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Original Article

Mitochondrial manganese superoxide dismutase mRNA expression in human chorioamniotic membranes and its association with labor, inflammation, and infection

, , , , , , , , & show all
Pages 1000-1013 | Received 28 Feb 2009, Accepted 05 May 2009, Published online: 17 Mar 2010

References

  • 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, Mazor M. Infection and preterm labor. Clin Obstet Gynecol 1988;31:553–584.
  • Romero R, Mazor M, Munoz H, Gomez R, Galasso M, Sherer DM. The preterm labor syndrome. Ann N Y Acad Sci 1994;734:414–429.
  • McLaren J, Malak TM, Bell SC. Structural characteristics of term human fetal membranes prior to labour: identification of an area of altered morphology overlying the cervix. Hum Reprod 1999;14:237–241.
  • Marvin KW, Keelan JA, Eykholt RL, Sato TA, Mitchell MD. Use of cDNA arrays to generate differential expression profiles for inflammatory genes in human gestational membranes delivered at term and preterm. Mol Hum Reprod 2002;8:399–408.
  • Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD. Cytokines, prostaglandins and parturition – a review. Placenta 2003;24Suppl AS33–S46.
  • Haddad R, Gould BR, Romero R, Tromp G, Farookhi R, Edwin SS, Kim MR, Zingg HH. Uterine transcriptomes of bacteria-induced and ovariectomy-induced preterm labor in mice are characterized by differential expression of arachidonate metabolism genes. Am J Obstet Gynecol 2006;195:822–828.
  • 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;195:394–424.
  • Tromp G, Kuivaniemi H, Romero R, Chaiworapongsa T, Kim YM, Kim MR, Maymon E, Edwin S. Genome-wide expression profiling of fetal membranes reveals a deficient expression of proteinase inhibitor 3 in premature rupture of membranes. Am J Obstet Gynecol 2004;191:1331–1338.
  • Weisiger RA, Fridovich I. Mitochondrial superoxide simutase. Site of synthesis and intramitochondrial localization. J Biol Chem 1973;248:4793–4796.
  • Whittaker JW. The irony of manganese superoxide dismutase. Biochem Soc Trans 2003;31:1318–1321.
  • Landis GN, Tower J. Superoxide dismutase evolution and life span regulation. Mech Ageing Dev 2005;126:365–379.
  • Culotta VC, Yang M, O'Halloran TV. Activation of superoxide dismutases: putting the metal to the pedal. Biochim Biophys Acta 2006;1763:747–758.
  • Mittal CK, Murad F. Activation of guanylate cyclase by superoxide dismutase and hydroxyl radical: a physiological regulator of guanosine 3′,5′-monophosphate formation. Proc Natl Acad Sci USA 1977;74:4360–4364.
  • Decoursey TE, Ligeti E. Regulation and termination of NADPH oxidase activity. Cell Mol Life Sci 2005;62:2173–2193.
  • Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007;39:44–84.
  • Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956;11:298–300.
  • Miquel J, Economos AC, Fleming J, Johnson J E Jr.. Mitochondrial role in cell aging. Exp Gerontol 1980;15:575–591.
  • Shigenaga MK, Hagen TM, Ames BN. Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci USA 1994;91:10771–10778.
  • Lyall F, Gibson JL, Greer IA, Brockman DE, Eis AL, Myatt L. Increased nitrotyrosine in the diabetic placenta: evidence for oxidative stress. Diabetes Care 1998;21:1753–1758.
  • Myatt L, Kossenjans W, Sahay R, Eis A, Brockman D. Oxidative stress causes vascular dysfunction in the placenta. J Matern Fetal Med 2000;9:79–82.
  • Graham CH, Postovit LM, Park H, Canning MT, Fitzpatrick TE. Adriana and Luisa Castellucci award lecture 1999: role of oxygen in the regulation of trophoblast gene expression and invasion. Placenta 2000;21:443–450.
  • Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 2000;29:222–230.
  • Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, Burton GJ. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 2000;157:2111–2122.
  • Burton GJ, Caniggia I. Hypoxia: implications for implantation to delivery-a workshop report. Placenta 2001;22Suppl AS63–S65.
