Proteins of the lectin pathway of the complement system activation: immunobiological functions, genetics and involvement in the pathogenesis of human diseases

Cover Page

Cite item

Full Text

Abstract

The complement system is the most ancient components in the innate immunity, mainly functioning to primarily eliminate bacterial agents intravascularly. Moreover, the complement complex proteins play a role as a “bridge” between the systems of innate and adaptive immunity providing adequate conditions for maturation and differentiation of B- and T-lymphocytes. The complement system consists of plasma proteins and membrane receptors. Plasma proteins interact with each other via the three described cascade pathways — lectin (which is most ancient phylogenetically), alternative and classical. Lectins are proteins comprising a separate superfamily of pattern-recognizing receptors able to sense molecules of oligo- and polysaccharide nature and induce their aggregation. Among all the lectins, ficolins (FCN) (common domain — fibrinogen) and collectins (common domain — collagen) — mannose-binding lectin (MBL), hepatic and renal collectins have exert unique functions by complexing with carbohydrate components of microbial wall. Formation of a compound complex “microbial wall polysaccharides + collectin/ficolin + specific mannose-binding lectin-associated serine proteases (MARP)” results in the complement system activation, inflammatory reaction and bacterium elimination. Such scenario is proceeded along the lectin pathway compared to the two other pathways called classical and alternative. Examining a role of the complement system and congenital protein defects in the pathogenesis of various diseases is of topical interest because inborn deficiency of the complement components comprises at least 5% out of total primary immunodeficiency rate, whereas the aspects of their prevalence and pathogenesis remain unexplored. Relevance of investigating the complement system components for diverse populations is tremendous, taking into consideration accumulated evidence regarding an important role of the lectin pathway in viral infections. Lectins, the main proteins in the lectin pathway of the complement activation, are encoded by polymorphic genes, wherein single nucleotide polymorphisms (SNPs) result in altered protein conformation and expression, which, in turn, affects functionality and potential to respond to a pathogen. The distribution of the lectin polymorphic gene frequencies and their haplotypes displays extremely marked population differences. According to analyzing available data, population SNP frequencies including those associated with inborn deficiencies for components of the lectin pathway have been currently scarce or unexplored. hence, here we review major lectins and their functions, their functionally significant SNPs in diverse populations and their pathogenetic importance for host defense functions.

About the authors

Marina V. Smolnikova

Research Institute of Medical Problems of the North, Krasnoyarsk Scientific Center, Siberian Branch, Russian Academy of Sciences

Email: smarinv@ya.ru
ORCID iD: 0000-0001-9984-2029

PhD (Biology), Head of the Molecular Genetic Research Group, Leading Researcher

Russian Federation, 660022, Krasnoyarsk, Partizana Zheleznyaka str., 3g

Sergey Yu. Tereshchenko

Research Institute of Medical Problems of the North, Krasnoyarsk Scientific Center, Siberian Branch, Russian Academy of Sciences

Author for correspondence.
Email: legise@mail.ru
ORCID iD: 0000-0002-1605-7859

PhD, MD (Medicine), Head of the Clinical Department of Somatic and Mental Health of Children

