A Novel Role for FOXO3 in Human Labor: Increased Expression in Laboring Myometrium, and Regulation of Proinflammatory and Prolabor Mediators in Pregnant Human Myometrial Cells

Biology of Reproduction

Volumn 88, Issue 6, 2013, Pages

  Lim, Ratana ^a   Barker, Gillian ^a   Lappas, Martha ^b  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MERCY HOSPITAL FOR WOMEN   (Australia)

Author keywords

FOXO3; Human labor; Inflammation; Myometrium

Indexed keywords

COMPLEMENTARY DNA; CYCLOOXYGENASE 2; GELATINASE B; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; PROSTAGLANDIN E2; PROSTAGLANDIN F2 ALPHA; TRANSCRIPTION FACTOR FKHRL1;

ADIPOCYTE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; LABOR; MEDIATOR RELEASE; MYOMETRIUM; PRIORITY JOURNAL; PROSTAGLANDIN RELEASE; PROTEIN EXPRESSION; PROTEIN SECRETION;

FOXO3; HUMAN LABOR; INFLAMMATION; MYOMETRIUM;

FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION; HUMANS; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTERLEUKIN-8; MYOMETRIUM; PARTURITION; RNA, SMALL INTERFERING; UTERINE CONTRACTION;

EID: 84882250225     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.108126     Document Type: Article

References (80)

