Advertisement

Reproductive Sciences

, Volume 20, Issue 2, pp 140–153 | Cite as

Extracellular Matrix Dynamics and Fetal Membrane Rupture

  • Jerome F. StraussIIIEmail author
Review

Abstract

The extracellular matrix (ECM) plays an important role in determining cell and organ function: (1) it is an organizing substrate that provides tissue tensile strength; (2) it anchors cells and influences cell morphology and function via interaction with cell surface receptors; and (3) it is a reservoir for growth factors. Alterations in the content and the composition of the ECM determine its physical and biological properties, including strength and susceptibility to degradation. The ECM components themselves also harbor cryptic matrikines, which when exposed by conformational change or proteolysis have potent effects on cell function, including stimulating the production of cytokines and matrix metalloproteinases (MMPs). Collectively, these properties of the ECM reflect a dynamic tissue component that influences both tissue form and function. This review illustrates how defects in ECM synthesis and metabolism and the physiological process of ECM turnover contribute to changes in the fetal membranes that precede normal parturition and contribute to the pathological events leading to preterm premature rupture of membranes (PPROM).

Keywords

extracellular matrix PPROM matrix metalloproteinase collagens fibronectin amnion chorion 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci. 2010;123(Pt 24):4195–4200.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Egeblad M, Rasch MG, Weaver VM. Dynamic interplay between the collagen scaffold and tumor evolution. Curr Opin Cell Biol. 2010;22(5):697–706.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Hadler-Olsen E, Fadnes B, Sylte I, Uhlin-Hansen L, Winberg JO. Regulation of matrix metalloproteinase activity in health and disease. FaEBS J. 2011;278(1):28–45.CrossRefGoogle Scholar
  4. 4.
    Whitley GS, Cartwright JE. Cellular and molecular regulation of spiral artery remodelling: lessons from the cardiovascular field. Placenta. 2010;31(6):465–474.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Parry S, Strauss JF 3rd. Premature rupture of the fetal membranes. N Engl J Med. 1998;338(10):663–670.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Timmons B, Akins M, Mahendroo M. Cervical remodeling during pregnancy and parturition. Trends Endocrinol Metab. 2010;21(6):353–361.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Park JS, Park CW, Lockwood CJ, Norwitz ER. Role of cytokines in preterm labor and birth. Minerva Ginecol. 2005;57(4):349–366.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Cockle JV, Gopichandran N, Walker JJ, Levene MI, Orsi NM. Matrix metalloproteinases and their tissue inhibitors in preterm perinatal complications. Reprod Sci. 2007;14(7):629–645.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Klipple GL, Riordan KK. Rare inflammatory and hereditary connective tissue diseases. Rheum Dis Clin North Am. 1989;15(2):383–398.PubMedPubMedCentralGoogle Scholar
  10. 10.
    Abramowitch SD, Feola A, Jallah Z, Moalli PA. Tissue mechanics, animal models, and pelvic organ prolapse: a review. Eur J Obstet Gynecol Reprod Biol. 2009;144(suppl 1):S146–S158.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Sozen I, Arici A. Interactions of cytokines, growth factors, and the extracellular matrix in the cellular biology of uterine leiomyomata. Fertil Steril. 2002;78(1):1–12.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Pitsos M, Kanakas N. The role of matrix metalloproteinases in the pathogenesis of endometriosis. Reprod Sci. 2009;16(8):717–726.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Helleman J, Jansen MP, Burger C, van der Burg ME, Berns EM. Integrated genomics of chemotherapy resistant ovarian cancer: a role for extracellular matrix, TGFbeta and regulating microRNAs. Int J Biochem Cell Biol. 2010;42(1):25–30.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Hynes RO. The extracellular matrix: not just pretty fibrils. Science. 2009;326(5957):1216–1219.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Aszódi A, Legate KR, Nakchbandi I, Fässler R. What mouse mutants teach us about extracellular matrix function. Annu Rev Cell Dev Biol. 2006;22:591–621.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Clark IM, Swingler TE, Sampieri CL, Edwards DR. The regulation of matrix metalloproteinases and their inhibitors. Int J Biochem Cell Biol. 2008;40(6–7):1362–1378.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Ricard-Blum S, Ballut L. Matricryptins derived from collagens and proteoglycans. Front Biosci. 2011;16:674–97.CrossRefGoogle Scholar
  18. 18.
