Cited by 163Telomeres, Telomerase, and SenescencePreterm Birth and ChorioamnionitisReproductive System and Pregnancy

Chorioamniotic membrane senescence: a signal for parturition?

Open access
Behnia, Faranak, Taylor, Brandie D., Woodson, Michael, Kacerovsky, Marian, Hawkins, Hal, Fortunato, Stephen J., Saade, George R., Menon, Ramkumar·2015·American Journal of Obstetrics and Gynecology

Abstract

Objective Senescence is an important biological phenomenon involved in both physiologic and pathologic processes. We propose that chorioamniotic membrane senescence is a mechanism associated with human parturition. The present study was conducted to explore the association between senescence and normal term parturition by examining the morphologic and biochemical evidences in chorioamniotic membranes.Study design Chorioamniotic membranes were collected from normal term deliveries; group 1: term labor and group 2: term, not in labor. Senescence-related morphologic changes were determined by transmission electron microscopy and biochemical changes were studied by senescence-associated (SA) β-galactosidase staining. Amniotic fluid samples collected from both term labor and term not in labor were analyzed for 14 SA secretory phenotype (SASP) markers.Results Morphologic evidence of cellular senescence (enlarged cells and organelles) and a higher number of SA β-galactosidase-stained amnion and chorion cells were observed in chorioamniotic membranes obtained from women in labor at term, when compared to term not in labor. The concentration of proinflammatory SASP markers (granulocyte macrophage colony-stimulating factor, interleukin-6 and -8) was significantly higher in the amniotic fluid of women in labor at term than women not in labor. In contrast, SASP factors that protect against cell death (eotaxin-1, soluble Fas ligand, osteoprotegerin, and intercellular adhesion molecule-1) were significantly lower in the amniotic fluid samples from term labor.Conclusion Morphologic and biochemical features of senescence were more frequent in chorioamniotic membranes from women who experienced term labor. Senescence of chorioamniotic membranes were also associated with amniotic fluid SASP markers.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.ajog.2015.05.041

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

The citation lists haven’t been fetched yet

References 129 · Cited by 163

Research works printed but not linked: 93

  1. Romero R, Dey SK, Fisher SJ. Preterm labor: one syndrome, many causes. Science 2014; 345:760-5.
  2. Smith R. Alterations in the hypothalamic pituitary adrenal axis during pregnancy and the placental clock that determines the length of parturition. J Reprod Immunol 1998;39:215-20.
  3. Munoz-Espin D, Serrano M. Cellular senes- cence: from physiology to pathology. Nat Rev Mol Cell Biol 2014;15:482-96.
  4. Hayflick L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 1965;37:614-36.
  5. Hayflick L. Human cells and aging. Sci Am 1968;218:32-7.
  6. van der Zee EA. Synapses, spines and ki- nases in mammalian learning and memory, and the impact of aging. Neurosci Biobehav Rev 2015;50:77-85.
  7. Campisi J. Suppressing cancer: the impor- tance of being senescent. Science 2005;309: 886-7.
  8. Campisi J, Robert L. Cell senescence: role in aging and age-related diseases. Interdiscip Top Gerontol 2014;39:45-61.
  9. Gubbels Bupp MR. Sex, the aging immune system, and chronic disease. Cell Immunol 2015;294:102-10.
  10. Campisi J, Yaswen P. Aging and cancer cell biology, 2009. Aging Cell 2009;8:221-5.
  11. Rodier F, Munoz DP, Teachenor R, et al. DNA-SCARS: distinct nuclear structures that sustain damage-induced senescence growth arrest and inflammatory cytokine secretion. J Cell Sci 2011;124:68-81.
  12. Menon R, Boldogh I, Hawkins HK, et al. Histological evidence of oxidative stress and premature senescence in preterm prema- ture rupture of the human fetal membranes recapitulated in vitro. Am J Pathol 2014;184: 1740-51.
