Mouse oocyte control of granulosa cell development and function: Paracrine regulation of cumulus cell metabolism

Seminars in Reproductive Medicine

Volumn 27, Issue 1, 2009, Pages 32-42

  Su, You Qiang ^a   Sugiura, Koji ^a   Eppig, John J ^a  

^a JACKSON LABORATORY   (United States)

Author keywords

Cumulus cells; Metabolisms; Oocyte derived factors; Oocytes

Indexed keywords

AMINO ACID; BONE MORPHOGENETIC PROTEIN 15; CHOLESTEROL; FIBROBLAST GROWTH FACTOR 8; GLYCOGEN; GROWTH DIFFERENTIATION FACTOR 9;

AMINO ACID TRANSPORT; AUTOCRINE EFFECT; CELL MATURATION; CELL METABOLISM; CHOLESTEROL SYNTHESIS; CUMULUS CELL; GAP JUNCTION; GLYCOLYSIS; GRANULOSA CELL; NONHUMAN; OOCYTE; OVARY FOLLICLE DEVELOPMENT; PARACRINE SIGNALING; PROTEIN EXPRESSION; REVIEW;

ANIMALS; CELL DIFFERENTIATION; CUMULUS CELLS; FEMALE; GRANULOSA CELLS; MICE; MODELS, BIOLOGICAL; OOCYTES; PARACRINE COMMUNICATION;

EID: 61449115988     PISSN: 15268004     EISSN: 15264564     Source Type: Journal    
DOI: 10.1055/s-0028-1108008     Document Type: Review

References (99)

1. Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction 2001;122:829-838
2. Buccione R, Schroeder AC, Eppig JJ. Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol Reprod 1990;43:543-547
3. Eppig JJ, Viveiros MM, Marin Bivens C, De La Fuente R. Regulation of Mammalian Oocyte Maturation. In: Leung PCK, Adashi EY, eds. The Ovary. San Diego, CA: Elsevier Academic Press; 2004:113-129
4. Soyal SM, Amleh A, Dean J. FIGα, a germ cell-specific transcription factor required for ovarian follicle formation. Development 2000;127(21):4645-4654
5. Reddy P, Liu L, Adhikari D, et al. Oocyte-specific deletion of Pten causes premature activation of the primordial follicle pool. Science 2008;319(5863):611-613
6. Diaz FJ, Wigglesworth K, Eppig JJ. Oocytes are required for the preantral granulosa cell to cumulus cell transition in mice. Dev Biol 2007;305(1):300-311
7. Diaz FJ, Wigglesworth K, Eppig JJ. Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci 2007;120(Pt 8):1330-1340
8. Dong J, Albertini DF, Nishimori K, et al. Growth differentiation factor-9 is required during early ovarian folliculo-genesis. Nature 1996;383:531-535
9. Galloway SM, McNatty KP, Cambridge LM, et al. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat Genet 2000;25(3):279-283
10. Latham KE, Wigglesworth K, McMenamin M, Eppig JJ. Stage-dependent effects of oocytes and growth differentiation factor 9 on mouse granulosa cell development: advance programming and subsequent control of the transition from preantral secondary follicles to early antral tertiary follicles. Biol Reprod 2004;70(5):1253-1262
11. Orisaka M, Orisaka S, Jiang JY, et al. Growth differentiation factor 9 is antiapoptotic during follicular development from preantral to early antral stage. Mol Endocrinol 2006;20(10):2456-2468
12. Gilchrist RB, Morrissey MP, Ritter LJ, Armstrong DT. Comparison ofoocyte factors and transforming growth factor-beta in the regulation of DNA synthesis in bovine granulosa cells. Mol Cell Endocrinol 2003;201(1-2):87-95
13. Gilchrist RB, Ritter LJ, Armstrong DG. Growth-promoting activity of mouse oocytes is developmentally regulated. Biol Reprod 2000;62(suppl 1):422
14. Gilchrist RB, Ritter LJ, Armstrong DG. Mouse oocyte mitogenic activity is developmentally coordinated throughout folliculogenesis and meiotic maturation. Dev Biol 2001;240:289-298
15. Otsuka F, Moore RK, Wang X, et al. Essential role of the oocyte in estrogen amplification of follicle-stimulating hormone signaling in granulosa cells. Endocrinology 2005;146(8):3362-3367
16. Otsuka F, Yao Z, Lee T, et al. Bone morphogenetic protein-15. Identification of target cells and biological functions. J Biol Chem 2000;275(50):39523-39528
17. Vanderhyden BC, Telfer EE, Eppig JJ. Mouse oocytes promote proliferation of granulosa cells from preantral and antral follicles in vitro. Biol Reprod 1992;46:1196-1204
18. Vitt UA, Hayashi M, Klein C, Hsueh AJ. Growth differentiation factor-9 stimulates proliferation but suppresses the follicle-stimulating hormone-induced differentiation of cultured granulosa cells from small antral and preovulatory rat follicles. Biol Reprod 2000;62(2):370-377
19. Buccione R, Vanderhyden BC, Caron PJ, Eppig JJ. FSH-induced expansion of the mouse cumulus oophorus in vitro is dependent upon a specific factor(s) secreted by the oocyte. Dev Biol 1990;138:16-25
20. Dragovic RA, Ritter LJ, Schulz SJ, et al. Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol Reprod 2007;76(5):848-857
21. Joyce IM, Pendola FL, O'Brien M, Eppig JJ. Regulation of prostaglandin-endoperoxide synthase 2 messenger ribonucleic acid expression in mouse granulosa cells during ovulation. Endocrinology 2001;142(7):3187-3197
22. Su YQ, Wigglesworth K, Pendola FL, O'Brien MJ, Eppig JJ. Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. Endocrinology 2002;143(6):2221-2232
23. Su YQ, Wu X, O'Brien MJ, et al. Synergistic roles of BMP15 and GDF9 in the development and function of the oocyte-cumulus cell complex in mice: genetic evidence for an oocyte- granulosa cell regulatory loop. Dev Biol 2004;276(1): 64-73
24. Vanderhyden BC, Caron PJ, Buccione R, Eppig JJ. Developmental pattern of the secretion of cumulus-expansion enabling factor by mouse oocytes and the role of oocytes in promoting granulosa cell differentiation. Dev Biol 1990;140: 307-317
