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Original Article

Evidence for complement activation in the amniotic fluid of women with spontaneous preterm labor and intra-amniotic infection

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Pages 983-992 | Received 18 Feb 2009, Accepted 09 Apr 2009, Published online: 17 Mar 2010

References

  • Medzhitov R, Janeway C Jr.. Innate immunity. N Engl J Med 2000;343:338–344.
  • Gasque P. Complement: a unique innate immune sensor for danger signals. Mol Immunol 2004;41:1089–1098.
  • Walport MJ. Complement. First of two parts. N Engl J Med 2001;344:1058–1066.
  • Carroll MC. The complement system in regulation of adaptive immunity. Nat Immunol 2004;5:981–986.
  • Medzhitov R, Janeway C A Jr.. Decoding the patterns of self and nonself by the innate immune system. Science 2002;296:298–300.
  • Ember JA, Jagels MA, Hugli TE. Characterization of complement anaphylatoxins and their biological responses In: Volanakis JE, Frank MM, editors. The Human Complement System in Health and DiseaseNew York: Marcel Dekker; 1998. pp 241–284.
  • Cochrane CG, Muller-Eberhard HJ. The derivation of two distinct anaphylatoxin activities from the third and fifth components of human complement. J Exp Med 1968;127:371–386.
  • Dias DS, Lepow IH. Complement as a mediator of inflammation. II. Biological properties of anaphylatoxin prepared with purified components of human complement. J Exp Med 1967;125:921–946.
  • Gorski JP, Hugli TE, Muller-Eberhard HJ. C4a: the third anaphylatoxin of the human complement system. Proc Natl Acad Sci USA 1979;76:5299–5302.
  • Schumacher WA, Fantone JC, Kunkel SE, Webb RC, Lucchesi BR. The anaphylatoxins C3a and C5a are vasodilators in the canine coronary vasculature in vitro and in vivo. Agents Actions 1991;34:345–349.
  • Shin HS, Snyderman R, Friedman E, Mellors A, Mayer MM. Chemotactic and anaphylatoxic fragment cleaved from the fifth component of guinea pig complement. Science 1968;162:361–363.
  • Daffern PJ, Pfeifer PH, Ember JA, Hugli TE. C3a is a chemotaxin for human eosinophils but not for neutrophils. I. C3a stimulation of neutrophils is secondary to eosinophil activation. J Exp Med 1995;181:2119–2127.
  • Hartmann K, Henz BM, Kruger-Krasagakes S, Kohl J, Burger R, Guhl S, Haase I, Lippert U, Zuberbier T. C3a and C5a stimulate chemotaxis of human mast cells. Blood 1997;89:2863–2870.
  • Hack CE, Nuijens JH, Felt-Bersma RJ, Schreuder WO, Eerenberg-Belmer AJ, Paardekooper J, Bronsveld W, Thijs LG. Elevated plasma levels of the anaphylatoxins C3a and C4a are associated with a fatal outcome in sepsis. Am J Med 1989;86:20–26.
  • Nakae H, Endo S, Inada K, Yoshida M. Chronological changes in the complement system in sepsis. Surg Today 1996;26:225–229.
  • Czermak BJ, Sarma V, Pierson CL, Warner RL, Huber-Lang M, Bless NM, Schmal H, Friedl HP, Ward PA. Protective effects of C5a blockade in sepsis. Nat Med 1999;5:788–792.
  • Ward PA. The dark side of C5a in sepsis. Nat Rev Immunol 2004;4:133–142.
  • Humbles AA, Lu B, Nilsson CA, Lilly C, Israel E, Fujiwara Y, Gerard NP, Gerard C. A role for the C3a anaphylatoxin receptor in the effector phase of asthma. Nature 2000;406:998–1001.
  • Nakano Y, Morita S, Kawamoto A, Suda T, Chida K, Nakamura H. Elevated complement C3a in plasma from patients with severe acute asthma. J Allergy Clin Immunol 2003;112:525–530.
  • Moxley G, Ruddy S. Elevated plasma C3 anaphylatoxin levels in rheumatoid arthritis patients. Arthritis Rheum 1987;30:1097–1104.