  13. Coppe JP, Desprez PY, Krtolica A, Campisi J. The senescence-associated secre- tory phenotype: the dark side of tumor sup- pression. Annu Rev Pathol 2010;5:99-118.
  14. Keelan JA, Coleman M, Mitchell MD. The molecular mechanisms of term and preterm la- bor: recent progress and clinical implications. Clin Obstet Gynecol 1997;40:460-78.
  15. Romero R, Brody DT, Oyarzun E, et al. Infection and labor, III, interleukin-1: a signal for the onset of parturition. Am J Obstet Gynecol 1989;160:1117-23.
  16. Romero R, Parvizi ST, Oyarzun E, et al. Amniotic fluid interleukin-1 in spontaneous labor at term. J Reprod Med 1990;35:235-8.
  17. Romero R, Mazor M, Brandt F, et al. Inter- leukin-1 alpha and interleukin-1 beta in preterm and term human parturition. Am J Reprod Immunol 1992;27:117-23.
  18. Romero R, Mazor M, Tartakovsky B. Sys- temic administration of interleukin-1 induces preterm parturition in mice. Am J Obstet Gyne- col 1991;165:969-71.
  19. Romero R, Avila C, Santhanam U, Sehgal PB. Amniotic fluid interleukin 6 in preterm labor: association with infection. J Clin Invest 1990;85:1392-400.
  20. Romero R, Manogue KR, Mitchell MD, et al. Infection and labor, IV, cachectin-tumor necrosis factor in the amniotic fluid of women with intra- amniotic infection and preterm labor. Am J Obstet Gynecol 1989;161:336-41.
  21. 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;166:1576-87.
  22. Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel LA, Nien JK. Inflammation in preterm and term labor and delivery. Semin Fetal Neonatal Med 2006;11:317-26.
  23. Maymon E, Romero R, Pacora P, et al. Ev- idence of in vivo differential bioavailability of the active forms of matrix metalloproteinases 9 and 2 in parturition, spontaneous rupture of mem- branes, and intra-amniotic infection. Am J Obstet Gynecol 2000;183:887-94.
  24. Maymon E, Romero R, Pacora P, et al. A role for the 72 kDa gelatinase (MMP-2) and its in- hibitor (TIMP-2) in human parturition, premature rupture of membranes and intraamniotic infec- tion. J Perinat Med 2001;29:308-16.
  25. Lonergan M, Aponso D, Marvin KW, et al. Tumor necrosis factor-related apoptosis- inducing ligand (TRAIL), TRAIL receptors, and the soluble receptor osteoprotegerin in human gestational membranes and amniotic fluid dur- ing pregnancy and labor at term and preterm. J Clin Endocrinol Metab 2003;88:3835-44.
  26. Romero R, Mazor M, Wu YK, Avila C, Oyarzun E, Mitchell MD. Bacterial endotoxin and tumor necrosis factor stimulate prostaglandin production by human decidua. Prostaglandins Leukot Essent Fatty Acids 1989;37:183-6.
  27. Romero R, Gotsch F, Pineles B, Kusanovic JP. Inflammation in pregnancy: its roles in reproductive physiology, obstetrical complications, and fetal injury. Nutr Rev 2007;65:S194-202.
  28. Edwin SS, Romero RJ, Munoz H, Branch DW, Mitchell MD. 5-Hydroxyeicosatetraenoic acid and human parturition. Prostaglandins 1996;51: 403-12.
  29. Mitchell MD, Romero RJ, Edwin SS, Trautman MS. Prostaglandins and parturition. Reprod Fertil Dev 1995;7:623-32.
  30. Molnar M, Romero R, Hertelendy F. Inter- leukin-1 and tumor necrosis factor stimulate arachidonic acid release and phospholipid metabolism in human myometrial cells. Am J Obstet Gynecol 1993;169:825-9.
  31. Mitchell MD, Edwin S, Romero RJ. Prosta- glandin biosynthesis by human decidual cells: effects of inflammatory mediators. Prostaglan- dins Leukot Essent Fatty Acids 1990;41:35-8.