Russian Federation, 660022, Krasnoyarsk, Partizana Zheleznyaka str., 3g

References

  1. Романов А.О., Беляева Т.В., Красильщикова И.В. Частота встречаемости полиморфизма +230G/A гена MBL у жителей Санкт-Петербурга // Medline.Ru. 2006. Т. 7, № 1. С. 372–377. [Romanov A.O., Belyaeva T.V., Krasilshchikova I.V. Frequency of occurrence of +230G/A polymorphism of the MBL gene in residents of St. Petersburg. Medline.Ru, 2006, vol. 7, no. 1, pp. 372–377. (In Russ.)]
  2. Aittoniemi J., Baer M., Soppi E., Vesikari T., Miettinen A. Mannan-binding lectin deficiency and concomitant immunodefects. Arch. Dis. Child., 1998, vol. 78, pp. 245–248. doi: 10.1136/adc.78.3.245
  3. Aittoniemi J., Miettinen A., Laippala P., Isolauri E., Viikari J., Ruuska T., Soppi E. Age-dependent variation in the serum concentration of mannan-binding protein. Acta Paediatr., 1996, vol. 85, pp. 906–909. doi: 10.1111/j.1651-2227.1996.tb14182.x.
  4. Akaiwa M., Yae Y., Sugimoto R., Suzuki S.O., Iwaki T., Izuhara K., Hamasaki N. Hakata antigen, a new member of the ficolin/opsonin p35 family, is a novel human lectin secreted into bronchus/alveolus and bile. J. Histochem. Cytochem., 1999, vol. 47, pp. 777–786. doi: 10.1177/002215549904700607
  5. Ali Y.M., Ferrari M., Lynch N.J., Yaseen S., Dudler T., Gragerov S., Demopulos G., Heeney J.L., Schwaeble W.J. Lectin pathway mediates complement activation by SARS-CoV-2 proteins. Front. Immunol., 2021, vol. 12: 714511. doi: 10.3389/fimmu.2021.714511
  6. Ali Y.M., Lynch N.J., Haleem K.S., Fujita T., EndoY., Hansen S., Holmskov U., Takahashi K., Stahl G.L., Dudler T., Girija U.V., Wallis R., Kadioglu A., Stover C.M., Andrew P.W., Schwaeble W.J. The lectin pathway of complement activation is a critical component of the innate immune response to pneumococcal infection. PLoS Pathog., 2012, vol. 8, no. 7: e1002793. doi: 10.1371/journal.ppat.1002793
  7. Ambrosio A.R., De Messias-Reason I.J. Leishmania (Viannia) braziliensis: interaction of mannose-binding lectin with surface glycoconjugates and complement activation. An antibody-independent defence mechanism. Parasite Immunol., 2005, vol. 27, pp. 333–340. doi: 10.1111/j.1365-3024.2005.00782.x
  8. Ammitzbøll C.G., Kjær T.R., Steffensen R., Stengaard-Pedersen K., Nielsen H.J., Thiel S., Bøgsted M., Jensenius J.C. Non-synonymous polymorphisms in the FCN1 gene determine ligand-binding ability and serum levels of M-ficolin. PLoS One, 2012, vol. 7, no. 11: e50585. doi: 10.1371/journal.pone.0050585
  9. Arai T., Tabona P., Summerfield J.A. Human mannose-binding protein gene is regulated by interleukins, dexamethasone and heat shock. Q. J. Med., 1993, vol. 86, pp. 575–582. doi: 10.1093/oxfordjournals.qjmed.a068848
  10. Areeshi M.Y., Mandal R.K., Akhter N., Dar S.A., Jawed A., Wahid M., Mahto H., Panda A.K., Lohani M., Haque S. A meta-analysis of MBL2 polymorphisms and tuberculosis risk. Sci. Rep., 2016, vol. 6: 35728. doi: 10.1038/srep35728
  11. Bernig T., Breunis W., Brouwer N., Hutchinson A., Welch R., Roos D., Kuijpers T., Chanock S. An analysis of genetic variation across the MBL2 locus in Dutch Caucasians indicates that 3′ haplotypes could modify circulating levels of mannose-binding lectin. Hum. Genet., 2005, vol. 118, no. 3–4, pp. 404–415 doi: 10.1007/s00439-005-0053-5
  12. Bernig T., Taylor J.G., Foster C.B., Staats B., Yeager M., Chanock S.J. Sequence analysis of the mannose-binding lectin (MBL2) gene reveals a high degree of het-erozygosity with evidence of selection. Genes Immun., 2004, vol. 5, pp. 461–476. doi: 10.1038/sj.gene.6364116
  13. Best L.G., Davidson M., North K.E., Maccluer J.W., Zhang Y., Lee E.T., Howard B.V., Decroo S., Ferrell R.E. Prospective analysis of mannose-binding lectin genotypes and coronary artery disease in American Indians: the strong heart study. Circulation, 2004, vol. 109, no. 4, pp. 471–475. doi: 10.1161/01.CIR.0000109757.95461.10
  14. Bjarnadottir H., Arnardottir M., Ludviksson B.R. Frequency and distribution of FCN2 and FCN3 functional variants among MBL2 genotypes. Immunogenetics, 2016, vol. 68, no. 5, pp. 315–325. doi: 10.1007/s00251-016-0903-4
