Developmental adaptations of neonatal neutrophils (review)

Cover Page

Cite item

Full Text

Abstract

Neutrophils are crucial components of the innate immunity. Differences exist in the physiological, phenotypic, and functional characteristics between neonatal and adult neutrophils. The severity of these changes is inversely proportional to gestational age, which indicates the dynamic development of these cells throughout pregnancy. Therefore, functional insufficiency of neonatal neutrophils is associated with an extremely high risk of developing neonatal infections and sepsis in infants born premature. Neonatal neutrophils are adapted to conditions that prevent unwanted triggering of proinflammatory factors. In addition, suppression of neutrophil functions is necessary to create a healthy microbiome in the postpartum period; however, it can be inhibit the development of a response to pathogenic organisms. Mechanisms underlying the normal transition of functionally limited neutrophils, capable of fully resisting pathogenic microorganisms, have not been established. This review presents features of neutrophil ontogenetic adaptation to intrauterine conditions and early neonatal period and their potential role in neonatal pathology.

About the authors

Vladimir E. Mukhin

Centre for Strategic Planning and Management of Biomedical Health Risks

Author for correspondence.
Email: muhinvldmr@gmail.com
ORCID iD: 0000-0001-8973-7890
SPIN-code: 9048-2290
Russian Federation, 10 bld. 1 Pogodinskaya street, 119435, Moscow

Liudmila L. Pankratyeva

Dmitry Rogachev NMRC PHOI of the MOH of Russia

Email: liudmila.pankratyeva@gmail.com
ORCID iD: 0000-0002-1339-4155

MD, PhD, Professor of the Department of Pediatrics and Health Organization

Russian Federation, 1 Zamory Machela street, 117198, Moscow

Mikhail N. Yartsev

NRC – Institute of Immunology, FMBA of Russia

Email: m_yartsev@mail.ru
ORCID iD: 0000-0003-0952-2801
SPIN-code: 7411-6674

MD, PhD, Leader Researcher of the Department of Immunopathology of Children

Russian Federation, 24 Kashirskoe sh., 115522, Moscow

Nikolay N. Volodin

NMRC PHOI of the MOH of Russia

Email: 0209nnv@mail.ru
ORCID iD: 0000-0002-2667-8229
SPIN-code: 1899-7484

Acad. of RAS, MD, PhD, Professor, Professor of the Department of Pediatrics and Health Organization

