The molecular pathophysiology of bacterially induced preterm labor: Insights from the murine model

Journal of the Society for Gynecologic Investigation

Volumn 12, Issue 3, 2005, Pages 145-155

  Hirsch, Emmet ^a   Wang, Hao ^a  

^a Evanston Northwestern Healthcare ^*  (United States)

Author keywords

Infection; Parturition; Premature labor

Indexed keywords

ANTIOXIDANT; BETAMETHASONE; CHORIONIC GONADOTROPIN; CYTOKINE; DEXAMETHASONE; INDOMETACIN; INTERLEUKIN 10; LACTOFERRIN; MEDROXYPROGESTERONE ACETATE; METALLOPROTEINASE INHIBITOR; PROGESTERONE; PROSTAGLANDIN RECEPTOR BLOCKING AGENT; PROSTAGLANDIN SYNTHASE INHIBITOR; PROTEIN TYROSINE KINASE INHIBITOR; THROMBOCYTE ACTIVATING FACTOR ANTAGONIST; TOLL LIKE RECEPTOR; ULINASTATIN;

ANIMAL MODEL; BACTERIAL INFECTION; CHILDBIRTH; FEMALE; GENOMICS; GESTATION PERIOD; IMMUNE RESPONSE; INTRAUTERINE INFECTION; LABOR INDUCTION; LITERATURE; MOUSE; NONHUMAN; PREMATURE LABOR; PRIORITY JOURNAL; PROTEOMICS; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; BACTERIAL INFECTIONS; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; GENOMICS; HUMANS; INFLAMMATION MEDIATORS; MEMBRANE GLYCOPROTEINS; MICE; MICE, MUTANT STRAINS; OBSTETRIC LABOR, PREMATURE; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PROGESTERONE; PROTEOMICS; RECEPTORS, CELL SURFACE; TOLL-LIKE RECEPTORS;

EID: 15244343466     PISSN: 10715576     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsgi.2005.01.007     Document Type: Review

References (104)