  15. Blom A.M., Villoutreix B.O., Dahlbäck B. Complement inhibitor C4b-binding protein-friend or foe in the innate immune system? Mol. Immunol., 2004, vol. 40, pp. 1333–1346. doi: 10.1016/j.molimm.2003.12.002
  16. Bohlson S.S., Fraser D.A., Tenner A.J. Complement proteins C1q and MBL are pattern recognition molecules that signal immediate and long-term protective immune functions. Mol. Immunol., 2007, vol. 44, pp. 33–43. doi: 10.1016/j.molimm.2006.06.021
  17. Boldt A.B., Culpi L., Tsuneto L.T., De Souza I.R., Kun J.F., Petzl-Erler M.L. Diversity of the MBL2 gene in various Brazilian populations and the case of selection at the mannose-binding lectin locus. Hum. Immunol., 2006, vol. 67, no. 9, pp. 722–734. doi: 10.1016/j.humimm.2006.05.009
  18. Boldt A.B., Goeldner I., Stahlke E.R., Thiel S., Jensenius J.C., de Messias-Reason I.J. Leprosy association with low MASP-2 levels generated by MASP2 haplotypes and polymorphisms flanking MAp19 exon 5. PLoS One, 2013, vol. 8, no. 7: e69054. doi: 10.1371/journal.pone.0069054
  19. Boldt A.B., Luty A., Grobusch M.P., Dietz K., Dzeing A., Kombila M., Kremsner P.G., Kun J.F. Association of a new mannose-binding lectin variant with severe malaria in Gabonese children. Genes Immun., 2006, vol. 7, pp. 393–400. doi: 10.1038/sj.gene.6364312
  20. Boldt A.B., Messias-Reason I.J., Meyer D., Schrago C.G., Lang F., Lell B., Dietz K., Kremsner P.G., Petzl-Erler M.L., Kun J.F. Phylogenetic nomenclature and evolution of mannose-binding lectin (MBL2) haplotypes. BMC Genet., 2010, vol. 11: 38. doi: 10.1186/1471-2156-11-38
  21. Brodszki N., Frazer-Abel A., Grumach A.S., Kirschfink M., Litzman J., Perez E., Seppänen M.R.J., Sullivan K.E., Jolles S. European Society for Immunodeficiencies (ESID) and European Reference Network on Rare Primary Immunodeficiency, Autoinflammatory and Autoimmune Diseases (ERN RITA) Complement Guideline: Deficiencies, Diagnosis, and Management. J. Clin. Immunol., 2020, vol. 40, no. 4, pp. 576–591. doi: 10.1007/s10875-020-00754-1
  22. Cao Y., Wang X., Cao Z., Wu C., Wu D., Cheng X. Genetic polymorphisms of MBL2 and tuberculosis susceptibility: a meta-analysis of 22 case-control studies. Arch. Med. Sci., 2018, vol. 14, no. 6, pp. 1212–1232. doi: 10.5114/aoms.2017.65319
  23. Cedzynski M., Nuytinck L., Atkinson A.P., St Swierzko A., Zeman K., SzemraJ. J., Szala A., Turner M.L., Kilpatrick D.C. Extremes of L-ficolin concentration in children with recurrent infections are associated with single nucleotide polymorphisms in the FCN2 gene. Clin. Exp. Immunol., 2007, vol. 150, pp. 99–104. doi: 10.1111/j.1365-2249.2007.03471.x
  24. Chalmers J.D., Mchugh B.J., Doherty C., Smith M.P., Govan J.R., Kilpatrick D.C., Hill A.T. Mannose-binding lectin deciency and disease severity in non-cystic fibrosis bronchiectasis: a prospective study. Lancet Respir. Med., 2013, vol. 1, no. 3, pp. 224–232. doi: 10.1016/S2213-2600(13)70001-8
  25. Charchaflieh J., Wei J., Labaze G., Hou Y.J., Babarsh B., Stutz H., Lee H., Worah M., Zhang M. The role of complement system in septic shock. Clin. Dev. Immunol., 2012, vol. 2012: 407324. doi: 10.1155/2012/407324
  26. Czerewaty M., Tarnowski M., Safranow K., Domanski L., Pawlik A. Mannose binding lectin 2 gene polymorphisms in patients after renal transplantation with acute graft rejection. Transpl. Immunol., 2019, vol. 54, pp. 29–37. doi: 10.1016/j.trim.2019.01.004
  27. Dahl M., Tybjaerg-Hansen A., Schnohr P., Nordestgaard B.G. A population-based study of morbidity and mortality in mannose-binding lectin deficiency. J. Exp. Med., 2004, vol. 199, pp. 1391–1399. doi: 10.1084/jem.20040111
  28. De Rooij B.J.F., van Hoek B., ten Hove W.R., Roos A., Bouwman L.H., Schaapherder A.F., Porte R.G., Daha M.R., van der Reijden J.J., Coenraad M.J., Ringers J., Baranski A.G., Hepkema B.G., Hommes D.W., Verspaget H.W. Lectin complement pathway gene profile of donor and recipient determine the risk of bacterial infections after orthotopic liver transplantation. Hepatology, 2010, vol. 52, pp. 1100–1110. doi: 10.1002/hep.23782