    Gordon MK, Hahn RA. Collagens. Cell Tissue Res. 2010;339(1):247–257.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Shoulders MD, Raines RT. Collagen structure and stability. Annu Rev Biochem. 2009;78:929–958.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Han S, Makareeva E, Kuznetsova NV, et al. Molecular mechanism of type I collagen homotrimer resistance to mammalian collagenases. J Biol Chem. 2010;285(29):22276–22281.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Arikat S, Novince RW, Mercer BM, et al. Separation of amnion from choriodecidua is an integral event to the rupture of normal term fetal membranes and constitutes a significant component of the work required. Am J Obstet Gynecol. 2006;194(1):211–217.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Oyen ML, Calvin SE, Landers DV. Premature rupture of the fetal membranes: is the amnion the major determinant? Am J Obstet Gynecol. 2006;195(2):510–515.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Joyce EM, Moore JJ, Sacks MS. Biomechanics of the fetal membrane prior to mechanical failure: review and implications. Eur J Obstet Gynecol Reprod Biol. 2009;144(suppl 1):S121–S127.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Helmig R, Oxlund H, Petersen LK, Uldbjerg N. Different biomechanical properties of human fetal membranes obtained before and after delivery. Eur J Obstet Gynecol Reprod Biol. 1993;48(3):183–189.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Jabareen M, Mallik AS, Bilic G, Zisch AH, Mazza E. Relation between mechanical properties and microstructure of human fetal membranes: an attempt towards a quantitative analysis. Eur J Obstet Gynecol Reprod Biol. 2009;144(suppl 1):S134–S141.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Pressman EK, Cavanaugh JL, Woods JR. Physical properties of the chorioamnion throughout gestation. Am J Obstet Gynecol. 2002;187(3):672–675.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Moore RM, Mansour JM, Redline RW, Mercer BM, Moore JJ. The physiology of fetal membrane rupture: insight gained from the determination of physical properties. Placenta. 2006;27(11-12):1037–1051.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Ockleford C, Malak T, Hubbard A, et al. Confocal and conventional immunofluorescence and ultrastructural localisation of intracellular strength-giving components of human amniochorion. J Anat. 1993;183(pt 3):483–505.PubMedPubMedCentralGoogle Scholar
  29. 29.
    Malak TM, Ockleford CD, Bell SC, Dalgleish R, Bright N, Macvicar J. Confocal immunofluorescence localization of collagen types I, III, IV, V and VI and their ultrastructural organization in term human fetal membranes. Placenta. 1993;14(4):385–406.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Moore RM, Redline RW, Kumar D, et al. Differential expression of fibulin family proteins in the para-cervical weak zone and other areas of human fetal membranes. Placenta. 2009;30(4):335–341.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Casey ML, MacDonald PC. Lysyl oxidase (ras recision gene) expression in human amnion: ontogeny and cellular localization. J Clin Endocrinol Metab. 1997;82(1):167–172.PubMedPubMedCentralGoogle Scholar
  32. 32.
    Casey ML, MacDonald PC. Interstitial collagen synthesis and processing in human amnion: a property of the mesenchymal cells. Biol Reprod. 1996;55(6):1253–1260.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Kalamajski S, Oldberg A. The role of small leucine-rich proteoglycans in collagen fibrillogenesis. Matrix Biol. 2010; 29(4):248–253.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Meinert M, Malmstrom A, Tufvesson E, et al. Labour induces increased concentrations of biglycan and hyaluronan in human fetal membranes. Placenta. 2007;28(5–6):482–486.PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Dev Biol 2001;17:463–465.Google Scholar
  36. 36.