  • Poston L, Chappell LC. Is oxidative stress involved in the aetiology of pre-eclampsia?. Acta Paediatr Suppl 2001;90:3–5.
  • Myatt L. Role of placenta in preeclampsia. Endocrine 2002;19:103–111.
  • Vina J, Sastre J, Pallardo F, Borras C. Mitochondrial theory of aging: importance to explain why females live longer than males. Antioxid Redox Signal 2003;5:549–556.
  • Burton GJ, Hempstock J, Jauniaux E. Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod Biomed Online 2003;6:84–96.
  • Burton GJ, Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig 2004;11:342–352.
  • Myatt L, Cui X. Oxidative stress in the placenta. Histochem Cell Biol 2004;122:369–382.
  • Balaban RS, Nemoto S, Finkel T. Mitochondria, oxidants, and aging. Cell 2005;120:483–495.
  • Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2005;3:28
  • Vanderlelie J, Venardos K, Clifton VL, Gude NM, Clarke FM, Perkins AV. Increased biological oxidation and reduced anti-oxidant enzyme activity in pre-eclamptic placentae. Placenta 2005;26:53–58.
  • Webster RP, Brockman D, Myatt L. Nitration of p38 MAPK in the placenta: association of nitration with reduced catalytic activity of p38 MAPK in pre-eclampsia. Mol Hum Reprod 2006;12:677–685.
  • Webster RP, Macha S, Brockman D, Myatt L. Peroxynitrite treatment in vitro disables catalytic activity of recombinant p38 MAPK. Proteomics 2006;6:4838–4844.
  • Burton GJ, Charnock-Jones DS, Jauniaux E. Working with oxygen and oxidative stress in vitro. Methods Mol Med 2006;122:413–425.
  • Jauniaux E, Poston L, Burton GJ. Placental-related diseases of pregnancy: involvement of oxidative stress and implications in human evolution. Hum Reprod Update 2006;12:747–755.
  • Sugino N, Takiguchi S, Umekawa T, Heazell A, Caniggia I. Oxidative stress and pregnancy outcome: a workshop report. Placenta 2007;28Suppl AS48–S50.
  • Ornoy A. Embryonic oxidative stress as a mechanism of teratogenesis with special emphasis on diabetic embryopathy. Reprod Toxicol 2007;24:31–41.
  • Gupta S, Agarwal A, Banerjee J, Alvarez JG. The role of oxidative stress in spontaneous abortion and recurrent pregnancy loss: a systematic review. Obstet Gynecol Surv 2007;62:335–347.
  • Webster RP, Roberts VH, Myatt L. Protein nitration in placenta – functional significance. Placenta 2008;29:985–994.
  • Vina J, Sastre J, Pallardo FV, Gambini J, Borras C. Modulation of longevity-associated genes by estrogens or phytoestrogens. Biol Chem 2008;389:273–277.
  • Shadel GS. Expression and maintenance of mitochondrial DNA: new insights into human disease pathology. Am J Pathol 2008;172:1445–1456.
  • Sugino N, Karube-Harada A, Taketani T, Sakata A, Nakamura Y. Withdrawal of ovarian steroids stimulates prostaglandin F2alpha production through nuclear factor-kappaB activation via oxygen radicals in human endometrial stromal cells: potential relevance to menstruation. J Reprod Dev 2004;50:215–225.
  • Belt AR, Baldassare JJ, Molnar M, Romero R, Hertelendy F. The nuclear transcription factor NF-κB mediates interleukin-1beta-induced expression of cyclooxygenase-2 in human myometrial cells. Am J Obstet Gynecol 1999;181:359–366.
  • Sacks T, Moldow CF, Craddock PR, Bowers TK, Jacob HS. Endothelial damage provoked by toxic oxygen radicals released from complement-triggered granulocytes. Prog Clin Biol Res 1978;21:719–726.
  • Wong GH, Goeddel DV. Induction of manganous superoxide dismutase by tumor necrosis factor: possible protective mechanism. Science 1988;242:941–944.
