K., Schmid D., Kohan D.E. 2000. Cytotoxic effect of Shiga toxin-1 on human glomerular epithelial cells. Kidney Int. 57, 2350–2359. https://doi.org/10.1046/j.1523-1755.2000.00095.x
- Morigi M., Buelli S., Zanchi C., Longaretti L., Macconi D., Benigni A., Moioli D., Remuzzi G., Zoja C. 2006. Shigatoxin-induced endothelin-1 expression in cultured podocytes autocrinally mediates actin remodeling. Am. J. Pathol. 169, 1965–1975. https://doi.org/10.2353/ajpath.2006.051331
- Hughes A.K., Stricklett P.K., Kohan D.E. 2001. Shiga toxin-1 regulation of cytokine production by human glomerular epithelial cells. Nephron. 88, 14–23. https://doi.org/10.1159/000045953
- Keir L.S., Saleem M.A. 2014. Current evidence for the role of complement in the pathogenesis of Shiga toxin haemolytic uraemic syndrome. Pediatr. Nephrol. 29, 1895–1902. https://doi.org/10.1007/s00467-013-2561-1
- Mele C., Remuzzi G., Noris M. 2014. Hemolytic uremic syndrome. Semin. Immunopathol. 36, 399–420. https://doi.org/10.1007/s00281-014-0416-x
- Orth-Holler D., Wurzner R. 2014. Role of complement in enterohemorrhagic Escherichia coli-induced hemolytic uremic syndrome. Semin. Thromb. Hemost. 40, 503–507. https://doi.org/10.1055/s-0034-1375295
- Zoja C., Buelli S., Morigi M. 2019. Shiga toxin triggers endothelial and podocyte injury: The role of complement activation. Pediatr. Nephrol. 34, 379–388. https://doi.org/10.1007/s00467-017-3850-x
- Koster F.T., Boonpucknavig V., Sujaho S., Gilman R.H., Rahaman M.M. 1984. Renal histopathology in the hemolytic-uremic syndrome following shigellosis. Clin. Nephrol. 21, 126–133.
- Monnens L., Molenaar J., Lambert P.H., Proesmans W., van Munster P. 1980. The complement system in hemolytic-uremic syndrome in childhood. Clin. Nephrol. 13, 168–171.
- Robson W.L., Leung A.K., Fick G.H., McKenna A.I. 1992. Hypocomplementemia and leukocytosis in diarrhea-associated hemolytic uremic syndrome. Nephron. 62, 296–299. https://doi.org/10.1159/000187063
- Stahl A.L., Sartz L., Karpman D. 2011. Complement activation on platelet-leukocyte complexes and microparticles in enterohemorrhagic Escherichia coli-induced hemolytic uremic syndrome. Blood. 117, 5503–5513. https://doi.org/10.1182/blood-2010-09-309161
- Thurman J.M., Marians R., Emlen W., Wood S., Smith C., Akana H., Holers V.M., Lesser M., Kline M., Hoffman C., Christen E., Trachtman H. 2009. Alternative pathway of complement in children with diarrhea-associated hemolytic uremic syndrome. Clin. J. Am. Soc. Nephrol. 4, 1920–1924. https://doi.org/10.2215/CJN.02730409
- Ferraris J.R., Ferraris V., Acquier A.B., Sorroche P.B., Saez M.S., Ginaca A., Mendez C.F. 2015. Activation of the alternative pathway of complement during the acute phase of typical haemolytic uraemic syndrome. Clin. Exp. Immunol. 181, 118–125. https://doi.org/10.1111/cei.12601
- Arvidsson I., Rebetz J., Loos S., Herthelius M., Kristoffersson A.C., Englund E., Chromek M., Karpman D. 2016. Early terminal complement blockade and C6 deficiency are protective in enterohemorrhagic Escherichia coli-infected mice. J. Immunol. 197, 1276–1286. https://doi.org/10.4049/jimmunol.1502377
- Orth D., Khan A.B., Naim A., Grif K., Brockmeyer J., Karch H., Joannidis M., Clark S.J., Day A.J., Fidanzi S., Stoiber H., Dierich M.P., Zimmerhackl L.B., Wurzner R. 2009. Shiga toxin activates complement and binds factor H: Evidence for an active role of complement in hemolytic uremic syndrome. J. Immunol. 182, 6394–6400. https://doi.org/10.4049/jimmunol.0900151
- Poolpol K., Orth-Holler D., Speth C., Zipfel P.F., Skerka C., de Cordoba S.R., Brockmeyer J., Bielaszewska M., Wurzner R. 2014. Interaction of Shiga toxin 2 with complement regulators of the factor H protein family. Mol. Immunol. 58, 77–84. https://doi.org/10.1016/j.molimm.2013.11.009
- Ehrlenbach S., Rosales A., Posch W., Wilflingseder D., Hermann M., Brockmeyer J., Karch H., Satchell S.C., Wurzner R., Orth-Holler D. 2013. Shiga toxin 2 reduces complement inhibitor CD59 expression on human renal tubular epithelial and glomerular endothelial cells. Infect. Immun. 81, 2678–2685. https://doi.org/10.1128/IAI.01079-12
- Iwaki D., Kanno K., Takahashi M., Endo Y., Matsushita M., Fujita T. 2011. The role of mannose-binding lectin-associated serine protease-3 in activation of the alternative complement pathway. J. Immunol. 187, 3751–3758. https://doi.org/10.4049/jimmunol.1100280
- Ozaki M., Kang Y., Tan Y.S., Pavlov V.I., Liu B., Boyle D.C., Kushak R.I., Skjoedt M.O., Grabowski E.F., Taira Y., Stahl G.L. 2016. Human mannose-binding lectin inhibitor prevents Shiga toxin-induced renal injury. Kidney Int. 90, 774–782. https://doi.org/10.1016/j.kint.2016.05.011
- Lathem W.W., Grys T.E., Witowski S.E., Torres A.G., Kaper J.B., Tarr P.I., Welch R.A. 2002. StcE, a metalloprotease secreted by Escherichia coli O157:H7, specifically cleaves C1 esterase inhibitor. Mol. Microbiol. 45, 277– 288. https://doi.org/10.1046/j.1365-2958.2002.02997.x