25. Eppig JJ, Wigglesworth K, Pendola FL. The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc Natl Acad Sci U S A 2002;99:2890-2894
26. Anderson E, Albertini DF. Gap junctions between the oocyte and companion follicle cells in the mammalian ovary. J Cell Biol 1976;71:680-686
27. Albertini DF, Combelles CMH, Benecchi E, Carabatsos MJ. Cellular basis for paracrine regulation of ovarian follicle development. Reproduction 2001;121(5):647-653
28. Ackert CL, Gittens JE, O'Brien MJ, Eppig JJ, Kidder GM. Intercellular communication via connexin43 gap junctions is required for ovarian folliculogenesis in the mouse. Dev Biol 2001;233(2):258-270
29. Juneja SC, Barr KJ, Enders GC, Kidder GM. Defects in the germ line and gonads of mice lacking connexin43. Biol Reprod 1999;60(5):1263-1270
30. Simon AM, Goodenough DA, Li E, Paul DL. Female infertility in mice lacking connexin 37. Nature 1997;385(6616):525-529
31. Gittens JE, Kidder GM. Differential contributions of connexin37 and connexin43 to oogenesis revealed in chimeric reaggregated mouse ovaries. J Cell Sci 2005;118(Pt 21):5071-5078
32. Gershon E, Plaks V, Aharon I, et al. Oocyte-directed depletion of connexin43 using the Cre-LoxP system leads to subfertility in female mice. Dev Biol 2008;313(1):1-12
33. Li TY, Colley D, Barr KJ, Yee SP, Kidder GM. Rescue of oogenesis in Cx37-null mutant mice by oocyte-specific replacement with Cx43. J Cell Sci 2007;120(Pt 23):4117-4125
34. Paladino G. I ponti intercellulari tra l'uovo ovarico e le cellule follicolari e la formazione della zona pellucida. Anat Anz 1890;15:254-259
35. Biggers JD, Whittingham DG, Donahue RP. The pattern of energy metabolism in the mouse oocyte and zygote. Proc Natl Acad Sci U S A 1967;58:560-567
36. Donahue RP, Stern S. Follicular cell support of oocyte maturation: production of pyruvate in vitro. J Reprod Fertil 1968;17(2):395-398
37. Leese HJ, Barton AM. Production of pyruvate by isolated mouse cumulus cells. J Exp Zool 1985;234(2):231-236
38. Herubel F, El Mouatassim S, Guerin P, Frydman R, Menezo Y. Genetic expression of monocarboxylate transporters during human and murine oocyte maturation and early embryonic development. Zygote 2002;10(2):175-181
39. Brinster RL. Oxidation of pyruvate and glucose by oocytes of the mouse and rhesus monkey. J Reprod Fertil 1971;24(2):187-191
40. Eppig JJ. Analysis of mouse oogenesis in vitro. Oocyte isolation and the utilization of exogenous energy sources by growing oocytes. J Exp Zool 1976;198:375-386
41. Downs SM, Humpherson PG, Leese HJ. Pyruvate utilization by mouse oocytes is influenced by meiotic status and the cumulus oophorus. Mol Reprod Dev 2002;62(1):113-123
42. Johnson MT, Freeman EA, Gardner DK, Hunt PA. Oxidative metabolism of pyruvate is required for meiotic maturation of murine oocytes in vivo. Biol Reprod 2007;77(1):2-8
43. Sugiura K, Pendola FL, Eppig JJ. Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev Biol 2005;279(1):20-30
44. Tsutsumi O, Satoh K, Taketani Y, Kato T. Determination of enzyme activities of energy metabolism in the maturing rat oocyte. Mol Reprod Dev 1992;33(3):333-337
45. Cetica P, Pintos L, Dalvit G, Beconi M. Activity of key enzymes involved in glucose and triglyceride catabolism during bovine oocyte maturation in vitro. Reproduction 2002;124(5):675-681
46. Rieger D, Loskutoff NM. Changes in the metabolism of glucose, pyruvate, glutamine and glycine during maturation of cattle oocytes in vitro. J Reprod Fertil 1994;100(1):257-262
47. Rushmer RA, Brinster RL. Carbon dioxide production from pyruvate and glucose by bovine oocytes. Exp Cell Res 1973;82(2):252-254
48. Tsutsumi O, Yano T, Satoh K, Mizuno M, Kato T. Studies of hexokinase activity in human and mouse oocyte. Am J Obstet Gynecol 1990;162(5):1301-1304
49. Dworkin MB, Dworkin-Rastl E. Carbon metabolism in early amphibian embryos. Trends Biochem Sci 1991;16(6):229-234
50. Eppig JJ, Steckman ML. Comparison of exogenous energy sources for in vitro maintenance of follicle cell-free Xenopus laevis oocytes. In Vitro 1976;12(3):173-179
51. Colonna R, Mangia F. Mechanisms of amino acid uptake in cumulus-enclosed mouse oocytes. Biol Reprod 1983;28:797-803
52. Eppig JJ, Pendola FL, Wigglesworth K, Pendola JK. Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport. Biol Reprod 2005;73(2):351-357