  29. Degn S.E., Jensen L., Gál P., Dobó J., Holmvad S.H., Jensenius J.C., Thiel S. Biological variations of MASP-3 and MAp44, two splice products of the MASP1 gene involved in regulation of the complement system. J. Immunol. Methods, 2010, vol. 361, pp. 37–50. doi: 10.1016/j.jim.2010.07.006
  30. Degn S.E., Jensen L., Hansen A.G., Duman D., Tekin M., Jensenius J.C., Thiel S. Mannan-binding lectin-associated serine protease (MASP)-1 is crucial for lectin pathway activation in human serum, whereas neither MASP-1 nor MASP-3 is required for alternative pathway function. J. Immunol., 2012, vol. 189, pp. 3957–3969. doi: 10.4049/jimmunol.1201736
  31. Eisen D.P., Dean M.M., Boermeester M.A., Fidler K.J., Gordon A.C., Kronborg G., Kun J.F.J., Lau Y.L., Payeras A., Valdimarsson H., Brett S.J., Ip W.K.E., Mila J., Peters M.J., Saevarsdottir S., van Till J.W.O., Hinds C.J., McBryde E.S. Low serum mannose-binding lectin level increases the risk of death due to pneumococcal infection. Clin. Infect. Dis., 2008, vol. 47, no. 4, pp. 510–516. doi: 10.1086/590006
  32. Eisen D.P., Ostho M. If there is an evolutionary selection pressure for the high frequency of MBL2 polymorphisms, what is it? Clin. Exp. Immunol., 2014, vol. 176, no. 2, pp. 165–171. doi: 10.1111/cei.12241
  33. Eriksson O., Hultström M., Persson B., Lipcsey M., Ekdahl K.N., Nilsson B., Frithiof R. Mannose-binding lectin is associated with thrombosis and coagulopathy in critically ill COVID-19 patients. Thromb. Haemost., 2020, vol. 120, no. 12, pp. 1720–1724. doi: 10.1055/s-0040-1715835
  34. Ezekowitz R.A., Day L.E., Herman G.A. A human mannose-binding protein is an acute-phase reactant that shares sequence homology with other vertebrate lectins. J. ExpMed., 1988, vol. 167, pp. 1034–1046. doi: 10.1084/jem.167.3.1034
  35. Fisch U.P., Zehnder A., Hirt A., Niggli F.K., Simon A., Ozsahin H., Schlapbach L.J., Ammann R.A. Mannan-binding lectin (MBL) and MBL-associated serine protease-2 in children with cancer. Swiss Med. Wkly, 2011, vol. 141: w13191. doi: 10.4414/smw.2011.13191
  36. Garcia-Laorden M.I., Sole-Violan J., Rodriguez de Castro F., Aspa J., Briones M.L., Garcia-Saavedra A., Rajas O., Blanquer J., Caballero-Hidalgo A., Marcos-Ramos J.A., Hernandez-Lopez J., Rodriguez-Gallego C. Mannose-binding lectin and mannose-binding lectin-associated serine protease 2 in susceptibility, severity, and outcome of pneumonia in adults. J. Allergy Clin. Immunol., 2008, vol. 122, no. 2, pp. 368–374. doi: 10.1016/j.jaci.2008.05.037
  37. Garred P., Honore C., Ma Y.J., Munthe-Fog L., Hummelshøj T. MBL2, FCN1, FCN2 and FCN3 — the genes behind the initiation of the lectin pathway of complement. Mol. Immunol., 2009, vol. 46, no. 14, pp. 2737–2744. doi: 10.1016/j.molimm.2009.05.005
  38. Hegele R.A., Busch C.P., Young T.K., Connelly P.W., Cao H. Mannose-binding lectin gene variation and cardiovascular disease in Canadian inuit. Clin. Chem., 1999, vol. 45, no. 8 (pt 1), pp. 1283–1285. doi: 10.1093/clinchem/45.8.1283
  39. Heitzeneder S., Seidel M., Förster-Wald l.E., Heitger A. Mannan-binding lectin deficiency — good news, bad news, doesn’t matter? Clin. Immunol., 2012, vol. 143, pp. 22–38. doi: 10.1016/j.clim.2011.11.002
  40. Héja D., Harmat V., Fodor K., Wilmanns M., Dobó J., Kékesi K.A. Monospecific inhibitors show that both mannan-binding lectin-associated serine protease-1 (MASP-1) and -2 are essential for lectin pathway activation and reveal structural plasticity of MASP-2. J. Biol. Chem., 2012, vol. 287, pp. 20290–20300. doi: 10.1074/jbc.M112.354332
  41. Héja D., Kocsis A., Dobó J., Szilágyi K., Szász R., Závodszky P., Pál G., Gál P. Revised mechanism of complement lectin-pathway activation revealing the role of serine protease MASP-1 as the exclusive activator of MASP-2. Proc. Natl. Acad. Sci. USA, 2012, vol. 109, pp. 10498–10503. doi: 10.1073/pnas.1202588109
  42. Herpers B.L., Immink M.M., de Jong B.A., van Velzen-Blad H., de Jongh B.M., van Hannen E.J. Coding and non-coding polymorphisms in the lectin pathway activator L-ficolin gene in 188 Dutch blood bank donors. Mol. Immunol., 2006, vol. 43, pp. 851–855. doi: 10.1016/j.molimm.2005.06.035
