Abstract
A gradient of immunological mediators exists in the fetal membranes from the periplacental zone (PZ) to the rupture zone (RZ) at term delivery (rupture of fetal membranes [ROM]). However, it is unknown if this gradient is different in premature rupture of these tissues (premature rupture of fetal membranes [PROM]). We therefore analyzed leukocyte chemotactic activity and chemokine/cytokine production in fetal membrane zones in ROM and PROM. In ROM, leukocyte chemotactic activity increased from the PZ to the RZ; however, this did not occur in PROM. This was due to consistently elevated leukocyte chemotactic activity in PROM compared to ROM tissues. In the RZ, ROM was characterized by increased T-cell attraction and high levels of chemokine (C-X-C motif) ligand 8 (CXCL-8)/interleukin 8, and PROM by increased granulocyte attraction and high levels of granulocyte-macrophage colony-stimulating factor and CXCL-10/interferon gamma-induced protein 10. We conclude that normal and premature rupture of fetal membranes differ in regional chemotactic activity and related chemokine/cytokine production, which may represent evidence for differential mechanisms of rupture at term delivery.
Similar content being viewed by others
References
Alger LS, Pupkin MJ. Etiology of preterm premature rupture of the membranes. Clin Obstet Gynecol. 1986;29(4):758–770.
Parry S, Strauss JF 3rd. Premature rupture of the fetal membranes. N Engl J Med. 1998;338(10):663–670.
Lockwood CJ, Kuczynski E. Markers of risk for preterm delivery. J Perinat Med. 1999;27(1):5–20.
Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infection and preterm delivery. N Engl J Med. 2000;342(20):1500–1507.
Hack M, Fanaroff AA. Outcomes of extremely immature infants–a perinatal dilemma. N Engl J Med. 1993;329(22):1649–1650.
McCormick MC. The contribution of low birth weight to infant mortality and childhood morbidity. N Engl J Med. 1985;312(2): 82–90.
Menon R, Fortunato SJ. The role of matrix degrading enzymes and apoptosis in rupture of membranes. J Soc Gynecol Investig. 2004;11(7):427–437.
Lappas M, Riley C, Lim R, et al. MAPK and AP-1 proteins are increased in term pre-labour fetal membranes overlying the cervix: regulation of enzymes involved in the degradation of fetal membranes. Placenta. 2011;32(12):1016–1025.
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.
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 e481–e410.
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.
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.
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.
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.
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.
Thomson AJ, Telfer JF, Young A, et al. Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. Hum Reprod. 1999;14(1):229–236.
Bowen JM, Chamley L, Keelan JA, Mitchell MD. Cytokines of the placenta and extra-placental membranes: roles and regulation during human pregnancy and parturition. Placenta. 2002;23(4): 257–273.
Bowen JM, Chamley L, Mitchell MD, Keelan JA. Cytokines of the placenta and extra-placental membranes: biosynthesis, secretion and roles in establishment of pregnancy in women. Placenta. 2002;23(4):239–256.
Osman I, Young A, Ledingham MA, et al. Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol Hum Reprod. 2003;9(1):41–45.
Osman I, Young A, Jordan F, Greer IA, Norman JE. Leukocyte density and proinflammatory mediator expression in regional human fetal membranes and decidua before and during labor at term. J Soc Gynecol Investig. 2006;13(2):97–103.
Gomez Lopez NY, Estrada Gutierrez G, Beltran Montoya J, Vadillo Ortega F. Assessment of a microarray of solid-phase antibodies to the study of chemokines secreted by the chorioamniotic membrane. Ginecol Obstet Mex. 2006;74(12):666–670.
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(1–2):122–131.
Gomez-Lopez N, Vadillo-Perez L, Nessim S, Olson DM, Vadillo-Ortega F. Choriodecidua and amnion exhibit selective leukocyte chemotaxis during term human labor. Am J Obstet Gynecol. 2011;204:364(4) e369–e316.
Vadillo-Ortega F, Gonzalez-Avila G, Karchmer S, Cruz NM, Ayala-Ruiz A, Lama MS. Collagen metabolism in premature rupture of amniotic membranes. Obstet Gynecol. 1990;75(1):84–88.
Redline RW, Faye-Petersen O, Heller D, Qureshi F, Savell V, Vogler C. Amniotic infection syndrome: nosology and reproducibility of placental reaction patterns. Pediatr Dev Pathol. 2003;6: 435–448.
