Cervical ripening and parturition in cows are driven by a cascade of pro-inflammatory cytokines

Reproduction in Domestic Animals

Volumn 44, Issue 5, 2009, Pages 834-841

  Van Engelen, E ^a   De Groot, M W ^a   Breeveld Dwarkasing, V N A ^a   Everts, M E ^a   Van Der Weyden, G C ^a   Taverne, M A M ^a   Rutten, V P M G ^a,b  

^a UTRECHT UNIVERSITY   (Netherlands)

^b UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MESSENGER RNA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; ARTICLE; BIRTH; CHEMISTRY; CYTOLOGY; FEMALE; GENE EXPRESSION; GENETICS; GESTATIONAL AGE; INFLAMMATION; LEUKOCYTE COUNT; NEUTROPHIL; PHYSIOLOGY; PREGNANCY; UTERINE CERVIX; UTERINE CERVIX RIPENING;

ANIMALS; CERVICAL RIPENING; CERVIX UTERI; CYTOKINES; FEMALE; GENE EXPRESSION; GESTATIONAL AGE; INFLAMMATION; INTERLEUKIN-10; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTERLEUKIN-8; LEUKOCYTE COUNT; NEUTROPHILS; PARTURITION; PREGNANCY; RNA, MESSENGER; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA; BOVINAE;

EID: 70349198000     PISSN: 09366768     EISSN: 14390531     Source Type: Journal    
DOI: 10.1111/j.1439-0531.2008.01096.x     Document Type: Article

References (58)