  43. Holmberg V., Onkamo P., Lahtela E., Lahermo P., Bedu-Addo G., Mockenhaupt F.P., Meri S. Mutations of complement lectin pathway genes MBL2 and MASP2 associated with placental malaria. Malar J., 2012, vol. 11: 61. doi: 10.1186/1475-2875-11-61
  44. Hummelshøj T., Fog L.M., Madsen H.O., Sim R.B., Garred P. Comparative study of the human ficolins reveals unique features of ficolin-3 (Hakata antigen). Mol. Immunol., 2008, vol. 45, pp. 1623–1632. doi: 10.1016/j.molimm.2007.10.006
  45. Hummelshøj T., Munthe-Fog L., Madsen H.O., Fujita T., Matsushita M., Garred P. Polymorphisms in the FCN2 gene determine serum variation and function of ficolin-2. Hum. Mol. Genet., 2005, vol. 14, pp. 1651–1658. doi: 10.1093/hmg/ddi173
  46. Ingels C., Vanhorebeek I., Steffensen R., Derese I., Jensen L., Wouters P.J., Hermans G., Thiel S., den Berghe G.V. Lectin pathway of complement activation and relation with clinical complications in critically ill children. Pediatr. Res., 2014, vol. 75, pp. 99–108. doi: 10.1038/pr.2013.180
  47. Ip W.K.E., Chan K.H., Law H.K.W., Tso G.H.W., Kong E.K.P., Wong W.H.S., To Y.F., Yung R.W.H., Chow E.Y., Au K.L., Chan E.Y.T., Lim W., Jensenius J.C., Turner M.W., Peiris J.S.M., Lau Y.L. Mannose-binding lectin in severe acute respiratory syndrome coronavirus infection. J. Infect. Dis., 2005, vol. 191, no. 10, pp. 1697–1704. doi: 10.1086/429631
  48. Jack D., Turner M. Antimicrobial activities of mannose-binding lectin. Biochem. Soc. Trans., 2003, vol. 31, pp. 753–757. doi: 10.1042/bst0310753
  49. Jensen P.H., Laursen I., Matthiesen F., Højrup P. Post translational modifications in human plasma MBL and human recombinant MBL. Biochim. Biophys. Acta., 2007, vol. 1774, pp. 335–344. doi: 10.1016/j.bbapap.2006.12.008
  50. Kang H.J., Lee S.-M., Lee H.-H., Kim J.Y., Lee B.-C., Yum J.-S., Moon H.M., Lee B.L. Mannose-binding lectin without the aid of its associated serine proteases alters lipopolysaccharide-mediated cytokine/chemokine secretion from human endothelial cells. Immunology, 2007, vol. 122, pp. 335–342. doi: 10.1111/j.1365-2567.2007.02644.x
  51. Kilpatrick D. Mannan-binding lectin and its role in innate immunity. Transfus. Med., 2003, vol. 12, no. 6, pp. 335–352. doi: 10.1046/j.1365-3148.2002.00408.x
  52. Kilpatrick D.C., Chalmers J.D. Human L-ficolin (ficolin-2) and its clinical significance. J. Biomed. Biotechnol., 2012, vol. 2012. doi: 10.1155/2012/138797
  53. Kilpatrick D.C., St Swierzko A., Matsushita M., Domzalska-Popadiuk I., Borkowska-Klos M., Szczapa J., Cedzynski M. The relationship between FCN2 genotypes and serum ficolin-2 (L-ficolin) protein concentrations from a large cohort of neonates. Hum. Immunol., 2013, vol. 74, pp. 867–871. doi: 10.1016/j.humimm.2013.04.011
  54. Kjaer T.R., Thiel S., Andersen G.R. Toward a structure-based comprehension of the lectin pathway of complement. Mol. Immunol., 2013, vol. 56, pp. 413–422. doi: 10.1016/j.molimm.2013.05.220
  55. Klabunde J., Berger J., Jensenius J.C., Klinkert M.Q., Zelck U.E., Kremsner P.G., Kun J.F. Schistosoma mansoni: adhesion of mannan-binding lectin to surface glycoproteins of cercariae and adult worms. Exp. Parasitol., 2000, vol. 95, pp. 231–239. doi: 10.1006/expr.2000.4539
  56. Klabunde J., Uhlemann A.-C., Tebo A.E., Kimmel J., Schwarz R.T., Kremsner P.G., Kun J.F. Recognition of plasmodium falciparum proteins by mannan-binding lectin, a component of the human innate immune system. Parasitol. Res., 2002, vol. 88, pp. 113–117. doi: 10.1007/s00436-001-0518-y
  57. Lipscombe R.J., Sumiya M., Summerfield J.A., Turner M.W. Distinct physico-chemical characteristics of human mannose binding protein expressed by individuals of differing genotype. Immunology, 1995, vol. 85, pp. 660–667.
  58. Luo J., Xu F., Lu G.-J., Lin H.-C., Feng Z.-C. Low mannose-binding lectin (MBL) levels and MBL genetic polymorphisms associated with the risk of neonatal sepsis: an updated meta-analysis. Early Hum. Dev., 2014, vol. 90, no. 10, pp. 557–564. doi: 10.1016/ j.earlhumdev.2014.07.007
