Acceleration of the Glycolytic Flux by Steroid Receptor Coactivator-2 Is Essential for Endometrial Decidualization

PLoS Genetics

Volumn 9, Issue 10, 2013, Pages

  Kommagani, Ramakrishna ^a   Szwarc, Maria M ^a   Kovanci, Ertug ^a   Gibbons, William E ^a   Putluri, Nagireddy ^a   Maity, Suman ^a   Creighton, Chad J ^a   Sreekumar, Arun ^a   DeMayo, Francesco J ^a   Lydon, John P ^a   O'Malley, Bert W ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTO 2 KINASE; ESTROGEN; NUCLEAR RECEPTOR COACTIVATOR 2; PROGESTERONE; PROLACTIN; SOMATOMEDIN BINDING PROTEIN 1; PFKFB3 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL DIVISION; CELL PROLIFERATION; CELL TRANSFORMATION; DECIDUALIZATION; ENDOMETRIUM; ENDOMETRIUM CELL; GLUCOSE METABOLISM; GLYCOLYSIS; HOMEOSTASIS; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; TRANSCRIPTION REGULATION; ABORTION, SPONTANEOUS; ANIMAL; BIOSYNTHESIS; CELL CULTURE; CYTOLOGY; DECIDUA; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NIDATION; PATHOLOGY; PREGNANCY; SIGNAL TRANSDUCTION; STROMA CELL;

ABORTION, SPONTANEOUS; ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; DECIDUA; EMBRYO IMPLANTATION; FEMALE; GENE EXPRESSION REGULATION; HUMANS; MICE; NUCLEAR RECEPTOR COACTIVATOR 2; PHOSPHOFRUCTOKINASE-2; PREGNANCY; SIGNAL TRANSDUCTION; STROMAL CELLS;

EID: 84887287834     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003900     Document Type: Article

References (62)

