Periovulatory expression of hyaluronan and proteoglycan link protein 1 (Hapln1) in the rat ovary: Hormonal regulation and potential function

Molecular Endocrinology

Volumn 24, Issue 6, 2010, Pages 1203-1217

  Liu, Jing ^a,b   Park, Eun Sil ^a   Curry Jr , Thomas E ^a   Jo, Misung ^a  

^a UNIVERSITY OF KENTUCKY MEDICAL CENTER   (United States)

^b ZHEJIANG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CHORIONIC GONADOTROPIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; EPIDERMAL GROWTH FACTOR; GONADOTROPIN; HYALURONAN AND PROTEOGLYCAN LINK PROTEIN 1; LUTEINIZING HORMONE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL KINASE; PROSTAGLANDIN; PROTEOGLYCAN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR RUNX2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL SURVIVAL; CELL VIABILITY; CHROMATIN IMMUNOPRECIPITATION; ENZYME INHIBITION; FEMALE; GRANULOSA CELL; HORMONAL REGULATION; LUTEAL CELL; NONHUMAN; OVARY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RAT;

ANIMALS; BASE SEQUENCE; BINDING SITES; CELL SURVIVAL; CHORIONIC GONADOTROPIN; CORE BINDING FACTOR ALPHA 1 SUBUNIT; CORE BINDING FACTOR ALPHA 2 SUBUNIT; CUMULUS CELLS; EXTRACELLULAR MATRIX PROTEINS; FEMALE; GENES, DOMINANT; GENES, REPORTER; HUMANS; HYALURONIC ACID; MOLECULAR SEQUENCE DATA; MUTATION; OOCYTES; OVARY; OVULATION; PROTEIN BINDING; PROTEOGLYCANS; RATS; RESPONSE ELEMENTS; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANSCRIPTIONAL ACTIVATION;

RATTUS;

EID: 77954831388     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2009-0325     Document Type: Article

References (62)