- Zeerleder S. 2011. C1-inhibitor: More than a serine protease inhibitor. Semin. Thromb. Hemost. 37, 362–374. https://doi.org/10.1055/s-0031-1276585
- Morigi M., Galbusera M., Gastoldi S., Locatelli M., Buelli S., Pezzotta A., Pagani C., Noris M., Gobbi M., Stravalaci M., Rottoli D., Tedesco F., Remuzzi G., Zoja C. 2011. Alternative pathway activation of complement by Shiga toxin promotes exuberant C3a formation that triggers microvascular thrombosis. J. Immunol. 187, 172–180. https://doi.org/10.4049/jimmunol.1100491
- Del Conde I., Cruz M.A., Zhang H., Lopez J.A., Afshar-Kharghan V. 2005. Platelet activation leads to activation and propagation of the complement system. J. Exp. Med. 201, 871–879. https://doi.org/10.1084/jem.20041497
- Locatelli M., Buelli S., Pezzotta A., Corna D., Perico L., Tomasoni S., Rottoli D., Rizzo P., Conti D., Thurman J.M., Remuzzi G., Zoja C., Morigi M. 2014. Shiga toxin promotes podocyte injury in experimental hemolytic uremic syndrome via activation of the alternative pathway of complement. J. Am. Soc. Nephrol. 25, 1786–1798. https://doi.org/10.1681/ASN.2013050450
- Arvidsson I., Stahl A.L., Hedstrom M.M., Kristoffersson A.C., Rylander C., Westman J.S., Storry J.R., Olsson M.L., Karpman D. 2015. Shiga toxin-induced complement-mediated hemolysis and release of complement-coated red blood cell-derived microvesicles in hemolytic uremic syndrome. J. Immunol. 194, 2309–2318. https://doi.org/10.4049/jimmunol.1402470
- Sims P.J., Faioni E.M., Wiedmer T., Shattil S.J. 1988. Complement proteins C5b-9 cause release of membrane vesicles from the platelet surface that are enriched in the membrane receptor for coagulation factor Va and express prothrombinase activity. J. Biol. Chem. 263, 18205–18212.
- Butler T. 2012. Haemolytic uraemic syndrome during shigellosis. Trans. R. Soc. Trop. Med. Hyg. 106, 395–399. https://doi.org/10.1016/j.trstmh.2012.04.001
- Al-Qarawi S., Fontaine R.E., Al-Qahtani M.S. 1995. An outbreak of hemolytic uremic syndrome associated with antibiotic treatment of hospital inpatients for dysentery. Emerg. Infect. Dis. 1, 138–140. https://doi.org/10.3201/eid0104.950407
- Bin Saeed A.A., El Bushra H.E., Al-Hamdan N.A. 1995. Does treatment of bloody diarrhea due to Shigella dysenteriae type 1 with ampicillin precipitate hemolytic uremic syndrome? Emerg. Infect. Dis. 1, 134–137. https://doi.org/10.3201/eid0104.950406
- Bloom P.D., MacPhail A.P., Klugman K., Louw M., Raubenheimer C., Fischer C. 1994. Haemolytic-uraemic syndrome in adults with resistant Shigella dysenteriae type I. Lancet. 344, 206. https://doi.org/10.1016/s0140-6736(94)92815-0
- Houdouin V., Doit C., Mariani P., Brahimi N., Loirat C., Bourrillon A., Bingen E. 2004. A pediatric cluster of Shigella dysenteriae serotype 1 diarrhea with hemolytic uremic syndrome in 2 families from France. Clin. Infect. Dis. 38, e96–99. https://doi.org/10.1086/383474
- Oneko M., Nyathi M.N., Doehring E. 2001. Post-dysenteric hemolytic uremic syndrome in Bulawayo, Zimbabwe. Pediatr. Nephrol. 16, 1142–1145. https://doi.org/10.1007/s004670100049
- Parsonnet J., Greene K.D., Gerber A.R., Tauxe R.V., Vallejo Aguilar O.J., Blake P.A. 1989. Shigella dysenteriae type 1 infections in US travellers to Mexico. 1988. Lancet. 2, 543–545. https://doi.org/10.1016/s0140-6736(89)90662-4
- Rollins N.C., Wittenberg D.F., Coovadia H.M., Pillay D.G., Karas A.J., Sturm A.W. 1995. Epidemic Shigella dysenteriae type 1 in Natal. J. Trop. Pediatr. 41, 281–284. https://doi.org/10.1093/tropej/41.5.281
- Bennish M.L., Khan W.A., Begum M., Bridges E.A., Ahmed S., Saha D., Salam M.A., Acheson D., Ryan E.T. 2006. Low risk of hemolytic uremic syndrome after early effective antimicrobial therapy for Shigella dysenteriae type 1 infection in Bangladesh. Clin. Infect. Dis. 42, 356–362. https://doi.org/10.1086/499236
- Tzipori S., Sheoran A., Akiyoshi D., Donohue-Rolfe A., Trachtman H. 2004. Antibody therapy in the management of shiga toxin-induced hemolytic uremic syndrome. Clin. Microbiol. Rev. 17, 926–941. https://doi.org/10.1128/CMR.17.4.926-941.2004
- Koster F., Levin J., Walker L., Tung K.S., Gilman R.H., Rahaman M.M., Majid M.A., Islam S., Williams R.C., Jr. 1978. Hemolytic-uremic syndrome after shigellosis. Relation to endotoxemia and circulating immune complexes. N. Engl. J. Med. 298, 927–933. https://doi.org/10.1056/NEJM197804272981702
- Butler T., Rahman H., Al-Mahmud K.A., Islam M., Bardhan P., Kabir I., Rahman M.M. 1985. An animal model of haemolytic–uraemic syndrome in shigellosis: Lipopolysaccharides of Shigella dysenteriae I and S. flexneri produce leucocyte-mediated renal cortical necrosis in rabbits. Br. J. Exp. Pathol. 66, 7–15.
