Activin-Like Kinase 2 Functions in Peri-implantation Uterine Signaling in Mice and Humans

PLoS Genetics

Volumn 9, Issue 11, 2013, Pages

  Clementi, Caterina ^a   Tripurani, Swamy K ^a   Large, Michael J ^a   Edson, Mark A ^a   Creighton, Chad J ^a   Hawkins, Shannon M ^a   Kovanci, Ertug ^a   Kaartinen, Vesa ^b   Lydon, John P ^a   Pangas, Stephanie A ^a   DeMayo, Francesco J ^a   Matzuk, Martin M ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN RECEPTOR 1; CCAAT ENHANCER BINDING PROTEIN BETA; MESSENGER RNA; PROGESTERONE RECEPTOR; PROTEIN ALK2; SMAD1 PROTEIN; SMAD5 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLASTOCYTE; BREEDING; CELL INVASION; CHROMATIN IMMUNOPRECIPITATION; DECIDUALIZATION; EMBRYO; ENDOMETRIUM CELL; FEMALE; FEMALE FERTILITY; FEMALE STERILITY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MALE; MICROARRAY ANALYSIS; MOLECULAR MECHANICS; MOUSE; NIDATION; NONHUMAN; PHENOTYPE; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; STROMA CELL;

ACTIVIN RECEPTORS, TYPE I; ACTIVINS; ANIMALS; BONE MORPHOGENETIC PROTEIN 2; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO IMPLANTATION; FEMALE; HUMANS; MICE; PREGNANCY; RECEPTORS, PROGESTERONE; SIGNAL TRANSDUCTION; STROMAL CELLS; UTERUS;

EID: 84888264302     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003863     Document Type: Article

References (50)