  • Robbins RA, Russ WD, Rasmussen JK, Clayton MM. Activation of the complement system in the adult respiratory distress syndrome. Am Rev Respir Dis 1987;135:651–658.
  • Riedemann NC, Ward PA. Complement in ischemia reperfusion injury. Am J Pathol 2003;162:363–367.
  • Arumugam TV, Shiels IA, Woodruff TM, Granger DN, Taylor SM. The role of the complement system in ischemia-reperfusion injury. Shock 2004;21:401–409.
  • Hopkins P, Belmont HM, Buyon J, Philips M, Weissmann G, Abramson SB. Increased levels of plasma anaphylatoxins in systemic lupus erythematosus predict flares of the disease and may elicit vascular injury in lupus cerebritis. Arthritis Rheum 1988;31:632–641.
  • Girardi G, Berman J, Redecha P, Spruce L, Thurman JM, Kraus D, Hollmann TJ, Casali P, Caroll MC, Wetsel RA, et al. Complement C5a receptors and neutrophils mediate fetal injury in the antiphospholipid syndrome. J Clin Invest 2003;112:1644–1654.
  • Holers VM, Girardi G, Mo L, Guthridge JM, Molina H, Pierangeli SS, Espinola R, Xiaowei LE, Mao D, Vialpando CG, et al. Complement C3 activation is required for antiphospholipid antibody-induced fetal loss. J Exp Med 2002;195:211–220.
  • Salmon JE, Girardi G, Holers VM. Complement activation as a mediator of antiphospholipid antibody induced pregnancy loss and thrombosis. Ann Rheum Dis 2002;61Suppl. 2ii46–ii50.
  • Xu C, Mao D, Holers VM, Palanca B, Cheng AM, Molina H. A critical role for murine complement regulator crry in fetomaternal tolerance. Science 2000;287:498–501.
  • Stoll BJ, Hansen NI, Adams-Chapman I, Fanaroff AA, Hintz SR, Vohr B, Higgins RD. Neurodevelopmental and growth impairment among extremely low-birth-weight infants with neonatal infection. JAMA 2004;292:2357–2365.
  • Minkoff H. Prematurity: infection as an etiologic factor. Obstet Gynecol 1983;62:137–144.
  • Romero R, Mazor M. Infection and preterm labor. Clin Obstet Gynecol 1988;31:553–584.
  • Romero R, Mazor M, Wu YK, Sirtori M, Oyarzun E, Mitchell MD, Hobbins JC. Infection in the pathogenesis of preterm labor. Semin Perinatol 1988;12:262–279.
  • McGregor JA, French JI, Lawellin D, Todd JK. Preterm birth and infection: pathogenic possibilities. Am J Reprod Immunol Microbiol 1988;16:123–132.
  • Romero R, Sirtori M, Oyarzun E, Avila C, Mazor M, Callahan R, Sabo V, Athanassiadis AP, Hobbins JC. Infection and labor. V. Prevalence, microbiology, and clinical significance of intraamniotic infection in women with preterm labor and intact membranes. Am J Obstet Gynecol 1989;161:817–824.
  • Goldenberg RL, Culhane JF. Infection as a cause of preterm birth. Clin Perinatol 2003;30:677–700.
  • Boggess KA. Pathophysiology of preterm birth: emerging concepts of maternal infection. Clin Perinatol 2005;32:561–569.
  • Romero R, Espinoza J, Kusanovic J, Gotsch F, Hassan S, Erez O, Chaiworapongsa T, Mazor M. The preterm parturition syndrome. BJOG 2006;113Suppl. 317–42.
  • Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel L, Hassan S. The role of inflammation and infection in preterm birth. Semin Reprod Med 2007;25:21–39.
  • Soto E, Romero R, Richani K, Espinoza J, Nien JK, Chaiworapongsa T, Santolaya-Forgas J, Edwin SS, Mazor M. Anaphylatoxins in preterm and term labor. J Perinat Med 2005;33:306–313.
  • Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996;87:163–168.