- Cody E. M., Dixon B.P. 2019. Hemolytic uremic syndrome. Pediatr. Clin. North. Am. 66 (1), 235–246. https://doi.org/10.1016/j.pcl.2018.09.011
- Vaith P., Uhlenbruck G. 1978. The Thomsen agglutination phenomenon: A discovery revisited 50 years later. Z. Immunitatsforsch Immunobiol. 154, 1–15.
- Copelovitch L., Kaplan B.S. 2008. Streptococcus pneumoniae-associated hemolytic uremic syndrome. Pediatr. Nephrol. 23, 1951–1956. https://doi.org/10.1007/s00467-007-0518-y
- Huang D.T., Chi H., Lee H.C., Chiu N.C., Huang F.Y. 2006. T-antigen activation for prediction of pneumococcus-induced hemolytic uremic syndrome and hemolytic anemia. Pediatr. Infect. Dis. J. 25, 608–610. https://doi.org/10.1097/01.inf.0000223494.83542.ad
- Rose P.E., Armour J.A., Williams C.E., Hill F.G. 1985. Verotoxin and neuraminidase induced platelet aggregating activity in plasma: Their possible role in the pathogenesis of the haemolytic uraemic syndrome. J. Clin. Pathol. 38, 438–441. https://doi.org/10.1136/jcp.38.4.438
- Gilbert R.D., Nagra A., Haq M.R. 2013. Does dysregulated complement activation contribute to haemolytic uraemic syndrome secondary to Streptococcus pneumoniae? Med. Hypotheses. 81, 400–403. https://doi.org/10.1016/j.mehy.2013.05.030
- Johnson S., Waters A. 2012. Is complement a culprit in infection-induced forms of haemolytic uraemic syndrome? Immunobiology. 217, 235–243. https://doi.org/10.1016/j.imbio.2011.07.022
- Gomez Delgado I., Corvillo F., Nozal P., Arjona E., Madrid A., Melgosa M., Bravo J., Szilagyi A., Csuka D., Veszeli N., Prohaszka Z., Sanchez-Corral P. 2021. Complement genetic variants and FH desialylation in S. pneumoniae-haemolytic uraemic syndrome. Front. Immunol. 12, 641656. https://doi.org/10.3389/fimmu.2021.641656
- Poschmann A., Fischer K., Grundmann A., Vongjirad A. 1976. Neuraminidase induced hemolytic anemia. Experimental and clinical observations. Monatsschr. Kinderheilkd. (1902). 124, 15–24.
- Eber S.W., Polster H., Quentin S.H., Rumpf K.W., Lynen R. 1993. Hemolytic-uremic syndrome in pneumococcal meningitis and infection. Importance of T-transformation. Monatsschr. Kinderheilkd. 141, 219– 222.
- Loupiac A., Elayan A., Cailliez M., Adra A.L., Decramer S., Thouret M.C., Harambat J., Guigonis V. 2013. Diagnosis of Streptococcus pneumoniae-associated hemolytic uremic syndrome. Pediatr. Infect. Dis. J. 32, 1045–1049. https://doi.org/10.1097/INF.0b013e31829ee872
- Herbert A.P., Makou E., Chen Z.A., Kerr H., Richards A., Rappsilber J., Barlow P.N. 2015. Complement evasion mediated by enhancement of captured factor H: Implications for protection of self-surfaces from complement. J. Immunol. 195, 4986–4998. https://doi.org/10.4049/jimmunol.1501388
- Lu L., Ma Z., Jokiranta T.S., Whitney A.R., DeLeo F.R., Zhang J.R. 2008. Species-specific interaction of Streptococcus pneumoniae with human complement factor H. J. Immunol. 181, 7138–7146. https://doi.org/10.4049/jimmunol.181.10.7138
- Bollaert P.E., Bauer P., Judlin P., Laprevote-Heully M.C., Lambert H., Larcan A. 1989. Hemorrhagic colitis with Streptococcus pyogenes preceding hemolytic uremic syndrome during early pregnancy. Nephron. 52, 103–104. https://doi.org/10.1159/000185598
- Izumi T., Hyodo T., Kikuchi Y., Imakiire T., Ikenoue T., Suzuki S., Yoshizawa N., Miura S. 2005. An adult with acute poststreptococcal glomerulonephritis complicated by hemolytic uremic syndrome and nephrotic syndrome. Am. J. Kidney Dis. 46, e59–63. https://doi.org/10.1053/j.ajkd.2005.06.010
- Yildiz B., Kural N., Yarar C. 2004. Atypical hemolytic uremic syndrome associated with group A beta hemolytic streptococcus. Pediatr. Nephrol. 19, 943–944. https://doi.org/10.1007/s00467-004-1536-7
- Shepherd A.B., Palmer A.L., Bigler S.A., Baliga R. 2003. Hemolytic uremic syndrome associated with group A beta-hemolytic streptococcus. Pediatr. Nephrol. 18, 949–951. https://doi.org/10.1007/s00467-003-1191-4
- Pandiripally V., Gregory E., Cue D. 2002. Acquisition of regulators of complement activation by Streptococcus pyogenes serotype M1. Infect. Immun. 70, 6206–6214. https://doi.org/10.1128/IAI.70.11.6206-6214.2002
- Pandiripally V., Wei L., Skerka C., Zipfel P.F., Cue D. 2003. Recruitment of complement factor H-like protein 1 promotes intracellular invasion by group A streptococci. Infect. Immun. 71, 7119–7128. https://doi.org/10.1128/IAI.71.12.7119-7128.2003
- Inoue D., Oda T., Iwama S., Hoshino T., Mukae M., Sakai T., Kojima A., Uchida T., Kojima T., Sugisaki K., Tomiyasu T., Yoshikawa N., Yamada M. 2022. Thrombotic microangiopathy with transiently positive direct Coombs test in an adult with poststreptococcal acute glomerulonephritis: a case report. BMC Nephrol. 23, 56. https://doi.org/10.1186/s12882-022-02684-z
- Oda T., Yoshizawa N., Yamakami K., Sakurai Y., Takechi H., Yamamoto K., Oshima N., Kumagai H. 2012. The role of nephritis-associated plasmin receptor (NAPlr) in glomerulonephritis associated with streptococcal infection. J. Biomed. Biotechnol. 2012, 417675. https://doi.org/10.1155/2012/417675
- Poschmann A., Fischer K. 1979. Exchange transfusion with heparinised fresh blood in necrotising enterocolitis. Lancet. 1, 824–825. https://doi.org/10.1016/s0140-6736(79)91343-6
- Seger R., Joller P., Bird G.W., Wingham J., Wuest J., Kenny A., Rapp A., Garzoni D., Hitzig W.H., Duc G. 1980. Necrotising enterocolitis and neuraminidase-producing bacteria. Helv. Paediatr. Acta. 35, 121–128.