  32. Romero R, Durum S, Dinarello CA, Oyarzun E, Hobbins JC, Mitchell MD. Inter- leukin-1 stimulates prostaglandin biosynthesis by human amnion. Prostaglandins 1989;37: 13-22.
  33. Sadowsky DW, Novy MJ, Witkin SS, Gravett MG. Dexamethasone or interleukin-10 blocks interleukin-1beta-induced uterine con- tractions in pregnant rhesus monkeys. Am J Obstet Gynecol 2003;188:252-63.
  34. Mitchell MD, Dudley DJ, Edwin SS, Schiller SL. Interleukin-6 stimulates prosta- glandin production by human amnion and decidual cells. Eur J Pharmacol 1991;192: 189-91.
  35. 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: 60-7.
  36. Fortunato SJ, Menon R, Lombardi SJ. MMP/TIMP imbalance in amniotic fluid during PROM: an indirect support for endogenous pathway to membrane rupture. J Perinat Med 1999;27:362-8.
  37. Fortunato SJ, LaFleur B, Menon R. Colla- genase-3 (MMP-13) in fetal membranes and amniotic fluid during pregnancy. Am J Reprod Immunol 2003;49:120-5.
  38. Vadillo-Ortega F, Gonzalez-Avila G, Furth EE, et al. 92-kd Type IV collagenase (matrix metalloproteinase-9) activity in human amnio- chorion increases with labor. Am J Pathol 1995;146:148-56.
  39. Unal ER, Cierny JT, Roedner C, Newman R, Goetzl L. Maternal inflammation in spontaneous term labor. Am J Obstet Gynecol 2011;204: 223-5.
  40. Cierny JT, Unal ER, Flood P, et al. Maternal inflammatory markers and term labor perfor- mance. Am J Obstet Gynecol 2014;210:447.e1-6.
  41. Menon R, Boldogh I, Urrabaz-Garza R, et al. Senescence of primary amniotic cells via oxida- tive DNA damage. PLoS One 2013;8:e83416.
  42. Menon R, Thorsen P, Vogel I, Jacobsson B, Williams SM, Fortunato SJ. Increased bioavail- ability of TNF-alpha in African Americans during in vitro infection: predisposing evidence for im- mune imbalance. Placenta 2007;28:946-50.
  43. Menon R, Williams SM, Fortunato SJ. Am- niotic fluid interleukin-1beta and interleukin-8 concentrations: racial disparity in preterm birth. Reprod Sci 2007;14:253-9.
  44. Menon R, Thorsen P, Vogel I, et al. Racial disparity in amniotic fluid concentrations of tu- mor necrosis factor (TNF)-alpha and soluble TNF receptors in spontaneous preterm birth. Am J Obstet Gynecol 2008;198:533.e1-10.
  45. Menon R, Velez DR, Morgan N, Lombardi SJ, Fortunato SJ, Williams SM. Genetic regulation of amniotic fluid TNF-alpha and soluble TNF receptor concentrations affected by race and preterm birth. Hum Genet 2008;124:243-53.
  46. Menon R, Fortunato SJ, Milne GL, et al. Amniotic fluid eicosanoids in preterm and term births: effects of risk factors for spontaneous preterm labor. Obstet Gynecol 2011;118: 121-34.
  47. Fortunato SJ, Menon R, Swan KF. Expres- sion of TNF-a and TNF-R p55 in cultured amniochorion. Am J Reprod Immunol 1994;32: 188-93.
  48. Fortunato SJ, Menon R, Lombardi SJ. Role of tumor necrosis factor-alpha in the premature rupture of membranes and preterm labor path- ways. Am J Obstet Gynecol 2002;187:1159-62.
  49. Hirota Y, Daikoku T, Tranguch S, Xie H, Bradshaw HB, Dey SK. Uterine-specific p53 deficiency confers premature uterine senes- cence and promotes preterm birth in mice. J Clin Invest 2010;120:803-15.
