Rhesus monkey cumulus cells revert to a mural granulosa cell state after an ovulatory stimulus

Endocrinology

Volumn 153, Issue 11, 2012, Pages 5535-5545

  Chaffin, Charles L ^a   Lee, Young S ^b   VandeVoort, Catherine A ^c   Patel, Bela G ^b   Latham, Keith E ^b  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINANT CHORIONIC GONADOTROPIN; RECOMBINANT FOLLITROPIN; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CELL TYPE; CUMULUS CELL; FEMALE; GENE EXPRESSION; GRANULOSA CELL; NONHUMAN; OOCYTE; OVULATION INDUCTION; PHENOTYPE; PRIORITY JOURNAL; REPRODUCTION; RHESUS MONKEY;

ANIMALS; CELL DIFFERENTIATION; CHORIONIC GONADOTROPIN; CUMULUS CELLS; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION; GRANULOSA CELLS; MACACA MULATTA; OVARIAN FOLLICLE;

EID: 84867802039     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1733     Document Type: Article

References (43)

1. Su YQ, Sugiura K, Eppig JJ 2009 Mouse oocyte control of granulosa cell development and function: paracrine regulation of cumulus cell metabolism. Semin Reprod Med 27:32-42
2. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M 2004 EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303:682-684
3. Peluffo MC, Ting AY, Zamah AM, Conti M, Stouffer RL, Zelinski MB, Hennebold JD 2012 Amphiregulin promotes the maturation of oocytes isolated from the small antral follicles of the rhesus macaque. Hum Reprod 27:2430-2437
4. Conti M 2010 Signaling networks in somatic cells and oocytes activated during ovulation. Ann Endocrinol 71:189-190
5. Koike K, Watanabe H, Hiroi M, Tonosaki A 1993 Gap junction of stratum granulosum cells of mouse follicles: immunohistochemistry and electron microscopy. J Electron Microsc 42:94-106
6. Lenhart JA, Downey BR, Bagnell CA 1998 Connexin 43 gap junction protein expression during follicular development in the porcine ovary. Biol Reprod 58:583-590
7. Hernandez-Gonzalez I, Gonzalez-Robayna I, Shimada M, Wayne CM, Ochsner SA, White L, Richards JS 2006 Gene expression profiles of cumulus cell oocyte complexes during ovulation reveal cumulus cells express neuronal and immune-related genes: does this expand their role in the ovulation process? Mol Endocrinol 20: 1300-1321
8. Khamsi F, Roberge S 2001 Granulosa cells of the cumulus oophorus are different from mural granulosa cells in their response to gonadotrophins and IGF-I. J Endocrinol 170:565-573
9. Khamsi F, Roberge S 2001 Differential effects of insulin-like growth factor-I and gonadotropins on the proliferative activity of two subgroups of granulosa cells: cumulus oophorus and mural granulosa cells. Fert Steril 75:997-1003
10. Smitz JE, Thompson JG, Gilchrist RB 2011 The promise of in vitro maturation in assisted reproduction and fertility preservation. Semin Reprod Med 29:24-37
11. Lee YS, VandeVoort CA, Gaughan JP, Midic U, Obradovic Z, Latham KE 2011 Extensive effects of in vitro oocyte maturation on rhesus monkey cumulus cell transcriptome. Am J Physiol Endocrinol Metab 301:E196-E209
12. de Prada JK, Hill DL, Chaffin CL, VandeVoort CA 2009 Nuclear maturation and structural components of nonhuman primate cumulus-oocyte complexes during in vivo and in vitro maturation. Fert Steril 91:2043-2050
13. VandeVoort CA, Tarantal AF 1991 The macaque model for in vitro fertilization: superovulation techniques and ultrasound-guided follicular aspiration. J Med Primatol 20:110-116
14. VandeVoort CA, Tarantal AF 2001 Recombinant human gonadotropins for macaque superovulation: repeated stimulations and post-treatment pregnancies. J Med Primatol 30:304-307
15. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, Speed TP 2003 Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31:e15
16. Tusher VG, Tibshirani R, Chu G 2001 Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116-5121
17. Edgar R, Domrachev M, Lash AE 2002 Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30:207-210
18. Livak KJ, Schmittgen TD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-ΔΔC(T)) method. Methods 25:402-408
19. Pfaffl MW, Horgan GW, Dempfle L 2002 Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36
20. Lee YS, Latham KE, Vandevoort CA 2008 Effects of in vitro maturation on gene expression in rhesus monkey oocytes. Physiol Genomics 35:145-158