1. Aalberts M, van Dissel-Emiliani FM, van Tol TA, Taverne MA, Breeveld-Dwarkasing VN, 2007 : High iNOS mRNA and protein levels during early third trimester suggest a role for NO in prelabor cervical ripening in the bovine. Mol Reprod Dev 74, 378 385.
2. Argiles JM, Carbo N, Lopez-Soriano FJ, 1997 : TNF and pregnancy: the paradigm of a complex interaction. Cytokine Growth Factor Rev 8, 181 188.
3. Breeveld-Dwarkasing VN, te Koppele JM, Bank RA, van der Weijden GC, Taverne MA, van Dissel-Emiliani FM, 2003 : Changes in water content, collagen degradation, collagen content, and concentration in repeated biopsies of the cervix of pregnant cows. Biol Reprod 69, 1608 1614.
4. Bytautiene E, Vedernikov YP, Saade GR, Romero R, Garfield RE, 2002 : Endogenous mast cell degranulation modulates cervical contractility in the guinea pig. Am J Obstet Gynecol 186, 438 445.
5. Chwalisz K, Garfield RE, 1998 : Nitric oxide as the final metabolic mediator of cervical ripening. Hum Reprod 13, 245 248.
6. Chwalisz K, Benson M, Scholz P, Daum J, Beier HM, Hegele-Hartung C, 1994 : Cervical ripening with the cytokines interleukin 8, interleukin 1 beta and tumour necrosis factor alpha in guinea-pigs. Hum Reprod 9, 2173 2181.
7. De Preter K, Speleman F, Combaret V, Lunec J, Laureys G, Eussen BH, Francotte N, Board J, Pearson AD, De Paepe A, Van Roy N, Vandesompele J, 2002 : Quantification of MYCN, DDX1, and NAG gene copy number in neuroblastoma using a real-time quantitative PCR assay. Mod Pathol 15, 159 166.
8. Denison FC, Kelly RW, Calder AA, Riley SC, 1998 : Cytokine secretion by human fetal membranes, decidua and placenta at term. Hum Reprod 13, 3560 3565.
9. van Engelen E, Taverne MA, Everts ME, van der Weijden GC, Doornenbal A, Breeveld-Dwarkasing VN, 2007 : EMG activity of the muscular and stromal layer of the cervix in relation to EMG activity of the myometrium and cervical dilatation in PGF2alpha induced parturition in the cow. Theriogenology 67, 1158 1167.
10. van Engelen E, Breeveld Dwarkasing VN, Rutten VP, Everts ME, van der Weijden GC, Taverne MA 2008a : Smooth muscle cells of the bovine cervical stroma may have a secretory, rather than a contractile function during parturition. Reprod Dom Anim. In press.
11. van Engelen E, Breeveld Dwarkasing VN, Taverne MA, Everts ME, van der Weijden GC, Rutten VP 2008b : MMP-2 expression precedes the final cervical ripening process of the bovine cervix. Mol Reprod Dev. In press.
12. Ertel W, Kremer JP, Kenney J, Steckholzer U, Jarrar D, Trentz O, Schildberg FW, 1995 : Downregulation of proinflammatory cytokine release in whole blood from septic patients. Blood 85, 1341 1347.
13. Fujimoto T, Savani RC, Watari M, Day AJ, Strauss JF III, 2002 : Induction of the hyaluronic acid-binding protein, tumor necrosis factor-stimulated gene-6, in cervical smooth muscle cells by tumor necrosis factor-alpha and prostaglandin E(2). Am J Pathol 160, 1495 1502.
14. Hanna N, Hanna I, Hleb M, Wagner E, Dougherty J, Balkundi D, Padbury J, Sharma S, 2000 : Gestational age-dependent expression of IL-10 and its receptor in human placental tissues and isolated cytotrophoblasts. J Immunol 164, 5721 5728.
15. Hanna N, Bonifacio L, Weinberger B, Reddy P, Murphy S, Romero R, Sharma S, 2006 : Evidence for interleukin-10-mediated inhibition of cyclo-oxygenase-2 expression and prostaglandin production in preterm human placenta. Am J Reprod Immunol 55, 19 27.
16. Hassan SS, Romero R, Haddad R, Hendler I, Khalek N, Tromp G, Diamond MP, Sorokin Y, Malone J Jr, 2006 : The transcriptome of the uterine cervix before and after spontaneous term parturition. Am J Obstet Gynecol 195, 778 786.
17. Hegele-Hartung C, Chwalisz K, Beier HM, Elger W, 1989 : Ripening of the uterine cervix of the guinea-pig after treatment with the progesterone antagonist onapristone (ZK 98.299): an electron microscopic study. Hum Reprod 4, 369 377.
18. Howard M, O'Garra A, Ishida H, de Waal Malefyt R, de Vries J, 1992 : Biological properties of interleukin 10. J Clin Immunol 12, 239 247.