  50. Brou L, Almli L, Drobek C, et al. Dysregu- lated biomarkers induce distinct pathways in preterm birth. BJOG 2012;119:458-73.
  51. Greenland S. Avoiding power loss associ- ated with categorization and ordinal scores in Research Obstetrics ajog.org dose-response and trend analysis. Epidemi- ology 1995;6:450-4.
  52. Hastie T, Tibshirani R. Generalized additive models for medical research. Stat Methods Med Res 1995;4:187-96.
  53. Weng HY, Hsueh YH, Messam LL, Hertz- Picciotto I. Methods of covariate selection: directed acyclic graphs and the change-in- estimate procedure. Am J Epidemiol 2009; 169:1182-90.
  54. Bhat G, Williams SM, Saade GR, Menon R. Biomarker interactions are better predictors of spontaneous preterm birth. Reprod Sci 2014;21:340-50.
  55. Menon R, Yu J, Basasnta-Henry P, et al. Short fetal leukocyte telomere length and pre- term prelabor rupture of the membranes. PLoS One 2012;7:e31136.
  56. Kawamura K, Kitamura S, Sekida S, Tsuda M, Sunanaga T. Molecular anatomy of tunicate senescence: reversible function of mitochondrial and nuclear genes associated with budding cycles. Development 2012;139: 4083-93.
  57. Bendotti C, Calvaresi N, Chiveri L, et al. Early vacuolization and mitochondrial damage in mo- tor neurons of FALS mice are not associated with apoptosis or with changes in cytochrome oxidase histochemical reactivity. J Neurol Sci 2001;191:25-33.
  58. Anglade P, Vyas S, Javoy-Agid F, et al. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol Histo- pathol 1997;12:25-31.
  59. Vays VB, Vangeli IM, Bakeeva LE. Ultra- structural changes in ageing lacrimal gland in Wistar rats. Membrane and Cell Biology 2014;157:268-72.
  60. Bakeevaa LE, VBVI. Age-related alterations of mitochondria from muscle tissue. Biochem- istry (Moscow) Supplement Series 2014;8: 16-22.
  61. Toescu EC, Verkhratsky A. Neuronal aging from an intraneuronal perspective: roles of endoplasmic reticulum and mitochondria. Cell Calcium 2003;34:311-23.
  62. Dimri GP, Lee X, Basile G, et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci U S A 1995;92:9363-7.
  63. Itahana K, Campisi J, Dimri GP. Methods to detect biomarkers of cellular senescence: the senescence-associated beta-galactosidase assay. Methods Mol Biol 2007;371:21-31.
  64. Mesiano S, Chan EC, Fitter JT, Kwek K, Yeo G, Smith R. Progesterone withdrawal and estrogen activation in human parturition are co- ordinated by progesterone receptor A expres- sion in the myometrium. J Clin Endocrinol Metab 2002;87:2924-30.
  65. Gregory MS, Hackett CG, Abernathy EF, et al. Opposing roles for membrane bound and soluble Fas ligand in glaucoma-associated retinal ganglion cell death. PLoS One 2011;6: e17659.
  66. Suzuki A, Sugimura K, Ohtsuka K, et al. Fas/ Fas ligand expression and characteristics of primed CD45RO þ T cells in the inflamed mucosa of ulcerative colitis. Scand J Gastroenterol 2000;35:1278-83.
  67. Sood SK, Balasubramanian S, Higham S, Fernando M, Harrison B. Osteoprotegerin (OPG) and related proteins (RANK, RANKL and TRAIL) in thyroid disease. World J Surg 2011;35: 1984-92.
  68. Shin M, Matsuo K, Tada T, et al. The inhi- bition of RANKL/RANK signaling by osteopro- tegerin suppresses bone invasion by oral squamous cell carcinoma cells. Carcinogenesis 2011;32:1634-40.