Russian Federation, 1 Zamory Machela street, 117198, Moscow

References

  1. Cuenca AG, Joiner DN, Gentile LF, et al. TRIF-dependent innate immune activation is critical for survival to neonatal gram-negative sepsis. J Immunol. 2015;194(3):1169–1177. doi: 10.4049/jimmunol.1302676
  2. Kemp AS, Campbell DE. The neonatal immune system. Seminars in Neonatology. 1996; 1(2):67–75. doi: 10.1016/S1084-2756(05)80002-8
  3. Azizia M, Lloyd J, Allen M, et al. Immune status in very preterm neonates. Pediatrics. 2012;129(4):e967–974. doi: 10.1542/peds.2011-1579
  4. Urlichs F, Speer CP. Neutrophil function in preterm and term infants. NeoReviews. 2004;5(10):e417–e430. doi: 10.1542/neo.5-10-e417
  5. Makoni M, Eckert J, Pereira AH, et al. Alterations in neonatal neutrophil function attributable to increased immature forms. Early Hum Dev. 2016;103:1–7. doi: 10.1016/j.earlhumdev.2016.05.016
  6. Ander SE, Diamond MS, Coyne CB. Immune responses at the maternal-fetal interface. Sci Immunol. 2019;4(31):eaat6114. doi: 10.1126/sciimmunol.aat6114
  7. Amulic B, Cazalet C, Hayes GL, et al. Neutrophil function: from mechanisms to disease. Annu Rev Immunol. 2012;30:459–489. doi: 10.1146/annurev-immunol-020711-074942
  8. Khaitov RM. Immunology. Moscow: GEOTAR-Media; 2016. 496 p. (In Russ).
  9. Slayton WB, Li Y, Calhoun DA, et al. The first-appearance of neutrophils in the human fetal bone marrow cavity. Early Hum Dev. 1998;53(2):129–144. doi: 10.1016/s0378-3782(98)00049-8
  10. Laver J, Duncan E, Abboud M, et al. High levels of granulocyte and granulocyte-macrophage colony-stimulating factors in cord blood of normal full-term neonates. J Pediatr. 1990;116(4):627–632. doi: 10.1016/s0022-3476(05)81617-8
  11. Nauseef WM, Borregaard N. Neutrophils at work. Nat Immunol. 2014;15(7):602–611. doi: 10.1038/ni.2921
  12. Jiao J, Dragomir AC, Kocabayoglu P, et al. Central role of conventional dendritic cells in regulation of bone marrow release and survival of neutrophils. J Immunol. 2014;192(7):3374–3382. doi: 10.4049/jimmunol.1300237
  13. Tak T, Tesselaar K, Pillay J, et al. What’s your age again? Determination of human neutrophil half-lives revisited. J Leukoc Biol. 2013;94(4):595–601. doi: 10.1189/jlb.1112571
  14. Strydom N, Rankin SM. Regulation of circulating neutrophil numbers under homeostasis and in disease. J Innate Immun. 2013;5(4):304–314. doi: 10.1159/000350282
  15. Edwards SW. Biochemistry and physiology of the neutrophil. Cambridge: Cambridge University Press; 2005.
  16. Schmutz N, Henry E, Jopling J, Christensen RD. Expected ranges for blood neutrophil concentrations of neonates: the Manroe and Mouzinho charts revisited. J Perinatol. 2008;28(4):275–281. doi: 10.1038/sj.jp.7211916
  17. Nittala S, Subbarao GC, Maheshwari A. Evaluation of neutropenia and neutrophilia in preterm infants. J Matern Fetal Neonatal Med. 2012;25(Suppl 5):100–103. doi: 10.3109/14767058.2012.715468
  18. Christensen RD, Yoder BA, Baer VL, Snow GL. Early-onset neutropenia in small-for-gestational-age infants. Pediatrics. 2015;136(5):e1259–e1267. doi: 10.1542/peds.2015-1638
  19. Liu G, Yang H, Chen X, et al. Modulation of neutrophil development and homeostasis. Curr Mol Med. 2013;13(8):1270–1283. doi: 10.2174/15665240113139990062
  20. Lawrence SM, Corriden R, Nizet V. Age-Appropriate functions and dysfunctions of the neonatal neutrophil. Front Pediatr. 2017;5:23. doi: 10.3389/fped.2017.00023
  21. Quinn MT, Gauss KA. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. J Leukoc Biol. 2004;76(4):760–781. doi: 10.1189/jlb.0404216
  22. Vorobyova NV, Kondratenko IV, Vakhlyarskaya S, et al. The role of the mitochondrial pore in the effector functions of human neutrophils. Immunology. 2020;41(1):42–53. (In Russ). doi: 10.33029/0206-4952-2020-41-1-42-53
  23. Mantovani A, Cassatella MA, Costantini C, Jaillon S. Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol. 2011;11(8):519–531. doi: 10.1038/nri3024
  24. Fox SE, Lu W, Maheshwari A, et al. The effects and comparative differences of neutrophil specific chemokines on neutrophil chemotaxis of the neonate. Cytokine. 2005;29(3):135–140. doi: 10.1016/j.cyto.2004.10.007
  25. Weinberger B, Laskin DL, Mariano TM, et al. Mechanisms underlying reduced responsiveness of neonatal neutrophils to distinct chemoattractants. J Leukoc Biol. 2001;70(6):969–976. doi: 10.1016/j.cyto.2004.10.007
  26. Raymond SL, Mathias BJ, Murphy TJ, et al. Neutrophil chemotaxis and transcriptomics in term and preterm neonates. Transl Res. 2017;190:4–15. doi: 10.1016/j.trsl.2017.08.003