21. Fru KN, Cherian-Shaw M, Puttabyatappa M, VandeVoort CA, Chaffin CL 2007 Regulation of granulosa cell proliferation and EGF-like ligands during the periovulatory interval in monkeys. Hum Reprod 22:1247-1252
22. Nyholt de Prada JK, Lee YS, Latham KE, Chaffin CL, VandeVoort CA 2009 Role for cumulus cell-produced EGF-like ligands during primate oocyte maturation in vitro. Am J Physiol Endocrinol Metab 296:E1049-E1058
23. Chaffin CL, Schwinof KM, Stouffer RL 2001 Gonadotropin and steroid control of granulosa cell proliferation during the periovulatory interval in rhesus monkeys. Biol Reprod 65:755-762
24. Robker RL, Richards JS 1998 Hormone-induced proliferation and differentiation of granulosa cells: a coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1. Mol Endocrinol 12:924-940
25. Eppig JJ, Chesnel F, Hirao Y, O'Brien MJ, Pendola FL, Watanabe S, Wigglesworth K 1997 Oocyte control of granulosa cell development: how and why. Hum Reprod 12:127-132
26. Watson LN, Mottershead DG, Dunning KR, Robker RL, Gilchrist RB, Russell DL 2012 Heparan sulfate proteoglycans regulate responses to oocyte paracrine signals in ovarian follicle morphogenesis. Endocrinology 153:4544-4555
27. Diaz FJ, Wigglesworth K, Eppig JJ 2007 Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci 120:1330-1340
28. Eppig JJ, Wigglesworth K, Pendola F, Hirao Y 1997 Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biol Reprod 56:976-984
29. Duffy DM 2003 Growth differentiation factor-9 is expressed by the primate follicle throughout the periovulatory interval. Biol Reprod 69:725-732
30. Cannon JD, Cherian-Shaw M, Chaffin CL 2005 Proliferation of rat granulosa cells during the periovulatory interval. Endocrinology 146:414-422
31. Channing CP, Schaerf FW, Anderson LD, Tsafriri A 1980 Ovarian follicular and luteal physiology. Int Rev Physiol 22:117-201
32. Usanov SA, Chashchin VL 1991 Interaction of cytochrome P-450scc with cytochrome b5. FEBS Lett 278:279-282
33. Chaffin CL, Dissen GA, Stouffer RL 2000 Hormonal regulation of steroidogenic enzyme expression in granulosa cells during the periovulatory interval in monkeys. Mol Hum Reprod 6:11-18
34. Chaffin CL, Hess DL, Stouffer RL 1999 Dynamics of periovulatory steroidogenesis in the rhesus monkey follicle after ovarian stimulation. Hum Reprod 14:642-649
35. Cherian-Shaw M, Puttabyatappa M, Greason E, Rodriguez A, VandeVoort CA, Chaffin CL 2009 Expression of scavenger receptor-BI and low-density lipoprotein receptor and differential use of lipoproteins to support early steroidogenesis in luteinizing macaque granulosa cells. Endocrinology 150:957-965
36. Armstrong DT, Xia P, de Gannes G, Tekpetey FR, Khamsi F 1996 Differential effects of insulin-like growth factor-I and follicle-stimulating hormone on proliferation and differentiation of bovine cumulus cells and granulosa cells. Biol Reprod 54:331-338
37. Grupen CG, Armstrong DT 2010 Relationship between cumulus cell apoptosis, progesterone production and porcine oocyte developmental competence: temporal effects of follicular fluid during IVM. Reprod Fertil Dev 22:1100-1109
38. Svensson EC, Markstrom E, Shao R, Andersson M, Billig H 2001 Progesterone receptor antagonists Org 31710 and RU 486 increase apoptosis in human periovulatory granulosa cells. Fert Steril 76: 1225-1231
39. Jaiswal BS, Tur-Kaspa I, Dor J, Mashiach S, Eisenbach M 1999 Human sperm chemotaxis: is progesterone a chemoattractant? Biol Reprod 60:1314-1319
40. Xu F, Stouffer RL, Müller J, Hennebold JD, Wright JW, Bahar A, Leder G, Peters M, Thorne M, Sims M, Wintermantel T, Lindenthal B 2011 Dynamics of the transcriptome in the primate ovulatory follicle. Mol Hum Reprod 17:152-165
41. Carletti MZ, Christenson LK 2009 Rapid effects of LH on gene expression in the mural granulosa cells of mouse periovulatory follicles. Reproduction 137:843-855
42. Hirshfield AN 1986 Patterns of [3H] thymidine incorporation differ in immature rats and mature, cycling rats. Biol Reprod 34:229-235
43. Cannon JD, Cherian-Shaw M, Lovekamp-Swan T, Chaffin CL 2007 Granulosa cell expression of G1/S phase cyclins and cyclin-dependent kinases in PMSG-induced follicle growth. Mol Cell Endocrinol 264:6-15