  • Soto E, Richani K, Romero R, Espinoza J, Chaiworapongsa T, Nien JK, Edwin S, Kim YM, Hong JS, Goncalves L, et al. Increased concentration of the complement split product C5a in acute pyelonephritis during pregnancy. J Matern Fetal Neonatal Med 2005;17:247–252.
  • Takafuji S, Tadokoro K, Ito K, Dahinden CA. Degranulation from human eosinophils stimulated with C3a and C5a. Int Arch Allergy Immunol 1994;104Suppl. 127–29.
  • Jagels MA, Daffern PJ, Hugli TE. C3a and C5a enhance granulocyte adhesion to endothelial and epithelial cell monolayers: epithelial and endothelial priming is required for C3a-induced eosinophil adhesion. Immunopharmacology 2000;46:209–222.
  • Elsner J, Oppermann M, Czech W, Kapp A. C3a activates the respiratory burst in human polymorphonuclear neutrophilic leukocytes via pertussis toxin-sensitive G-proteins. Blood 1994;83:3324–3331.
  • Elsner J, Oppermann M, Czech W, Dobos G, Schopf E, Norgauer J, Kapp A. C3a activates reactive oxygen radical species production and intracellular calcium transients in human eosinophils. Eur J Immunol 1994;24:518–522.
  • Takabayashi T, Vannier E, Burke JF, Tompkins RG, Gelfand JA, Clark BD. Both C3a and C3a(desArg) regulate interleukin-6 synthesis in human peripheral blood mononuclear cells. J Infect Dis 1998;177:1622–1628.
  • Takabayashi T, Vannier E, Clark BD, Margolis NH, Dinarello CA, Burke JF, Gelfand JA. A new biologic role for C3a and C3a desArg: regulation of TNF-α and IL-1 β synthesis. J Immunol 1996;156:3455–3460.
  • Tsuruta T, Yamamoto T, Matsubara S, Nagasawa S, Tanase S, Tanaka J, Takagi K, Kambara T. Novel function of C4a anaphylatoxin. Release from monocytes of protein which inhibits monocyte chemotaxis. Am J Pathol 1993;142:1848–1857.
  • Haeger M, Unander M, Norder-Hansson B, Tylman M, Bengtsson A. Complement, neutrophil, and macrophage activation in women with severe preeclampsia and the syndrome of hemolysis, elevated liver enzymes, and low platelet count. Obstet Gynecol 1992;79:19–26.
  • Wymann MP, Kernen P, Deranleau DA, Baggiolini M. Respiratory burst oscillations in human neutrophils and their correlation with fluctuations in apparent cell shape. J Biol Chem 1989;264:15829–15834.
  • Goldstein IM, Roos D, Kaplan HB, Weissmann G. Complement and immunoglobulins stimulate superoxide production by human leukocytes independently of phagocytosis. J Clin Invest 1975;56:1155–1163.
  • Ehrengruber MU, Geiser T, Deranleau DA. Activation of human neutrophils by C3a and C5A. Comparison of the effects on shape changes, chemotaxis, secretion, and respiratory burst. FEBS Lett 1994;346:181–184.
  • Perianayagam MC, Balakrishnan VS, King AJ, Pereira BJ, Jaber BL. C5a delays apoptosis of human neutrophils by a phosphatidylinositol 3-kinase-signaling pathway. Kidney Int 2002;61:456–463.
  • Okusawa S, Dinarello CA, Yancey KB, Endres S, Lawley TJ, Frank MM, Burke JF, Gelfand JA. C5a induction of human interleukin 1. Synergistic effect with endotoxin or interferon-gamma. J Immunol 1987;139:2635–2640.
  • Okusawa S, Yancey KB, van der Meer JW, Endres S, Lonnemann G, Hefter K, Frank MM, Burke JF, Dinarello CA, Gelfand JA. C5a stimulates secretion of tumor necrosis factor from human mononuclear cells in vitro. Comparison with secretion of interleukin 1 β and interleukin 1 α. J Exp Med 1988;168:443–448.