  • Okada T, Matsuzaki N, Sawai K, Nobunaga T, Shimoya K, Suzuki K, Taniguchi N, Saji F, Murata Y. Chorioamnionitis reduces placental endocrine functions: the role of bacterial lipopolysaccharide and superoxide anion. J Endocrinol 1997;155:401–410.
  • Sugino N, Telleria CM, Gibori G. Differential regulation of copper-zinc superoxide dismutase and manganese superoxide dismutase in the rat corpus luteum: induction of manganese superoxide dismutase messenger ribonucleic acid by inflammatory cytokines. Biol Reprod 1998;59:208–215.
  • Manna SK, Zhang HJ, Yan T, Oberley LW, Aggarwal BB. Overexpression of manganese superoxide dismutase suppresses tumor necrosis factor-induced apoptosis and activation of nuclear transcription factor-kappaB and activated protein-1. J Biol Chem 1998;273:13245–13254.
  • Oberley LW. Mechanism of the tumor suppressive effect of MnSOD overexpression. Biomed Pharmacother 2005;59:143–148.
  • Strehlow K, Rotter S, Wassmann S, Adam O, Grohe C, Laufs K, Bohm M, Nickenig G. Modulation of antioxidant enzyme expression and function by estrogen. Circ Res 2003;93:170–177.
  • Alexander GR, Himes JH, Kaufman RB, Mor J, Kogan M. A United States national reference for fetal growth. Obstet Gynecol 1996;87:163–168.
  • Chaiworapongsa T, Espinoza J, Yoshimatsu J, Kim YM, Bujold E, Edwin S, Yoon BH, Romero R. Activation of coagulation system in preterm labor and preterm premature rupture of membranes. J Matern Fetal Neonatal Med 2002;11:368–373.
  • Redline RW, Heller D, Keating S, Kingdom J. Placental diagnostic criteria and clinical correlation – a workshop report. Placenta 2005;26Suppl AS114–S117.
  • Pacora P, Chaiworapongsa T, Maymon E, Kim YM, Gomez R, Yoon BH, Ghezzi F, Berry SM, Qureshi F, Jacques SM, et al. Funisitis and chorionic vasculitis: the histological counterpart of the fetal inflammatory response syndrome. J Matern Fetal Neonatal Med 2002;11:18–25.
  • Redline RW. Inflammatory responses in the placenta and umbilical cord. Semin Fetal Neonatal Med 2006;11:296–301.
  • Maniatis T, Fritsch EF, Sambrook J. Molecular cloning: a laboratory manualCold Spring Harbor, NY: Cold Spring Harbor Laboratory; 1982.
  • R Development Core Team. R: a language and environment for statistical computingVienna, Austria: R Foundation for Statistical Computing; 2007.
  • Winer J, Jung CK, Shackel I, Williams PM. Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 1999;270:41–49.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001;25:402–408.
  • Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001;125:279–284.
  • Gerschman R, Gilbert DL, Nye SW, Dwyer P, Fenn WO. Oxygen poisoning and x-irradiation: a mechanism in common. Science 1954;119:623–626.
  • Moll SJ, Jones CJ, Crocker IP, Baker PN, Heazell AE. Epidermal growth factor rescues trophoblast apoptosis induced by reactive oxygen species. Apoptosis 2007;12:1611–1622.
  • Heazell AE, Moll SJ, Jones CJ, Baker PN, Crocker IP. Formation of syncytial knots is increased by hyperoxia, hypoxia and reactive oxygen species. Placenta 2007;28Suppl AS33–S40.
  • Heazell AE, Taylor NN, Greenwood SL, Baker PN, Crocker IP. Does altered oxygenation or reactive oxygen species alter cell turnover of BeWo choriocarcinoma cells?. Reprod Biomed Online 2009;18:111–119.
  • Sohal RS, Svensson I, Brunk UT. Hydrogen peroxide production by liver mitochondria in different species. Mech Ageing Dev 1990;53:209–215.
  • Ku HH, Brunk UT, Sohal RS. Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radic Biol Med 1993;15:621–627.
  • Longo VD, Gralla EB, Valentine JS. Superoxide dismutase activity is essential for stationary phase survival in Saccharomyces cerevisiae. Mitochondrial production of toxic oxygen species in vivo. J Biol Chem 1996;271:12275–12280.