  69. Krakauer T. Nuclear factor-kappaB: fine- tuning a central integrator of diverse biologic stimuli. Int Rev Immunol 2008;27:286-92.
  70. Gardiner EE, D'Souza SE. Sequences within fibrinogen and intercellular adhesion molecule-1 (ICAM-1) modulate signals required for mito- genesis. J Biol Chem 1999;274:11930-6.
  71. Pluskota E, D'Souza SE. Fibrinogen in- teractions with ICAM-1 (CD54) regulate endo- thelial cell survival. Eur J Biochem 2000;267: 4693-704.
  72. Dudley DJ. Immunoendocrinology of pre- term labor: the link between corticotropin- releasing hormone and inflammation. Am J Obstet Gynecol 1999;180:S251-6.
  73. Thomson AJ, Telfer JF, Young A, et al. Leukocytes infiltrate the myometrium during human parturition: further evidence that labor is an inflammatory process. Hum Reprod 1999;14:229-36.
  74. Gomez-Lopez N, Estrada-Gutierrez G, Jimenez-Zamudio L, Vega-Sanchez R, Vadillo- Ortega F. Fetal membranes exhibit selective leukocyte chemotaxic activity during human labor. J Reprod Immunol 2009;80:122-31.
  75. Bredeson S, Papaconstantinou J, Deford JH, et al. HMGB1 promotes a p38MAPK associated non-infectious inflammatory res- ponse pathway in human fetal membranes. PLoS One 2014;9:e113799.
  76. Romero R, Miranda J, Chaiworapongsa T, et al. Prevalence and clinical significance of sterile intra-amniotic inflammation in patients with preterm labor and intact membranes. Am J Reprod Immunol 2014;72:458-74.
  77. Cobo T, Kacerovsky M, Jacobsson B. Amniotic fluid infection, inflammation, and colo- nization in preterm labor with intact membranes. Am J Obstet Gynecol 2014;211:708.
  78. Hirsch E, Filipovich Y, Mahendroo M. Signaling via the type I IL-1 and TNF receptors is necessary for bacterially induced preterm labor in a murine model. Am J Obstet Gynecol 2006;194:1334-40.
  79. Maddipati KR, Romero R, Chaiworapongsa T, et al. Eicosanomic profiling reveals dominance of the epoxygenase pathway in human amniotic fluid at term in spontaneous labor. FASEB J 2014;28:4835-46.
  80. Weber E, Vatti R, Berti G. Morphological aspects in phase-contrast and transmission electron microscopy of senescent cultures of bovine aortic endothelial cells. Boll Soc Ital Biol Sper 1984;60:1643-9.
  81. Solhaug A, Torgersen ML, Holme JA, Lagadic-Gossmann D, Eriksen GS. Autophagy and senescence, stress responses induced by the DNA-damaging mycotoxin alternariol. Toxi- cology 2014;326:119-29.
  82. Sarsour EH, Goswami M, Kalen AL, Goswami PC. MnSOD activity protects mito- chondrial morphology of quiescent fibroblasts from age associated abnormalities. Mitochon- drion 2010;10:342-9.
  83. Bayreuther K, Rodemann HP, Hommel R, Dittmann K, Albiez M, Francz PI. Human skin fibroblasts in vitro differentiate along a terminal cell lineage. Proc Natl Acad Sci U S A 1988;85: 5112-6.
  84. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972;26:239-57.
  85. Saraste A, Pulkki K. Morphologic and biochemical hallmarks of apoptosis. Cardiovasc Res 2000;45:528-37.
  86. Hacker G. The morphology of apoptosis. Cell Tissue Res 2000;301:5-17.
  87. Toussaint O, Dumont P, Dierick JF, et al. Stress-induced premature senescence: essen- ce of life, evolution, stress, and aging. Ann N Y Acad Sci 2000;908:85-98.
  88. Brunk U, Ericsson JL, Ponten J, Westermark B. Residual bodies and "aging" in cultured human glia cells: effect of entrance into phase 3 and prolonged periods of confluence. Exp Cell Res 1973;79:1-14.
