Heparan sulfate proteoglycans regulate responses to oocyte paracrine signals in ovarian follicle morphogenesis

Endocrinology

Volumn 153, Issue 9, 2012, Pages 4544-4555

  Watson, Laura N ^a   Mottershead, David G ^a   Dunning, Kylie R ^a   Robker, Rebecca L ^a   Gilchrist, Robert B ^a   Russell, Darryl L ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLESTEROL MONOOXYGENASE (SIDE CHAIN CLEAVING); CHORIONIC GONADOTROPIN; GLYPICAN; GLYPICAN 1; GLYPICAN 6; GROWTH DIFFERENTIATION FACTOR 9; HAS2 PROTEIN; HEPARIN; LHCGR PROTEIN; PROTEOHEPARAN SULFATE; SMAD2 PROTEIN; SYNDECAN 1; SYNDECAN 4; TNFAIP6 PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL FUNCTION; CELL MATURATION; CONTROLLED STUDY; CUMULUS CELL; FEMALE; GENE; GENE EXPRESSION; GRANULOSA CELL; IN VITRO STUDY; MORPHOGENESIS; MOUSE; NONHUMAN; OOCYTE; OVARY FOLLICLE; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; REGULATORY MECHANISM; UPREGULATION;

ANIMALS; BENZAMIDES; DIOXOLES; FEMALE; GROWTH DIFFERENTIATION FACTOR 9; HEPARAN SULFATE PROTEOGLYCANS; MICE; MORPHOGENESIS; OOCYTES; OVARIAN FOLLICLE; POLYMERASE CHAIN REACTION;

EID: 84865431102     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2012-1181     Document Type: Article

References (53)

