Amphiregulin co-operates with bone morphogenetic protein 15 to increase bovine oocyte developmental competence: Effects on gap junction-mediated metabolite supply

Molecular Human Reproduction

Volumn 20, Issue 6, 2014, Pages 499-513

  Sugimura, Satoshi ^a,b   Ritter, Lesley J ^a   Sutton McDowall, Melanie L ^a   Mottershead, David G ^a   Thompson, Jeremy G ^a   Gilchrist, Robert B ^a,c  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^c UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Amphiregulin; BMP15; Cumulus oocyte complex; Gap junction; Metabolism

Indexed keywords

AMPHIREGULIN; BONE MORPHOGENETIC PROTEIN 15; COMPLEMENTARY DNA; GLUCOSE; LACTIC ACID; RNA; FOLLITROPIN; GLUCURONOSYLTRANSFERASE;

ANIMAL CELL; ARTICLE; AUTOFLUORESCENCE; BLASTOCYST; CATTLE; CELL COMMUNICATION; CONTROLLED STUDY; CUMULUS CELL; EMBRYO DEVELOPMENT; FEMALE; GAP JUNCTION; GENE SEQUENCE; GLYCOLYSIS; IN VITRO OOCYTE MATURATION; INNER CELL MASS; METABOLITE; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; BOVINAE; CELL CULTURE; COCULTURE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OOCYTE DEVELOPMENT; SIGNAL TRANSDUCTION;

AMPHIREGULIN; ANIMALS; BONE MORPHOGENETIC PROTEIN 15; CATTLE; CELL COMMUNICATION; CELLS, CULTURED; COCULTURE TECHNIQUES; CUMULUS CELLS; FEMALE; FOLLICLE STIMULATING HORMONE; GAP JUNCTIONS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GLUCOSE; GLUCURONOSYLTRANSFERASE; GLYCOLYSIS; IN VITRO OOCYTE MATURATION TECHNIQUES; LACTIC ACID; OOCYTES; OOGENESIS; SIGNAL TRANSDUCTION;

EID: 84900545042     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gau013     Document Type: Article

References (76)