  89. Romero R, Gonzalez R, Baumann P, et al. Topographic differences in amniotic fluid con- centrations of prostanoids in women in sponta- neous labor at term. Prostaglandins Leukot Essent Fatty Acids 1994;50:97-104.
  90. Romero R, Ceska M, Avila C, Mazor M, Behnke E, Lindley I. Neutrophil attractant/acti- vating peptide-1/interleukin-8 in term and pre- term parturition. Am J Obstet Gynecol 1991;165:813-20. 100. Uszynski M, Uszynski W, Kielkowski A. Tissue plasminogen activator and plasminogen activator inhibitors of types 1 and 2 in amniotic fluid before labor and after childbirth. Gynecol Obstet Invest 1995;39:93-6. 101.
  91. Romero R, Wu YK, Oyarzun E, Hobbins JC, Mitchell MD. A potential role for ajog.org Obstetrics Research SEPTEMBER 2015 American Journal of Obstetrics & Gynecology 359.e15 epidermal growth factor/alpha-transforming growth factor in human parturition. Eur J Obstet Gynecol Reprod Biol 1989;33:55-60. 102. Cohen J, Ghezzi F, Romero R, et al. GRO alpha in the fetomaternal and amniotic fluid compartments during pregnancy and parturi- tion. Am J Reprod Immunol 1996;35:23-9. 103. Romero R, Gomez R, Galasso M, et al. Macrophage inflammatory protein-1 alpha in term and preterm parturition: effect of microbial invasion of the amniotic cavity. Am J Reprod Immunol 1994;32:108-13. 104. Olah KS, Vince GS, Neilson JP, Deniz G, Johnson PM. Interleukin-6, interferon-gamma, interleukin-8, and granulocyte-macrophage col- ony stimulating factor levels in human amniotic fluid at term. J Reprod Immunol 1996;32:89-98. 105. Tsatas D, Baker MS, Moses EK, Rice GE. Gene expression of plasminogen activation cascade components in human term gestational tissues with labor onset. Mol Hum Reprod 1998;4:101-6. 106. Athayde N, Romero R, Gomez R, et al. Matrix metalloproteinases-9 in preterm and term human parturition. J Matern Fetal Med 1999;8: 213-9. 107. Marinoni E, Di IR, Villaccio B, Alberini A, Rota F, Cosmi EV. Amniotic fluid nitric oxide metabolite levels and nitric oxide synthase localization in feto-placental tissues are modified in association with human labor. Eur J Obstet Gynecol Reprod Biol 2000;89:47-54. 108. Hirnle L, Gospodarek A, Katnik- Prastowska I. Concentration of the cellular fibronectin in amniotic fluid and plasma in the peripartum period [in Polish]. Ginekol Pol 2001;72:1149-53. 109. Calhoun DA, Chegini N, Polliotti BM, Gersting JA, Miller RK, Christensen RD. Granulocyte colony-stimulating factor in pre- term and term pregnancy, parturition, and intra-amniotic infection. Obstet Gynecol 2001;97:229-34. 110.