53. Su YQ, Sugiura K, Wigglesworth K, et al. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development 2008;135(1):111-121
54. Sato N, Kawamura K, Fukuda J, et al. Expression of LDL receptor and uptake of LDL in mouse preimplantation embryos. Mol Cell Endocrinol 2003;202(1-2):191-194
55. Trigatti B, Rayburn H, Vinals M, et al. Influence of the high density lipoprotein receptor SR-BI on reproductive and cardiovascular pathophysiology. Proc Natl Acad Sci U S A 1999;96(16):9322-9327
56. Li X, Peegel H, Menon KM. In situ hybridization of high density lipoprotein (scavenger, type 1) receptor messenger ribonucleic acid (mRNA) during folliculogenesis and lutei-nization: evidence for mRNA expression and induction by human chorionic gonadotropin specifically in cell types that use cholesterol for steroidogenesis. Endocrinology 1998;139(7):3043-3049
57. Miettinen HE, Rayburn H, Krieger M. Abnormal lipoprotein metabolism and reversible female infertility in HDL receptor (SR-BI)-deficient mice. J Clin Invest 2001;108(11):1717-1722
58. Perret BP, Parinaud J, Ribbes H, et al. Lipoprotein and phospholipid distribution in human follicular fluids. Fertil Steril 1985;43(3):405-409
59. Simpson ER, Rochelle DB, Carr BR, MacDonald PC. Plasma lipoproteins in follicular fluid of human ovaries. J Clin Endocrinol Metab 1980;51(6):1469-1471
60. Ishibashi S, Brown MS, Goldstein JL, et al. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J Clin Invest 1993;92(2):883-893
61. Sugiura K, Eppig JJ. Control of metabolic cooperativity between oocytes and their companion granulosa cells by mouse oocytes. Reprod Fertil Dev 2005;17(7):667-674
62. Zuelke KA, Brackett BG. Effects of luteinizing hormone on glucose metabolism in cumulus-enclosed bovine oocytes matured in vitro. Endocrinology 1992;131(6):2690-2696
63. Sutton ML, Cetica PD, Beconi MT, et al. Influence of oocyte-secreted factors and culture duration on the metabolic activity of bovine cumulus cell complexes. Reproduction 2003;126(1):27-34
64. Gilchrist RB, Ritter LJ, Armstrong DT. Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 2004;82-83:431-446
65. Ralph JH, Telfer EE, Wilmut I. Bovine cumulus cell expansion does not depend on the presence of an oocyte secreted factor. Mol Reprod Dev 1995;42(2):248-253
66. Juengel JL, McNatty KP. The role of proteins of the transforming growth factor-beta superfamily in the intra- ovarian regulation of follicular development. Hum Reprod Update 2005;11(2):143-160
67. Dube JL, Wang P, Elvin J, et al. The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol Endocrinol 1998;12(12):1809-1817
68. McGrath SA, Esquela AF, Lee SJ. Oocyte-specific expression of growth differentiation factor-9. Mol Endocrinol 1995;9(1):131-136
69. McPherron AC, Lee SJ. GDF-3 and GDF-9: two new members of the transforming growth factor-beta superfamily containing a novel pattern of cysteines. J Biol Chem 1993;268(5):3444-3449
70. Elvin JA, Yan CN, Wang P, Nishimori K, Matzuk MM. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol Endocrinol 1999;13(6):1018-1034
71. Yan C, Wang P, DeMayo J, et al. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 2001;15(6):854-866
72. Bodin L, Di Pasquale E, Fabre S, et al. A novel mutation in the bone morphogenetic protein 15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in Lacaune sheep. Endocrinology 2007;148(1):393-400
73. Juengel JL, Hudson NL, Heath DA, et al. Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol Reprod 2002;67(6):1777-1789
74. Chand AL, Ponnampalam AP, Harris SE, Winship IM, Shelling AN. Mutational analysis of BMP15 and GDF9 as candidate genes for premature ovarian failure. Fertil Steril 2006;86(4):1009-1012
75. Di Pasquale E, Rossetti R, Marozzi A, et al. Identification of new variants of human BMP15 gene in a large cohort of women with premature ovarian failure. J Clin Endocrinol Metab 2006;91(5):1976-1979
76. Dixit H, Rao LK, Padmalatha VV, et al. Missense mutations in the BMP15 gene are associated with ovarian failure. Hum Genet 2006;119(4):408-415
77. Palmer JS, Zhao ZZ, Hoekstra C, et al. Novel variants in growth differentiation factor 9 in mothers of dizygotic twins. J Clin Endocrinol Metab 2006;91(11):4713-4716