19. Junqueira LC, Zugaib M, Montes GS, Toledo OM, Krisztan RM, Shigihara KM, 1980 : Morphologic and histochemical evidence for the occurrence of collagenolysis and for the role of neutrophilic polymorphonuclear leukocytes during cervical dilation. Am J Obstet Gynecol 138, 273 281.
20. Katsikis PD, Chu CQ, Brennan FM, Maini RN, Feldmann M, 1994 : Immunoregulatory role of interleukin 10 in rheumatoid arthritis. J Exp Med 179, 1517 1527.
21. Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD, 2003 : Cytokines, prostaglandins and parturition - a review. Placenta 24 (Suppl A S33 S46.
22. Kelly RW, 2002 : Inflammatory mediators and cervical ripening. J Reprod Immunol 57, 217 224.
23. Livak KJ, Schmittgen TD, 2001 : Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) method. Methods 25, 402 408.
24. Luna L (ed.) 1968 : Manual of Histologic Staining Methods of the Armed Forces Institute of Pathology. McGraw-Hill, New York, pp. 111.
25. Luque EH, Ramos JG, Rodriguez HA, Munoz de Toro MM, 1996 : Dissociation in the control of cervical eosinophilic infiltration and collagenolysis at the end of pregnancy or after pseudopregnancy in ovariectomized steroid-treated rats. Biol Reprod 55, 1206 1212.
26. Luque EH, Bassani MM, Ramos JG, Maffini M, Canal A, Kass L, Caldini EG, Ferreira Junior JM, Munoz de Toro M, Montes GS, 1997 : Leukocyte infiltration and collagenolysis in cervical tissue from intrapartum sheep. Zentralbl Veterinarmed A 44, 501 510.
27. Mackler AM, Iezza G, Akin MR, McMillan P, Yellon SM, 1999 : Macrophage trafficking in the uterus and cervix precedes parturition in the mouse. Biol Reprod 61, 879 883.
28. Malmstrom E, Sennstrom M, Holmberg A, Frielingsdorf H, Eklund E, Malmstrom L, Tufvesson E, Gomez MF, Westergren-Thorsson G, Ekman-Ordeberg G, Malmstrom A, 2007 : The importance of fibroblasts in remodelling of the human uterine cervix during pregnancy and parturition. Mol Hum Reprod 13, 333 341.
29. Maul H, Nagel S, Welsch G, Schafer A, Winkler M, Rath W 2002 : Messenger ribonucleic acid levels of interleukin-1 beta, interleukin-6 and interleukin-8 in the lower uterine segment increased significantly at final cervical dilatation during term parturition, while those of tumor necrosis factor alpha remained unchanged. Eur J Obstet Gynecol Reprod Biol 102, 143 147.
30. Maul H, Mackay L, Garfield RE, 2006 : Cervical ripening: biochemical, molecular, and clinical considerations. Clin Obstet Gynecol 49, 551 563.
31. Mehlhop PD, van de Rijn M, Goldberg AB, Brewer JP, Kurup VP, Martin TR, Oettgen HC, 1997 : Allergen-induced bronchial hyperreactivity and eosinophilic inflammation occur in the absence of IgE in a mouse model of asthma. Proc Natl Acad Sci U S A 94, 1344 1349.
32. Morita Y, Yamamura M, Kawashima M, Aita T, Harada S, Okamoto H, Inoue H, Makino H, 2001 : Differential in vitro effects of IL-4, IL-10, and IL-13 on proinflammatory cytokine production and fibroblast proliferation in rheumatoid synovium. Rheumatol Int 20, 49 54.
33. Osman I, Young A, Ledingham MA, Thomson AJ, Jordan F, Greer IA, Norman JE, 2003 : Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol Hum Reprod 9, 41 45.
34. Peltier MR, 2003 : Immunology of term and preterm labor. Reprod Biol Endocrinol 1, 122 133.
35. Rath W, Winkler M, Kemp B, 1998 : The importance of extracellular matrix in the induction of preterm delivery. J Perinat Med 26, 437 441.
36. Read CP, Word RA, Ruscheinsky MA, Timmons BC, Mahendroo MS, 2007 : Cervical remodeling during pregnancy and parturition: molecular characterization of the softening phase in mice. Reproduction 134, 327 340.
37. Sadowsky DW, Novy MJ, Witkin SS, Gravett MG, 2003 : Dexamethasone or interleukin-10 blocks interleukin-1beta-induced uterine contractions in pregnant rhesus monkeys. Am J Obstet Gynecol 188, 252 263.
38. Sakamoto Y, Moran P, Searle RF, Bulmer JN, Robson SC, 2004 : Interleukin-8 is involved in cervical dilatation but not in prelabour cervical ripening. Clin Exp Immunol 138, 151 157.