    Hampson V, Liu D, Billett E, Kirk S. Amniotic membrane collagen content and type distribution in women with preterm premature rupture of the membranes in pregnancy. Br J Obstet Gynaecol. 1997;104(9):1087–1091.PubMedCrossRefPubMedCentralGoogle Scholar
  37. 37.
    Meirowitz NB, Smulian JC, Hahn RA, et al. Collagen messenger RNA expression in the human amniochorion in premature rupture of membranes. Am J Obstet Gynecol. 2002;187(6):1679–1685.PubMedCrossRefPubMedCentralGoogle Scholar
  38. 38.
    Frigo P, Lang C, Sator M, Ulrich R, Husslein P. Membrane thickness and PROM—high-frequency ultrasound measurements. Prenat Diagn. 1998;18(4):333–337.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Calmus ML, Macksoud EE, Tucker R, Iozzo RV, Lechner BE. A mouse model of spontaneous preterm birth based on the genetic ablation of biglycan and decorin. Reproduction. 2011;142(1):183–194.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Strohl A, Kumar D, Novince R, et al. Decreased adherence and spontaneous separation of fetal membrane layers—amnion and choriodecidua—a possible part of the normal weakening process. Placenta. 2010;31(1):18–24.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Pandey V, Jaremko K, Moore RM, et al. The force required to rupture fetal membranes paradoxically increases with acute in vitro repeated stretching. Am J Obstet Gynecol. 2007;196(2):165.e1–e7.CrossRefGoogle Scholar
  42. 42.
    Malak TM, Bell SC. Structural characteristics of term human fetal membranes: a novel zone of extreme morphological alteration within the rupture site. Br J Obstet Gynaecol. 1994;101(5):375–386.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    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(1):237–241.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    El Khwad M, Stetzer B, Moore RM, et al. Term human fetal membranes have a weak zone overlying the lower uterine pole and cervix before onset of labor. Biol Reprod. 2005;72(3):720–726.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    El Khwad M, Pandey V, Stetzer B, et al. Fetal membranes from term vaginal deliveries have a zone of weakness exhibiting characteristics of apoptosis and remodeling. J Soc Gynecol Investig. 2006;13(3):191–195.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    McParland PC, Taylor DJ, Bell SC. Mapping of zones of altered morphology and chorionic connective tissue cellular phenotype in human fetal membranes (amniochorion and decidua) overlying the lower uterine pole and cervix before labor at term. Am J Obstet Gynecol. 2003;189(5):1481–1488.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Lappas M, Odumetse TL, Riley C, et al. Pre-labour fetal membranes overlying the cervix display alterations in inflammation and NF-kappaB signalling pathways. Placenta. 2008;29(12):995–1002.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Lappas M, Riley C, Rice GE, Permezel M. Increased expression of ac-FoxO1 protein in prelabor fetal membranes overlying the cervix: possible role in human fetal membrane rupture. Reprod Sci. 2009;16(7):635–641.PubMedCrossRefPubMedCentralGoogle Scholar
  49. 49.
    Lappas M, Lim R, Riley C, Menon R, Permezel M. Expression and localisation of FoxO3 and FoxO4 in human placenta and fetal membranes. Placenta. 2010;31(12):1043–1050.PubMedCrossRefPubMedCentralGoogle Scholar
  50. 50.
    Connon CJ, Nakamura T, Hopkinson A, et al. The biomechanics of amnion rupture: an X-ray diffraction study. PLoS One. 2007;2(11):e1147.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Shen ZY, Li EM, Lu SQ, et al. Autophagic and apoptotic cell death in amniotic epithelial cells. Placenta. 2008;29(11):956–961.PubMedCrossRefPubMedCentralGoogle Scholar
  52. 52.