1. Preterm labor. ACOG Technical Bulletin Vol 206 1995 American College of Obstetricians and Gynecologists Washington, DC
2. R.L. Goldenberg, J.C. Hauth, W.W. Andrews Intrauterine infection and preterm delivery N Engl J Med 342 2000 1500 1507
3. M.M. Slattery, J.J. Morrison Preterm delivery Lancet 360 2002 1489 1497
4. R. Romero, J. Espinoza, T. Chaiworapongsa, K. Kalache Infection and prematurity and the role of preventive strategies Semin Neonatol 7 2002 259 274
5. R.J. Ruiz, J. Fullerton, D.J. Dudley The interrelationship of maternal stress, endocrine factors and inflammation on gestational length Obstet Gynecol Surv 58 2003 415 428
6. E.B. da Fonseca, R.E. Bittar, M.H. Carvalho, M. Zugaib Prophylactic administration of progesterone by vaginal suppository to reduce the incidence of spontaneous preterm birth in women at increased risk A randomized placebo-controlled double-blind study Am J Obstet Gynecol 188 2003 419 424
7. P.J. Meis, M. Klebanoff, E. Thom Prevention of recurrent preterm delivery by 17 alpha-hydroxyprogesterone caproate N Engl J Med 348 2003 2379 2385
8. K. Takeda, T. Kaisho, S. Akira Toll-like receptors Annu Rev Immunol 21 2003 335 376
9. K.A. Zarember, P.J. Godowski Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines J Immunol 168 2002 554 561
10. A. Mazzoni, D.M. Segal Controlling the toll road to dendritic cell polarization J Leukoc Biol 75 2004 721 730
11. E.J. Molloy, A.J. O'Neill, J.J. Grantham Labor induces a maternal inflammatory response syndrome Am J Obstet Gynecol 190 2004 448 455
12. U. Holmlund, G. Cebers, A.R. Dahlfors Expression and regulation of the pattern recognition receptors toll-like receptor-2 and toll-like receptor-4 in the human placenta Immunology 107 2002 145 151
13. K. Kumazaki, M. Nakayama, I. Yanagihara, N. Suehara, Y. Wada Immunohistochemical distribution of toll-like receptor 4 in term and preterm human placentas from normal and complicated pregnancy including chorioamnionitis Hum Pathol 35 2004 47 54
14. K. Harju, V. Glumoff, M. Hallman Ontogeny of toll-like receptors Tlr2 and Tlr4 in mice Pediatr Res 49 2001 81 83
15. R. Romero, R. Gomez, F. Ghezzi A fetal systemic inflammatory response is followed by the spontaneous onset of preterm parturition Am J Obstet Gynecol 179 1998 186 193
16. G.C. Liggins, R.J. Fairclough, S.A. Grieves, C.S. Forster, B.S. Knox Parturition in the sheep J. Knight M. O'Connor The fetus and birth 1977 Elsevier Amsterdam 5 30
17. I. Osman, A. Young, M.A. Ledingham 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 2003 41 45
18. S.M. Yellon, A.M. Mackler, M.A. Kirby The role of leukocyte traffic and activation in parturition J Soc Gynecol Investig 10 2003 323 338
19. R. Romero, B. Tartakovsky The natural interleukin-1 receptor antagonist prevents interleukin-1-induced preterm delivery in mice Am J Obstet Gynecol 167 1992 1041 1045
20. A. Jeyabalan, S.N. Caritis Pharmacologic inhibition of preterm labor Clin Obstet Gynecol 45 2002 99 113
21. D.A. Terrone, B.K. Rinehart, J.P. Granger, P.S. Barrilleaux, J.N. Martin Jr, W.A. Bennett Interleukin-10 administration and bacterial endotoxin-induced preterm birth in a rat model Obstet Gynecol 98 2001 476 480
22. I.A. Buhimschi, C.S. Buhimschi, C.P. Weiner Protective effect of N-acetylcysteine against fetal death and preterm labor induced by maternal inflammation Am J Obstet Gynecol 188 2003 203 208
23. T. Kimura, K. Ogita, C. Kusui, K. Ohashi, C. Azuma, Y. Murata What knockout mice can tell us about parturition Rev Reprod 4 1999 73 80