1. Carson DD, Bagchi I, Dey SK, Enders AC, Fazleabas AT, et al. (2000) Embryo implantation. Dev Biol 223: 217-237.
2. Norwitz ER, Schust DJ, Fisher SJ, (2001) Implantation and the survival of early pregnancy. N Engl J Med 345: 1400-1408.
3. Wilcox AJ, Baird DD, Weinberg CR, (1999) Time of implantation of the conceptus and loss of pregnancy. N Engl J Med 340: 1796-1799.
4. Cha J, Sun X, Dey SK, (2012) Mechanisms of implantation: strategies for successful pregnancy. Nat Med 18: 1754-1767.
5. Diedrich K, Fauser BC, Devroey P, Griesinger G, (2007) Evian Annual Reproduction Workshop G (2007) The role of the endometrium and embryo in human implantation. Hum Reprod Update 13: 365-377.
6. Strowitzki T, Germeyer A, Popovici R, von Wolff M, (2006) The human endometrium as a fertility-determining factor. Hum Reprod Update 12: 617-630.
7. Das SK, (2009) Cell cycle regulatory control for uterine stromal cell decidualization in implantation. Reproduction 137: 889-899.
8. Sroga JM, Ma X, Das SK, (2012) Developmental regulation of decidual cell polyploidy at the site of implantation. Front Biosci (Schol Ed) 4: 1475-1486.
9. Finn CA, Martin L, (1972) Endocrine control of the timing of endometrial sensitivity to a decidual stimulus. Biol Reprod 7: 82-86.
10. Xu J, Wu RC, O'Malley BW, (2009) Normal and cancer-related functions of the p160 steroid receptor co-activator (SRC) family. Nat Rev Cancer 9: 615-630.
11. Mukherjee A, Amato P, Allred DC, DeMayo FJ, Lydon JP, (2007) Steroid receptor coactivator 2 is required for female fertility and mammary morphogenesis: insights from the mouse, relevance to the human. Nucl Recept Signal 5: e011.
12. Mukherjee A, Soyal SM, Fernandez-Valdivia R, Gehin M, Chambon P, et al. (2006) Steroid receptor coactivator 2 is critical for progesterone-dependent uterine function and mammary morphogenesis in the mouse. Mol Cell Biol 26: 6571-6583.
13. Gregory CW, Wilson EM, Apparao KB, Lininger RA, Meyer WR, et al. (2002) Steroid receptor coactivator expression throughout the menstrual cycle in normal and abnormal endometrium. J Clin Endocrinol Metab 87: 2960-2966.
14. Condon JC, Jeyasuria P, Faust JM, Wilson JW, Mendelson CR, (2003) 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: 9518-9523.
15. Konno T, Graham AR, Rempel LA, Ho-Chen JK, Alam SM, et al. (2010) Subfertility linked to combined luteal insufficiency and uterine progesterone resistance. Endocrinology 151: 4537-4550.
16. Yin P, Lin Z, Reierstad S, Wu J, Ishikawa H, et al. (2010) Transcription factor KLF11 integrates progesterone receptor signaling and proliferation in uterine leiomyoma cells. Cancer Res 70: 1722-1730.
17. Chopra AR, Kommagani R, Saha P, Louet JF, Salazar C, et al. (2011) Cellular energy depletion resets whole-body energy by promoting coactivator-mediated dietary fuel absorption. Cell Metab 13: 35-43.
18. Chopra AR, Louet JF, Saha P, An J, Demayo F, et al. (2008) Absence of the SRC-2 coactivator results in a glycogenopathy resembling Von Gierke's disease. Science 322: 1395-1399.
19. York B, O'Malley BW, (2010) Steroid receptor coactivator (SRC) family: masters of systems biology. J Biol Chem 285: 38743-38750.
20. 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.
21. Franco HL, Dai D, Lee KY, Rubel CA, Roop D, et al. (2011) WNT4 is a key regulator of normal postnatal uterine development and progesterone signaling during embryo implantation and decidualization in the mouse. FASEB J 25: 1176-1187.
22. Huyen DV, Bany BM, (2011) Evidence for a conserved function of heart and neural crest derivatives expressed transcript 2 in mouse and human decidualization. Reproduction 142: 353-368.
23. 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.
24. 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.
25. Brosens JJ, Hayashi N, White JO, (1999) Progesterone receptor regulates decidual prolactin expression in differentiating human endometrial stromal cells. Endocrinology 140: 4809-4820.
26. Brosens JJ, Takeda S, Acevedo CH, Lewis MP, Kirby PL, et al. (1996) Human endometrial fibroblasts immortalized by simian virus 40 large T antigen differentiate in response to a decidualization stimulus. Endocrinology 137: 2225-2231.
27. DeBerardinis RJ, Lum JJ, Hatzivassiliou G, Thompson CB, (2008) The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab 7: 11-20.
28. Lunt SY, Vander Heiden MG, (2011) Aerobic glycolysis: meeting the metabolic requirements of cell proliferation. Annu Rev Cell Dev Biol 27: 441-464.
29. Vander Heiden MG, Cantley LC, Thompson CB, (2009) Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324: 1029-1033.
30. Vander Heiden MG, Lunt SY, Dayton TL, Fiske BP, Israelsen WJ, et al. (2011) Metabolic pathway alterations that support cell proliferation. Cold Spring Harb Symp Quant Biol 76: 325-334.
31. Metallo CM, Vander Heiden MG, (2013) Understanding metabolic regulation and its influence on cell physiology. Mol Cell 49: 388-398.
32. York B, Sagen JV, Tsimelzon A, Louet JF, Chopra AR, et al. (2013) Research resource: tissue- and pathway-specific metabolomic profiles of the steroid receptor coactivator (SRC) family. Mol Endocrinol 27: 366-380.
33. Louet JF, Chopra AR, Sagen JV, An J, York B, et al. (2010) The coactivator SRC-1 is an essential coordinator of hepatic glucose production. Cell Metab 12: 606-618.
34. Frolova AI, Moley KH, (2011) Quantitative analysis of glucose transporter mRNAs in endometrial stromal cells reveals critical role of GLUT1 in uterine receptivity. Endocrinology 152: 2123-2128.