  27. Kim SK, Keeney SE, Alpard SK, Schmalstieg FC. Comparison of L-selectin and CD11b on neutrophils of adults and neonates during the first month of life. Pediatr Res. 2003;53(1):132–136. doi: 10.1203/00006450-200301000-00022
  28. Carr R. Neutrophil production and function in newborn infants. Br J Haematol. 2000;110(1):18–28. doi: 10.1046/j.1365-2141.2000.01992.x
  29. Moriguchi N, Yamamoto S, Isokawa S, et al. Granulocyte functions and changes in ability with age in newborns; Report no. 2: activation of granulocyte functions by cytokines. Pediatr Int. 2006;48(1):22–28. doi: 10.1111/j.1442-200X.2006.02150.x
  30. Nussbaum C, Sperandio M. Innate immune cell recruitment in the fetus and neonate. J Reprod Immunol. 2011;90(1):74–81. doi: 10.1016/j.jri.2011.01.022
  31. McEvoy LT, Zakem-Cloud H, Tosi MF. Total cell content of CR3 (CD11b/CD18) and LFA-1 (CD11a/CD18) in neonatal neutrophils: relationship to gestational age. Blood. 1996;87(9):3929–3933.
  32. Anderson DC, Rothlein R, Marlin SD, et al. Impaired transendothelial migration by neonatal neutrophils: abnormalities of Mac-1 (CD11b/CD18)-dependent adherence reactions. Blood. 1990;76(12):2613–2621.
  33. Levy O. Impaired innate immunity at birth: deficiency of bactericidal/permeability-increasing protein (BPI) in the neutrophils of newborns. Pediatr Res. 2002;51(6):667–669. doi: 10.1203/00006450-200206000-00001
  34. Decembrino L, De Amici M, De Silvestri A, et al. Plasma lactoferrin levels in newborn preterm infants with sepsis. J Matern Fetal Neonatal Med. 2017;30(23):2890–2893. doi: 10.1080/14767058.2016.1266479
  35. Linden JR, De Paepe ME, Laforce-Nesbitt SS, Bliss JM. Galectin-3 plays an important role in protection against disseminated candidiasis. Med Mycol. 2013;51(6):641–651. doi: 10.3109/13693786.2013.770607
  36. Fermino ML, Polli CD, Toledo KA, et al. LPS-induced galectin-3 oligomerization results in enhancement of neutrophil activation. PLoS One. 2011;6(10):e26004. doi: 10.1371/journal.pone.0026004
  37. Sundqvist M, Osla V, Jacobsson B, et al. Cord blood neutrophils display a galectin-3 responsive phenotype accentuated by vaginal delivery. BMC Pediatr. 2013;13:128. doi: 10.1186/1471-2431-13-128
  38. Haridan US, Mokhtar U, Machado LR, et al. A comparison of assays for accurate copy number measurement of the low-affinity Fc gamma receptor genes FCGR3A and FCGR3B. PLoS One. 2015;10(1):e0116791. doi: 10.1371/journal.pone.0116791
  39. Nagelkerke SQ, Kuijpers TW. Immunomodulation by IVIg and the Role of Fc-Gamma Receptors: Classic Mechanisms of Action after all? Front Immunol. 2015;5:674. doi: 10.3389/fimmu.2014.00674
  40. Filias A, Theodorou GL, Mouzopoulou S, et al. Phagocytic ability of neutrophils and monocytes in neonates. BMC Pediatr. 2011;11:29. doi: 10.1186/1471-2431-11-29
  41. Falconer AE, Carr R, Edwards SW. Impaired neutrophil phagocytosis in preterm neonates: lack of correlation with expression of immunoglobulin or complement receptors. Biol Neonate. 1995;68(4):264–269. doi: 10.1159/000244245
  42. Källman J, Schollin J, Schalèn C, et al. Impaired phagocytosis and opsonisation towards group B streptococci in preterm neonates. Arch Dis Child Fetal Neonatal Ed. 1998;78(1):F46–50. doi: 10.1136/fn.78.1.f46
  43. Ohlsson A, Lacy JB. Intravenous immunoglobulin for suspected or proven infection in neonates. Cochrane Database Syst Rev. 2020;1(1):CD001239. doi: 10.1002/14651858.CD001239.pub6
  44. Allen RC. Neutrophil leukocyte: combustive microbicidal action and chemiluminescence. J Immunol Res. 2015;2015:794072. doi: 10.1155/2015/794072
  45. Grunwell JR, Giacalone VD, Stephenson S, et al. Neutrophil dysfunction in the airways of children with acute respiratory failure due to lower respiratory tract viral and bacterial coinfections. Sci Rep. 2019;9(1):2874. doi: 10.1038/s41598-019-39726-w
  46. Brinkmann V, Reichard U, Goosmann C, et al. Neutrophil extracellular traps kill bacteria. Science. 2004;303(5663):1532–1535. doi: 10.1126/science.1092385
  47. Mesa MA, Vasquez G. NETosis. Autoimmune Dis. 2013;2013:651497. doi: 10.1155/2013/651497
  48. Sørensen OE, Borregaard N. Neutrophil extracellular traps – the dark side of neutrophils. J Clin Invest. 2016;126(5):1612–1620. doi: 10.1172/JCI84538
  49. Desai J, Mulay SR, Nakazawa D, Anders HJ. Matters of life and death. How neutrophils die or survive along NET release and is “NETosis” = necroptosis? Cell Mol Life Sci. 2016;73(11-12):2211–2219. doi: 10.1007/s00018-016-2195-0
  50. Yost CC, Cody MJ, Harris ES, et al. Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates. Blood. 2009;113(25):6419–6427. doi: 10.1182/blood-2008-07-171629