1. Cha J, Sun X, Dey SK, (2012) Mechanisms of implantation: strategies for successful pregnancy. Nat Med 18: 1754-1767.
2. Large MJ, DeMayo FJ, (2012) The regulation of embryo implantation and endometrial decidualization by progesterone receptor signaling. Mol Cell Endocrinol 358: 155-165.
3. Ramathal CY, Bagchi IC, Taylor RN, Bagchi MK, (2010) Endometrial decidualization: of mice and men. Semin Reprod Med 28: 17-26.
4. Bagchi IC, Li Q, Cheon YP, Mantena SR, Kannan A, et al. (2005) Use of the progesterone receptor antagonist RU 486 to identify novel progesterone receptor-regulated pathways in implantation. Semin Reprod Med 23: 38-45.
5. Zhang H, Bradley A, (1996) Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122: 2977-2986.
6. Soyal SM, Mukherjee A, Lee KY, Li J, Li H, et al. (2005) Cre-mediated recombination in cell lineages that express the progesterone receptor. Genesis 41: 58-66.
7. Clementi C, Pangas SA, Matzuk MM (2013) In: Barbieri, Strauss, editors. Yen and Jaffe's Reproductive Endocrinology 7th ed: Elsevier Inc.
8. Lee KY, Jeong JW, Wang J, Ma L, Martin JF, et al. (2007) Bmp2 is critical for the murine uterine decidual response. Mol Cell Biol 27: 5468-5478.
9. Li Q, Kannan A, Wang W, Demayo FJ, Taylor RN, et al. (2007) Bone morphogenetic protein 2 functions via a conserved signaling pathway involving Wnt4 to regulate uterine decidualization in the mouse and the human. J Biol Chem 282: 31725-31732.
10. Paria BC, Ma W, Tan J, Raja S, Das SK, et al. (2001) Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors. Proc Natl Acad Sci U S A 98: 1047-1052.
11. Ying Y, Zhao GQ, (2000) Detection of multiple bone morphogenetic protein messenger ribonucleic acids and their signal transducer, Smad1, during mouse decidualization. Biol Reprod 63: 1781-1786.
12. Edson MA, Nalam RL, Clementi C, Franco HL, Demayo FJ, et al. (2010) Granulosa cell-expressed BMPR1A and BMPR1B have unique functions in regulating fertility but act redundantly to suppress ovarian tumor development. Mol Endocrinol 24: 1251-1266.
13. Gu Z, Reynolds EM, Song J, Lei H, Feijen A, et al. (1999) The type I serine/threonine kinase receptor ActRIA (ALK2) is required for gastrulation of the mouse embryo. Development 126: 2551-2561.
14. Mishina Y, Crombie R, Bradley A, Behringer RR, (1999) Multiple roles for activin-like kinase-2 signaling during mouse embryogenesis. Dev Biol 213: 314-326.
15. Kaartinen V, Nagy A, (2001) Removal of the floxed neo gene from a conditional knockout allele by the adenoviral Cre recombinase in vivo. Genesis 31: 126-129.
16. Tong W, Pollard JW, (1999) Progesterone inhibits estrogen-induced cyclin D1 and cdk4 nuclear translocation, cyclin E- and cyclin A-cdk2 kinase activation, and cell proliferation in uterine epithelial cells in mice. Mol Cell Biol 19: 2251-2264.
17. Nagashima T, Li Q, Clementi C, Lydon JP, DeMayo FJ, Matzuk MM, (2013) BMPR2 is required for post-implantation uterine function and pregnancy maintenance. The Journal of Clinical Investigation 123 (6) (): 2539-50.
18. Chakraborty I, Das SK, Wang J, Dey SK, (1996) Developmental expression of the cyclo-oxygenase-1 and cyclo-oxygenase-2 genes in the peri-implantation mouse uterus and their differential regulation by the blastocyst and ovarian steroids. J Mol Endocrinol 16: 107-122.
19. Mantena SR, Kannan A, Cheon YP, Li Q, Johnson PF, et al. (2006) C/EBPbeta is a critical mediator of steroid hormone-regulated cell proliferation and differentiation in the uterine epithelium and stroma. Proc Natl Acad Sci U S A 103: 1870-1875.
20. Dunn CL, Kelly RW, Critchley HO, (2003) Decidualization of the human endometrial stromal cell: an enigmatic transformation. Reprod Biomed Online 7: 151-161.
21. Christian M, Pohnke Y, Kempf R, Gellersen B, Brosens JJ, (2002) Functional association of PR and CCAAT/enhancer-binding protein beta isoforms: promoter-dependent cooperation between PR-B and liver-enriched inhibitory protein, or liver-enriched activatory protein and PR-A in human endometrial stromal cells. Mol Endocrinol 16: 141-154.
22. Wang W, Li Q, Bagchi IC, Bagchi MK, (2010) The CCAAT/enhancer binding protein beta is a critical regulator of steroid-induced mitotic expansion of uterine stromal cells during decidualization. Endocrinology 151: 3929-3940.
23. Bagchi MK, Mantena SR, Kannan A, Bagchi IC, (2006) Control of uterine cell proliferation and differentiation by C/EBPbeta: functional implications for establishment of early pregnancy. Cell Cycle 5: 922-925.