35. Frolova AI, O'Neill K, Moley KH, (2011) Dehydroepiandrosterone inhibits glucose flux through the pentose phosphate pathway in human and mouse endometrial stromal cells, preventing decidualization and implantation. Mol Endocrinol 25: 1444-1455.
36. Hackl H, (1973) Metabolism of glucose in the human endometrium with special reference to fertility and contraception. Acta Obstet Gynecol Scand 52: 135-140.
37. von Wolff M, Ursel S, Hahn U, Steldinger R, Strowitzki T, (2003) Glucose transporter proteins (GLUT) in human endometrium: expression, regulation, and function throughout the menstrual cycle and in early pregnancy. J Clin Endocrinol Metab 88: 3885-3892.
38. Yalcin A, Telang S, Clem B, Chesney J, (2009) Regulation of glucose metabolism by 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatases in cancer. Exp Mol Pathol 86: 174-179.
39. Wu M, Neilson A, Swift AL, Moran R, Tamagnine J, et al. (2007) Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am J Physiol Cell Physiol 292: C125-136.
40. Clem B, Telang S, Clem A, Yalcin A, Meier J, et al. (2008) Small-molecule inhibition of 6-phosphofructo-2-kinase activity suppresses glycolytic flux and tumor growth. Mol Cancer Ther 7: 110-120.
41. Chesney J, (2006) 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase and tumor cell glycolysis. Curr Opin Clin Nutr Metab Care 9: 535-539.
42. Chesney J, Telang S, Yalcin A, Clem A, Wallis N, et al. (2005) Targeted disruption of inducible 6-phosphofructo-2-kinase results in embryonic lethality. Biochem Biophys Res Commun 331: 139-146.
43. Galassi L, (1968) Autoradiographic study of the decidual cell reaction in the rat. Dev Biol 17: 75-84.
44. Germeyer A, von Wolff M, Jauckus J, Strowitzki T, Sharma T, et al. (2010) Changes in cell proliferation, but not in vascularisation are characteristic for human endometrium in different reproductive failures-a pilot study. Reprod Biol Endocrinol 8: 67.
45. Moulton BC, Barker KL, (1974) Effects of 8-azaguanine on the induction of uterine glucose-6-phosphate dehydrogenase activity by estradiol or NADP plus. Proc Soc Exp Biol Med 146: 742-746.
46. Surani MA, Heald PJ, (1971) Changes in enzymes of carbohydrate metabolism in rat uterus during early pregnancy. Acta Endocrinol (Copenh) 68: 805-816.
47. Surani MA, Heald PJ, (1971) The metabolism of glucose by rat uterus tissue in early pregnancy. Acta Endocrinol (Copenh) 66: 16-24.
48. Hamilton JA, Callaghan MJ, Sutherland RL, Watts CKW, (1997) Identification of PRG1, a novel progestin-responsive gene with sequence homology to 6-phosphofructo-2-kinase/fructose-2, 6-bisphosphatase. Mol Endo 11: 490-502.
49. Novellasdemunt L, Obach M, Millan-Arino L, Manzano A, Ventura F, et al. Progestins activate 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase 3 (PFKFB3) in breast cancer cells. Biochem J 442: 345-356.
50. Atsumi T, Chesney J, Metz C, Leng L, Donnelly S, et al. (2002) High expression of inducible 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase (iPFK-2; PFKFB3) in human cancers. Cancer Res 62: 5881-5887.
51. Marotta LL, Almendro V, Marusyk A, Shipitsin M, Schemme J, et al. (2011) The JAK2/STAT3 signaling pathway is required for growth of CD44(+)CD24(-) stem cell-like breast cancer cells in human tumors. J Clin Invest 121: 2723-2735.
52. Minchenko A, Leshchinsky I, Opentanova I, Sang N, Srinivas V, et al. (2002) Hypoxia-inducible factor-1-mediated expression of the 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase-3 (PFKFB3) gene. Its possible role in the Warburg effect. J Biol Chem 277: 6183-6187.
53. Reddy MM, Fernandes MS, Deshpande A, Weisberg E, Inguilizian HV, et al. (2012) The JAK2V617F oncogene requires expression of inducible phosphofructokinase/fructose-bisphosphatase 3 for cell growth and increased metabolic activity. Leukemia 26: 481-489.
54. Rodriguez-Rodriguez P, Fernandez E, Almeida A, Bolanos JP, (2012) Excitotoxic stimulus stabilizes PFKFB3 causing pentose-phosphate pathway to glycolysis switch and neurodegeneration. Cell Death Differ 19: 1582-1589.
55. Telang S, Yalcin A, Clem AL, Bucala R, Lane AN, et al. (2006) Ras transformation requires metabolic control by 6-phosphofructo-2-kinase. Oncogene 25: 7225-7234.
56. Fukasawa M, Tsuchiya T, Takayama E, Shinomiya N, Uyeda K, et al. (2004) Identification and characterization of the hypoxia-responsive element of the human placental 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase gene. J Biochem 136: 273-277.
57. 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.
58. Gehin M, Mark M, Dennefeld C, Dierich A, Gronemeyer H, et al. (2002) The function of TIF2/GRIP1 in mouse reproduction is distinct from those of SRC-1 and p/CIP. Mol Cell Biol 22: 5923-5937.
59. WMA Declaration of Helsinki Serves as Guide to Physicians. Calif Med 105: 149-150.
60. Khokhar SK, Kommagani R, Kadakia MP, (2008) Differential effects of p63 mutants on transactivation of p53 and/or p63 responsive genes. Cell Res 18: 1061-1073.
61. Mukherjee A, Soyal SM, Li J, Ying Y, Szwarc MM, et al. (2011) A mouse transgenic approach to induce beta-catenin signaling in a temporally controlled manner. Transgenic Res 20: 827-840.
62. Putluri N, Shojaie A, Vasu VT, Nalluri S, Vareed SK, et al. Metabolomic profiling reveals a role for androgen in activating amino acid metabolism and methylation in prostate cancer cells. PLoS One 6: e21417.