  51. Byrd AS, O’Brien XM, Laforce-Nesbitt SS, et al. NETosis in neonates: evidence of a reactive oxygen species-independent pathway in response to fungal challenge. J Infect Dis. 2016;213(4):634–639. doi: 10.1093/infdis/jiv435
  52. Bizzarro MJ, Dembry LM, Baltimore RS, Gallagher PG. Changing patterns in neonatal Escherichia coli sepsis and ampicillin resistance in the era of intrapartum antibiotic prophylaxis. Pediatrics. 2008;121(4):689–696. doi: 10.1542/peds.2007-2171
  53. Cotten CM, Taylor S, Stoll B, et al.; NICHD Neonatal Research Network. Prolonged duration of initial empirical antibiotic treatment is associated with increased rates of necrotizing enterocolitis and death for extremely low birth weight infants. Pediatrics. 2009;123(1):58–66. doi: 10.1542/peds.2007-3423
  54. Zeissig S, Blumberg RS. Life at the beginning: perturbation of the microbiota by antibiotics in early life and its role in health and disease. Nat Immunol. 2014;15(4):307–310. doi: 10.1038/ni.2847
  55. Kanoh S, Rubin BK. Mechanisms of action and clinical application of macrolides as immunomodulatory medications. Clin Microbiol Rev. 2010;23(3):590–615. doi: 10.1128/CMR.00078-09
  56. Warner BB, Deych E, Zhou Y, et al. Gut bacteria dysbiosis and necrotising enterocolitis in very low birthweight infants: a prospective case-control study. Gut bacteria dysbiosis and necrotising enterocolitis in very low birthweight infants: a prospective case-control study. Lancet. 2016;387(10031):1928–1936. doi: 10.1016/S0140-6736(16)00081-7
  57. Khosravi A, Yáñez A, Price JG, et al. Gut bacteria dysbiosis and necrotising enterocolitis in very low birthweight infants: a prospective case-control study. Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe. 2014;15(3):374–381. doi: 10.1016/j.chom.2014.02.006
  58. Iwamura C, Bouladoux N, Belkaid Y, et al. Sensing of the microbiota by NOD1 in mesenchymal stromal cells regulates murine hematopoiesis. Blood. 2017;129(2):171–176. doi: 10.1182/blood-2016-06-723742
  59. Koh A, De Vadder F, Kovatcheva-Datchary P, Bäckhed F. From dietary fiber to host physiology: short-chain fatty acids as key bacterial metabolites. Cell. 2016;165(6):1332–1345. doi: 10.1016/j.cell.2016.05.041
  60. Vieira AT, Galvão I, Macia LM, et al. Dietary fiber and the short-chain fatty acid acetate promote resolution of neutrophilic inflammation in a model of gout in mice. J Leukoc Biol. 2017;101(1):275–284. doi: 10.1189/jlb.3A1015-453RRR
  61. Guo C, Xie S, Chi Z, et al. Bile acids control inflammation and metabolic disorder through inhibition of NLRP3 inflammasome. Immunity. 2016;45(4):802–816. doi: 10.1016/j.immuni.2016.09.008
  62. Kobayashi SD, Voyich JM, Whitney AR, DeLeo FR. Spontaneous neutrophil apoptosis and regulation of cell survival by granulocyte macrophage-colony stimulating factor. J Leukoc Biol. 2005;78(6):1408–1418. doi: 10.1189/jlb.0605289
  63. Contrino J, Krause PJ, Slover N, Kreutzer D. Elevated interleukin-1 expression in human neonatal neutrophils. Pediatr Res. 1993;34(3):249–252. doi: 10.1203/00006450-199309000-00002
  64. Wynn JL, Levy O. Role of innate host defenses in susceptibility to early-onset neonatal sepsis. Clin Perinatol. 2010;37(2):307–337. doi: 10.1016/j.clp.2010.04.001
  65. Hou PC, Yu HR, Kuo HC, et al. Different modulating effects of adenosine on neonatal and adult polymorphonuclear leukocytes. Scientific World Journal. 2012;2012:387923. doi: 10.1100/2012/387923
  66. Sundqvist M, Osla V, Jacobsson B, et al. Cord blood neutrophils display a galectin-3 responsive phenotype accentuated by vaginal delivery. BMC Pediatr. 2013;13:128. doi: 10.1186/1471-2431-13-128
  67. Liu W, Yan M, Sugui JA, et al. Olfm4 deletion enhances defense against Staphylococcus aureus in chronic granulomatous disease. J Clin Invest. 2013;123(9):3751–3755. doi: 10.1172/JCI68453
  68. Welin A, Amirbeagi F, Christenson K, et al. The human neutrophil subsets defined by the presence or absence of OLFM4 both transmigrate into tissue in vivo and give rise to distinct NETs in vitro. PLoS One. 2013;8(7):e69575. doi: 10.1371/journal.pone.0069575
  69. Hanna N, Vasquez P, Pham P, et al. Mechanisms underlying reduced apoptosis in neonatal neutrophils. Pediatr Res. 2005;57(1):56–62. doi: 10.1203/01.PDR.0000147568.14392.F0
  70. Kotecha S, Mildner RJ, Prince LR, et al. The role of neutrophil apoptosis in the resolution of acute lung injury in newborn infants. Thorax. 2003;58(11):961–967. doi: 10.1136/thorax.58.11.961.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2021 Pharmarus Print Media

This website uses cookies

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

About Cookies