  • Schindler R, Gelfand JA, Dinarello CA. Recombinant C5a stimulates transcription rather than translation of interleukin-1 (IL-1) and tumor necrosis factor: translational signal provided by lipopolysaccharide or IL-1 itself. Blood 1990;76:1631–1638.
  • Riedemann NC, Guo RF, Hollmann TJ, Gao H, Neff TA, Reuben JS, Speyer CL, Sarma JV, Wetsel RA, Zetoune FS, et al. Regulatory role of C5a in LPS-induced IL-6 production by neutrophils during sepsis. FASEB J 2004;18:370–372.
  • Scholz W, McClurg MR, Cardenas GJ, Smith M, Noonan DJ, Hugli TE, Morgan EL. C5a-mediated release of interleukin 6 by human monocytes. Clin Immunol Immunopathol 1990;57:297–307.
  • Albrecht EA, Chinnaiyan AM, Varambally S, Kumar-Sinha C, Barrette TR, Sarma JV, Ward PA. C5a-induced gene expression in human umbilical vein endothelial cells. Am J Pathol 2004;164:849–859.
  • Ember JA, Sanderson SD, Hugli TE, Morgan EL. Induction of interleukin-8 synthesis from monocytes by human C5a anaphylatoxin. Am J Pathol 1994;144:393–403.
  • Fireman P, Zuchowski DA, Taylor PM. Development of human complement system. J Immunol 1969;103:25–31.
  • Ballow M, Fang F, Good RA, Day NK. Developmental aspects of complement components in the newborn. The presence of complement components and C3 proactivator (properdin factor B) in human colostrum. Clin Exp Immunol 1974;18:257–266.
  • Miyano A, Nakayama M, Fujita T, Kitajima H, Imai S, Shimizu A. Complement activation in fetuses: assessment by the levels of complement components and split products in cord blood. Diagn Clin Immunol 1987;5:86–90.
  • Stabile I, Nicolaides KH, Bach A, Teisner B, Rodeck C, Westergaard JG, Grudzinskas JG. Complement factors in fetal and maternal blood and amniotic fluid during the second trimester of normal pregnancy. Br J Obstet Gynaecol 1988;95:281–285.
  • Zilow G, Zilow EP, Burger R, Linderkamp O. Complement activation in newborn infants with early onset infection. Pediatr Res 1993;34:199–203.
  • Enskog A, Bengtsson A, Bengtson JP, Heideman M, Andreasson S, Larsson L. Complement anaphylatoxin C3a and C5a formation in premature children with respiratory distress. Eur J Pediatr 1996;155:41–45.
  • Sonntag J, Brandenburg U, Polzehl D, Strauss E, Vogel M, Dudenhausen JW, Obladen M. Complement system in healthy term newborns: reference values in umbilical cord blood. Pediatr Dev Pathol 1998;1:131–135.
  • Kohler PF. Maturation of the human complement system. I. Onset time and sites of fetal C1q, C4, C3, and C5 synthesis. J Clin Invest 1973;52:671–677.
  • Goldberg M, Luknar-Gabor N, Keidar R, Katz Y. Synthesis of complement proteins in the human chorion is differentially regulated by cytokines. Mol Immunol 2007;44:1737–1742.
  • Holmes CH, Simpson KL. Complement and pregnancy: new insights into the immunobiology of the fetomaternal relationship. Baillieres Clin Obstet Gynaecol 1992;6:439–460.
  • Vanderpuye OA, Labarrere CA, McIntyre JA. Expression of CD59, a human complement system regulatory protein, in extraembryonic membranes. Int Arch Allergy Immunol 1993;101:376–384.
  • Richani K, Soto E, Romero R, Han Y, Pineles B, Kim YM, Cushenberry E, Yoon BH, Kusanovic J, Kim CJ. Decreased mRNA expression of complement regulatory proteins in chorioamnionitis. Am J Obstet Gynecol 2006;195Suppl.S71
  • Sharma A, Prabhakar P, Sharma DP, Jayasinghe RG. Immunoglobulin and C3 levels in normal human amniotic fluid. West Indian Med J 1983;32:140–146.