1. Callaghan WM, MacDorman MF, Rasmussen SA, Qin C, Lackritz EM. The contribution of preterm birth to infant mortality rates in the United States. Pediatrics 2006; 118:1566-1573.
2. Saigal S, Doyle LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet 2008; 371:261-269.
3. Moster D, Lie RT, Markestad T. Long-term medical and social consequences of preterm birth. N Engl J Med 2008; 359:262-273.
4. Romero R, Espinoza J, Goncalves LF, Kusanovic JP, Friel L, Hassan S. The role of inflammation and infection in preterm birth. Semin Reprod Med 2007; 25:21-39.
5. Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, Olson DM. Inflammatory processes in preterm and term parturition. J Reprod Immunol 2008; 79:50-57.
6. 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; 11:317-326.
7. Keelan JA, Blumenstein M, Helliwell RJ, Sato TA, Marvin KW, Mitchell MD. Cytokines, prostaglandins and parturition-a review. Placenta 2003; 24(suppl A):S33-S46.
8. 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; 23:257-273.
9. Olson DM. The role of prostaglandins in the initiation of parturition. Best Pract Res Clin Obstet Gynaecol 2003; 17:717-730.
10. Fata JE, Ho AT, Leco KJ, Moorehead RA, Khokha R. Cellular turnover and extracellular matrix remodeling in female reproductive tissues: functions of metalloproteinases and their inhibitors. Cell Mol Life Sci 2000; 57:77-95.
11. Rice GE. Cytokines and the initiation of parturition. Front Horm Res 2001; 27:113-146.
12. Lappas M, Rice GE. Phospholipase A2 isozymes in pregnancy and parturition. Prostaglandins Leukot Essent Fatty Acids 2004; 70:87-100.
13. Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE, McDowell EP, Lazo-Kallanian S, Williams IR, Sears C, Armstrong SA, Passegué E, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007; 128:325-339.
14. Yang X-F, Fang P, Meng S, Jan M, Xiong X, Yin Y, Wang H. The forkhead transcription factors play important roles in vascular pathology and immunology In: Maiese K (ed.), Forkhead Transcription Factors, vol. 665. New York: Springer; 2010:90-105.
15. Lin L, Hron JD, Peng SL. Regulation of NF-kappaB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 2004; 21:203-213.
16. Snoeks L, Weber CR, Turner JR, Bhattacharyya M, Wasland K, Savkovic SD. Tumor suppressor Foxo3a is involved in the regulation of lipopolysaccharide-induced interleukin-8 in intestinal HT-29 cells. Infect Immun 2008; 76:4677-4685.
17. Snoeks L, Weber CR, Wasland K, Turner JR, Vainder C, Qi WT, Savkovic SD. Tumor suppressor FOXO3 participates in the regulation of intestinal inflammation. Lab Invest 2009; 89:1053-1062.
18. Dejean AS, Beisner DR, Ch'en IL, Kerdiles YM, Babour A, Arden KC, Castrillon DH, DePinho RA, Hedrick SM. Transcription factor Foxo3 controls the magnitude of T cell immune responses by modulating the function of dendritic cells. Nat Immunol 2009; 10:504-513.
19. Hosaka T, Biggs WH, Tieu D, Boyer AD, Varki NM, Cavenee WK, Arden KC. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci U S A 2004; 101:2975-2980.
20. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 2003; 301:215-218.
21. Lee HY, You HJ, Won JY, Youn SW, Cho HJ, Park KW, Park WY, Seo JS, Park YB, Walsh K, Oh BH, Kim HS. Forkhead factor, FOXO3a, induces apoptosis of endothelial cells through activation of matrix metalloproteinases. Arterioscler Thromb Vasc Biol 2008; 28:302-308.
22. Storz P, Doppler H, Copland JA, Simpson KJ, Toker A. FOXO3a promotes tumor cell invasion through the induction of matrix metalloproteinases. Mol Cell Biol 2009; 29:4906-4917.
23. Cui M, Huang Y, Zhao Y, Zheng J. Transcription factor FOXO3a mediates apoptosis in HIV-1-infected macrophages. J Immunol 2008; 180: 898-906.