24. J.L. Cook, D.B. Zaragoza, D.H. Sung, D.M. Olson Expression of myometrial activation and stimulation genes in a mouse model of preterm labor Myometrial activation, stimulation, and preterm labor Endocrinology 141 2000 1718 1728
25. G. Gross, T. Imamura, L.J. Muglia Gene knockout mice in the study of parturition J Soc Gynecol Investig 7 2000 88 95
26. E. Hirsch, R.A. Muhle, G.M. Mussalli, R. Blanchard Bacterially induced preterm labor in the mouse does not require maternal interleukin-1 signaling Am J Obstet Gynecol 186 2002 523 530
27. S. Astle, D.M. Slater, S. Thornton The involvement of progesterone in the onset of human labour Eur J Obstet Gynecol Reprod Biol 108 2003 177 181
28. J.C. Condon, P. Jeyasuria, J.M. Faust, J.W. Wilson, C.R. Mendelson A decline in the levels of progesterone receptor coactivators in the pregnant uterus at term may antagonize progesterone receptor function and contribute to the initiation of parturition Proc Natl Acad Sci U S A 100 2003 9518 9523
29. G.J. Haluska, T.R. Wells, J.J. Hirst, R.M. Brenner, D.W. Sadowsky, M.J. Novy Progesterone receptor localization and isoforms in myometrium, decidua, and fetal membranes from rhesus macaques evidence for functional progesterone withdrawal at parturition J Soc Gynecol Investig 9 2002 125 136
30. S. Mesiano, E.C. Chan, J.T. Fitter, K. Kwek, G. Yeo, R. Smith Progesterone withdrawal and estrogen activation in human parturition are coordinated by progesterone receptor A expression in the myometrium J Clin Endocrinol Metab 87 2002 2924 2930
31. D. Henderson, T. Wilson Reduced binding of progesterone receptor to its nuclear response element after human labor onset Am J Obstet Gynecol 185 2001 579 585
32. T.A. Tibbetts, O.M. Conneely, B.W. O'Malley Progesterone via its receptor antagonizes the pro-inflammatory activity of estrogen in the mouse uterus Biol Reprod 60 1999 1158 1165
33. S. Mesiano Myometrial progesterone responsiveness and the control of human parturition J Soc Gynecol Investig 11 2004 193 202
34. R. Frydman, C. Lelaidier, C. Baton-Saint-Mleux, H. Fernandez, M. Vial, P. Bourget Labor induction in women at term with mifepristone (RU 486) A double-blind, randomized, placebo-controlled study Obstet Gynecol 80 1992 972 975
35. E. Hirsch, I. Saotome, D. Hirsh A model of intrauterine infection and preterm delivery in mice Am J Obstet Gynecol 172 1995 1598 1603
36. G.M. Mussalli, R. Blanchard, S.R. Brunnert, E. Hirsch Inflammatory cytokines in a murine model of infection-induced preterm labor Cause or effect? J Soc Gynecol Investig 6 1999 188 195
37. L.L. Reznikov, G. Fantuzzi, C.H. Selzman Utilization of endoscopic inoculation in a mouse model of intrauterine infection-induced preterm birth role of interleukin 1beta Biol Reprod 60 1999 1231 1238
38. G.M. Mussalli, S.R. Brunnert, E. Hirsch Preterm delivery in mice with renal abscess Obstet Gynecol 95 2000 453 456
39. Y.W. Han, R.W. Redline, M. Li, L. Yin, G.B. Hill, T.S. McCormick Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice Implication of oral bacteria in preterm birth Infect Immun 72 2004 2272 2279
40. S. Kajikawa, N. Kaga, Y. Futamura, C. Kakinuma, Y. Shibutani Lipoteichoic acid induces preterm delivery in mice J Pharmacol Toxicol Methods 39 1998 147 154
41. D.J. Dudley, C.L. Chen, D.W. Branch, E. Hammond, M.D. Mitchell A murine model of preterm labor Inflammatory mediators regulate the production of prostaglandin E2 and interleukin-6 by murine decidua Biol Reprod 48 1993 33 39
42. P.L. Fidel Jr, R. Romero, N. Wolf Systemic and local cytokine profiles in endotoxin-induced preterm parturition in mice Am J Obstet Gynecol 170 1994 1467 1475