39. Sakamoto Y, Moran P, Bulmer JN, Searle RF, Robson SC, 2005 : Macrophages and not granulocytes are involved in cervical ripening. J Reprod Immunol 66, 161 173.
40. Sennstrom MK, Brauner A, Lu Y, Granstrom LM, Malmstrom AL, Ekman GE, 1997 : Interleukin-8 is a mediator of the final cervical ripening in humans. Eur J Obstet Gynecol Reprod Biol 74, 89 92.
41. Sennstrom MB, Ekman G, Westergren-Thorsson G, Malmstrom A, Bystrom B, Endresen U, Mlambo N, Norman M, Stabi B, Brauner A, 2000 : Human cervical ripening, an inflammatory process mediated by cytokines. Mol Hum Reprod 6, 375 381.
42. Simpson KL, Keelan JA, Mitchell MD, 1998 : Labor-associated changes in interleukin-10 production and its regulation by immunomodulators in human choriodecidua. J Clin Endocrinol Metab 83, 4332 4337.
43. Steinborn A, Kuhnert M, Halberstadt E, 1996 : Immunmodulating cytokines induce term and preterm parturition. J Perinat Med 24, 381 390.
44. Terrone DA, Rinehart BK, Granger JP, Barrilleaux PS, Martin JN Jr, Bennett WA, 2001 : Interleukin-10 administration and bacterial endotoxin-induced preterm birth in a rat model. Obstet Gynecol 98, 476 480.
45. Timmons BC, Mahendroo MS, 2006 : Timing of neutrophil activation and expression of proinflammatory markers do not support a role for neutrophils in cervical ripening in the mouse. Biol Reprod 74, 236 245.
46. Tornblom SA, Klimaviciute A, Bystrom B, Chromek M, Brauner A, Ekman-Ordeberg G, 2005 : Non-infected preterm parturition is related to increased concentrations of IL-6, IL-8 and MCP-1 in human cervix. Reprod Biol Endocrinol 3, 39 49.
47. Vowles G, Francis R 2002 : Sirius Red technique. In : Bancroft J, Gamble M (eds Theory and Practice of Histological Techniques. Churchill Livingstone, London, pp. 313.
48. Watari M, Watari H, DiSanto ME, Chacko S, Shi GP, Strauss JF III, 1999 : Pro-inflammatory cytokines induce expression of matrix-metabolizing enzymes in human cervical smooth muscle cells. Am J Pathol 154, 1755 1762.
49. Watari M, Watari H, Nachamkin I, Strauss JF, 2000 : Lipopolysaccharide induces expression of genes encoding pro-inflammatory cytokines and the elastin-degrading enzyme, cathepsin S, in human cervical smooth-muscle cells. J Soc Gynecol Invest 7, 190 198.
50. Watkins LR, Hansen MK, Nguyen KT, Lee JE, Maier SF, 1999 : Dynamic regulation of the proinflammatory cytokine, interleukin-1beta: molecular biology for non-molecular biologists. Life Sci 65, 449 481.
51. Wehrend A, Gumbel B, Leiser R, Failing K, Bostedt H, 2004 : Vaginal and cervical dilatation intrapartum is associated with eosinophilic infiltration in the cow but not in the sheep. Reprod Dom Anim 39, 442 446.
52. Whitworth MK, Pafilis I, Vince G, Quenby S, 2007 : Cervical leukocyte sub-populations in idiopathic preterm labour. J Reprod Immunol 75, 48 55.
53. Winkler M, 2003 : Role of cytokines and other inflammatory mediators. BJOG 110 (Suppl 20 118 123.
54. Winkler M, Fischer DC, Hlubek M, Rath W, 1998 : Expression of TNFa, IL-b, IL-6 and IL-8 in the lower uterine segment in term and preterm parturition. Perinat Med 10, 12 15.
55. Winkler M, Fischer DC, Ruck P, Marx T, Kaiserling E, Oberpichler A, Tschesche H, Rath W, 1999a : Parturition at term: parallel increases in interleukin-8 and proteinase concentrations and neutrophil count in the lower uterine segment. Hum Reprod 14, 1096 1100.
56. Winkler M, Oberpichler A, Tschesche H, Ruck P, Fischer DC, Rath W, 1999b : Collagenolysis in the lower uterine segment during parturition at term: correlations with stage of cervical dilatation and duration of labor. Am J Obstet Gynecol 181, 153 158.
57. Word RA, Li XH, Hnat M, Carrick K, 2007 : Dynamics of cervical remodeling during pregnancy and parturition: mechanisms and current concepts. Semin Reprod Med 25, 69 79.
58. Young A, Thomson AJ, Ledingham M, Jordan F, Greer IA, Norman JE, 2002 : Immunolocalization of proinflammatory cytokines in myometrium, cervix, and fetal membranes during human parturition at term. Biol Reprod 66, 445 449.