24. Kristof AS, Fielhaber J, Triantafillopoulos A, Nemoto S, Moss J. Phosphatidylinositol 3-kinase-dependent suppression of the human inducible nitric-oxide synthase promoter is mediated by FKHRL1. J Biol Chem 2006; 281:23958-23968.
25. Li Z, Zhang H, Chen Y, Fan L, Fang J. Forkhead transcription factor FOXO3a protein activates nuclear factor kappaB through B-cell lymphoma/leukemia 10 (BCL10) protein and promotes tumor cell survival in serum deprivation. J Biol Chem 2012; 287:17737-17745.
26. Lappas M, Lim R, Riley C, Menon R, Permezel M. Expression and localisation of FoxO3 and FoxO4 in human placenta and fetal membranes. Placenta 2010; 31:1043-1050.
27. Sooranna SR, Engineer N, Loudon JA, Terzidou V, Bennett PR, Johnson MR. The mitogen-activated protein kinase dependent expression of prostaglandin H synthase-2 and interleukin-8 messenger ribonucleic acid by myometrial cells: the differential effect of stretch and interleukin- 1fbetag. J Clin Endocrinol Metab 2005; 90:3517-3527.
28. Hua R, Pease JE, Sooranna SR, Viney JM, Nelson SM, Myatt L, Bennett PR, Johnson MR. Stretch and inflammatory cytokines drive myometrial chemokine expression via NF-kappaB activation. Endocrinology 2012; 153:481-491.
29. Kovacs KA, Lengyel F, Wilhelm F, Vertes Z, Sumegi B, Vertes M. Involvement of FKHR (FOXO1) transcription factor in human uterus leiomyoma growth. Fertil Steril 2010; 94:1491-1495.
30. Kyo S, Sakaguchi J, Kiyono T, Shimizu Y, Maida Y, Mizumoto Y, Mori N, Nakamura M, Takakura M, Miyake K, Sakamoto M, Inoue M. Forkhead transcription factor FOXO1 is a direct target of progestin to inhibit endometrial epithelial cell growth. Clin Cancer Res 2011; 17: 525-537.
31. Tattersall M, Engineer N, Khanjani S, Sooranna SR, Roberts VH, Grigsby PL, Liang Z, Myatt L, Johnson MR. Pro-labor myometrial gene expression: are preterm labor and term labor the same?. Reproduction 2008; 135:569-579.
32. Chevillard G, Derjuga A, Devost D, Zingg HH, Blank V. Identification of interleukin-1beta regulated genes in uterine smooth muscle cells. Reproduction 2007; 134:811-822.
33. Lappas M, Odumetse TL, Riley C, Reti NG, Holdsworth-Carson SJ, Rice GE, Permezel M. Pre-labor fetal membranes overlying the cervix display alterations in inflammation and NF-kappaB signaling pathways. Placenta 2008; 29:995-1002.
34. Lindstrom TM, Bennett PR. The role of nuclear factor kappa B in human labor. Reproduction 2005; 130:569-581.
35. Lim R, Riley C, Barker G, Rice GE, Lappas M. Human labor is associated with decreased cytoplasmic Foxo4. Placenta 2012; 33:52-59.
36. Lim R, Barker G, Riley C, Lappas M. Apelin is decreased with human preterm and term labor and regulates prolabor mediators in human primary amnion cells. Reprod Sci 2013; (in press). Published online ahead of print 11 January 2013; DOI10.1177/1933719112472741.
37. Lim R, Barker G, Lappas M. SIRT6 is decreased with preterm labor and regulates key terminal effector pathways of human labor in fetal membranes. Biol Reprod 2013; 88:17.
38. Lappas M, Permezel M, Rice GE. N-Acetyl-cysteine inhibits phospholipid metabolism, proinflammatory cytokine release, protease activity, and nuclear factor-kappaB deoxyribonucleic acid-binding activity in human fetal membranes in vitro. J Clin Endocrinol Metab 2003; 88:1723-1729.
39. Lanoix D, St-Pierre J, Lacasse AA, Viau M, Lafond J, Vaillancourt C. Stability of reference proteins in human placenta: general protein stains are the benchmark. Placenta 2012; 33:151-156.
40. Lappas M, Permezel M, Georgiou HM, Rice GE. Nuclear factor kappa B regulation of proinflammatory cytokines in human gestational tissues in vitro. Biol Reprod 2002; 67:668-673.
41. Lappas M, Permezel M, Georgiou HM, Rice GE. Regulation of phospholipase isozymes by nuclear factor-kappaB in human gestational tissues in vitro. J Clin Endocrinol Metab 2004; 89:2365-2372.