    George RB, Kalich J, Yonish B, Murtha AP. Apoptosis in the chorion of fetal membranes in preterm premature rupture of membranes. Am J Perinatol. 2008;25(1):29–32.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Reti NG, Lappas M, Riley C, et al. Why do membranes rupture at term? Evidence of increased cellular apoptosis in the supracervical fetal membranes. Am J Obstet Gynecol. 2007;196(5):484.e1–e10.CrossRefGoogle Scholar
  54. 54.
    McLaren J, Taylor DJ, Bell SC. Increased incidence of apoptosis in non-labour-affected cytotrophoblast cells in term fetal membranes overlying the cervix. Hum Reprod. 1999;14(11):2895–2900.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Kumagai K, Otsuki Y, Ito Y, Shibata MA, Abe H, Ueki M. Apoptosis in the normal human amnion at term, independent of Bcl-2 regulation and onset of labour. Mol Hum Reprod. 2001;7(7):681–689.PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Sağol S, Sağol O, Ozkal S, Asena U. Role of apoptosis, bcl-2 and bax protein expression in premature rupture of fetal membranes. J Reprod Med. 2002;47(10):809–815.PubMedPubMedCentralGoogle Scholar
  57. 57.
    Kataoka S, Furuta I, Yamada H, et al. Increased apoptosis of human fetal membranes in rupture of the membranes and chorioamnionitis. Placenta. 2002;23(2–3):224–231.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    McLaren J, Taylor DJ, Bell SC. Increased concentration of pro-matrix metalloproteinase 9 in term fetal membranes overlying the cervix before labor: implications for membrane remodeling and rupture. Am J Obstet Gynecol. 2000;182(2):409–416.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Arechavaleta-Velasco F, Mayon-Gonzalez J, Gonzalez-Jimenez M, Hernandez-Guerrero C, Vadillo-Ortega F. Association of type II apoptosis and 92-kDa type IV collagenase expression in human amniochorion in prematurely ruptured membranes with tumor necrosis factor receptor-1 expression. J Soc Gynecol Investig. 2002;9(2):60–67.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Fortunato SJ, Menon R, Bryant C, Lombardi SJ. Programmed cell death (apoptosis) as a possible pathway to metalloproteinase activation and fetal membrane degradation in premature rupture of membranes. Am J Obstet Gynecol. 2000;182(6):1468–1476.PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Athayde N, Edwin SS, Romero R, et al. A role for matrix metalloproteinase-9 in spontaneous rupture of the fetal membranes. Am J Obstet Gynecol. 1998;179(5):1248–1253.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Lei H, Furth EE, Kalluri R, et al. A program of cell death and extracellular matrix degradation is activated in the amnion before the onset of labor. J Clin Invest. 1996;98(9):1971–1978.PubMedPubMedCentralCrossRefGoogle Scholar
  63. 63.
    Lei H, Kalluri R, Furth EE, Baker AH, Strauss JF 3rd. Rat amnion type IV collagen composition and metabolism: implications for membrane breakdown. Biol Reprod. 1999;60(1):176–182.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Luo G, Abrahams VM, Tadesse S, et al. Progesterone inhibits basal and TNF-alpha-induced apoptosis in fetal membranes: a novel mechanism to explain progesterone-mediated prevention of preterm birth. Reprod Sci. 2010;17(6):532–539.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Anum EA, Hill LD, Pandya A, Strauss JF 3rd. Connective tissue and related disorders and preterm birth: clues to genes contributing to prematurity. Placenta. 2009;30(3):207–215.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Romero R, Friel LA, Velez Edwards DR, et al. A genetic association study of maternal and fetal candidate genes that predispose to preterm prelabor rupture of membranes (PROM). Am J Obstet Gynecol. 2010;203(4):361.e1–361.e30.CrossRefGoogle Scholar
  67. 67.