- Seges R.A., Kenny A., Bird G.W., Wingham J., Baals H., Stauffer U.G. 1981. Pediatric surgical patients with severe anaerobic infection: Report of 16 T-antigen positive cases and possible hazards of blood transfusion. J. Pediatr. Surg. 16, 905–910. https://doi.org/10.1016/s0022-3468(81)80844-5
- Seitz R.C., Poschmann A., Hellwege H.H. 1997. Monoclonal antibodies for the detection of desialylation of erythrocyte membranes during haemolytic disease and haemolytic uraemic syndrome caused by the in vivo action of microbial neuraminidase. Glycoconj. J. 14, 699–706. https://doi.org/10.1023/a:1018565316310
- Paddock C.D., Sanden G.N., Cherry J.D., Gal A.A., Langston C., Tatti K.M., Wu K.H., Goldsmith C.S., Greer P.W., Montague J.L., Eliason M.T., Holman R.C., Guarner J., Shieh W.J., Zaki S.R. 2008. Pathology and pathogenesis of fatal Bordetella pertussis infection in infants. Clin. Infect. Dis. 47, 328–338. https://doi.org/10.1086/589753
- Berner R., Krause M.F., Gordjani N., Zipfel P.F., Boehm N., Krueger M., Brandis M., Zimmerhackl L.B. 2002. Hemolytic uremic syndrome due to an altered factor H triggered by neonatal pertussis. Pediatr. Nephrol. 17, 190–192. https://doi.org/10.1007/s00467-001-0798-6
- Chaturvedi S., Licht C., Langlois V. 2010. Hemolytic uremic syndrome caused by Bordetella pertussis infection. Pediatr. Nephrol. 25, 1361–1364. https://doi.org/10.1007/s00467-010-1449-6
- Pela I., Seracini D., Caprioli A., Castelletti F., Giammanco A. 2006. Hemolytic uremic syndrome in an infant following Bordetella pertussis infection. Eur. J. Clin. Microbiol. Infect. Dis. 25, 515–517. https://doi.org/10.1007/s10096-006-0171-6
- Saida K., Ogura M., Kano Y., Ishimori S., Yoshikawa T., Nagata H., Sato M., Kamei K., Ishikura K. 2018. Treatment of hemolytic uremic syndrome related to Bordetella pertussis infection – is plasma exchange or eculizumab use necessary? BMC Nephrol. 19, 365. https://doi.org/10.1186/s12882-018-1168-y
- Jongerius I., Schuijt T.J., Mooi F.R., Pinelli E. 2015. Complement evasion by Bordetella pertussis: Implications for improving current vaccines. J. Mol. Med. (Berl.). 93, 395–402. https://doi.org/10.1007/s00109-015-1259-1
- Barnes M.G., Weiss A.A. 2001. BrkA protein of Bordetella pertussis inhibits the classical pathway of complement after C1 deposition. Infect. Immun. 69, 3067–3072. https://doi.org/10.1128/IAI.69.5.3067-3072.2001
- Marr N., Shah N.R., Lee R., Kim E.J., Fernandez R.C. 2011. Bordetella pertussis autotransporter Vag8 binds human C1 esterase inhibitor and confers serum resistance. PLoS One. 6, e20585. https://doi.org/10.1371/journal.pone.0020585
- Mooi F.R., van Loo I.H., van Gent M., He Q., Bart M.J., Heuvelman K.J., de Greeff S.C., Diavatopoulos D., Teunis P., Nagelkerke N., Mertsola J. 2009. Bordetella pertussis strains with increased toxin production associated with pertussis resurgence. Emerg. Infect. Dis. 15, 1206–1213. https://doi.org/10.3201/eid1508.081511
- Berggard K., Johnsson E., Mooi F.R., Lindahl G. 1997. Bordetella pertussis binds the human complement regulator C4BP: Role of filamentous hemagglutinin. Infect. Immun. 65, 3638–3643. https://doi.org/10.1128/iai.65.9.3638-3643.1997
- Berggard K., Lindahl G., Dahlback B., Blom A.M. 2001. Bordetella pertussis binds to human C4b-binding protein (C4BP) at a site similar to that used by the natural ligand C4b. Eur. J. Immunol. 31, 2771–2780. https://doi.org/10.1002/1521-4141(200109)31:9<2771:: aid-immu2771>3.0.co;2-0
- Fernandez R.C., Weiss A.A. 1998. Serum resistance in bvg-regulated mutants of Bordetella pertussis. FEMS Microbiol. Lett. 163, 57–63. https://doi.org/10.1111/j.1574-6968.1998.tb13026.x
- Zipfel P.F., Hallstrom T., Riesbeck K. 2013. Human complement control and complement evasion by pathogenic microbes–tipping the balance. Mol. Immunol. 56, 152–160. https://doi.org/10.1016/j.molimm.2013.05.222
- Amdahl H., Jarva H., Haanpera M., Mertsola J., He Q., Jokiranta T.S., Meri S. 2011. Interactions between Bordetella pertussis and the complement inhibitor factor H. Mol. Immunol. 48, 697–705. https://doi.org/10.1016/j.molimm.2010.11.015
- Meri T., Amdahl H., Lehtinen M.J., Hyvarinen S., McDowell J.V., Bhattacharjee A., Meri S., Marconi R., Goldman A., Jokiranta T.S. 2013. Microbes bind complement inhibitor factor H via a common site. PLoS Pathog. 9, e1003308. https://doi.org/10.1371/journal.ppat.1003308
- Albaqali A., Ghuloom A., Al Arrayed A., Al Ajami A., Shome D.K., Jamsheer A., Al Mahroos H., Jelacic S., Tarr P.I., Kaplan B.S., Dhiman R.K. 2003. Hemolytic uremic syndrome in association with typhoid fever. Am. J. Kidney Dis. 41, 709–713. https://doi.org/10.1053/ajkd.2003.50135
- Beutin L., Strauch E., Fischer I. 1999. Isolation of Shigella sonnei lysogenic for a bacteriophage encoding gene for production of Shiga toxin. Lancet. 353, 1498. https://doi.org/10.1016/S0140-6736(99)00961-7