42. Lappas M, Permezel M, Rice GE. 15-Deoxy-delta(12, 14)-prostaglandin J(2) and troglitazone regulation of the release of phospholipid metabolites, inflammatory cytokines and proteases from human gestational tissues. Placenta 2006; 27:1060-1072.
43. Lappas M, Rice GE. The role and regulation of the nuclear factor kappa B signaling pathway in human labor. Placenta 2007; 28:543-556.
44. Lappas M, Rice GE. Transcriptional regulation of the processes of human labor and delivery. Placenta 2009; 30(suppl A):S90-S95.
45. Seiler F, Hellberg J, Lepper PM, Kamyschnikow A, Herr C, Bischoff M, Langer F, Schäfers H-J, Lammert F, Menger MD, Bals R, Beisswenger C. FOXO transcription factors regulate innate immune mechanisms in respiratory epithelial cells. J Immunol 2013; 190:1603-1613.
46. Turrel-Davin F, Tournadre A, Pachot A, Arnaud B, Cazalis MA, Mougin B, Miossec P. FoxO3a involved in neutrophil and T cell survival is overexpressed in rheumatoid blood and synovial tissue. Ann Rheum Dis 2010; 69(4):755-760.
47. Su B, Liu H, Wang X, Chen S, Siedlak S, Kondo E, Choi R, Takeda A, Castellani R, Perry G, Smith M, Zhu X, et al. Ectopic localization of FOXO3a protein in Lewy bodies in Lewy body dementia and Parkinson's disease. Mol Neurodegen 2009; 4:32.
48. Myatt L, Cui X. Oxidative stress in the placenta. Histochem Cell Biol 2004; 122:369-382.
49. Bollapragada S, Youssef R, Jordan F, Greer I, Norman J, Nelson S. Term labor is associated with a core inflammatory response in human fetal membranes, myometrium, and cervix. Am J Obstet Gynecol 2009. 200: 104 e101-e111.
50. Osman I, Young A, Ledingham MA, Thomson AJ, Jordan F, Greer IA, Norman JE. Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labor at term. Mol Human Reprod 2003; 9: 41-45
51. Keski-Nisula L, Aalto ML, Katila ML, Kirkinen P Intrauterine inflammation at term: a histopathologic study. Hum Pathol 2000; 31: 841-846.
52. Ledingham MA, Thomson AJ, Young A, Macara LM, Greer IA, Norman JE. Changes in the expression of nitric oxide synthase in the human uterine cervix during pregnancy and parturition. Mol Hum Reprod 2000; 6: 1041-1048.
53. Rauk PN, Chiao JP. Interleukin-1 stimulates human uterine prostaglandin production through induction of cyclooxygenase-2 expression. Am J Reprod Immunol 2000; 43:152-159.
54. Greig PC, Ernest JM, Teot L, Erikson M, Talley R. Amniotic fluid interleukin-6 levels correlate with histologic chorioamnionitis and amniotic fluid cultures in patients in premature labor with intact membranes. Am J Obstet Gynecol 1993; 169:1035-1044.
55. Greig PC, Murtha AP, Jimmerson CJ, Herbert WN, Roitman-Johnson B, Allen J. Maternal serum interleukin-6 during pregnancy and during term and preterm labor. Obstet Gynecol 1997; 90:465-469.
56. Rauk PN, Friebe-Hoffmann U, Winebrenner LD, Chiao JP. Interleukin-6 up-regulates the oxytocin receptor in cultured uterine smooth muscle cells. Am J Reprod Immunol 2001; 45:148-153.
57. El Maradny E, Kanayama N, Halim A, Maehara K, Sumimoto K, Terao T. Biochemical changes in the cervical tissue of rabbit induced by interleukin-8, interleukin-1beta, dehydroepiandrosterone sulphate and prostaglandin E2: a comparative study. Hum Reprod 1996; 11:1099-1104.
58. Thomson AJ, Telfer JF, Young A, Campbell S, Stewart CJ, Cameron IT, Greer IA, Norman JE. Leukocytes infiltrate the myometrium during human parturition: further evidence that labor is an inflammatory process. Hum Reprod 1999; 14:229-236.
59. Karim SM, Trussell RR, Petl RC, Hillier K. Response of pregnant human uterus to prostaglandin-F2-alpha-induction of labor. Br Med J 1968; 4: 621-623.
60. Sawdy R, Knock GA, Bennett PR, Poston L, Aaronson PI. Effect of nimesulide and indomethacin on contractility and the Ca2 channel current in myometrial smooth muscle from pregnant women. Br J Pharmacol 1998; 125:1212-1217.