  • Barja G, Herrero A. Oxidative damage to mitochondrial DNA is inversely related to maximum life span in the heart and brain of mammals. FASEB J 2000;14:312–318.
  • Fabrizio P, Liou LL, Moy VN, Diaspro A, Valentine JS, Gralla EB, Longo VD. SOD2 functions downstream of Sch9 to extend longevity in yeast. Genetics 2003;163:35–46.
  • McCord JM, Fridovich I. Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein). J Biol Chem 1969;244:6049–6055.
  • Keele B B Jr., McCord JM, Fridovich I. Superoxide dismutase from Escherichia coli B. A new manganese-containing enzyme. J Biol Chem 1970;245:6176–6181.
  • Li Y, Huang TT, Carlson EJ, Melov S, Ursell PC, Olson JL, Noble LJ, Yoshimura MP, Berger C, Chan PH, et al. Dilated cardiomyopathy and neonatal lethality in mutant mice lacking manganese superoxide dismutase. Nat Genet 1995;11:376–381.
  • Lebovitz RM, Zhang H, Vogel H, Cartwright J Jr., Dionne L, Lu N, Huang S, Matzuk MM. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci USA 1996;93:9782–9787.
  • Melov S, Coskun P, Patel M, Tuinstra R, Cottrell B, Jun AS, Zastawny TH, Dizdaroglu M, Goodman SI, Huang TT, et al. Mitochondrial disease in superoxide dismutase 2 mutant mice. Proc Natl Acad Sci USA 1999;96:846–851.
  • Macmillan-Crow LA, Cruthirds DL. Invited review: manganese superoxide dismutase in disease. Free Radic Res 2001;34:325–336.
  • Kirby K, Hu J, Hilliker AJ, Phillips JP. RNA interference-mediated silencing of Sod2 in Drosophila leads to early adult-onset mortality and elevated endogenous oxidative stress. Proc Natl Acad Sci USA 2002;99:16162–16167.
  • Duttaroy A, Paul A, Kundu M, Belton A. A Sod2 null mutation confers severely reduced adult life span in Drosophila. Genetics 2003;165:2295–2299.
  • Sen CK, Packer L. Antioxidant and redox regulation of gene transcription. FASEB J 1996;10:709–720.
  • Muller JM, Rupec RA, Baeuerle PA. Study of gene regulation by NF-kappa B and AP-1 in response to reactive oxygen intermediates. Methods 1997;11:301–312.
  • Suzuki YJ, Forman HJ, Sevanian A. Oxidants as stimulators of signal transduction. Free Radic Biol Med 1997;22:269–285.
  • Dong W, Simeonova PP, Gallucci R, Matheson J, Fannin R, Montuschi P, Flood L, Luster MI. Cytokine expression in hepatocytes: role of oxidant stress. J Interferon Cytokine Res 1998;18:629–638.
  • Fan J, Marshall JC, Jimenez M, Shek PN, Zagorski J, Rotstein OD. Hemorrhagic shock primes for increased expression of cytokine-induced neutrophil chemoattractant in the lung: role in pulmonary inflammation following lipopolysaccharide. J Immunol 1998;161:440–447.
  • Sen CK. Redox signaling and the emerging therapeutic potential of thiol antioxidants. Biochem Pharmacol 1998;55:1747–1758.
  • Ryan KA, Smith M F Jr., Sanders MK, Ernst PB. Reactive oxygen and nitrogen species differentially regulate Toll-like receptor 4-mediated activation of NF-kappa B and interleukin-8 expression. Infect Immun 2004;72:2123–2130.
  • Matsuzawa A, Saegusa K, Noguchi T, Sadamitsu C, Nishitoh H, Nagai S, Koyasu S, Matsumoto K, Takeda K, Ichijo H. ROS-dependent activation of the TRAF6-ASK1-p38 pathway is selectively required for TLR4-mediated innate immunity. Nat Immunol 2005;6:587–592.
  • Tse HM, Milton MJ, Schreiner S, Profozich JL, Trucco M, Piganelli JD. Disruption of innate-mediated proinflammatory cytokine and reactive oxygen species third signal leads to antigen-specific hyporesponsiveness. J Immunol 2007;178:908–917.