- Lamba K., Nelson J.A., Kimura A.C., Poe A., Collins J., Kao A.S., Cruz L., Inami G., Vaishampayan J., Garza A., Chaturvedi V., Vugia D.J. 2016. Shiga toxin 1-producing Shigella sonnei infections, California, United States, 2014–2015. Emerg. Infect. Dis. 22, 679–686. https://doi.org/10.3201/eid2204.151825
- Nyholm O., Lienemann T., Halkilahti J., Mero S., Rimhanen-Finne R., Lehtinen V., Salmenlinna S., Siitonen A. 2015. Characterization of Shigella sonnei isolate carrying Shiga toxin 2-producing gene. Emerg. Infect. Dis. 21, 891–892. https://doi.org/10.3201/eid2105.140621
- Schmidt H. 2001. Shiga-toxin-converting bacteriophages. Res. Microbiol. 152, 687–695. https://doi.org/10.1016/s0923-2508(01)01249-9
- Martinez-Castillo A., Quiros P., Navarro F., Miro E., Muniesa M. 2013. Shiga toxin 2-encoding bacteriophages in human fecal samples from healthy individuals. Appl. Environ. Microbiol. 79, 4862–4868. https://doi.org/10.1128/AEM.01158-13
- Muniesa M., Jofre J. 1998. Abundance in sewage of bacteriophages that infect Escherichia coli O157:H7 and that carry the Shiga toxin 2 gene. Appl. Environ. Microbiol. 64, 2443–2448. https://doi.org/10.1128/AEM.64.7.2443-2448.1998
- Muniesa M., Lucena F., Jofre J. 1999. Comparative survival of free shiga toxin 2-encoding phages and Escherichia coli strains outside the gut. Appl. Environ. Microbiol. 65, 5615–5618. https://doi.org/10.1128/AEM.65.12.5615-5618.1999
- Chan Y.S., Ng T.B. 2016. Shiga toxins: From structure and mechanism to applications. Appl. Microbiol. Biotechnol. 100, 1597–1610. https://doi.org/10.1007/s00253-015-7236-3
- Adams C., Vose A., Edmond M.B., Lyckholm L. 2017. Shigella sonnei and hemolytic uremic syndrome: A case report and literature review. IDCases. 8, 6–8. https://doi.org/10.1016/j.idcr.2017.02.003
- Armstrong S.M., Wang C., Tigdi J., Si X., Dumpit C., Charles S., Gamage A., Moraes T.J., Lee W.L. 2012. Influenza infects lung microvascular endothelium leading to microvascular leak: role of apoptosis and claudin-5. PLoS One. 7, e47323. https://doi.org/10.1371/journal.pone.0047323
- Hutchinson E.C. 2018. Influenza virus. Trends. Microbiol. 26, 809–810. https://doi.org/10.1016/j.tim.2018.05.013
- Allen U., Licht C. 2011. Pandemic H1N1 influenza A infection and (atypical) HUS - more than just another trigger? Pediatr. Nephrol. 26, 3–5. https://doi.org/10.1007/s00467-010-1690-z
- Bento D., Mapril J., Rocha C., Marchbank K.J., Kavanagh D., Barge D., Strain L., Goodship T.H., Meneses-Oliveira C. 2010. Triggering of atypical hemolytic uremic syndrome by influenza A (H1N1). Ren. Fail. 32, 753–756. https://doi.org/10.3109/0886022X.2010.486491
- Caltik A., Akyuz S.G., Erdogan O., Demircin G. 2011. Hemolytic uremic syndrome triggered with a new pandemic virus: influenza A (H1N1). Pediatr. Nephrol. 26, 147–148. https://doi.org/10.1007/s00467-010-1649-0
- Trachtman H., Sethna C., Epstein R., D’Souza M., Rubin L.G., Ginocchio C.C. 2011. Atypical hemolytic uremic syndrome associated with H1N1 influenza A virus infection. Pediatr. Nephrol. 26, 145–146. https://doi.org/10.1007/s00467-010-1636-5
- Watanabe T. 2001. Hemolytic uremic syndrome associated with influenza A virus infection. Nephron. 89, 359–360. https://doi.org/10.1159/000046102
- Kobbe R., Schild R., Christner M., Oh J., Loos S., Kemper M.J. 2017. Case report - atypical hemolytic uremic syndrome triggered by influenza B. BMC Nephrol. 18, 96. https://doi.org/10.1186/s12882-017-0512-y
- Mittal N., Hartemayer R., Jandeska S., Giordano L. 2019. Steroid responsive atypical hemolytic uremic syndrome triggered by influenza B infection. J. Pediatr. Hematol. Oncol. 41, e63–e67. https://doi.org/10.1097/MPH.0000000000001180
- van Hoeve K., Vandermeulen C., Van Ranst M., Levtchenko E., van den Heuvel L., Mekahli D. 2017. Occurrence of atypical HUS associated with influenza B. Eur. J. Pediatr. 176, 449–454. https://doi.org/10.1007/s00431-017-2856-5
- Boilard E., Pare G., Rousseau M., Cloutier N., Dubuc I., Levesque T., Borgeat P., Flamand L. 2014. Influenza virus H1N1 activates platelets through FcgammaRIIA signaling and thrombin generation. Blood. 123, 2854–2863. https://doi.org/10.1182/blood-2013-07-515536
- Rondina M.T., Brewster B., Grissom C.K., Zimmerman G.A., Kastendieck D.H., Harris E.S., Weyrich A.S. 2012. In vivo platelet activation in critically ill patients with primary 2009 influenza A(H1N1). Chest. 141, 1490–1495. https://doi.org/10.1378/chest.11-2860
- Lambre C.R., Kazatchkine M.D., Maillet F., Thibon M. 1982. Guinea pig erythrocytes, after their contact with influenza virus, acquire the ability to activate the human alternative complement pathway through virus-induced desialation of the cells. J. Immunol. 128, 629–634.