61. Khan RN, Matharoo-Ball B, Shaw RW. Antioxidant enzyme expression, lipid peroxidation, and protein oxidation in human myometrium with parturition. Reprod Sci 2010; 17:78-84.
62. Shynlova O, Oldenhof A, Dorogin A, Xu Q, Mu J, Nashman N, Lye SJ. Myometrial apoptosis: activation of the caspase cascade in the pregnant rat myometrium at midgestation. Biol Reprod 2006; 74:839-849.
63. Shynlova O, Tsui P, Jaffer S, Lye SJ. Integration of endocrine and mechanical signals in the regulation of myometrial functions duringpregnancy and labor. Eur J Obstet Gynecol Reprod Biol 2009; 144(suppl 1):S2-S10.
64. Breuiller-Fouche M, Germain G. Gene and protein expression in the myometrium in pregnancy and labor. Reproduction 2006; 131:837-850.
65. Buhimschi IA, Buhimschi CS, Pupkin M, Weiner CP. Beneficial impact of term labor: nonenzymatic antioxidant reserve in the human fetus. Am J Obstet Gynecol 2003; 189:181-188.
66. Stipek S, Mechurova A, Crkovska J, Zima T, Platenik J. Lipid peroxidation and superoxide dismutase activity in umbilical and maternal blood. Biochem Mol Biol Int 1995; 35:705-711.
67. Stygar D, Wang H, Vladic YS, Ekman G, Eriksson H, Sahlin L. Increased level of matrix metalloproteinases 2 and 9 in the ripening process of the human cervix. Biol Reprod 2002; 67:889-894.
68. Leong AS, Norman JE, Smith R. Vascular and myometrial changes in the human uterus at term. Reprod Sci 2008; 15:59-65.
69. Charpigny G, Leroy MJ, Breuiller-Fouche M, Tanfin Z, Mhaouty-Kodja S, Robin P, Leiber D, Cohen-Tannoudji J, Cabrol D, Barberis C, Germain G. A functional genomic study to identify differential gene expression in the preterm and term human myometrium. Biol Reprod 2003; 68: 2289-2296.
70. Lirussi F, Rakotoniaina Z, Madani S, Goirand F, Breuiller-Fouche M, Leroy MJ, Sagot P, Morrison JJ, Dumas M, Bardou M. ADRB3 adrenergic receptor is a key regulator of human myometrial apoptosis and inflammation during chorioamnionitis. Biol Reprod 2008; 78: 497-505.
71. Senokuchi T, Liang CP, Seimon TA, Han S, Matsumoto M, Banks AS, Paik JH, DePinho RA, Accili D, Tabas I, Tall AR. Forkhead transcription factors (FoxOs) promote apoptosis of insulin-resistant macrophages during cholesterol-induced endoplasmic reticulum stress. Diabetes 2008; 57: 2967-2976.
72. Kajihara T, Jones M, Fusi L, Takano M, Feroze-Zaidi F, Pirianov G, Mehmet H, Ishihara O, Higham JM, Lam EW, Brosens JJ. Differential expression of FOXO1 and FOXO3a confers resistance to oxidative cell death upon endometrial decidualization. Mol Endocrinol 2006; 20: 2444-2455.
73. Chai M, Barker G, Menon R, Lappas M. Increased oxidative stress in human fetal membranes overlying the cervix from term non-laboring and post labor deliveries. Placenta 2012; 33:604-610.
74. 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; 27:1037-1051.
75. McLaren J, Taylor DJ, Bell SC. Increased incidence of apoptosis in nonlabor- affected cytotrophoblast cells in term fetal membranes overlying the cervix. Hum Reprod 1999; 14:2895-2900.
76. Khanjani S, Terzidou V, Johnson MR, Bennett PR. NFkappaB and AP-1 drive human myometrial IL8 expression. Mediators Inflamm 2012; 2012: 504952.
77. van der Heide LP, Smidt MP. Regulation of FoxO activity by CBP/p300- mediated acetylation. Trends Biochem Sci 2005; 30:81-86.
78. Hwang JW, Rajendrasozhan S, Rahman I. Deficiency of FoxO3 augments lung inflammation in response to cigarette smoke in mice. Am J Respir Crit Care Med 2010; 181:A3888.
79. Al-Gubory KH, Fowler PA, Garrel C. The roles of cellular reactive oxygen species, oxidative stress and antioxidants in pregnancy outcomes. Int J Biochem Cell Biol 2010; 42:1634-1650.
80. Romero R, Chaiworapongsa T, Kuivaniemi H, Tromp G. Bacterial vaginosis, the inflammatory response and the risk of preterm birth: a role for genetic epidemiology in the prevention of preterm birth. Am J Obstet Gynecol 2004; 190:1509-1519.