  92. Chaiworapongsa T, Romero R, Espinoza J, et al. Macrophage migration in- hibitory factor in patients with preterm parturi- tion and microbial invasion of the amniotic cavity. J Matern Fetal Neonatal Med 2005;18: 405-16. 111. Maymon E, Romero R, Pacora P, et al. Evidence for the participation of interstitial collagenase (matrix metal- loproteinase 1) in preterm premature rupture of membranes. Am J Obstet Gynecol 2000;183:914-20. 112. Park KH, Chaiworapongsa T, Kim YM, et al. Matrix metalloproteinase 3 in parturition, premature rupture of the membranes, and mi- crobial invasion of the amniotic cavity. J Perinat Med 2003;31:12-22. 113. Keelan JA, Yang J, Romero RJ, et al. Epithelial cell-derived neutrophil-activating peptide-78 is present in fetal membranes and amniotic fluid at increased concentrations with intra-amniotic infection and preterm delivery. Biol Reprod 2004;70:253-9. 114. Gomez Lopez NY, Estrada GG, Beltran MJ, Vadillo OF. Assessment of a microarray of solid-phase antibodies to the study of chemokines secreted by the cho- rioamniotic membrane [in Spanish]. Ginecol Obstet Mex 2006;74:666-70. 115. Hayashi M, Hombo Y, Shibazaki M, Nakajima A, Inaba N. Elevation of macrophage colony-stimulating factor in amniotic fluid at late stage of normal pregnancy. Am J Reprod Immunol 2006;55:226-31. 116. Hayashi M, Zhu K, Sagesaka T, Fukasawa I, Inaba N. Amniotic fluid levels of tu- mor necrosis factor-alpha and soluble tumor necrosis factor receptor 1 before and after the onset of labor in normal pregnancies. Horm Metab Res 2008;40:251-6. 117. Lee SE, Romero R, Park IS, Seong HS, Park CW, Yoon BH. Amniotic fluid prostaglandin concentrations increase before the onset of spontaneous labor at term. J Matern Fetal Neonatal Med 2008;21:89-94. 118.
  93. Hamill N, Romero R, Gotsch F, et al. Exodus-1 (CCL20): evidence for the participa- tion of this chemokine in spontaneous labor at term, preterm labor, and intrauterine infection. J Perinat Med 2008;36:217-27. 119. Kemp B, von RU, Brehme A, Rath W. Amniotic fluid adhesion molecules during parturition at term. J Perinat Med 2009;37: 28-31. 120. Vega-Sanchez R, de Jesus-Torres E, Arenas-Hernandez M, et al. Expression of cell adhesion molecules in the maternal fetal period of human gestation [in Spanish]. Ginecol Obstet Mex 2010;78:677-84.

Authors
Behnia, F., Taylor, B. D., Woodson, M., Kacerovsky, M., Hawkins, H., Fortunato, S. J., Saade, G. R., & Menon, R.
Affiliations
  • The University of Texas Medical Branch at Galveston (US)
  • Texas A&M Health Science Center (US)
Corresponding author
Menon, Ramkumar
Venue
American Journal of Obstetrics and Gynecology
Publisher
Elsevier BV
Published
2015-09
Volume
213
Issue
3
Pages
359.e1-359.e16
ISSN
0002-9378 (ISSN-L)
OpenAlex
W1894868021
Cited by
163
References
129
Citations by year
2026: 9 · 2025: 14 · 2024: 13 · 2023: 13 · 2022: 16 · 2021: 11 · 2020: 23 · 2019: 22 · 2018: 13 · 2017: 15 · 2016: 11 · 2015: 3
FWCI
10.32
Type
journal article
Language
en
Open access
Locations
  • American Journal of Obstetrics and Gynecology (publishedVersion)
  • PubMed (publishedVersion)
Topics
  • Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
  • Health Sciences › Medicine › Epidemiology › Preterm Birth and Chorioamnionitis
  • Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
Keywords
cellular senescence, fetal membranes, childbirth, term labor, senescence-associated β-galactosidase, senescence-associated secretory phenotype, amniotic fluid, chorion, amniotic membrane, inflammatory cytokines, interleukin-6, interleukin-8, GM-CSF, eotaxin, soluble Fas ligand, osteoprotegerin, ICAM-1
MeSH terms
Adult, Amnion, Amniotic Fluid, beta-Galactosidase, Chorion, Cross-Sectional Studies, Female, Humans, Labor, Obstetric, Mitochondria, Pregnancy, Interleukin-6, Case-Control Studies, Granulocyte-Macrophage Colony-Stimulating Factor, Interleukin-8, Cellular Senescence, Intercellular Adhesion Molecule-1, Term Birth, Fas Ligand Protein, Osteoprotegerin, Chemokine CCL11, Young Adult

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review