    Hermanns-Lê T, Piérard G, Quatresooz P. Ehlers-Danlos-like dermal abnormalities in women with recurrent preterm premature rupture of fetal membranes. Am J Dermatopathol. 2005;27(5):407–410.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Ishida Y, Kubota H, Yamamoto A, Kitamura A, Bächinger HP, Nagata K. Type I collagen in Hsp47-null cells is aggregated in endoplasmic reticulum and deficient in N-propeptide processing and fibrillogenesis. Mol Biol Cell. 2006;17(5):2346–2355.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Nagai N, Hosokawa M, Itohara S, et al. Embryonic lethality of molecular chaperone hsp47 knockout mice is associated with defects in collagen biosynthesis. J Cell Biol. 2000;150(6):1499–1506.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Christiansen HE, Schwarze U, Pyott SM, et al. Homozygosity for a missense mutation in SERPINH1, which encodes the collagen chaperone protein HSP47, results in severe recessive osteogenesis imperfecta. Am J Hum Genet. 2010;86(3):389–398.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Wang H, Parry S, Macones G, et al. A functional SNP in the promoter of the SERPINH1 gene increases risk of preterm premature rupture of membranes in African American. Proc Natl Acad Sci U S A. 2006;103(36):13463–13467. Erratum in: Proc Natl Acad Sci U S A. 2006;103(50):19212.CrossRefGoogle Scholar
  72. 72.
    Wang H, Sammel MD, Tromp G, et al. 12 bp Wang SERPINH1A 12-bp deletion in the 5’-flanking region of the SERPINH1 gene affects promoter activity and protects against preterm premature rupture of membranes in African Americans. Hum Mutat. 2008;29(2):332.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Vadillo-Ortega F, González-Avila G, Furth EE, et al. 92-kd type IV collagenase (matrix metalloproteinase-9) activity in human amniochorion increases with labor. Am J Pathol. 1995;146(1):148–156.PubMedPubMedCentralGoogle Scholar
  74. 74.
    Nishihara S, Someya A, Yonemoto H, et al. Evaluation of the expression and enzyme activity of matrix metalloproteinase-7 in fetal membranes during premature rupture of membranes at term in humans. Reprod Sci. 2008;15(2):156–165.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Yonemoto H, Young CB, Ross JT, Guilbert LL, Fairclough RJ, Olson DM. Changes in matrix metalloproteinase (MMP)-2 and MMP-9 in the fetal amnion and chorion during gestation and at term and preterm labor. Placenta. 2006;27(6–7):669–677.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Ota A, Yonemoto H, Someya A, Itoh S, Kinoshita K, Nagaoka I. Changes in matrix metalloproteinase 2 activities in amniochorions during premature rupture of membranes. J Soc Gynecol Investig. 2006;13(8):592–597.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Xu P, Alfaidy N, Challis JR. Expression of matrix metalloproteinase (MMP)-2 and MMP-9 in human placenta and fetal membranes in relation to preterm and term labor. J Clin Endocrinol Metab. 2002;87(3):1353–1361.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Tromp G, Kuivaniemi H, Romero R, et al. 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(4):1331–1338.PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Li W, Alfaidy N, Challis JR. Expression of extracellular matrix metalloproteinase inducer in human placenta and fetal membranes at term labor. J Clin Endocrinol Metab. 2004;89(6):2897–2904.PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Fortunato SJ, Menon R. Screening of novel matrix metalloproteinases (MMPs) in human fetal membranes. J Assist Reprod Genet. 2002;19(10):483–486.PubMedPubMedCentralCrossRefGoogle Scholar
  81. 81.
    Fortunato SJ, Menon R, Lombardi SJ. Presence of four tissue inhibitors of matrix metalloproteinases (TIMP-1, -2, -3 and -4) in human fetal membranes. Am J Reprod Immunol. 1998;40(6):395–400.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Fujimoto T, Parry S, Urbanek M, et al. A single nucleotide polymorphism in the matrix metalloproteinase-1 (MMP-1) promoter influences amnion cell MMP-1 expression and risk for preterm premature rupture of the fetal membranes. J Biol Chem. 2002;277(8):6296–6302.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Wang Wang H, Parry S, Macones G, et al. Functionally significant SNP MMP8 promoter haplotypes and preterm premature rupture of membranes (PPROM). Hum Mol Genet. 2004;13(21):2659–2669.CrossRefGoogle Scholar
  84. 84.