  59. Madsen H.O., Garred P., Kurtzhals J.A., Lamm L.U., Ryder L.P., Thiel S., Svejgaard A. A new frequent allele is the missing link in the structural polymorphism of the human mannan-binding protein. Immunogenetics, 1994, vol. 40, pp. 37–44. doi: 10.1007/BF00163962
  60. Madsen H.O., Garred P., Thiel S., Kurtzhals J.A., Lamm L.U., Ryder L.P., Svejgaard A. Interplay between promoter and structural gene variants control basal serum level of mannan-binding protein. J. Immunol., 1995, vol. 155, no. 6, pp. 3013–3020.
  61. Madsen H.O., Satz M.L., Hogh B., Svejgaard A., Garred P. Different molecular events result in low protein levels of mannan-binding lectin in populations from southeast Africa and South America. J. Immunol., 1998, vol. 161, no. 6, pp. 3169–3175.
  62. Madsen H.O., Videm V., Svejgaard A., Svennevig J.L., Garred P. Association of mannose-binding lectin deficiency with severe atherosclerosis. Lancet, 1998, vol. 352, pp. 959–960. doi: 10.1016/S0140-6736(05)61513-9
  63. Manolis A.S., Manolis T.A., Manolis A.A., Papatheou D., Melita H. COVID-19 Infection: Viral Macro- and micro-vascular coagulopathy and thromboembolism/prophylactic and therapeutic management. J. Cardiovasc. Pharmacol. Ther., 2021, vol. 26, no. 1, pp. 12–24. doi: 10.1177/1074248420958973
  64. Matricardi P.M., Negro R.W.D., Nisin R. The first, holistic immunological model of COVID-19: implications for prevention, diagnosis, and public health measures. Pediatr. Allergy Immunol., 2020, vol. 31, no. 5, pp. 454–470. doi: 10.1111/pai.13271
  65. Matsushita M., Endo Y., Taira S., Sato Y., Fujita T., Ichikawa N., Nakata M., Mizuochi T. A novel human serum lectin with collagen and fibrinogen-like domains that functions as an opsonin. J. Biol. Chem., 1996, vol. 271, pp. 2448–2454. doi: 10.1074/jbc.271.5.2448
  66. Mayilyan K.R., Arnold J.N., Presanis J.S., Soghoyan A.F., Sim R.B. Increased complement classical and mannan-binding lectin pathway activities in schizo-phrenia. Neurosci. Lett., 2006, vol. 404, pp. 336–341. doi: 10.1016/j.neulet.2006.06.051
  67. Michalski M., St Swierzko A., Lukasiewicz J., Man-Kupisinska A., Karwaciak I., Przygodzka P., Cedzynski M. Ficolin-3 activity towards the opportunistic patho-gen, Hafnia alvei. Immunobiology, 2015, vol. 220, pp. 117–123. doi: 10.1016/j.imbio.2014.08.012
  68. Michalski M., Szala A., St Swierzko A., Lukasiewicz J., Maciejewska A., Kilpatrick D.C., Matsushita M., Domzalska-Popadiuk I., Borkowska-Klos M., Sokolowska A., Szczapa J., Lugowski C., Cedzynski M. H-ficolin (ficolin-3) concentrations and FCN3 gene polymorphism in neonates. Immunobiology, 2011, vol. 217, pp. 730–737. doi: 10.1016/j.imbio.2011.12.004
  69. Mishra A., Antony J.S., Sundaravadivel P., Tong H.V., Meyer C.G., Jalli R.D., Velavan T.P., ThangaraJ. K. Association of ficolin-2 serum levels and FCN2 genetic variants with Indian visceral leishmaniasis. PLoS One, 2015, vol. 10, no. 5: e0125940. doi: 10.1371/journal.pone.0125940
  70. Monsey L., Best L.G., Zhu J., Decroo S., Anderson M.Z. The association of mannose binding lectin genotype and immune response to Chlamydia pneumoniae: the strong heart study. PLoS One, 2019, vol. 14, no. 1: e0210640. doi: 10.1371/journal.pone.0210640
  71. Munthe-Fog L., Hummelshøj T., Hansen B.E., Koch C., Madsen H.O., Skjodt K., Garred P. The impact of FCN2 polymorphisms and haplotypes on the ficolin-2 serum levels. Scand. J. Immunol., 2007, vol. 65, pp. 383–392. doi: 10.1111/j.1365-3083.2007.01915.x
  72. Nauta A.J., Castellano G., Xu W., Woltman A.M., Borrias M.C., Daha M.R., Kooten C., Roos A. Opsonization with C1q and mannose-binding lectin targets apoptotic cells to dendritic cells. J. Immunol., 2004, vol. 173, pp. 3044–3050. doi: 10.4049/jimmunol.173.5.3044
  73. Notarangelo L., Casanova J.-L., Fischer A., Puck J., Rosen F., Seger R., Geha R. Primary immunodeficiency diseases: an update. J. Allergy Clin. Immunol., 2004, vol. 114, no. 3, pp. 677–687. doi: 10.1016/j.jaci.2004.06.044