1. 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 (Pubitemid 38141636)
2. Russell DL, Robker RL 2007 Molecular mechanisms of ovulation: co-ordination through the cumulus complex. Hum Reprod Update 13:289-312 (Pubitemid 47061635)
3. Diaz FJ, Wigglesworth K, Eppig JJ 2007 Oocytes determine cumulus cell lineage in mouse ovarian follicles. J Cell Sci 120:1330-1340 (Pubitemid 46780026)
4. Li R, Norman RJ, Armstrong DT, Gilchrist RB 2000 Oocyte-secreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol Reprod 63:839-845 (Pubitemid 30662057)
5. Elvin JA, Yan C, Wang P, Nishimori K, Matzuk MM 1999 Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol Endocrinol 13:1018-1034 (Pubitemid 30645318)
6. Sugiura K, Su YQ, Diaz FJ, Pangas SA, Sharma S, Wigglesworth K, O'Brien MJ, Matzuk MM, Shimasaki S, Eppig JJ 2007 Oocyte-derived BMP15 and FGFs cooperate to promote glycolysis in cumulus cells. Development 134:2593-2603 (Pubitemid 47225956)
7. Sugiura K, Su YQ, Li Q, Wigglesworth K, Matzuk MM, Eppig JJ 2010 Estrogen promotes the development of mouse cumulus cells in coordination with oocyte-derived GDF9 and BMP15. Mol Endocrinol 24:2303-2314
8. Elvin JA, Clark AT, Wang P, Wolfman NM, Matzuk MM 1999 Paracrine actions of growth differentiation factor-9 in the mammalian ovary. Mol Endocrinol 13:1035-1048 (Pubitemid 30645319)
9. Zhang M, Su YQ, Sugiura K, Xia G, Eppig JJ 2010 Granulosa cell ligand NPPC and its receptor NPR2 maintain meiotic arrest in mouse oocytes. Science 330:366-369
10. Sugiura K, Pendola FL, Eppig JJ 2005 Oocyte control of metabolic cooperativity between oocytes and companion granulosa cells: energy metabolism. Dev Biol 279:20-30 (Pubitemid 40222166)
11. Eppig JJ, Pendola FL, Wigglesworth K 1998 Mouseoocytes suppress cAMP-induced expression of LH receptor mRNA by granulosa cells in vitro. Mol Reprod Dev 49:327-332 (Pubitemid 28080167)
12. Diaz FJ, Sugiura K, Eppig JJ 2008 Regulation of Pcsk6 expression during the preantral to antral follicle transition in mice: opposing roles of FSH and oocytes. Biol Reprod 78:176-183
13. Vanderhyden BC, Telfer EE, Eppig JJ 1992 Mouse oocytes promote proliferation of granulosa cells from preantral and antral follicles in vitro. Biol Reprod 46:1196-1204
14. Gilchrist RB, Ritter LJ, Myllymaa S, Kaivo-Oja N, Dragovic RA, Hickey TE, Ritvos O, Mottershead DG 2006 Molecular basis of oocyte-paracrine signalling that promotes granulosa cell proliferation. J Cell Sci 119:3811-3821 (Pubitemid 44614433)
15. Häcker U, Nybakken K, Perrimon N 2005 Heparan sulphate proteoglycans: the sweet side of development. Nat Rev Mol Cell Biol 6:530-541 (Pubitemid 40943044)
16. Belenkaya TY, Han C, Yan D, Opoka RJ, Khodoun M, Liu H, Lin X 2004 Drosophila Dpp morphogen movement is independent of dynamin-mediated endocytosis but regulated by the glypican members of heparan sulfate proteoglycans. Cell 119:231-244 (Pubitemid 39360905)
17. Lyon M, Rushton G, Gallagher JT 1997 The interaction of the transforming growth factor-βs with heparin/heparan sulfate is isoform-specific. J Biol Chem 272:18000-18006 (Pubitemid 27306378)
18. Li S, Shimono C, Norioka N, Nakano I, Okubo T, Yagi Y, Hayashi M, Sato Y, Fujisaki H, Hattori S, Sugiura N, Kimata K, Sekiguchi K 2010 Activin A binds to perlecan through its pro-region that has heparin/heparan sulfate binding activity. J Biol Chem 285:36645-36655
19. Ohkawara B, Iemura S, ten Dijke P, Ueno N 2002 Action range of BMP is defined by its N-terminal basic amino acid core. Curr Biol 12:205-209 (Pubitemid 34122375)
20. Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J, Zako M 1999 Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem 68:729-777 (Pubitemid 29449208)
21. Shah MM, Sakurai H, Gallegos TF, Sweeney DE, Bush KT, Esko JD, Nigam SK 2011 Growth factor-dependent branching of the ureteric bud is modulated by selective 6-O sulfation of heparan sulfate. Dev Biol 356:19-27
22. Shah MM, Sakurai H, Sweeney DE, Gallegos TF, Bush KT, Esko JD, Nigam SK 2010 Hs2st mediated kidney mesenchyme induction regulates early ureteric bud branching. Dev Biol 339:354-365
23. Patel VN, Likar KM, Zisman-Rozen S, Cowherd SN, Lassiter KS, Sher I, Yates EA, Turnbull JE, Ron D, Hoffman MP 2008 Specific heparan sulfate structures modulate FGF10-mediated submandibular gland epithelial morphogenesis and differentiation. J BiolChem 283:9308-9317
24. Casu B, Naggi A, Torri G 2010 Heparin-derived heparan sulfate mimics to modulate heparan sulfate-protein interaction in inflammation and cancer. Matrix Biol 29:442-452
25. Iozzo RV 1998 Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67:609-652 (Pubitemid 28411140)
26. Eppig JJ 1981 Ovarian glycosaminoglycans: evidence for a role in regulating the response of the oocyte-cumulus cell complex to FSH. Endocrinology 108:1992-1994 (Pubitemid 12196320)
27. Downs SM 1989 Specificity of epidermal growth factor action on maturation of the murine oocyte and cumulus oophorus in vitro. Biol Reprod 41:371-379 (Pubitemid 19273630)