- Berdal J.E., Mollnes T.E., Waehre T., Olstad O.K., Halvorsen B., Ueland T., Laake J.H., Furuseth M.T., Maagaard A., Kjekshus H., Aukrust P., Jonassen C.M. 2011. Excessive innate immune response and mutant D222G/N in severe A (H1N1) pandemic influenza. J. Infect. 63, 308–316. https://doi.org/10.1016/j.jinf.2011.07.004
- Sun S., Zhao G., Liu C., Wu X., Guo Y., Yu H., Song H., Du L., Jiang S., Guo R., Tomlinson S., Zhou Y. 2013. Inhibition of complement activation alleviates acute lung injury induced by highly pathogenic avian influenza H5N1 virus infection. Am. J. Respir. Cell. Mol. Biol. 49, 221–230. https://doi.org/10.1165/rcmb.2012-0428OC
- Noris M., Remuzzi G. 2015. Glomerular diseases dependent on complement activation, including atypical hemolytic uremic syndrome, membranoproliferative glomerulonephritis, and C3 glomerulopathy: Core curriculum 2015. Am. J. Kidney Dis. 66, 359–375. https://doi.org/10.1053/j.ajkd.2015.03.040
- Salvadori M., Bertoni E. 2013. Update on hemolytic uremic syndrome: Diagnostic and therapeutic recommendations. World J. Nephrol. 2, 56–76. https://doi.org/10.5527/wjn.v2.i3.56
- Thurman J.M. 2015. Complement in kidney disease: Core curriculum 2015. Am. J. Kidney Dis. 65, 156–168. https://doi.org/10.1053/j.ajkd.2014.06.035
- Bitzan M., Zieg J. 2018. Influenza-associated thrombotic microangiopathies. Pediatr. Nephrol. 33, 2009–2025. https://doi.org/10.1007/s00467-017-3783-4
- Silecchia V., D’Onofrio G., Valerio E., Rubin G., Vidal E., Murer L. 2021. Influenza-associated hemolytic uremic syndrome: The pathogenic role of the virus. Clin. Nephrol. Case Stud. 9, 45–48. https://doi.org/10.5414/CNCS110219
- Boccia R.V., Gelmann E.P., Baker C.C., Marti G., Longo D.L. 1984. A hemolytic-uremic syndrome with the acquired immunodeficiency syndrome. Ann. Intern. Med. 101, 716–717. https://doi.org/10.7326/0003-4819-101-5-716_2
- Freist M., Garrouste C., Szlavik N., Coppo P., Lautrette A., Heng A.E. 2017. Efficacy of eculizumab in an adult patient with HIV-associated hemolytic uremic syndrome: A case report. Medicine (Baltimore). 96, e9358. https://doi.org/10.1097/MD.0000000000009358
- Jin A., Boroujerdi-Rad L., Shah G., Chen J.L. 2016. Thrombotic microangiopathy and human immunodeficiency virus in the era of eculizumab. Clin. Kidney J. 9, 576–579. https://doi.org/10.1093/ckj/sfw035
- Huson M.A., Wouters D., van Mierlo G., Grobusch M.P., Zeerleder S.S., van der Poll T. 2015. HIV coinfection enhances complement activation during sepsis. J. Infect. Dis. 212, 474–483. https://doi.org/10.1093/infdis/jiv074
- Huber M., Fischer M., Misselwitz B., Manrique A., Kuster H., Niederost B., Weber R., von Wyl V., Gunthard H.F., Trkola A. 2006. Complement lysis activity in autologous plasma is associated with lower viral loads during the acute phase of HIV-1 infection. PLoS Med. 3, e441. https://doi.org/10.1371/journal.pmed.0030441
- Senaldi G., Peakman M., McManus T., Davies E.T., Tee D.E., Vergani D. 1990. Activation of the complement system in human immunodeficiency virus infection: Relevance of the classical pathway to pathogenesis and disease severity. J. Infect. Dis. 162, 1227–1232. https://doi.org/10.1093/infdis/162.6.1227
- Spear G.T., Takefman D.M., Sullivan B.L., Landay A.L., Zolla-Pazner S. 1993. Complement activation by human monoclonal antibodies to human immunodeficiency virus. J. Virol. 67, 53–59. https://doi.org/10.1128/JVI.67.1.53-59.1993
- Stoiber H., Kacani L., Speth C., Wurzner R., Dierich M.P. 2001. The supportive role of complement in HIV pathogenesis. Immunol. Rev. 180, 168–176. https://doi.org/10.1034/j.1600-065x.2001.1800115.x
- Humbert M., Dietrich U. 2006. The role of neutralizing antibodies in HIV infection. AIDS Rev. 8, 51–59.