78. Gueripel X, Brun V, Gougeon A. Oocyte bone morphoge-netic protein 15, but not growth differentiation factor 9, is increased during gonadotropin-induced follicular development in the immature mouse and is associated with cumulus oophorus expansion. Biol Reprod 2006;75(6):836-843
79. Yoshino O, McMahon HE, Sharma S, Shimasaki S. A unique preovulatory expression pattern plays a key role in the physiological functions of BMP-15 in the mouse. Proc Natl Acad Sci U S A 2006;103(28):10678-10683
80. McMahon HE, Hashimoto O, Mellon PL, Shimasaki S. Oocyte-specific overexpression of mouse BMP-15 leads to accelerated folliculogenesis and an early onset of acyclicity in transgenic mice. Endocrinology 2008;149(6):2807- 2815
81. Sugiura K, Su YQ, Diaz FJ, et al. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 2007;134(14):2593-2603
82. Buratini J Jr, Teixeira AB, Costa IB, et al. Expression of fibroblast growth factor-8 and regulation of cognate receptors, fibroblast growth factor receptor-3c and -4, in bovine antral follicles. Reproduction 2005;130(3):343-350
83. Valve E, Penttila TL, Paranko J, Harkonen P. FGF-8 is expressed during specific phases of rodent oocyte and spermatogonium development. Biochem Biophys Res Com-mun 1997;232(1):173-177
84. van Wezel IL, Umapathysivam K, Tilley WD, Rodgers RJ. Immunohistochemical localization of basic fibroblast growth factor in bovine ovarian follicles. Mol Cell Endocrinol 1995;115(2):133-140
85. Tamura H, Takasaki A, Miwa I, et al. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res 2008;44(3):280-287
86. Ito Y, Kihara M, Nakamura E, Yonezawa S, Yoshizaki N. Vitellogenin transport and yolk formation in the quail ovary. Zoolog Sci 2003;20(6):717-726
87. Monaco ME, Villecco EI, Sanchez SS. Implication of gap junction coupling in amphibian vitellogenin uptake. Zygote 2007;15(2):149-157
88. Waksmonski SL, Woodruff RI. For uptake of yolk precursors, epithelial cell-oocyte gap junctional communication is required by insects representing six different orders. J Insect Physiol 2002;48(6):667-675
89. Kayampilly PP, Menon KM. Follicle-stimulating hormone increases tuberin phosphorylation and mammalian target of rapamycin signaling through an extracellular signal-regulated kinase-dependent pathway in rat granulosa cells. Endocrinology 2007;148(8):3950-3957
90. Yaba A, Bianchi V, Borini A, Johnson J. A putative mitotic checkpoint dependent on mTOR function controls cell proliferation and survival in ovarian granulosa cells. Reprod Sci 2008;15(2):128-138
91. Alam H, Maizels ET, Park Y, et al. Follicle-stimulating hormone activation of hypoxia-inducible factor-1 by the phosphatidylinositol 3-kinase/AKT/Ras homolog enriched in brain (Rheb)/mammalian target of rapamycin (mTOR) path-way is necessary for induction of select protein markers of follicular differentiation. J Biol Chem 2004;279(19): 19431-19440
92. Chen YJ, Hsiao PW, Lee MT, et al. Interplay of PI3K and cAMP/PKA signaling, and rapamycin-hypersensitivity in TGFbeta1 enhancement of FSH-stimulated steroidogenesis in rat ovarian granulosa cells. J Endocrinol2007;192(2):405-419
93. Hunzicker-Dunn M, Maizels ET. FSH signaling pathways in immature granulosa cells that regulate target gene expression: branching out from protein kinase A. Cell Signal 2006;18(9):1351-1359
94. Hussein TS, Froiland DA, Amato F, Thompson JG, Gilchrist RB. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J Cell Sci 2005;118(Pt 22):5257-5268
95. Rung E, Friberg PA, Bergh C, Billig H. Depletion of substrates for protein prenylation increases apoptosis in human periovulatory granulosa cells. Mol Reprod Dev 2006;73(10):1277-1283
96. Rung E, Friberg PA, Shao R, et al. Progesterone-receptor antagonists and statins decrease de novo cholesterol synthesis and increase apoptosis in rat and human periovula-tory granulosa cells in vitro. Biol Reprod 2005;72(3):538-545
97. Johnson J, Espinoza T, McGaughey RW, Rawls A, Wilson-Rawls J. Notch pathway genes are expressed in mammalian ovarian follicles. Mech Dev 2001;109(2):355-361
98. Pan H, O'Brien MJ, Wigglesworth K, Eppig JJ, Schultz RM. Transcript profiling during mouse oocyte development and the effect of gonadotropin priming and development in vitro. Dev Biol 2005;286(2):493-506
99. Russell MC, Cowan RG, Harman RM, Walker AL, Quirk SM. The hedgehog signaling pathway in the mouse ovary. Biol Reprod 2007;77(2):226-236