  • Elimian A, Figueroa R, Canterino J, Verma U, Aguero-Rosenfeld M, Tejani N. Amniotic fluid complement C3 as a marker of intra-amniotic infection. Obstet Gynecol 1998;92:72–76.
  • Huffaker J, Witkin SS, Cutler L, Druzin ML, Ledger WJ. Total complement activity in maternal sera, amniotic fluids and cord sera in women with premature labor, premature rupture of membranes or chorioamnionitis. Surg Gynecol Obstet 1989;168:397–401.
  • Haeger M, Bengtson A, Karlsson K, Heideman M. Complement activation and anaphylatoxin (C3a and C5a) formation in preeclampsia and by amniotic fluid. Obstet Gynecol 1989;73:551–556.
  • Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD. Cytokines, prostaglandins and parturition – a review. Placenta 2003;24Suppl. AS33–S46.
  • Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel LA, Nien JK. Inflammation in preterm and term labour and delivery. Semin Fetal Neonatal Med 2006;11:317–326.
  • Siegel I, Gleicher N. Peripheral white blood cell alterations in early labor. Diagn Gynecol Obstet 1981;3:123–126.
  • Romero R, Brody DT, Oyarzun E, Mazor M, Wu YK, Hobbins JC, Durum SK. Infection and labor. III. Interleukin-1: a signal for the onset of parturition. Am J Obstet Gynecol 1989;160:1117–1123.
  • Hebisch G, Neumaier-Wagner PM, Huch R, von Mandach U. Maternal serum interleukin-1 β, -6 and -8 levels and potential determinants in pregnancy and peripartum. J Perinat Med 2004;32:475–480.
  • Buonocore G, De Filippo M, Gioia D, Picciolini E, Luzzi E, Bocci V, Bracci R. Maternal and neonatal plasma cytokine levels in relation to mode of delivery. Biol Neonate 1995;68:104–110.
  • Haddad R, Tromp G, Kuivaniemi H, Chaiworapongsa T, Kim YM, Mazor M, Romero R. Human spontaneous labor without histologic chorioamnionitis is characterized by an acute inflammation gene expression signature. Am J Obstet Gynecol 2006;195:394–324.
  • Romero R, Quintero R, Nores J, Avila C, Mazor M, Hanaoka S, Hagay Z, Merchant L, Hobbins JC. Amniotic fluid white blood cell count: a rapid and simple test to diagnose microbial invasion of the amniotic cavity and predict preterm delivery. Am J Obstet Gynecol 1991;165:821–830.
  • Romero R, Jimenez C, Lohda AK, Nores J, Hanaoka S, Avila C, Callahan R, Mazor M, Hobbins JC, Diamond MP. Amniotic fluid glucose concentration: a rapid and simple method for the detection of intraamniotic infection in preterm labor. Am J Obstet Gynecol 1990;163:968–974.
  • Romero R, Emamian M, Quintero R, Wan M, Hobbins JC, Mazor M, Edberg S. The value and limitations of the Gram stain examination in the diagnosis of intraamniotic infection. Am J Obstet Gynecol 1988;159:114–119.
  • Bobitt JR, Ledger WJ. Amniotic fluid analysis. Its role in maternal neonatal infection. Obstet Gynecol 1978;51:56–62.
  • Ahmed AE, Peter JB. Clinical utility of complement assessment. Clin Diagn Lab Immunol 1995;2:509–517.
  • Lynch AM, Gibbs RS, Murphy JR, Byers T, Neville MC, Giclas PC, Salmon JE, Van Hecke TM, Holers VM. Complement activation fragment Bb in early pregnancy and spontaneous preterm birth. Am J Obstet Gynecol 2008;199:354–358.
  • Vaisbuch E, Romero R, Erez O, Mazaki-Tovi S, Kusanovic JP, Soto E, Gotsch F, Dong Z, Chaiworapongsa T, Kim SW, et al. Fragment Bb in amniotic fluid: evidence for complement activation by the alternative pathway in women with intra-amniotic infection/inflammation. J Matern Fetal Neonatal Med in press

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