  • Taylor DE, Ghio AJ, Piantadosi CA. Reactive oxygen species produced by liver mitochondria of rats in sepsis. Arch Biochem Biophys 1995;316:70–76.
  • Ho YS, Dey MS, Crapo JD. Antioxidant enzyme expression in rat lungs during hyperoxia. Am J Physiol 1996;270:L810–L818.
  • Sugino N, Nakata M, Kashida S, Karube A, Takiguchi S, Kato H. Decreased superoxide dismutase expression and increased concentrations of lipid peroxide and prostaglandin F(2alpha) in the decidua of failed pregnancy. Mol Hum Reprod 2000;6:642–647.
  • Rogers RJ, Monnier JM, Nick HS. Tumor necrosis factor-alpha selectively induces MnSOD expression via mitochondria-to-nucleus signaling, whereas interleukin-1beta utilizes an alternative pathway. J Biol Chem 2001;276:20419–20427.
  • Tsan MF, Clark RN, Goyert SM, White JE. Induction of TNF-alpha and MnSOD by endotoxin: role of membrane CD14 and Toll-like receptor-4. Am J Physiol Cell Physiol 2001;280:C1422–C1430.
  • St Clair DK, Porntadavity S, Xu Y, Kiningham K. Transcription regulation of human manganese superoxide dismutase gene. Methods Enzymol 2002;349:306–312.
  • Robinson CJ, Johnson DD, Chang EY, Armstrong DM, Wang W. Evaluation of placenta growth factor and soluble Fms-like tyrosine kinase 1 receptor levels in mild and severe preeclampsia. Am J Obstet Gynecol 2006;195:255–259.
  • Mattson MP, Meffert MK. Roles for NF-kappaB in nerve cell survival, plasticity, and disease. Cell Death Differ 2006;13:852–860.
  • Tse HM, Milton MJ, Piganelli JD. Mechanistic analysis of the immunomodulatory effects of a catalytic antioxidant on antigen-presenting cells: implication for their use in targeting oxidation-reduction reactions in innate immunity. Free Radic Biol Med 2004;36:233–247.
  • Tocco G, Illigens BM, Malfroy B, Benichou G. Prolongation of alloskin graft survival by catalytic scavengers of reactive oxygen species. Cell Immunol 2006;241:59–65.
  • Hirabayashi J, Kasai K. Effect of amino acid substitution by sited-directed mutagenesis on the carbohydrate recognition and stability of human 14-kDa beta-galactoside-binding lectin. J Biol Chem 1991;266:23648–23653.
  • Barcellos-Hoff MH, Dix TA. Redox-mediated activation of latent transforming growth factor-beta 1. Mol Endocrinol 1996;10:1077–1083.
  • Zhang JG, Matthews JM, Ward LD, Simpson RJ. Disruption of the disulfide bonds of recombinant murine interleukin-6 induces formation of a partially unfolded state. Biochemistry 1997;36:2380–2389.
  • Poljak A, Grant R, Austin CJ, Jamie JF, Willows RD, Takikawa O, Littlejohn TK, Truscott RJ, Walker MJ, Sachdev P, et al. Inhibition of indoleamine 2,3 dioxygenase activity by H2O2. Arch Biochem Biophys 2006;450:9–19.
  • Than NG, Romero R, Erez O, Weckle A, Tarca AL, Hotra J, Abbas A, Han YM, Kim SS, Kusanovic JP, et al. Emergence of hormonal and redox regulation of galectin-1 in placental mammals: implication in maternal-fetal immune tolerance. Proc Natl Acad Sci USA 2008;105:15819–15824.
  • Telfer JF, Thomson AJ, Cameron IT, Greer IA, Norman JE. Expression of superoxide dismutase and xanthine oxidase in myometrium, fetal membranes and placenta during normal human pregnancy and parturition. Hum Reprod 1997;12:2306–2312.
  • Myatt L, Eis AL, Brockman DE, Kossenjans W, Greer IA, Lyall F. Differential localization of superoxide dismutase isoforms in placental villous tissue of normotensive, pre-eclamptic, and intrauterine growth-restricted pregnancies. J Histochem Cytochem 1997;45:1433–1438.
  • Cindrova-Davies T, Yung HW, Johns J, Spasic-Boskovic O, Korolchuk S, Jauniaux E, Burton GJ, Charnock-Jones DS. Oxidative stress, gene expression, and protein changes induced in the human placenta during labor. Am J Pathol 2007;171:1168–1179.
  • Keelan JA, Marvin KW, Sato TA, Coleman M, McCowan LM, Mitchell MD. Cytokine abundance in placental tissues: evidence of inflammatory activation in gestational membranes with term and preterm parturition. Am J Obstet Gynecol 1999;181:1530–1536.
  • 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.
  • 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.
  • Romero R, Manogue KR, Mitchell MD, Wu YK, Oyarzun E, Hobbins JC, Cerami A. Infection and labor. IV. Cachectin-tumor necrosis factor in the amniotic fluid of women with intraamniotic infection and preterm labor. Am J Obstet Gynecol 1989;161:336–341.
  • Romero R, Avila C, Santhanam U, Sehgal PB. Amniotic fluid interleukin 6 in preterm labor. Association with infection. J Clin Invest 1990;85:1392–1400.
  • Romero R, Mazor M, Sepulveda W, Avila C, Copeland D, Williams J. Tumor necrosis factor in preterm and term labor. Am J Obstet Gynecol 1992;166:1576–1587.
  • Romero R, Mazor M, Brandt F, Sepulveda W, Avila C, Cotton DB, Dinarello CA. Interleukin-1 alpha and interleukin-1 beta in preterm and term human parturition. Am J Reprod Immunol 1992;27:117–123.
  • Romero R, Yoon BH, Kenney JS, Gomez R, Allison AC, Sehgal PB. Amniotic fluid interleukin-6 determinations are of diagnostic and prognostic value in preterm labor. Am J Reprod Immunol 1993;30:167–183.
  • Maymon E, Ghezzi F, Edwin SS, Mazor M, Yoon BH, Gomez R, Romero R. The tumor necrosis factor alpha and its soluble receptor profile in term and preterm parturition 158. Am J Obstet Gynecol 1999;181:1142–1148.
  • Athayde N, Romero R, Maymon E, Gomez R, Pacora P, Araneda H, Yoon BH. A role for the novel cytokine RANTES in pregnancy and parturition. Am J Obstet Gynecol 1999;181:989–994.
  • Esplin MS, Romero R, Chaiworapongsa T, Kim YM, Edwin S, Gomez R, Mazor M, Adashi EY. Monocyte chemotactic protein-1 is increased in the amniotic fluid of women who deliver preterm in the presence or absence of intra-amniotic infection. J Matern Fetal Neonatal Med 2005;17:365–373.
  • Athayde N, Romero R, Maymon E, Gomez R, Pacora P, Yoon BH, Edwin SS. Interleukin 16 in pregnancy, parturition, rupture of fetal membranes, and microbial invasion of the amniotic cavity. Am J Obstet Gynecol 2000;182:135–141.
  • Hamill N, Romero R, Gotsch F, Pedro KJ, Edwin S, Erez O, Than NG, Mittal P, Espinoza J, Friel LA, et al. Exodus-1 (CCL20): evidence for the participation of this chemokine in spontaneous labor at term, preterm labor, and intrauterine infection. J Perinat Med 2008;36:217–227.
  • 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.
  • Bryant-Greenwood GD, Millar LK. Human fetal membranes: their preterm premature rupture. Biol Reprod 2000;63:1575–1579.
  • Mercer BM. Preterm premature rupture of the membranes. Obstet Gynecol 2003;101:178–193.
  • Srinivas SK, Macones GA. Preterm premature rupture of the fetal membranes: current concepts. Minerva Ginecol 2005;57:389–396.
  • Santolaya-Forgas J, Romero R, Espinoza J, Erez O, Friel LA, Kusanovic JP, Bahado-Singh R, Nien JK. Prelabor rupture of the membranes In: Reece EA, Hobbins JC, editors. Clinical Obstetrics: The Fetus and Mother. 3rd ed.Blackwell Publishing; 2007. pp 1130–1188.