43. N. Kaga, Y. Katsuki, M. Obata, Y. Shibutani Repeated administration of low-dose lipopolysaccharide induces preterm delivery in mice a model for human preterm parturition and for assessment of the therapeutic ability of drugs against preterm delivery Am J Obstet Gynecol 174 1996 754 759
44. Y. Nakanishi, M. Akutsu-hosomura, H. Narahara, F. Iwasa A model for local infection-induced preterm labor in the mouse Delivery of live pups before term following the intracervical administration of lipopolysaccharide Prenat Neonat Med 6 2001 116 121
45. M.A. Elovitz, Z. Wang, E.K. Chien, D.F. Rychlik, M. Phillippe A new model for inflammation-induced preterm birth The role of platelet-activating factor and toll-like receptor-4 Am J Pathol 163 2003 2103 2111
46. R. Romero, M. Mazor, B. Tartakovsky Systemic administration of interleukin-1 induces preterm parturition in mice Am J Obstet Gynecol 165 1991 969 971
47. J.T. Kurtzman, J.A. Spinnato, L.J. Goldsmith Human chorionic gonadotropin exhibits potent inhibition of preterm delivery in a small animal model Am J Obstet Gynecol 181 1999 853 857
48. D.J. Dudley, D.W. Branch, S.S. Edwin, M.D. Mitchell Induction of preterm birth in mice by RU486 Biol Reprod 55 1996 992 995
49. G.M. Tiboni, F. Giampietro Inhibition of nitric oxide synthesis causes preterm delivery in the mouse Hum Reprod 15 2000 1838 1842
50. G.M. Tiboni, F. Giampietro, D. Lamonaca The soluble guanylate cyclase inhibitor methylene blue evokes preterm delivery and fetal growth restriction in a mouse model In Vivo 15 2001 333 337
51. P.I. Fidel Jr, R. Romero, E. Maymon, F. Hertelendy Bacteria-induced or bacterial product-induced preterm parturition in mice and rabbits is preceded by a significant fall in serum progesterone concentrations J Matern Fetal Med 7 1998 222 226
52. E. Hirsch, R. Muhle Intrauterine bacterial inoculation induces labor in the mouse by mechanisms other than progesterone withdrawal Biol Reprod 67 2002 1337 1341
53. C.A. Dinarello Proinflammatory cytokines Chest 118 2000 503 508
54. B.B. Aggarwal Signalling pathways of the TNF superfamily A double-edged sword Nat Rev Immunol 3 2003 745 756
55. R. Romero, M. Mazor, F. Brandt Interleukin-1 alpha and interleukin-1 beta in preterm and term human parturition Am J Reprod Immunol 27 1992 117 123
56. R. Romero, M. Mazor, W. Sepulveda, C. Avila, D. Copeland, J. Williams Tumor necrosis factor in preterm and term labor Am J Obstet Gynecol 166 1992 1576 1587
57. D.J. Dudley, D. Collmer, M.D. Mitchell, M.S. Trautman Inflammatory cytokine mRNA in human gestational tissues Implications for term and preterm labor J Soc Gynecol Investig 3 1996 328 335
58. R.S. McDuffie Jr, M.P. Sherman, R.S. Gibbs Amniotic fluid tumor necrosis factor-alpha and interleukin-1 in a rabbit model of bacterially induced preterm pregnancy loss Am J Obstet Gynecol 167 1992 1583 1588
59. M.G. Gravett, S.S. Witkin, G.J. Haluska, J.L. Edwards, M.J. Cook, M.J. Novy An experimental model for intraamniotic infection and preterm labor in rhesus monkeys Am J Obstet Gynecol 171 1994 1660 1667
60. E. Hirsch, R. Blanchard, S.P. Mehta Differential fetal and maternal contributions to the cytokine milieu in a murine model of infection-induced preterm birth Am J Obstet Gynecol 180 1999 429 434
61. K. Bry, M. Hallman Transforming growth factor-beta 2 prevents preterm delivery induced by interleukin-1 alpha and tumor necrosis factor-alpha in the rabbit Am J Obstet Gynecol 168 1993 1318 1322
62. S. Baggia, M.G. Gravett, S.S. Witkin, G.J. Haluska, M.J. Novy Interleukin-1 beta intra-amniotic infusion induces tumor necrosis factor-alpha, prostaglandin production, and preterm contractions in pregnant rhesus monkeys J Soc Gynecol Investig 3 1996 121 126
63. N.L. Brown, S.A. Alvi, M.G. Elder, P.R. Bennett, M.H. Sullivan Interleukin-1beta and bacterial endotoxin change the metabolism of prostaglandins E2 and F2alpha in intact term fetal membranes Placenta 19 1998 625 630
64. J.R.G. Challis Mechanism of parturition and preterm labor Obstet Gynecol Surv 55 2000 650 660
65. S. Rodts-Palenik, P. Barrilleaux, B. Thigpen Intravenous interleukin-10/antibioic therapy prolongs gestation, improves birthweight, and reduces fetal wastage in E. coli-mediated preterm labor Am J Obstet Gynecol 187 2003 S65
66. K. Maeda, N. Matsuzaki, S. Fuke Value of the maternal interleukin 6 level for determination of histologic chorioamnionitis in preterm delivery Gynecol Obstet Invest 43 1997 225 231
67. M. Labow, D. Shuster, M. Zetterstrom Absence of IL-1 signaling and reduced inflammatory response in IL-1 type I receptor-deficient mice J Immunol 159 1997 2452 2461
68. R.D. Acton, P.S. Dahlberg, M.E. Uknis Differential sensitivity to Escherichia coli infection in mice lacking tumor necrosis factor p55 or interleukin-1 p80 receptors Arch Surg 131 1996 1216 1221
69. P.L. Fidel Jr, R. Romero, J. Cutright Treatment with the interleukin-I receptor antagonist and soluble tumor necrosis factor receptor Fc fusion protein does not prevent endotoxin-induced preterm parturition in mice J Soc Gynecol Investig 4 1997 22 26
70. K. Yoshimura, E. Hirsch Interleukin-6 is neither necessary nor sufficient for preterm labor in a murine infection model J Soc Gynecol Investig 10 2003 423 427
71. O. Takeuchi, K. Hoshino, T. Kawai Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components Immunity 11 1999 443 451
72. L. Alexopoulou, A.C. Holt, R. Medzhitov, R.A. Flavell Recognition of double-stranded RNA and activation of NF-kappaB by toll-like receptor 3 Nature 413 2001 732 738
73. A. Poltorak, X. He, I. Smirnova Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice mutations in Tlr4 gene Science 282 1998 2085 2088
74. S.T. Qureshi, L. Lariviere, G. Leveque Endotoxin-tolerant mice have mutations in toll-like receptor 4 (Tlr4) J Exp Med 189 1999 615 625
75. F. Hayashi, K.D. Smith, A. Ozinsky The innate immune response to bacterial flagellin is mediated by toll-like receptor 5 Nature 410 2001 1099 1103
76. H. Hemmi, O. Takeuchi, T. Kawai A toll-like receptor recognizes bacterial DNA Nature 408 2000 740 745
77. S. Akira, K. Takeda Toll-like receptor signalling Nat Rev Immunol 4 2004 499 511
78. K. Takeda, S. Akira TLR signaling pathways Semin Immunol 16 2004 3 9
79. M. Lappas, M. Permezel, H.M. Georgiou, G.E. Rice Nuclear factor kappa B regulation of proinflammatory cytokines in human gestational tissues in vitro Biol Reprod 67 2002 668 673
80. A.R. Belt, J.J. Baldassare, M. Molnar, R. Romero, F. Hertelendy The nuclear transcription factor NF-kappaB mediates interleukin-1beta-induced expression of cyclooxygenase-2 in human myometrial cells Am J Obstet Gynecol 181 1999 359 366
81. R. Medzhitov Toll-like receptors and innate immunity Nat Rev Immunol 1 2001 135 145
82. S. Akira, K. Takeda, T. Kaisho Toll-like receptors Critical proteins linking innate and acquired immunity Nat Immunol 2 2001 675 680
83. H. Wang, E. Hirsch Bacterially-induced preterm labor and regulation of prostaglandin-metabolizing enzyme expression in mice The role of toll-like receptor 4 Biol Reprod 69 2003 1957 1963
84. K.L. Koscica, G. Sylvestre, S.E. Reznik The effect of phosphoramidon on inflammation-mediated preterm delivery in a mouse model Am J Obstet Gynecol 190 2004 528 531
85. M. Elovitz, Z. Wang Medroxyprogesterone acetate, but not progesterone, protects against inflammation-induced parturition and intrauterine fetal demise Am J Obstet Gynecol 190 2004 693 701
86. C.D. Loftin, D.B. Trivedi, R. Langenbach Cyclooxygenase-1-selective inhibition prolongs gestation in mice without adverse effects on the ductus arteriosus J Clin Invest 110 2002 549 557
87. G. Gross, T. Imamura, S.K. Vogt Inhibition of cyclooxygenase-2 prevents inflammation-mediated preterm labor in the mouse Am J Physiol Regul Integr Comp Physiol 278 2000 R1415 R1423
88. M. Sakai, K. Tanebe, Y. Sasaki, K. Momma, S. Yoneda, S. Saito Evaluation of the tocolytic effect of a selective cyclooxygenase-2 inhibitor in a mouse model of lipopolysaccharide-induced preterm delivery Mol Hum Reprod 7 2001 595 602
89. P.R. Lee, S.R. Kim, B.K. Jung Therapeutic effect of cyclo-oxygenase inhibitors with different isoform selectivity in lipopolysaccharide-induced preterm birth in mice Am J Obstet Gynecol 189 2003 261 266
90. W.J. Schwartz 3rd, H.D. Christensen, J.C. Carey, W.F. Rayburn, C. Gonzalez Systemic administration of betamethasone delays endotoxin-induced preterm labor in the murine model Am J Obstet Gynecol 188 2003 439 443
91. K.G. Peri, C. Quiniou, X. Hou THG113 A novel selective FP antagonist that delays preterm labor Semin Perinatol 26 2002 389 397
92. J.E. Mijovic, T. Zakar, D.B. Zaragoza, D.M. Olson Tyrphostins inhibit lipopolysaccharide induced preterm labor in mice J Perinat Med 30 2002 297 300
93. Y. Mitsuhashi, K. Otsuki, A. Yoda, Y. Shimizu, H. Saito, T. Yanaihara Effect of lactoferrin on lipopolysaccharide (LPS) induced preterm delivery in mice Acta Obstet Gynecol Scand 79 2000 355 358
94. Y. Futamura, S. Kajikawa, N. Kaga, Y. Shibutani Protection against preterm delivery in mice by urinary trypsin inhibitor Obstet Gynecol 93 1999 100 108
95. M. Gravett, D. Sadowsky, S. Witkin, M. Novy Immunomodulators plus antibiotics to prevent preterm delivery in experimental intra-amniotic infection (IAI) Am J Obstet Gynecol 189 2003 S56
96. R.A. Muhle, P. Pavlidis, W.N. Grundy, E. Hirsch A high-throughput study of gene expression in preterm labor with a subtractive microarray approach Am J Obstet Gynecol 185 2001 716 724
97. H. Wang, P. Pavlidis, W.S. Noble, E. Hirsch Analysis of gene expression in myometrium during heat-killed E. coli-induced preterm labor in mice J Soc Gynecol Investig 10 Suppl 2003 379A
98. E. Hirsch, H. Wang, P. Pavlidis, W.S. Noble Gene expression in bacterially induced preterm labor The lipopolysaccharide (LPS) receptor takes a toll J Soc Gynecol Investig 10 Suppl 2003 379A
99. K. Aguan, J.A. Carvajal, L.P. Thompson, C.P. Weiner Application of a functional genomics approach to identify differentially expressed genes in human myometrium during pregnancy and labour Mol Hum Reprod 6 2000 1141 1145
100. K.W. Marvin, J.A. Keelan, R.L. Eykholt, T.A. Sato, M.D. Mitchell Use of cDNA arrays to generate differential expression profiles for inflammatory genes in human gestational membranes delivered at term and preterm Mol Hum Reprod 8 2002 399 408
101. M. Girotti, H.H. Zingg Gene expression profiling of rat uterus at different stages of parturition Endocrinology 144 2003 2254 2265
102. K.E. Bethin, Y. Nagai, R. Sladek Microarray analysis of uterine gene expression in mouse and human pregnancy Mol Endocrinol 17 2003 1454 1469
103. H. Ishiwata, S. Katsuma, K. Kizaki Characterization of gene expression profiles in early bovine pregnancy using a custom cDNA microarray Mol Reprod Dev 65 2003 9 18
104. M.G. Gravett, M.J. Novy, R.G. Rosenfeld Diagnosis of intra-amniotic infection by proteomic profiling and identification of novel biomarkers JAMA 292 2004 462 469