24. Lydon JP, DeMayo FJ, Conneely OM, O'Malley BW, (1996) Reproductive phenotpes of the progesterone receptor null mutant mouse. J Steroid Biochem Mol Biol 56: 67-77.
25. Nair SC, Rimerman RA, Toran EJ, Chen S, Prapapanich V, et al. (1997) Molecular cloning of human FKBP51 and comparisons of immunophilin interactions with Hsp90 and progesterone receptor. Mol Cell Biol 17: 594-603.
26. Finn CA, Martin L, (1972) Endocrine control of the timing of endometrial sensitivity to a decidual stimulus. Biol Reprod 7: 82-86.
27. Li Q, Kannan A, DeMayo FJ, Lydon JP, Cooke PS, et al. (2011) The antiproliferative action of progesterone in uterine epithelium is mediated by Hand2. Science 331: 912-916.
28. Franco HL, Rubel CA, Large MJ, Wetendorf M, Fernandez-Valdivia R, et al. (2012) Epithelial progesterone receptor exhibits pleiotropic roles in uterine development and function. FASEB J 26: 1218-1227.
29. Lejeune B, Van Hoeck J, Leroy F, (1981) Transmitter role of the luminal uterine epithelium in the induction of decidualization in rats. J Reprod Fertil 61: 235-240.
30. Gellersen B, Brosens IA, Brosens JJ, (2007) Decidualization of the human endometrium: mechanisms, functions, and clinical perspectives. Semin Reprod Med 25: 445-453.
31. Wilcox AJ, Weinberg CR, O'Connor JF, Baird DD, Schlatterer JP, et al. (1988) Incidence of early loss of pregnancy. N Engl J Med 319: 189-194.
32. Norwitz ER, Schust DJ, Fisher SJ, (2001) Implantation and the survival of early pregnancy. N Engl J Med 345: 1400-1408.
33. Norwitz ER, (2006) Defective implantation and placentation: laying the blueprint for pregnancy complications. Reprod Biomed Online 13: 591-599.
34. Diedrich K, Fauser BC, Devroey P, Griesinger G, Evian Annual Reproduction Workshop G, (2007) The role of the endometrium and embryo in human implantation. Hum Reprod Update 13: 365-377.
35. Simon C, Landeras J, Zuzuarregui JL, Martin JC, Remohi J, et al. (1999) Early pregnancy losses in in vitro fertilization and oocyte donation. Fertil Steril 72: 1061-1065.
36. Jones RL, Salamonsen LA, Findlay JK, (2002) Activin A promotes human endometrial stromal cell decidualization in vitro. J Clin Endocrinol Metab 87: 4001-4004.
37. Trenor CC, (2011) Hormonal contraception and thrombotic risk: a multidisciplinary approach. Pediatrics 127: 347-357.
38. Mueck AO, (2010) Exogenous hormones, the risk of venous thromboembolism, and activated protein C resistance. Menopause 17: 1099-1103.
39. Mueck AO, Seeger H, Rabe T, (2010) Hormonal contraception and risk of endometrial cancer: a systematic review. Endocr Relat Cancer 17: R263-271.
40. Chang H, Brown CW, Matzuk MM, (2002) Genetic analysis of the mammalian transforming growth factor-beta superfamily. Endocr Rev 23: 787-823.
41. Massague J, (2008) TGFbeta in Cancer. Cell 134: 215-230.
42. Padua D, Massague J, (2009) Roles of TGFbeta in metastasis. Cell Res 19: 89-102.
43. Tan CK, Leuenberger N, Tan MJ, Yan YW, Chen Y, et al. (2011) Smad3 deficiency in mice protects against insulin resistance and obesity induced by a high-fat diet. Diabetes 60: 464-476.
44. Dabek J, Kulach A, Monastyrska-Cup B, Gasior Z, (2006) Transforming growth factor beta and cardiovascular diseases: the other facet of the 'protective cytokine'. Pharmacol Rep 58: 799-805.
45. Margadant C, Sonnenberg A, (2010) Integrin-TGF-beta crosstalk in fibrosis, cancer and wound healing. EMBO Rep 11: 97-105.
46. Wilkes JJ, Lloyd DJ, Gekakis N, (2009) Loss-of-function mutation in myostatin reduces tumor necrosis factor alpha production and protects liver against obesity-induced insulin resistance. Diabetes 58: 1133-1143.
47. Schleinitz D, Kloting N, Bottcher Y, Wolf S, Dietrich K, et al. (2011) Genetic and evolutionary analyses of the human bone morphogenetic protein receptor 2 (BMPR2) in the pathophysiology of obesity. PLoS One 6: e16155.
48. Dudas M, Sridurongrit S, Nagy A, Okazaki K, Kaartinen V, (2004) Craniofacial defects in mice lacking BMP type I receptor Alk2 in neural crest cells. Mech Dev 121: 173-182.
49. Deb K, Reese J, Paria BC, (2006) Methodologies to study implantation in mice. Methods Mol Med 121: 9-34.
50. Finn CA, Hinchliffe JR, (1964) Reaction of the Mouse Uterus during Implantation and Deciduoma Formation as Demonstrated by Changes in the Distribution of Alkaline Phosphatase. J Reprod Fertil 8: 331-338.