Gomez-Lopez N, Vadillo-Perez L, Hernandez-Carbajal A, Godines-Enriquez M, Olson DM, Vadillo-Ortega F. Specific inflammatory microenvironments in the zones of the fetal membranes at term delivery. Am J Obstet Gynecol. 2011;205(3):235 e215–e224.
Gomez-Lopez N, Vadillo-Ortega F, Estrada-Gutierrez G. Combined boyden-flow cytometry assay improves quantification and provides phenotypification of leukocyte chemotaxis. PLoS ONE. 2011;6(12): e28771.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976;72:248–254.
Kelly RW. Inflammatory mediators and parturition. Rev Reprod. 1996;1(2):89–96.
Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol. 2004;5(3): 266–271.
Gomez-Lopez N, Guilbert LJ, Olson DM. Invasion of the leukocytes into the fetal-maternal interface during pregnancy. J Leukoc Biol. 2010;88:625–633.
Gomez-Lopez N, Olson DM, Cubeiro-Arreola K, Vadillo-Ortega F. T cell recruitment and contribution to an inflammatory microenvironment in the choriodecidua during human labor. Reprod Sci. 2010;17:69A.
Kumar D, Fung W, Moore RM, et al. Proinflammatory cytokines found in amniotic fluid induce collagen remodeling, apoptosis, and biophysical weakening of cultured human fetal membranes. Biol Reprod. 2006;74(1):29–34.
Vadillo OF, Gonzalez AG, 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.
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.
Ito A, Mukaiyama A, Itoh Y, et al. Degradation of interleukin 1beta by matrix metalloproteinases. J Biol Chem. 1996;271(25): 14657–14660.
Casatella MN. The production of cytokines by polymorphonuclear neutrophils. Immunol Today. 1995;16(1):21–26.
Osmers R, Rath W, Adelmann-Grill BC, et al. Origin of cervical collagenase during parturition. Am J Obstet Gynecol. 1992; 166(5):1455–1460.
Pan PY, Li Y, Li Q, et al. In situ recruitment of antigen-presenting cells by intratumoral GM-CSF gene delivery. Cancer Immunol Immunother. 2004;53(1):17–25.
Tamassia N, Le Moigne V, Calzetti F, et al. The MyD88-independent pathway is not mobilized in human neutrophils stimulated via TLR4. J Immunol. 2007;178(11):7344–7356.
Seckinger P, Williamson K, Balavoine JF, et al. A urine inhibitor of interleukin 1 activity affects both interleukin 1 alpha and 1 beta but not tumor necrosis factor alpha. J Immunol. 1987; 139(5):1541–1545.
Arend WP. Interleukin 1 receptor antagonist. A new member of the interleukin 1 family. J Clin Invest. 1991;88(5):1445–1451.
Dinarello CA. Interleukin-1 and interleukin-1 antagonism. Blood. 1991;77(8):1627–1652.
Witkin SS, Gravett MG, Haluska GJ, Novy MJ. Induction of interleukin-1 receptor antagonist in rhesus monkeys after intraam-niotic infection with group B streptococci or interleukin-1 infusion. Am J Obstet Gynecol. 1994;171(6):1668–1672.
Hurme M, Santtila S. IL-1 receptor antagonist (IL-1Ra) plasma levels are co-ordinately regulated by both IL-1Ra and IL-1beta genes. Eur J Immunol. 1998;28(8):2598–2602.
Genc MR, Gerber S, Nesin M, Witkin SS. Polymorphism in the interleukin-1 gene complex and spontaneous preterm delivery. Am J Obstet Gynecol. 2002;187(1):157–163.
Romero R, Sepulveda W, Mazor M, et al. The natural interleukin-1 receptor antagonist in term and preterm parturition. Am J Obstet Gynecol. 1992;167(4 pt 1):863–872.
Romero R, Gomez R, Galasso M, et al. The natural interleukin-1 receptor antagonist in the fetal, maternal, and amniotic fluid compartments: the effect of gestational age, fetal gender, and intrauterine infection. Am J Obstet Gynecol. 1994; 171(4):912–921.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Gomez-Lopez, N., Hernandez-Santiago, S., Lobb, A.P. et al. Normal and Premature Rupture of Fetal Membranes at Term Delivery Differ in Regional Chemotactic Activity and Related Chemokine/Cytokine Production. Reprod. Sci. 20, 276–284 (2013). https://doi.org/10.1177/1933719112452473
Published:
Issue Date:
DOI: https://doi.org/10.1177/1933719112452473