  74. Rambaldi A., Gritti G., Micò M.C., Frigeni M., Borleri G., Salvi A., Landi F., Pavoni C., Sonzogni A., Gianatti A., Binda F., Fagiuoli S., Marco F.D., Lorini L., Remuzzi G., Whitaker S., Demopulos G. Endothelial injury and thrombotic microangiopathy in COVID-19: Treatment with the lectin-pathway inhibitor narsoplimab. Immunobiology, 2020, vol. 225, no. 6: 152001. doi: 10.1016/j.imbio.2020.152001
  75. Ren Y., Ding Q., Zhang X. Ficolins and infectious diseases. Virol. Sin., 2014, vol. 29, pp. 25–32. doi: 10.1007/s12250-014-3421-2
  76. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. Complement: a key system for immune surveillance and homeostasis. Nat. Immunol., 2010, vol. 11, pp. 785–797. doi: 10.1038/ni.1923
  77. Ruskamp J.M., Hoekstra M.O., Postma D.S., Kerkhof M., Bottema R.W., Koppelman G.H., Rovers M.M., Wijga A.H., de Jongste J.C., Brunekreef B., Sanders E.A.M. Exploring the role of polymorphisms in ficolin genes in respiratory tract infections in children. Clin. Exp. Immunol., 2009, vol. 155, no. 3, pp. 433–440. doi: 10.1111/j.1365-2249.2008.03844.x
  78. Sallenbach S., Thiel S., Aebi C., Otth M., Bigler S., Jensenius J.C., Schlapbach L.J., Ammann R.A. Serum concentrations of lectin-pathway components in healthy neonates, children and adults: mannan-binding lectin (MBL), M-, L-, and H-ficolin, and MBL-associated serine protease-2 (MASP-2). Pediatr. Allergy Immunol., 2011, vol. 22, pp. 424–430. doi: 10.1111/j.1399-3038.2010.01104.x
  79. Sastry K., Herman G.A., Day L., Deignan E., Bruns G., Morton C.C., Ezekowitz R.A.B. The human mannose-binding protein gene. Exon structure reveals its evolutionary relationship to a human pulmonary surfactant gene and localization to chromosome 10. J. Exp. Med., 1989, vol. 170, pp. 1175–1189. doi: 10.1084/jem.170.4.1175
  80. Skalnikova H., Freiberger T., Chumchalova J., Grombirikova H., Sediva A. Cost-effective genotyping of human MBL2 gene mutations using multiplex PCR. J. Immunol. Methods, 2004, vol. 295, no. 1–2, pp. 139–147. doi: 10.1016/j.jim.2004.10.007
  81. Skjoedt M.-O., Hummelshøj T., Palarasah Y., Honore C., Koch C., Skjodt K., Garred P. A novel mannose-binding lectin/ficolin-associated protein is highly expressed in heart and skeletal muscle tissues and inhibits complement activation. J. Biol. Chem., 2010, vol. 285, pp. 8234–8243. doi: 10.1074/jbc.M109.065805
  82. Smolnikova M.V., Freidin M.B., Tereshchenko S.Y. The prevalence of the variants of the L-ficolin gene (FCN2) in the arctic populations of East Siberia. Immunogenetics, 2017, vol. 69, no. 6, pp. 409–413. doi: 10.1007/s00251-017-0984-8
  83. Steffensen R., Thiel S., Varming K., Jersild C., Jensenius J.C. Detection of structural gene mutations and promoter polymorphisms in the mannan-binding lectin (MBL) gene by polymerase chain reaction with sequence-specific primers. J. Immunol. Methods, 2000, vol. 241, pp. 33–42. doi: 10.1016/s0022-1759(00)00198-8
  84. Stengaard-Pedersen K., Thiel S., Gadjeva M., Møller-Kristensen M., Sørensen R., Jensen L.T., Sjøholm A.G., Fugger L., Jensenius J.C. Inherited deficiency of mannan-binding lectin-associated serine protease 2. N. Engl. J. Med., 2003, vol. 349, no. 6, pp. 554–560. doi: 10.1056/NEJMoa022836
  85. Sullivan K.E., Wooten C., Goldman D., Petri M. Mannose-binding protein genetic polymorphisms in black patients with systemic lupus erythematosus. Arthritis Rheumatol., 1996, vol. 39, no. 12, pp. 2046–2051. doi: 10.1002/art.1780391214
  86. Sumiya M., Super M., Tabona P., Levinsky R.J., Arai T., Turner M.W., Summerfield J.A. Molecular basis of opsonic defect in immunodeficient children. Lancet, 1991, vol. 337, pp. 1569–1570. doi: 10.1016/0140-6736(91)93263-9
  87. Takahashi M., Iwaki D., Kanno K., Ishida Y., Xiong J., Matsushita M., Endo Y., Miura S., Ishii N., Sugamura K., Fujita T. Mannose-binding lectin (MBL)-associated serine protease (MASP)-1 contributes to activation of the lectin complement pathway. J. Immunol., 2008, vol. 180, pp. 6132–6138. doi: 10.4049/jimmunol.180.9.6132
  88. Tenner A.J., Robinson S.L., Ezekowitz R.A. Mannose binding protein (MBP) enhances mononuclear phagocyte function via a receptor that contains the 126,000 M(r) component of the C1q receptor. Immunity, 1995, vol. 3, pp. 485–493. doi: 10.1016/1074-7613(95)90177-9