28. Mottershead DG, Pulkki MM, Muggalla P, Pasternack A, Tolonen M, Myllymaa S, Korchynskyi O, Nishi Y, Yanase T, Lun S, Juengel JL, Laitinen M, Ritvos O 2008 Characterization of recombinant human growth differentiation factor-9 signaling in ovarian granulosa cells. Mol Cell Endocrinol 283:58-67
29. Pulkki MM, Myllymaa S, Pasternack A, Lun S, Ludlow H, Al-Qahtani A, Korchynskyi O, Groome N, Juengel JL, Kalkkinen N, Laitinen M, Ritvos O, Mottershead DG 2011 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 332:106-115
30. Hussein TS, Thompson JG, Gilchrist RB 2006 Oocyte-secreted factors enhance oocyte developmental competence. Dev Biol 296:514-521 (Pubitemid 44189356)
31. Yeo CX, Gilchrist RB, Thompson JG, Lane M 2008 Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum Reprod 23:67-73 (Pubitemid 351767304)
32. Dragovic RA, Ritter LJ, Schulz SJ, Amato F, Thompson JG, Armstrong DT, Gilchrist RB 2007 Oocyte-secreted factor activation of SMAD 2/3 signaling enables initiation of mouse cumulus cell expansion. Biol Reprod 76:848-857 (Pubitemid 46651226)
33. Mottershead DG, Ritter LJ, Gilchrist RB 2012 Signalling pathways mediating specific synergistic interactions between GDF9 and BMP15. Mol Hum Reprod 18:121-128
34. Asada M, Shinomiya M, Suzuki M, Honda E, Sugimoto R, Ikekita M, Imamura T 2009 Glycosaminoglycan affinity of the complete fibroblast growth factor family. Biochim Biophys Acta 1790:40-48
35. 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 (Pubitemid 27150428)
36. Fannon M, Forsten KE, Nugent MA 2000 Potentiation and inhibition of bFGF binding by heparin: a model for regulation of cellular response. Biochemistry 39:1434-1445 (Pubitemid 30090713)
37. Yan C, Wang P, DeMayo J, DeMayo FJ, Elvin JA, Carino C, Prasad SV, Skinner SS, Dunbar BS, Dube JL, Celeste AJ, Matzuk MM 2001 Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol Endocrinol 15:854-866 (Pubitemid 32510635)
38. Harrison CA, Al-Musawi SL, Walton KL 2011 Prodomains regulate the synthesis, extracellular localisation and activity of TGF-β superfamily ligands. Growth Factors 29:174-186
39. Borg N, Holland M 2008 The effect of glycosaminoglycans on rat gametes in vitro and the associated signal pathway. Reproduction 135:311-319 (Pubitemid 351405037)
40. Yokoo M, Kimura N, Sato E 2010 Induction of oocyte maturation by hyaluronan-CD44 interaction in pigs. J Reprod Dev 56:15-19
41. Tanaka SS, Kojima Y, Yamaguchi YL, Nishinakamura R, Tam PP 2011 Impact of WNT signaling on tissue lineage differentiation in the early mouse embryo. Dev Growth Differ 53:843-856
42. Li F, Shi W, Capurro M, Filmus J 2011 Glypican-5 stimulates rhabdomyosarcoma cell proliferation by activating Hedgehog signaling. J Cell Biol 192:691-704
43. Hempel N, How T, Dong M, Murphy SK, Fields TA, Blobe GC 2007 Loss of betaglycan expression in ovarian cancer: role in motility and invasion. Cancer Res 67:5231-5238 (Pubitemid 46997261)
44. Akison LK, Alvino ER, Dunning KR, Robker RL, Russell DL 2012 Transient invasive migration in mouse cumulus oocyte complexes induced at ovulation by luteinizing hormone. Biol Reprod 86:125
45. Farnworth PG, Wang Y, Escalona R, Leembruggen P, Ooi GT, Findlay JK 2007 Transforming growth factor-β blocks inhibin binding to different target cell types in a context-dependent manner through dual mechanisms involving betaglycan. Endocrinology 148:5355-5368 (Pubitemid 350012631)
46. Averbeck M, Gebhardt C, Anderegg U, Termeer C, Sleeman JP, Simon JC 2007 Switch in syndecan-1 and syndecan-4 expression controls maturation associated dendritic cell motility. Exp Dermatol 16:580-589 (Pubitemid 46958564)
47. Derksen PW, Keehnen RM, Evers LM, van Oers MH, Spaargaren M, Pals ST 2002 Cell surface proteoglycan syndecan-1 mediates hepatocyte growth factor binding and promotes Met signaling in multiple myeloma. Blood 99:1405-1410 (Pubitemid 34547098)
48. Matsuda K, Maruyama H, Guo F, Kleeff J, Itakura J, Matsumoto Y, Lander AD, Korc M 2001 Glypican-1 is overexpressed in human breast cancer and modulates the mitogenic effects of multiple heparin-binding growth factors in breast cancer cells. Cancer Res 61:5562-5569 (Pubitemid 32694943)
49. Guo Z, Wang Z 2009 The glypican Dally is required in the niche for the maintenance of germline stem cells and short-range BMP signaling in the Drosophila ovary. Development 136:3627-3635
50. Hayashi Y, Kobayashi S, Nakato H 2009 Drosophila glypicans regulate the germline stem cell niche. J Cell Biol 187:473-480
51. Li J, Kleeff J, Kayed H, Felix K, Penzel R, Büchler MW, Korc M, Friess H 2004 Glypican-1 antisense transfection modulates TGF-β-dependent signaling in Colo-357 pancreatic cancer cells. Biochem Biophys Res Commun 320:1148-1155 (Pubitemid 38916663)
52. Kayed H, Kleeff J, Keleg S, Jiang X, Penzel R, Giese T, Zentgraf H, Büchler MW, Korc M, Friess H 2006 Correlation of glypican-1 expression with TGF-β, BMP, and activin receptors in pancreatic ductal adenocarcinoma. Int J Oncol 29:1139-1148
53. Dunning KR, Lane M, Brown HM, Yeo C, Robker RL, Russell DL 2007 Altered composition of the cumulus-oocyte complex matrix during in vitro maturation of oocytes. Hum Reprod 22:2842-2850 (Pubitemid 351696813)