    Ferrand PE, Parry S, Sammel M, et al. A polymorphism in the matrix metalloproteinase-9 promoter is associated with increased risk of preterm premature rupture of membranes in African Americans. Mol Hum Reprod. 2002;8(5):494–501.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Michaelis SA, Okuducu AF, Sarioglu NM, von Deimling A, Dudenhausen JW. The transcription factor Ets-1 is expressed in human amniochorionic membranes and is up-regulated in term and preterm premature rupture of membranes. J Perinat Med. 2005;33(4):314–319.PubMedCrossRefPubMedCentralGoogle Scholar
  86. 86.
    York TP, Strauss JF 3rd, Neale MC, Eaves LJ. Racial differences in genetic and environmental risk to preterm birth. PLoS One. 2010;5(8):e12391.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Siega-Riz AM, Promislow JH, Savitz DA, et al. Vitamin C intake and the risk of preterm delivery. Am J Obstet Gynecol. 2003;189(2):519–525.PubMedCrossRefPubMedCentralGoogle Scholar
  88. 88.
    Casanueva E, Ripoll C, Tolentino M, et al. Vitamin C supplementation to prevent premature rupture of the chorioamniotic membranes: a randomized trial. Am J Clin Nutr. 2005;81(4):859–863.PubMedCrossRefPubMedCentralGoogle Scholar
  89. 89.
    Stuart EL, Evans GS, Lin YS, Powers HJ. Reduced collagen and ascorbic acid concentrations and increased proteolytic susceptibility with prelabor fetal membrane rupture in women. Biol Reprod. 2005;72(1):230–235.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Erichsen HC, Engel SA, Eck PK, et al. Genetic variation in the sodium-dependent vitamin C transporters, SLC23A1, and SLC23A2 and risk for preterm delivery. Am J Epidemiol. 2006;163(3):245–254.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Spinnato JA 2nd, Freire S, Pinto e Silva JL, et al. Antioxidant supplementation and premature rupture of the membranes: a planned secondary analysis. Am J Obstet Gynecol. 2008;199(4):433.e1–e8.CrossRefGoogle Scholar
  92. 92.
    Mercer BM, Abdelrahim A, Moore RM, et al. The impact of vitamin C supplementation in pregnancy and in vitro upon fetal membrane strength and remodeling. Reprod Sci. 2010;17(7):685–695.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Moore RM, Novak JB, Kumar D, Mansour JM, Mercer BM, Moore JJ. Alpha-lipoic acid inhibits tumor necrosis factor-induced remodeling and weakening of human fetal membranes. Biol Reprod. 2009;80(4):781–787.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Moore RM, Schatz F, Kumar D, et al. Alpha-lipoic acid inhibits thrombin-induced fetal membrane weakening in vitro. Placenta. 2010;31(10):886–892.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Savitz DA, Dole N, Terry JW Jr, Zhou H, Thorp JM Jr. Smoking and pregnancy outcome among African-American and white women in central North Carolina. Epidemiology. 2001;12(6):636–642.PubMedCrossRefPubMedCentralGoogle Scholar
  96. 96.
    Menon R, Fortunato SJ, Yu J, et al. Cigarette smoke induces oxidative stress and apoptosis in normal term fetal membranes. Placenta. 2011;32(4):317–322.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Jones HE, Harris KA, Azizia M, et al. Differing prevalence and diversity of bacterial species in fetal membranes from very preterm and term labor. PLoS One. 2009;4(12):e8205.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Gomez-Lopez N, Laresgoiti-Servitje E, Olson DM, Estrada-Gutiérrez G, Vadillo-Ortega F. The role of chemokines in term and premature rupture of the fetal membranes: a review. Biol Reprod. 2010;82(5):809–814.PubMedCrossRefPubMedCentralGoogle Scholar
  99. 99.
    Kim YM, Romero R, Chaiworapongsa T, 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(4):1346–1355.PubMedCrossRefPubMedCentralGoogle Scholar
  100. 100.
    McGregor JA, Lawellin D, Franco-Buff A, Todd JK, Makowski EL. Protease production by microorganisms associated with reproductive tract infection. Am J Obstet Gynecol. 1986;154(1):109–114.PubMedCrossRefPubMedCentralGoogle Scholar
  101. 101.
    Wang H, Ogawa M, Wood JR, et al. Genetic and epigenetic mechanisms combine to control MMP1 expression and its association with preterm premature rupture of membranes. Hum Mol Genet. 2008;17(8):1087–1096.PubMedCrossRefPubMedCentralGoogle Scholar
  102. 102.
    Montenegro D, Romero R, Pineles BL, et al. Differential expression of microRNAs with progression of gestation and inflammation in the human chorioamniotic membranes. Am J Obstet Gynecol. 2007;197(3):289.e1–e6.CrossRefGoogle Scholar
  103. 103.
    White ES, Muro AF. Fibronectin splice variants: understanding their multiple roles in health and disease using engineered mouse models. IUBMB Life. 2011;63(7):538–546.PubMedCrossRefPubMedCentralGoogle Scholar
  104. 104.
    McFadden JP, Basketter DA, Dearman RJ, Kimber IR. Extra domain A-positive fibronectin-positive feedback loops and their association with cutaneous inflammatory disease. Clin Dermatol. 2011;29(3):257–265.PubMedCrossRefPubMedCentralGoogle Scholar
  105. 105.
    Conde-Agudelo A, Romero R. Cervicovaginal fetal fibronectin for the prediction of spontaneous preterm birth in multiple pregnancies: a systematic review and meta-analysis. J Matern Fetal Neonatal Med. 2010;23(12):1365–1376.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Okamura Y, Watari M, Jerud ES, et al. The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem. 2001;276(13):10229–10233.PubMedCrossRefPubMedCentralGoogle Scholar
  107. 107.
    Gondokaryono SP, Ushio H, Niyonsaba F, et al. The extra domain A of fibronectin stimulates murine mast cells via tolllike receptor 4. J Leukoc Biol. 2007;82(3):657–665.PubMedCrossRefPubMedCentralGoogle Scholar
  108. 108.
    Lefebvre JS, Lévesque T, Picard S, et al. Extra domain a of fibronectin primes leukotriene biosynthesis and stimulates neutrophil migration through activation of Toll-like receptor 4. Arthritis Rheum. 2011;63(6):1527–1533.PubMedCrossRefPubMedCentralGoogle Scholar
  109. 109.
    Muro AF, Moretti FA, Moore BB, et al. An essential role for fibronectin extra type III domain A in pulmonary fibrosis. Am J Respir Crit Care Med. 2008;177(6):638–645.PubMedCrossRefPubMedCentralGoogle Scholar
  110. 110.
    Jiang D, Liang J, Noble PW. Hyaluronan in tissue injury and repair. Annu Rev Cell Dev Biol. 2007;23:435–461.PubMedCrossRefPubMedCentralGoogle Scholar
  111. 111.
    Taylor KR, Trowbridge JM, Rudisill JA, Termeer CC, Simon JC, Gallo RL. Hyaluronan fragments stimulate endothelial recognition of injury through TLR4. J Biol Chem. 2004;279(17):17079–17084.PubMedCrossRefPubMedCentralGoogle Scholar
  112. 112.
    Jiang D, Liang J, Fan J, et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med. 2005;11(11):1173–1179.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Society for Reproductive Investigation 2013

Authors and Affiliations

  1. 1.Department of Obstetrics & GynecologyVirginia Commonwealth UniversityRichmondUSA

Personalised recommendations