  89. Terai I., Kobayashi K. Perinatal changes in serum mannose-binding protein (MBP) levels. Immunol. Lett., 1993, vol. 38, pp. 185–187. doi: 10.1016/0165-2478(93)90004-l
  90. Tereshchenko S.Y., Kasparov E.V., Smolnikova M.V., Kuvshinova E.V. Mannose-binding lectin deciency in respiratory diseases. Rus. Pulmonol., 2016, vol. 26, no. 6, pp. 748–752. doi: 10.1159/000228159
  91. Tereshchenko S.Y., Smolnikova M.V., Freidin M.B. Mannose-binding lectin gene polymorphisms in the East Siberia and Russian Arctic populations. Immunogenetics, 2020, vol. 72, no. 6–7, pp. 347–354. doi: 10.1007/s00251-020-01175-5
  92. Thiel S. Complement activating soluble pattern recognition molecules with collagen-like regions, mannan-binding lectin, ficolins and associated proteins. Mol. Immunol., 2007, vol. 44, pp. 3875–3888. doi: 10.1016/j.molimm.2007.06.005
  93. Thiel S., Holmskov U., Hviid L., Laursen S.B., Jensenius J.C. The concentration of the C-type lectin, mannan-binding protein, in human plasma increases during an acute phase response. Clin. Exp. Immunol., 1992, vol. 90, pp. 31–35. doi: 10.1111/j.1365-2249.1992.tb05827.x
  94. Thiel S., Kolev M., Degn S., Steffensen R., Hansen A.G., Ruseva M., Jensenius J.C. Polymorphisms in mannan-binding lectin (MBL)-associated serine protease 2 affect stability, binding to MBL, and enzymatic activity. J. Immunol., 2009, vol. 182, pp. 2939–2947. doi: 10.4049/jimmunol.0802053
  95. Thiel S., Steffensen R., Christensen I.J., Ip W.K., Lau Y.L., Reason I.J., Eiberg H., Gadjeva M., Ruseva M., Jensenius J.C. Deficiency of mannan-binding lectin associated serine protease-2 due to missense polymorphisms. Genes Immun., 2007, vol. 8, pp. 154–163. doi: 10.1038/sj.gene.6364373
  96. Trégoat V., Montagne P., Béné M.-C., Faure G. Changes in the mannan binding lectin (MBL) concentration in human milk during lactation. J. Clin. Lab. Anal., 2002, vol. 16, pp. 304–307. doi: 10.1002/jcla.10055
  97. Tulio S., Faucz F.R., Werneck R.I., Olandoski M., Alexandre R.B., Boldt A.B., Pedroso M.L., de Messias-Reason I.J. MASP2 gene polymorphismis associated with susceptibility to hepatitis C virus infection. Hum. Immunol., 2011, vol. 72, pp. 912–915. doi: 10.1016/j.humimm.2011.06.016
  98. Verdu P., Barreiro L.B., Patin E., Gessain A., Cassar O., Kidd J.R., Kidd K.K., Behar D.M., Froment A., Heyer E., Sica L., Casanova J.L., Abel L., Quintana-Murci L. Evolutionary insights into the high worldwide prevalence of MBL2 deciency alleles. Hum. Mol. Genet., 2006, vol. 15, no. 17, pp. 2650–2658. doi: 10.1093/hmg/ddl193
  99. Walport M.J. Complement. First of two parts. N. Engl. J. Med., 2001, vol. 344, pp. 1058–1066. doi: 10.1056/NEJM200104053441406
  100. Wittenborn T., Thiel S., Jensen L., Nielsen H.J., Jensenius J.C. Characteristics and biological variations of M-ficolin, a pattern recognition molecule, in plasma. J. Innate Immun., 2010, vol. 2, pp. 167–180. doi: 10.1159/000218324
  101. Ytting H., Christensen I.J., Thiel S., Jensenius J.C., Nielsen H.J. Pre- and postoperative levels in serum of mannan-binding lectin associated serine protease-2 — a prognostic marker in colorectal cancer. Hum. Immunol., 2008, vol. 69, pp. 414–420. doi: 10.1016/ j.humimm.2008.05.005
  102. Ytting H., Christensen I.J., Thiel S., Jensenius J.C., Nielsen H.J. Serum mannan-binding lectin-associated serine protease-2 levels in colorectal cancer: relation to recurrence and mortality. Clin. Cancer Res., 2005, vol. 11, pp. 1441–1446. doi: 10.1158/1078-0432.CCR-04-1272
  103. Zhang J.X., Gong W.P., Zhu D.L., An H.R., Yang Y.R., Liang Y., Wang J., Tang J., Zhao W.G., Wu X.Q. Mannose-binding lectin 2 gene polymorphisms and their association with tuberculosis in a Chinese population. Infect. Dis. Poverty, 2020, vol. 9, no. 1: 46. doi: 10.1186/s40249-020-00664-9

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2. Figure. A scheme depicting lectin pathway of the complement system activation

Download (92KB)
Indexing metadata

Copyright (c) 2022 Smolnikova M.V., Tereshchenko S.Y.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies