Activator protein 1 is a key terminal mediator of inflammation-induced preterm labor in mice

FASEB Journal

Volumn 28, Issue 5, 2014, Pages 2358-2368

  MacIntyre, David A ^a   Lee, Yun S ^a   Migale, Roberta ^a   Herbert, Bronwen R ^a   Waddington, Simon N ^b,c   Peebles, Donald ^b   Hagberg, Henrik ^d,e   Johnson, Mark R ^a,f   Bennett, Phillip R ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF THE WITWATERSRAND   (South Africa)

^d UNIVERSITY OF GOTHENBURG   (Sweden)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

Author keywords

Infection; Myometrium; NFkB; Progesterone

Indexed keywords

ANTHRA[1,9 CD]PYRAZOL 6(2H) ONE; CONTRACTILE PROTEIN; CX43 PROTEIN; CYCLOOXYGENASE 2; DIMETHYL SULFOXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; MIFEPRISTONE; STROMELYSIN 2; TRANSCRIPTION FACTOR AP 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; ESCHERICHIA COLI; FEMALE; GESTATION PERIOD; INFLAMMATION; LABOR ONSET; MEDIATOR; MOUSE; MYOMETRIUM; NONHUMAN; PREGNANCY; PREMATURE LABOR; PRIORITY JOURNAL; PROTEIN CLEAVAGE; SEROTYPE;

INFECTION; MYOMETRIUM; NFKB; PROGESTERONE;

ANIMALS; ANTHRACENES; CYTOKINES; FEMALE; INFLAMMATION; LABOR, OBSTETRIC; LIPOPOLYSACCHARIDES; MICE; MYOMETRIUM; NF-KAPPA B; NF-KAPPA B P50 SUBUNIT; OBSTETRIC LABOR, PREMATURE; PREGNANCY; PREGNANCY, ANIMAL; PROGESTERONE; PROTO-ONCOGENE PROTEINS C-FOS; PROTO-ONCOGENE PROTEINS C-JUN; RECEPTORS, PROGESTERONE; TIME FACTORS; TOLL-LIKE RECEPTOR 4; TRANSCRIPTION FACTOR AP-1; UTERUS;

EID: 84901022976     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-247783     Document Type: Article

References (52)

1. Bisits, A. M., Smith, R., Mesiano, S., Yeo, G., Kwek, K., MacIntyre, D., and Chan, E. C. (2005) Inflammatory aetiology of human myometrial activation tested using directed graphs. PLoS Comput. Biol. 1, 132-136
2. Keelan, J. A., Marvin, K. W., Sato, T. A., Coleman, M., McCowan, L. M., and Mitchell, M. D. (1999) Cytokine abundance in placental tissues: evidence of inflammatory activation in gestational membranes with term and preterm parturition. Am. J. Obstet. Gynecol. 181, 1530-1536
3. Thomson, A. J., Telfer, J. F., Young, A., Campbell, S., Stewart, C. J., Cameron, I. T., Greer, I. A., and Norman, J. E. (1999) Leukocytes infiltrate the myometrium during human parturition: further evidence that labour is an inflammatory process. Hum. Reprod. 14, 229-236
4. Wood, N. S., Marlow, N., Costeloe, K., Gibson, A. T., and Wilkinson, A. R. (2000) Neurologic and developmental disability after extremely preterm birth. EPICure Study Group. N. Engl. J. Med. 343, 378-384
5. Romero, R., Espinoza, J., Goncalves, L. F., Kusanovic, J. P., Friel, L., and Hassan, S. (2007) The role of inflammation and infection in preterm birth. Semin. Reprod. Med. 25, 21-39
6. Lindstrom, T. M., and Bennett, P. R. (2005) The role of nuclear factor kappa B in human labour. Reproduction 130, 569-581
7. Condon, J. C., Jeyasuria, P., Faust, J. M., and Mendelson, C. R. (2004) Surfactant protein secreted by the maturing mouse fetal lung acts as a hormone that signals the initiation of parturition. Proc. Natl. Acad. Sci. U. S. A. 101, 4978-4983
8. Khanjani, S., Kandola, M. K., Lindstrom, T. M., Sooranna, S. R., Melchionda, M., Lee, Y. S., Terzidou, V., Johnson, M. R., and Bennett, P. R. (2011) NF-kappaB regulates a cassette of immune/ inflammatory genes in human pregnant myometrium at term. J. Cell. Mol. Med. 15, 809-824
9. Lim, S., MacIntyre, D. A., Lee, Y. S., Khanjani, S., Terzidou, V., Teoh, T. G., and Bennett, P. R. (2012) Nuclear factor kappa B activation occurs in the amnion prior to labour onset and modulates the expression of numerous labour associated genes. PLoS ONE 7, e34707
10. Sasaki, C. Y., Barberi, T. J., Ghosh, P., and Longo, D. L. (2005) Phosphorylation of RelA/p65 on serine 536 defines an I-B-independent NF-κB pathway. J. Biol. Chem. 280, 34538-34547
11. Vermeulen, L., De Wilde, G., Notebaert, S., Vanden Berghe, W., and Haegeman, G. (2002) Regulation of the transcriptional activity of the nuclear factor-kappaB p65 subunit. Biochem. Pharmacol. 64, 963-970
12. Libermann, T. A., and Baltimore, D. (1990) Activation of interleukin-6 gene expression through the NF-kappa B transcription factor. Mol. Cell. Biol. 10, 2327-2334
13. Cogswell, J. P., Godlevski, M. M., Wisely, G. B., Clay, W. C., Leesnitzer, L. M., Ways, J. P., and Gray, J. G. (1994) NF-kappa B regulates IL-1 beta transcription through a consensus NF-kappa B binding site and a nonconsensus CRE-like site. J. Immunol. 153, 712-723
14. Hiscott, J., Marois, J., Garoufalis, J., D'Addario, M., Roulston, A., Kwan, I., Pepin, N., Lacoste, J., Nguyen, H., Bensi, G., and Fenton, M. (1993) Characterization of a functional NF-kappa B site in the human interleukin 1 beta promoter: evidence for a positive autoregulatory loop. Mol. Cell. Biol. 13, 6231-6240
15. Belt, A. R., Baldassare, J. J., Molnar, M., Romero, R., and Hertelendy, F. (1999) The nuclear transcription factor NFkappaB mediates interleukin-1beta-induced expression of cyclooxygenase-2 in human myometrial cells. Am. J. Obstet. Gynecol. 181, 359-366
16. Soloff, M. S., Cook, D. L., Jr., Jeng, Y. J., and Anderson, G. D. (2004) In situ analysis of interleukin-1-induced transcription of cox-2 and il-8 in cultured human myometrial cells. Endocrinology 145, 1248-1254
17. Olson, D. M. (2003) The role of prostaglandins in the initiation of parturition. Best Pract. Res. Clin. Obstet. Gynaecol. 17, 717-730
18. Fuchs, A. R., Fuchs, F., Husslein, P., Soloff, M. S., and Fernstrom, M. J. (1982) Oxytocin receptors and human parturition: a dual role for oxytocin in the initiation of labor. Science 215, 1396-1398
19. Terzidou, V., Lee, Y., Lindstrom, T., Johnson, M., Thornton, S., and Bennett, P. R. (2006) Regulation of the human oxytocin receptor by nuclear factor-kappaB and CCAAT/enhancer-binding protein-beta. J. Clin. Endocrinol. Metab. 91, 2317-2326
20. Halazonetis, T. D., Georgopoulos, K., Greenberg, M. E., and Leder, P. (1988) c-Jun dimerizes with itself and with c-Fos, forming complexes of different DNA binding affinities. Cell 55, 917-924
21. Kouzarides, T., and Ziff, E. (1988) The role of the leucine zipper in the fos-jun interaction. Nature 336, 646-651
22. Ip, Y. T., and Davis, R. J. (1998) Signal transduction by the c-Jun N-terminal kinase (JNK): from inflammation to development. Curr. Opin. Cell Biol. 10, 205-219
23. Allport, V. C., Slater, D. M., Newton, R., and Bennett, P. R. (2000) NF-kappaB and AP-1 are required for cyclo-oxygenase 2 gene expression in amnion epithelial cell line (WISH). Mol. Hum. Reprod. 6, 561-565
24. Mohan, A. R., Sooranna, S. R., Lindstrom, T. M., Johnson, M. R., and Bennett, P. R. (2007) The effect of mechanical stretch on cyclooxygenase type 2 expression and activator protein-1 and nuclear factor-kappaB activity in human amnion cells. Endocrinology 148, 1850-1857
25. Loudon, J. A., Sooranna, S. R., Bennett, P. R., and Johnson, M. R. (2004) Mechanical stretch of human uterine smooth muscle cells increases IL-8 mRNA expression and peptide synthesis. Mol. Hum. Reprod. 10, 895-899
26. Sooranna, S. R., Lee, Y., Kim, L. U., Mohan, A. R., Bennett, P. R., and Johnson, M. R. (2004) Mechanical stretch activates type 2 cyclooxygenase via activator protein-1 transcription factor in human myometrial cells. Mol. Hum. Reprod. 10, 109-113
27. Terzidou, V., Sooranna, S. R., Kim, L. U., Thornton, S., Bennett, P. R., and Johnson, M. R. (2005) Mechanical stretch upregulates the human oxytocin receptor in primary human uterine myocytes. J. Clin. Endocrinol. Metab. 90, 237-246
28. Geimonen, E., Jiang, W., Ali, M., Fishman, G. I., Garfield, R. E., and Andersen, J. (1996) Activation of protein kinase C in human uterine smooth muscle induces connexin-43 gene transcription through an AP-1 site in the promoter sequence. J. Biol. Chem. 271, 23667-23674
29. Mitchell, J. A., and Lye, S. J. (2005) Differential activation of the connexin 43 promoter by dimers of activator protein-1 transcription factors in myometrial cells. Endocrinology 146, 2048-2054
30. Pirianov, G., Waddington, S. N., Lindstrom, T. M., Terzidou, V., Mehmet, H., and Bennett, P. R. (2009) The cyclopentenone 15-deoxy-delta 12,14-prostaglandin J(2) delays lipopolysaccharide-induced preterm delivery and reduces mortality in the newborn mouse. Endocrinology 150, 699-706
31. Dudley, D. J., Branch, D. W., Edwin, S. S., and Mitchell, M. D. (1996) Induction of preterm birth in mice by RU486. Biol. Reprod. 55, 992-995
32. Williams, A. S., Issa, R., Leung, S. Y., Nath, P., Ferguson, G. D., Bennett, B. L., Adcock, I. M., and Chung, K. F. (2007) Attenuation of ozone-induced airway inflammation and hyper-responsiveness by c-Jun NH2 terminal kinase inhibitor SP600125. J. Pharmacol. Exp. Therapeut. 322, 351-359
33. Ramirez-Alcantara, V., LoGuidice, A., and Boelsterli, U. A. (2009) Protection from diclofenac-induced small intestinal injury by the JNK inhibitor SP600125 in a mouse model of NSAID-associated enteropathy. Am. J. Physiol. Gastrointest. Liver Physiol. 297, G990-G998
34. Nath, P., Eynott, P., Leung, S. Y., Adcock, I. M., Bennett, B. L., and Chung, K. F. (2005) Potential role of c-Jun NH2-terminal kinase in allergic airway inflammation and remodelling: effects of SP600125. Eur. J. Pharmacol. 506, 273-283
35. Agrawal, V., Smart, K., Jilling, T., and Hirsch, E. (2013) Surfactant protein (SP)-A suppresses preterm delivery and inflammation via TLR2. PLoS ONE 8, e63990
36. Condon, J. C., Hardy, D. B., Kovaric, K., and Mendelson, C. R. (2006) Up-regulation of the progesterone receptor (PR)-C isoform in laboring myometrium by activation of nuclear factorkappaB may contribute to the onset of labor through inhibition of PR function. Mol. Endocrinol. 20, 764-775
37. Allport, V. C., Pieber, D., Slater, D. M., Newton, R., White, J. O., and Bennett, P. R. (2001) Human labour is associated with nuclear factor-kappaB activity which mediates cyclo-oxygenase-2 expression and is involved with the 'functional progesterone withdrawal'. Mol. Hum. Reprod. 7, 581-586
38. Benbow, U., and Brinckerhoff, C. E. (1997) The AP-1 site and MMP gene regulation: what is all the fuss about? Matrix Biol. J. Int. Soc. Matrix Biol. 15, 519-526
39. Imada, K., Sato, T., Hashizume, K., Tanimoto, A., Sasaguri, Y., and Ito, A. (2002) An antiprogesterone, onapristone, enhances the gene expression of promatrix metalloproteinase 3/prostromelysin-1 in the uterine cervix of pregnant rabbit. Biol. Pharmaceut. Bull. 25, 1223-1227
40. Slater, D. M., Dennes, W. J., Campa, J. S., Poston, L., and Bennett, P. R. (1999) Expression of cyclo-oxygenase types-1 and-2 in human myometrium throughout pregnancy. Mol. Hum. Reprod. 5, 880-884
41. MacIntyre, D. A., Chan, E. C., and Smith, R. (2007) Myometrial activation-coordination, connectivity and contratility. Fetal Maternal Med. Rev. 18, 333-356
42. Geimonen, E., Boylston, E., Royek, A., and Andersen, J. (1998) Elevated connexin-43 expression in term human myometrium correlates with elevated c-Jun expression and is independent of myometrial estrogen receptors. J. Clin. Endocrinol. Metab. 83, 1177-1185
43. Piersanti, M., and Lye, S. J. (1995) Increase in messenger ribonucleic acid encoding the myometrial gap junction protein, connexin-43, requires protein synthesis and is associated with increased expression of the activator protein-1, c-fos. Endocrinology 136, 3571-3578
44. Hutchinson, J. L., Rajagopal, S. P., Yuan, M., and Norman, J. E. (2014) Lipopolysaccharide promotes contraction of uterine myocytes via activation of Rho/ROCK signaling pathways. FASEB J. 28, 94-105
45. Martinon, F., and Tschopp, J. (2007) Inflammatory caspases and inflammasomes: master switches of inflammation. Cell Death Differ. 14, 10-22
46. Limjuco, G., Galuska, S., Chin, J., Cameron, P., Boger, J., and Schmidt, J. A. (1986) Antibodies of predetermined specificity to the major charged species of human interleukin 1. Proc. Natl. Acad. Sci. U. S. A. 83, 3972-3976
47. Auron, P. E., Warner, S. J., Webb, A. C., Cannon, J. G., Bernheim, H. A., McAdam, K. J., Rosenwasser, L. J., LoPreste, G., Mucci, S. F., and Dinarello, C. A. (1987) Studies on the molecular nature of human interleukin 1. J. Immunol. 138, 1447-1456
48. Wewers, M. D., Winnard, A. V., and Dare, H. A. (1999) Endotoxin-stimulated monocytes release multiple forms of IL-1 beta, including a proIL-1 beta form whose detection is affected by export. J. Immunol. 162, 4858-4863
49. Rubartelli, A., Cozzolino, F., Talio, M., and Sitia, R. (1990) A novel secretory pathway for interleukin-1 beta, a protein lacking a signal sequence. EMBO J. 9, 1503-1510
50. Lee, Y., Sooranna, S. R., Terzidou, V., Christian, M., Brosens, J., Huhtinen, K., Poutanen, M., Barton, G., Johnson, M. R., and Bennett, P. R. (2012) Interactions between inflammatory signals and the progesterone receptor in regulating gene expression in pregnant human uterine myocytes. J. Cell. Mol. Med. 16, 2487-2503
51. Mesiano, S., Chan, E. C., Fitter, J. T., Kwek, K., Yeo, G., and Smith, R. (2002) Progesterone withdrawal and estrogen activation in human parturition are coordinated by progesterone receptor A expression in the myometrium. J. Clin. Endocrinol. Metab. 87, 2924-2930
52. Pieber, D., Allport, V. C., and Bennett, P. R. (2001) Progesterone receptor isoform A inhibits isoform B-mediated transactivation in human amnion. Eur. J. Pharmacol. 427, 7-11