1. Adriaenssens T, Wathlet S, Segers I, Verheyen G, De Vos A, Van der Elst J, Coucke W, Devroey P, Smitz J. Cumulus cell gene expression is associated with oocyte developmental quality and influenced by patient and treatment characteristics. Hum Reprod (Oxford, England) 2010;25:1259-1270.
2. 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.
3. Conti M, Hsieh M, Park JY, Su YQ. Role of the epidermal growth factor network in ovarian follicles. Mol Endocrinol (Baltimore, Md) 2006;20:715-723.
4. Crawford JL, McNatty KP. The ratio of growth differentiation factor 9: bone morphogenetic protein 15 mRNA expression is tightly co-regulated and differs between species over a wide range of ovulation rates. Mol Cell Endocrinol 2012;348:339-343.
5. Davis BJ, Lennard DE, Lee CA, Tiano HF, Morham SG, Wetsel WC, Langenbach R. Anovulation in cyclooxygenase-2-deficient mice is restored by prostaglandin E2 and interleukin-1beta. Endocrinology 1999;140:2685-2695.
6. de Matos DG, Furnus CC, Moses DF. Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol Reprod 1997;57:1420-1425.
7. Demeestere I, Streiff AK, Suzuki J, Al-Khabouri S, Mahrous E, Tan SL, Clarke HJ. Follicle-stimulating hormone accelerates mouse oocyte development in vivo. Biol Reprod 2012;87:1-11.
8. Donahue RP, Stern S. Follicular cell support of oocytematuration: production of pyruvate in vitro. J Reprod Fertil 1968;17:395-398.
9. Dong J, Albertini DF, Nishimori K, Kumar TR, Lu N, Matzuk MM. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996;383:531-535.
10. Downs SM, Chen J. EGF-like peptides mediate FSH-induced maturation of cumulus cell-enclosed mouse oocytes. Mol Reprod Dev 2008;75:105-114.
11. Dragovic RA, Ritter LJ, Schulz SJ, Amato F, Thompson JG, Armstrong DT, Gilchrist RB. Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol Reprod 2007;76:848-857.
12. 2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development (Cambridge, England) 2004;131:3057-3067.
13. Dumollard R, Ward Z, Carroll J, Duchen MR. Regulation of redox metabolism in the mouse oocyte and embryo. Development (Cambridge, England) 2007;134:455-465.
14. Eppig JJ. Oocyte control of ovarian follicular development and function in mammals. Reproduction (Cambridge, England) 2001;122:829-838.
15. Eppig JJ, Wigglesworth K, Pendola F, Hirao Y. Murine oocytes suppress expression of luteinizing hormone receptor messenger ribonucleic acid by granulosa cells. Biol Reprod 1997;56:976-984.
16. Eppig JJ, Pendola FL, Wigglesworth K, Pendola JK. Mouse oocytes regulate metabolic cooperativity between granulosa cells and oocytes: amino acid transport. Biol Reprod 2005;73:351-357.
17. Fulop C, Salustri A, Hascall VC. Coding sequence of a hyaluronan synthase homologue expressed during expansion of the mouse cumulus-oocyte complex. Arch Biochem Biophys 1997;337:261-266.
18. Fulop C, Szanto S, Mukhopadhyay D, Bardos T, Kamath RV, Rugg MS, Day AJ, Salustri A, Hascall VC, Glant TT et al. Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development (Cambridge, England) 2003;130:2253-2261.
19. Gerdin MJ, Eiden LE. Regulation of PC12 cell differentiation by cAMP signaling to ERK independent of PKA: do all the connections add up? Sci STKE 2007;2007:pe15.
20. Gilchrist RB, Ritter LJ. Differences in the participation of TGFB superfamily signalling pathways mediating porcine and murine cumulus cell expansion. Reproduction (Cambridge, England) 2011;142:647-657.
21. Gilchrist RB, Thompson JG. Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 2007;67:6-15.
22. Gilchrist RB, Ritter LJ, Armstrong DT. Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 2004;82-83:431-446.
23. Gilchrist RB, Ritter LJ, Myllymaa S, Kaivo-Oja N, Dragovic RA, Hickey TE, Ritvos O, Mottershead DG. Molecular basis of oocyte-paracrine signalling that promotes granulosa cell proliferation. J Cell Sci 2006;119:3811-3821.
24. Gilchrist RB, Lane M, Thompson JG. Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum Reprod Update 2008;14:159-177.
25. Granot I, Dekel N. Phosphorylation and expression of connexin-43 ovarian gap junction protein are regulated by luteinizing hormone. J BiolChem 1994;269:30502-9.
26. Hardy K, Handyside AH, Winston RM. The human blastocyst: cell number, death and allocation during late preimplantation development in vitro. Development (Cambridge, England) 1989;107:597-604.
27. Hsieh M, Lee D, Panigone S, Horner K, Chen R, Theologis A, Lee DC, Threadgill DW, Conti M. Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol 2007;27:1914-1924.
28. 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;118:5257-5268.
29. Hussein TS, Thompson JG, Gilchrist RB. Oocyte-secreted factors enhance oocyte developmental competence. Dev Biol 2006;296:514-521.
30. Laitinen M, Vuojolainen K, Jaatinen R, Ketola I, Aaltonen J, Lehtonen E, Heikinheimo M, Ritvos O. A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech Dev 1998;78:135-140.
31. Li R, Norman RJ, Armstrong DT, Gilchrist RB. Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol Reprod 2000;63:839-845.
32. Li Q, Miao DQ, Zhou P, Wu YG, Gao D, Wei DL, Cui W, Tan JH. Glucose metabolism in mouse cumulus cells prevents oocyte aging by maintaining both energy supply and the intracellular redox potential. Biol Reprod 2011;84:1111-1118.
33. Luciano AM, Modina S, Vassena R, Milanesi E, Lauria A, Gandolfi F. Role of intracellular cyclic adenosine 3',5'-monophosphate concentration and oocyte-cumulus cells communications on the acquisition of the developmental competence during in vitro maturation of bovine oocyte. Biol Reprod 2004;70:465-472.
34. McNatty KP, Smith P, Moore LG, Reader K, Lun S, Hanrahan JP, Groome NP, Laitinen M, Ritvos O, Juengel JL. Oocyte-expressed genes affecting ovulation rate. Mol Cell Endocrinol 2005;234:57-66.
35. Mottershead DG, Pulkki MM, Muggalla P, Pasternack A, Tolonen M, Myllymaa S, Korchynskyi O, Nishi Y, Yanase T, Lun S et al. Characterization of recombinant human growth differentiation factor-9 signaling in ovarian granulosa cells. Mol Cell Endocrinol 2008;283:58-67.
36. Mtango NR, Potireddy S, Latham KE. Oocyte quality and maternal control of development. Int Rev Cell Mol Biol 2008;268:223-290.
37. Norris RP, Freudzon M, Mehlmann LM, Cowan AE, Simon AM, Paul DL, Lampe PD, Jaffe LA. Luteinizing hormone causes MAP kinase-dependent phosphorylation and closure of connexin 43 gap junctions in mouse ovarian follicles: one of two paths to meiotic resumption. Development (Cambridge, England) 2008;135:3229-3238.
38. Norris RP, Freudzon M, Nikolaev VO, Jaffe LA. Epidermal growth factor receptor kinase activity is required for gap junction closure and for part of the decrease in ovarian follicle cGMP in response to LH. Reproduction (Cambridge, England) 2010;140:655-662.
39. Paradis F, Moore HS, Pasternak JA, Novak S, Dyck MK, Dixon WT, Foxcroft GR. Pig preovulatory oocytes modulate cumulus cell protein and gene expression in vitro. Mol Cell Endocrinol 2010;320:87-96.
40. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M. EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science (New York, NY) 2004;303:682-684.
41. Prochazka R, Petlach M, Nagyova E, Nemcova L. Effect of epidermal growth factor-like peptides on pig cumulus cell expansion, oocyte maturation, and acquisition of developmental competence in vitro: comparison with gonadotropins. Reproduction (Cambridge, England) 2011;141:425-435.
42. Prochazka R, Blaha M, Nemcova L. Signaling pathways regulating FSH- and amphiregulin-induced meiotic resumption and cumulus cell expansion in the pig. Reproduction (Cambridge, England) 2012;144:535-546.
43. Pulkki MM, Myllymaa S, Pasternack A, Lun S, Ludlow H, Al-Qahtani A, Korchynskyi O, Groome N, Juengel JL, Kalkkinen N et al. The bioactivity of human bone morphogenetic protein-15 is sensitive to C-terminal modification: characterization of the purified untagged processed mature region. Mol Cell Endocrinol 2011;332:106-115.
44. Pulkki MM, Mottershead DG, Pasternack AH, Muggalla P, Ludlow H, van Dinther M, Myllymaa S, Koli K, ten Dijke P, Laitinen M et al. A covalently dimerized recombinant human bone morphogenetic protein-15 variant identifies bone morphogenetic protein receptor type 1B as a key cell surface receptor on ovarian granulosa cells. Endocrinology 2012;153:1509-1518.
45. 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;42:248-253.
46. Regassa A, Rings F, Hoelker M, Cinar U, Tholen E, Looft C, Schellander K, Tesfaye D. Transcriptome dynamics and molecular cross-talk between bovine oocyte and its companion cumulus cells. BMC Genomics 2011;12:57.
47. Richani D, Ritter LJ, Thompson JG, Gilchrist RB. Mode of oocyte maturation affects EGF-like peptide function and oocyte competence. Mol Hum Reprod 2013;19:500-509.
48. Rilla K, Oikari S, Jokela TA, Hyttinen JM, Karna R, Tammi RH, Tammi MI. Hyaluronan synthase 1 (HAS1) requires higher cellular UDP-GlcNAc concentration than HAS2 and HAS3. J Biol Chem 2013;288:5973-5983.
49. Roberts R, Stark J, Iatropoulou A, Becker DL, Franks S, Hardy K. Energy substrate metabolism of mouse cumulus-oocyte complexes: response to follicle-stimulating hormone is mediated by the phosphatidylinositol 3-kinase pathway and is associated with oocyte maturation. Biol Reprod 2004;71:199-209.
50. Salustri A, Garlanda C, Hirsch E, De Acetis M, Maccagno A, Bottazzi B, Doni A, Bastone A, Mantovani G, Beck Peccoz P et al. PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development (Cambridge, England) 2004;131:1577-1586.
51. Sasseville M, Gagnon MC, Guillemette C, Sullivan R, Gilchrist RB, Richard FJ. Regulation of gap junctions in porcine cumulus-oocyte complexes: contributions of granulosa cell contact, gonadotropins, and lipid rafts. Mol Endocrinol (Baltimore, Md) 2009;23:700-710.
52. Sasseville M, Ritter LJ, Nguyen TM, Liu F, Mottershead DG, Russell DL, Gilchrist RB. Growth differentiation factor 9 signaling requires ERK1/2 activity in mouse granulosa and cumulus cells. J Cell Sci 2010;123:3166-3176.
53. Schelbach CJ, Kind KL, Lane M, Thompson JG. Mechanisms contributing to the reduced developmental competence of glucosamine-exposed mouse oocytes. Reprod Fertil Dev 2010;22:771-779.
54. Schelbach CJ, Robker RL, Bennett BD, Gauld AD, Thompson JG, Kind KL. Altered pregnancy outcomes in mice following treatment with the hyperglycaemia mimetic, glucosamine, during the periconception period. Reprod Fertil Dev 2013;25:405-416.
55. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS. Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol (Baltimore, Md) 2006;20:1352-1365.
56. Simpson CM, Stanton PG, Walton KL, Chan KL, Ritter LJ, Gilchrist RB, Harrison CA. Activation of latent human GDF9 by a single residue change (Gly 391 Arg) in the mature domain. Endocrinology 2012;153:1301-1310.
57. Sommersberg B, Bulling A, Salzer U, Frohlich U, Garfield RE, Amsterdam A, Mayerhofer A. Gap junction communication and connexin 43 gene expression in a rat granulosa cell line: regulation by follicle-stimulating hormone. Biol Reprod 2000;63:1661-1668.
58. Su YQ, Wu X, O'Brien MJ, Pendola FL, Denegre JN, Matzuk MM, Eppig JJ. 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;276:64-73.
59. Su YQ, Sugiura K, Wigglesworth K, O'Brien MJ, Affourtit JP, Pangas SA, Matzuk MM, Eppig JJ. Oocyte regulation of metabolic cooperativity between mouse cumulus cells and oocytes: BMP15 and GDF9 control cholesterol biosynthesis in cumulus cells. Development (Cambridge, England) 2008;135:111-121.
60. Su YQ, Sugiura K, Li Q, Wigglesworth K, Matzuk MM, Eppig JJ. Mouse oocytes enable LH-induced maturation of the cumulus-oocyte complex via promoting EGF receptor-dependent signaling. Mol Endocrinol (Baltimore, Md) 2010;24:1230-1239.
61. Sugimura S, Akai T, Hashiyada Y, Somfai T, Inaba Y, Hirayama M, Yamanouchi T, Matsuda H, Kobayashi S, Aikawa Y et al. Promising system for selecting healthy in vitro-fertilized embryos in cattle. PLoS One 2012;7:e36627.
62. Sugiura K, Su YQ, Diaz FJ, Pangas SA, Sharma S, Wigglesworth K, O'Brien MJ, Matzuk MM, Shimasaki S, Eppig JJ. Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development (Cambridge, England) 2007;134:2593-2603.
63. Sutovsky P, Flechon JE, Flechon B, Motlik J, Peynot N, Chesne P, Heyman Y. Dynamic changes of gap junctions and cytoskeleton during in vitro culture of cattle oocyte cumulus complexes. Biol Reprod 1993;49:1277-1287.
64. Sutton-McDowall ML, Mitchell M, Cetica P, Dalvit G, Pantaleon M, Lane M, Gilchrist RB, Thompson JG. Glucosamine supplementation during in vitro maturation inhibits subsequent embryo development: possible role of the hexosamine pathway as a regulator of developmental competence. Biol Reprod 2006;74:881-888.
65. Sutton-McDowall ML, Gilchrist RB, ThompsonJG. The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 2010;139:685-695.
66. Sutton-McDowall ML, Mottershead DG, Gardner DK, Gilchrist RB, Thompson JG. Metabolic differences in bovine cumulus-oocyte complexes matured in vitro in the presence or absence of folliclestimulating hormone and bone morphogenetic protein 15. Biol Reprod 2012;87:87.
67. Thomas RE, Armstrong DT, Gilchrist RB. Bovine cumulus cell-oocyte gap junctional communication during in vitro maturation in response to manipulation of cell-specific cyclic adenosine 3',5'-monophosophate levels. Biol Reprod 2004;70:548-556.
68. 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.
69. Veitch GI, Gittens JE, Shao Q, Laird DW, Kidder GM. Selective assembly of connexin37 into heterocellular gap junctions at the oocyte/granulosa cell interface. J Cell Sci 2004;117:2699-2707.
70. Wathlet S, Adriaenssens T, Segers I, Verheyen G, Van de Velde H, Coucke W, Ron El R, Devroey P, Smitz J. Cumulus cell gene expression predicts better cleavage-stage embryo or blastocyst development and pregnancy for ICSI patients. Hum Reprod (Oxford, England) 2011;26:1035-1051.
71. Wayne CM, Fan HY, Cheng X, Richards JS. Follicle-stimulating hormone induces multiple signaling cascades: evidence that activation of Rous sarcoma oncogene, RAS, and the epidermal growth factor receptor are critical for granulosa cell differentiation. Mol Endocrinol (Baltimore, Md) 2007;21:1940-1957.
72. Wert SE, Larsen WJ. Meiotic resumption and gap junction modulation in the cultured rat cumulus-oocyte complex. Gamete Res 1989;22:143-162.
73. Yamashita Y, Kawashima I, Yanai Y, Nishibori M, Richards JS, Shimada M. Hormone-induced expression of tumor necrosis factor alpha-converting enzyme/A disintegrin and metalloprotease-17 impacts porcine cumulus cell oocyte complex expansion and meiotic maturation via ligand activation of the epidermal growth factor receptor. Endocrinology 2007;148:6164-6175.
74. Yeo CX, Gilchrist RB, Thompson JG, Lane M. Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum Reprod (Oxford, England) 2008;23:67-73.
75. Yogo K, Ogawa T, Akiyama M, Ishida N, Takeya T. Identification and functional analysis of novel phosphorylation sites in Cx43 in rat primary granulosa cells. FEBS Lett 2002;531:132-136.
76. Yogo K, Ogawa T, Akiyama M, Ishida-Kitagawa N, Sasada H, Sato E, Takeya T. PKA implicated in the phosphorylation of Cx43 induced by stimulation with FSH in rat granulosa cells. J Reprod Dev 2006;52:321-328.