- Ji X., Gewurz H., Spear G.T. 2005. Mannose binding lectin (MBL) and HIV. Mol. Immunol. 42, 145–152. https://doi.org/10.1016/j.molimm.2004.06.015
- Ezekowitz R.A., Kuhlman M., Groopman J.E., Byrn R.A. 1989. A human serum mannose-binding protein inhibits in vitro infection by the human immunodeficiency virus. J. Exp. Med. 169, 185–196. https://doi.org/10.1084/jem.169.1.185
- Haurum J.S., Thiel S., Jones I.M., Fischer P.B., Laursen S.B., Jensenius J.C. 1993. Complement activation upon binding of mannan-binding protein to HIV envelope glycoproteins. AIDS. 7, 1307–1313. https://doi.org/10.1097/00002030-199310000-00002
- Saifuddin M., Hart M.L., Gewurz H., Zhang Y., Spear G.T. 2000. Interaction of mannose-binding lectin with primary isolates of human immunodeficiency virus type 1. J. Gen. Virol. 81, 949–955. https://doi.org/10.1099/0022-1317-81-4-949
- Hart M.L., Saifuddin M., Spear G.T. 2003. Glycosylation inhibitors and neuraminidase enhance human immunodeficiency virus type 1 binding and neutralization by mannose-binding lectin. J. Gen. Virol. 84, 353–360. https://doi.org/10.1099/vir.0.18734-0
- Ying H., Ji X., Hart M.L., Gupta K., Saifuddin M., Zariffard M.R., Spear G.T. 2004. Interaction of mannose-binding lectin with HIV type 1 is sufficient for virus opsonization but not neutralization. AIDS Res. Hum. Retroviruses. 20, 327–335. https://doi.org/10.1089/088922204322996563
- Bajtay Z., Speth C., Erdei A., Dierich M.P. 2004. Cutting edge: Productive HIV-1 infection of dendritic cells via complement receptor type 3 (CR3, CD11b/ CD18). J. Immunol. 173, 4775–4778. https://doi.org/10.4049/jimmunol.173.8.4775
- Pruenster M., Wilflingseder D., Banki Z., Ammann C.G., Muellauer B., Meyer M., Speth C., Dierich M.P., Stoiber H. 2005. C-type lectin-independent interaction of complement opsonized HIV with monocyte-derived dendritic cells. Eur. J. Immunol. 35, 2691–2698. https://doi.org/10.1002/eji.200425940
- Prohaszka Z., Nemes J., Hidvegi T., Toth F.D., Kerekes K., Erdei A., Szabo J., Ujhelyi E., Thielens N., Dierich M.P., Spath P., Ghebrehiwet B., Hampl H., Kiss J., Arlaud G., Fust G. 1997. Two parallel routes of the complement-mediated antibody-dependent enhancement of HIV-1 infection. AIDS. 11, 949–958. https://doi.org/10.1097/00002030-199708000-00002
- Delibrias C.C., Kazatchkine M.D., Fischer E. 1993. Evidence for the role of CR1 (CD35), in addition to CR2 (CD21), in facilitating infection of human T cells with opsonized HIV. Scand. J. Immunol. 38, 183–189. https://doi.org/10.1111/j.1365-3083.1993.tb01711.x
- Kacani L., Banki Z., Zwirner J., Schennach H., Bajtay Z., Erdei A., Stoiber H., Dierich M.P. 2001. C5a and C5a(desArg) enhance the susceptibility of monocyte-derived macrophages to HIV infection. J. Immunol. 166, 3410–3415. https://doi.org/10.4049/jimmunol.166.5.3410
- Speth C., Schabetsberger T., Mohsenipour I., Stockl G., Wurzner R., Stoiber H., Lass-Florl C., Dierich M.P. 2002. Mechanism of human immunodeficiency virus-induced complement expression in astrocytes and neurons. J. Virol. 76, 3179–3188. https://doi.org/10.1128/jvi.76.7.3179-3188.2002
- Horakova E., Gasser O., Sadallah S., Inal J.M., Bourgeois G., Ziekau I., Klimkait T., Schifferli J.A. 2004. Complement mediates the binding of HIV to erythrocytes. J. Immunol. 173, 4236–4241. https://doi.org/10.4049/jimmunol.173.6.4236
- Stoiber H., Pinter C., Siccardi A.G., Clivio A., Dierich M.P. 1996. Efficient destruction of human immunodeficiency virus in human serum by inhibiting the protective action of complement factor H and decay accelerating factor (DAF, CD55). J. Exp. Med. 183, 307–310. https://doi.org/10.1084/jem.183.1.307
- Saifuddin M., Parker C.J., Peeples M.E., Gorny M.K., Zolla-Pazner S., Ghassemi M., Rooney I.A., Atkinson J.P., Spear G.T. 1995. Role of virion-associated glycosylphosphatidylinositol-linked proteins CD55 and CD59 in complement resistance of cell line-derived and primary isolates of HIV-1. J. Exp. Med. 182, 501–509. https://doi.org/10.1084/jem.182.2.501
- Schmitz J., Zimmer J.P., Kluxen B., Aries S., Bogel M., Gigli I., Schmitz H. 1995. Antibody-dependent complement-mediated cytotoxicity in sera from patients with HIV-1 infection is controlled by CD55 and CD59. J. Clin. Invest. 96, 1520–1526. https://doi.org/10.1172/JCI118190
- Glasgow L.A., Balduzzi P. 1965. Isolation of Coxsackie virus group A, type 4, from a patient with hemolytic-uremic syndrome. N. Engl. J. Med. 273, 754–756. https://doi.org/10.1056/NEJM196509302731407
- Austin T.W., Ray C.G. 1973. Coxsackie virus group B infections and the hemolytic-uremic syndrome. J. Infect. Dis. 127, 698–701. https://doi.org/10.1093/infdis/127.6.698
- De Petris L., Gianviti A., Caione D., Innocenzi D., Edefonti A., Montini G., De Palo T., Tozzi A.E., Caprioli A., Rizzoni G. 2002. Role of non-polio enterovirus infection in pediatric hemolytic uremic syndrome. Pediatr. Nephrol. 17, 852–855. https://doi.org/10.1007/s00467-002-0966-3
- Larke R.P., Preiksaitis J.K., Devine R.D., Harley F.L. 1983. Haemolytic uraemic syndrome: Evidence of multiple viral infections in a cluster of ten cases. J. Med. Virol. 12, 51–59. https://doi.org/10.1002/jmv.1890120106
- O’Regan S., Robitaille P., Mongeau J.G., McLaughlin B. 1980. The hemolytic uremic syndrome associated with ECHO 22 infection. Clin. Pediatr. (Phila). 19, 125–127. https://doi.org/10.1177/000992288001900207
- Ray C.G., Portman J.N., Stamm S.J., Hickman R.O. 1971. Hemolytic-uremic syndrome and myocarditis. Association with coxsackievirus B infection. Am. J. Dis. Child. 122, 418–420. https://doi.org/10.1001/archpedi.1971.02110050088010
- Ray C.G., Tucker V.L., Harris D.J., Cuppage F.E., Chin T.D. 1970. Enteroviruses associated with the hemolytic-uremic syndrome. Pediatrics. 46, 378–388.