  • Romero R, Gomez R, Ghezzi F, Yoon BH, Mazor M, Edwin SS, Berry SM. A fetal systemic inflammatory response is followed by the spontaneous onset of preterm parturition. Am J Obstet Gynecol 1998;179:186–193.
  • Chaiworapongsa T, Romero R, Espinoza J, Kim YM, Edwin S, Bujold E, Gomez R, Kuivaniemi H. Macrophage migration inhibitory factor in patients with preterm parturition and microbial invasion of the amniotic cavity. J Matern Fetal Neonatal Med 2005;18:405–416.
  • 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.
  • Romero R, Ceska M, Avila C, Mazor M, Behnke E, Lindley I. Neutrophil attractant/activating peptide-1/interleukin-8 in term and preterm parturition. Am J Obstet Gynecol 1991;165:813–820.
  • Parry S, Strauss J F III. Premature rupture of the fetal membranes. N Engl J Med 1998;338:663–670.
  • Tashima LS, Millar LK, Bryant-Greenwood GD. Genes upregulated in human fetal membranes by infection or labor. Obstet Gynecol 1999;94:441–449.
  • Fortunato SJ, Menon R. Distinct molecular events suggest different pathways for preterm labor and premature rupture of membranes. Am J Obstet Gynecol 2001;184:1399–1405.
  • Kim YM, Romero R, Chaiworapongsa T, Kim GJ, Kim MR, Kuivaniemi H, Tromp G, Espinoza J, Bujold E, Abrahams VM, et al. Toll-like receptor-2 and -4 in the chorioamniotic membranes in spontaneous labor at term and in preterm parturition that are associated with chorioamnionitis. Am J Obstet Gynecol 2004;191:1346–1355.
  • Mazaki-Tovi S, Romero R, Kusanovic JP, Erez O, Pineles BL, Gotsch F, Mittal P, Than NG, Espinoza J, Hassan SS. Recurrent preterm birth. Semin Perinatol 2007;31:142–158.
  • Woods J R Jr.. Reactive oxygen species and preterm premature rupture of membranes-a review. Placenta 2001;22Suppl AS38–S44.
  • Romero R, Chaiworapongsa T, Espinoza J. Micronutrients and intrauterine infection, preterm birth and the fetal inflammatory response syndrome. J Nutr 2003;133:1668S–1673S.
  • Longini M, Perrone S, Vezzosi P, Marzocchi B, Kenanidis A, Centini G, Rosignoli L, Buonocore G. Association between oxidative stress in pregnancy and preterm premature rupture of membranes. Clin Biochem 2007;40:793–797.
  • Sugino N, Kashida S, Takiguchi S, Nakamura Y, Kato H. Induction of superoxide dismutase by decidualization in human endometrial stromal cells. Mol Hum Reprod 2000;6:178–184.
  • Sugino N. The role of oxygen radical-mediated signaling pathways in endometrial function. Placenta 2007;28Suppl AS133–S136.
  • McGregor JA, Leff M, Orleans M, Baron A. Fetal gender differences in preterm birth: findings in a North American cohort. Am J Perinatol 1992;9:43–48.
  • Di Renzo GC, Rosati A, Sarti RD, Cruciani L, Cutuli AM. Does fetal sex affect pregnancy outcome?. Gend Med 2007;4:19–30.
  • Clifton VL, Murphy VE. Maternal asthma as a model for examining fetal sex-specific effects on maternal physiology and placental mechanisms that regulate human fetal growth. Placenta 2004;25Suppl AS45–S52.
  • Clifton VL. Sexually dimorphic effects of maternal asthma during pregnancy on placental glucocorticoid metabolism and fetal growth. Cell Tissue Res 2005;322:63–71.
  • Clifton VL, Vanderlelie J, Perkins AV. Increased anti-oxidant enzyme activity and biological oxidation in placentae of pregnancies complicated by maternal asthma. Placenta 2005;26:773–779.
  • Murphy VE, Gibson P, Talbot PI, Clifton VL. Severe asthma exacerbations during pregnancy. Obstet Gynecol 2005;106:1046–1054.

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