- Vecilla M.C., Ruiz Moreno M., Bernacer M., Casado S., Rocandio L. 1984. Familial hemolytic-uremic syndrome associated with Coxsackie B infection. An. Esp. Pediatr. 20, 369–374.
- Lee M.D., Tzen C.Y., Lin C.C., Huang F.Y., Liu H.C., Tsai J.D. 2013. Hemolytic uremic syndrome caused by enteroviral infection. Pediatr. Neonatol. 54, 207–210. https://doi.org/10.1016/j.pedneo.2012.10.012
- Spiller O.B., Goodfellow I.G., Evans D.J., Almond J.W., Morgan B.P. 2000. Echoviruses and coxsackie B viruses that use human decay-accelerating factor (DAF) as a receptor do not bind the rodent analogues of DAF. J. Infect. Dis. 181, 340–343. https://doi.org/10.1086/315210
- Fujita T., Inoue T., Ogawa K., Iida K., Tamura N. 1987. The mechanism of action of decay-accelerating factor (DAF). DAF inhibits the assembly of C3 convertases by dissociating C2a and Bb. J. Exp. Med. 166, 1221–1228. https://doi.org/10.1084/jem.166.5.1221
- Medof M.E., Kinoshita T., Nussenzweig V. 1984. Inhibition of complement activation on the surface of cells after incorporation of decay-accelerating factor (DAF) into their membranes. J. Exp. Med. 160, 1558–1578. https://doi.org/10.1084/jem.160.5.1558
- Nicholson-Weller A., Burge J., Fearon D.T., Weller P.F., Austen K.F. 1982. Isolation of a human erythrocyte membrane glycoprotein with decay-accelerating activity for C3 convertases of the complement system. J. Immunol. 129, 184–189.
- Nicholson-Weller A., Wang C.E. 1994. Structure and function of decay accelerating factor CD55. J. Lab. Clin. Med. 123, 485–491.
- Anderson D.R., Carthy C.M., Wilson J.E., Yang D., Devine D.V., McManus B.M. 1997. Complement component 3 interactions with coxsackievirus B3 capsid proteins: innate immunity and the rapid formation of splenic antiviral germinal centers. J. Virol. 71, 8841–8845. https://doi.org/10.1128/JVI.71.11.8841-8845.1997
- Zanone M.M., Favaro E., Conaldi P.G., Greening J., Bottelli A., Perin P.C., Klein N.J., Peakman M., Camussi G. 2003. Persistent infection of human microvascular endothelial cells by coxsackie B viruses induces increased expression of adhesion molecules. J. Immunol. 171, 438–446. https://doi.org/10.4049/jimmunol.171.1.438
- Richardson G.M., Su S.W., Iragorri S. 2022. Case report: Diarrhea-associated hemolytic uremic syndrome in the Era of COVID-19. Front. Pediatr. 10, 979850. https://doi.org/10.3389/fped.2022.979850
- Smarz-Widelska I., Syroka-Glowka M., Janowska-Jaremek J., Koziol M.M., Zaluska W. 2022. Atypical Hemolytic Uremic Syndrome after SARS-CoV-2 Infection: Report of Two Cases. Int. J. Environ. Res. Public Health. 19. https://doi.org/10.3390/ijerph191811437
- Dalkiran T., Kandur Y., Kara E.M., Dagoglu B., Taner S., Oncu D. 2021. Thrombotic microangiopathy in a severe pediatric case of COVID-19. Clin. Med. Insights. Pediatr. 15, 11795565211049897. https://doi.org/10.1177/11795565211049897
- Helms J., Tacquard C., Severac F., Leonard-Lorant I., Ohana M., Delabranche X., Merdji H., Clere-Jehl R., Schenck M., Fagot Gandet F., Fafi-Kremer S., Castelain V., Schneider F., Grunebaum L., Angles-Cano E., Sattler L., Mertes P.M., Meziani F., Group C.T. 2020. High risk of thrombosis in patients with severe SARS-CoV-2 infection: A multicenter prospective cohort study. Intensive Care Med. 46, 1089–1098. https://doi.org/10.1007/s00134-020-06062-x
- Magro C., Mulvey J.J., Berlin D., Nuovo G., Salvatore S., Harp J., Baxter-Stoltzfus A., Laurence J. 2020. Complement associated microvascular injury and thrombosis in the pathogenesis of severe COVID-19 infection: A report of five cases. Transl. Res. 220, 1–13. https://doi.org/10.1016/j.trsl.2020.04.007
- Beltrame M.H., Catarino S.J., Goeldner I., Boldt A.B., de Messias-Reason I.J. 2014. The lectin pathway of complement and rheumatic heart disease. Front. Pediatr. 2, 148. https://doi.org/10.3389/fped.2014.00148
- Krarup A., Wallis R., Presanis J.S., Gal P., Sim R.B. 2007. Simultaneous activation of complement and coagulation by MBL-associated serine protease 2. PLoS One. 2, e623. https://doi.org/10.1371/journal.pone.0000623