1. Russell DL, Ochsner SA, Hsieh M, Mulders S, Richards JS 2003 Hormone-regulated expression and localization of versican in the rodent ovary. Endocrinology 144:1020-1031 (Pubitemid 36262869)
2. Chen L, Mao SJ, McLean LR, Powers RW, Larsen WJ 1994 Proteins of the inter-α-trypsin inhibitor family stabilize the cumulus extracellular matrix through their direct binding with hyaluronic acid. J Biol Chem 269:28282-28287
3. Chen L, Mao SJ, Larsen WJ 1992 Identification of a factor in fetal bovine serum that stabilizes the cumulus extracellular matrix. A role for a member of the inter-α-trypsin inhibitor family. J Biol Chem 267:12380-12386
4. Mukhopadhyay D, Hascall VC, Day AJ, Salustri A, Fülöp C 2001 Two distinct populations of tumor necrosis factor-stimulated gene-6 protein in the extracellular matrix of expanded mouse cumulus cell-oocyte complexes. Arch Biochem Biophys 394:173-181
5. Salustri A, Garlanda C, Hirsch E, De Acetis M, Maccagno A, Bottazzi B, Doni A, Bastone A, Mantovani G, Beck Peccoz P, Salvatori G, Mahoney DJ, Day AJ, Siracusa G, Romani L, Mantovani A 2004 PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization. Development 131:1577-1586
6. Varani S, Elvin JA, Yan C, DeMayo J, DeMayo FJ, Horton HF, Byrne MC, Matzuk MM 2002 Knockout of pentraxin 3, a downstream target of growth differentiation factor-9, causes female subfertility. Mol Endocrinol 16:1154-1167
7. Fülöp C, Szántó S, Mukhopadhyay D, Bárdos T, Kamath RV, Rugg MS, Day AJ, Salustri A, Hascall VC, Glant TT, Mikecz K 2003 Impaired cumulus mucification and female sterility in tumor necrosis factor-induced protein-6 deficient mice. Development 130:2253-2261
8. Sato H, Kajikawa S, Kuroda S, Horisawa Y, Nakamura N, Kaga N, Kakinuma C, Kato K, Morishita H, Niwa H, Miyazaki J 2001 Impaired fertility in female mice lacking urinary trypsin inhibitor. Biochem Biophys Res Commun 281:1154-1160
9. Zhuo L, Yoneda M, Zhao M, Yingsung W, Yoshida N, Kitagawa Y, Kawamura K, Suzuki T, Kimata K 2001 Defect in SHAP-hyaluronan complex causes severe female infertility.Astudy by inactivation of the bikunin gene in mice. J Biol Chem 276:7693-7696
10. Swann DA, Powell S, Broadhurst J, Sordillo E, Sotman S 1976 The formation of a stable complex between dissociated proteoglycan and hyaluronic acid in the absence of a link protein. Biochem J 157:503-506
11. Neame PJ, Barry FP 1993 The link proteins. Experientia 49:393-402
12. Shi S, Grothe S, Zhang Y, O'Connor-McCourt MD, Poole AR, Roughley PJ, Mort JS 2004 Link protein has greater affinity for versican than aggrecan. J Biol Chem 279:12060-12066
13. Hirashima Y, Kobayashi H, Gotoh J, Terao T 1997 Inter-α-trypsin inhibitor is concentrated in the pericellular environment of mouse granulosa cells through hyaluronan-binding. Eur J Obstet Gynecol Reprod Biol 73:79-84 (Pubitemid 27224465)
14. Franzén A, Björnsson S, Heinegård D 1981 Cartilage proteoglycan aggregate formation. Role of link protein. Biochem J 197:669-674
15. Watanabe H, Yamada Y 1999 Mice lacking link protein develop dwarfism and craniofacial abnormalities. Nat Genet 21:225-229
16. Wirrig EE, Snarr BS, Chintalapudi MR, O'neal JL, Phelps AL, Barth JL, Fresco VM, Kern CB, Mjaatvedt CH, Toole BP, Hoffman S, Trusk TC, Argraves WS, Wessels A 2007 Cartilage link protein 1 (Crtl1), an extracellular matrix component playing an important role in heart development. Dev Biol 310:291-303
17. Kobayashi H, Sun GW, Hirashima Y, Terao T 1999 Identification of link protein during follicle development and cumulus cell cultures in rats. Endocrinology 140:3835-3842
18. Sun GW, Kobayashi H, Terao T 1999 Expression of link protein during mouse follicular development. J Histochem Cytochem 47:1433-1442
19. Sun GW, Kobayashi H, Suzuki M, Kanayama N, Terao T 2002 Production of cartilage link protein by human granulosa-lutein cells. J Endocrinol 175:505-515
20. Sun GW, Kobayashi H, Suzuki M, Kanayama N, Terao T 2002 Link protein as an enhancer of cumulus cell-oocyte complex expansion. Mol Reprod Dev 63:223-231
21. Komatsu K, Buchanan FG, Otaka M, Jin M, Odashima M, Horikawa Y, Watanabe S, Dubois RN 2006 Gene expression profiling following constitutive activation of MEK1 and transformation of rat intestinal epithelial cells. Mol Cancer 5:63
22. Rangel LB, Sherman-Baust CA, Wernyj RP, Schwartz DR, Cho KR, Morin PJ 2003 Characterization of novel human ovarian cancerspecific transcripts (HOSTs) identified by serial analysis of gene expression. Oncogene 22:7225-7232
23. Skandalis SS, Theocharis AD, Theocharis DA, Papadas T, Vynios DH, Papageorgakopoulou N 2004 Matrix proteoglycans are markedly affected in advanced laryngeal squamous cell carcinoma. Biochim Biophys Acta 1689:152-161
24. Yang L, Carlson SG, McBurney D, Horton Jr WE 2005 Multiple signals induce endoplasmic reticulum stress in both primary and immortalized chondrocytes resulting in loss of differentiation, impaired cell growth, and apoptosis. J Biol Chem 280:31156-31165
25. Aida Y, Maeno M, Ito-Kato E, Suzuki N, Shiratsuchi H, Matsumura H 2004 Effect of IL-1α on the expression of cartilage matrix proteins in human chondrosarcoma cell line OUMS-27. Life Sci 75:3173-3184 (Pubitemid 39361174)
26. 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
27. Quirk SM, Cowan RG, Harman RM, Hu CL, Porter DA 2004 Ovarian follicular growth and atresia: the relationship between cell proliferation and survival. J Anim Sci 82(Suppl E):E40-E52
28. Robker RL, Richards JS 1998 Hormonal control of the cell cycle in ovarian cells: proliferation versus differentiation. Biol Reprod 59:476-482
29. Sun GW, Kobayashi H, Suzuki M, Kanayama N, Terao T 2003 Follicle-stimulating hormone and insulin-like growth factor I synergistically induce up-regulation of cartilage link protein (Crtl1) via activation of phosphatidylinositol-dependent kinase/Akt in rat granulosa cells. Endocrinology 144:793-801
30. Jo M, Curry Jr TE 2006 Luteinizing hormone-induced RUNX1 regulates the expression of genes in granulosa cells of rat periovulatory follicles. Mol Endocrinol 20:2156-2172
31. Kagoshima H, Shigesada K, Satake M, Ito Y, Miyoshi H, Ohki M, Pepling M, Gergen P 1993 The Runt domain identifies a new family of heteromeric transcriptional regulators. Trends Genet 9:338-341
32. Cameron ER, Neil JC 2004 The Runx genes: lineage-specific oncogenes and tumor suppressors. Oncogene 23:4308-4314
33. 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
34. Richards JS, Russell DL, Ochsner S, Hsieh M, Doyle KH, Falender AE, Lo YK, Sharma SC 2002 Novel signaling pathways that control ovarian follicular development, ovulation, and luteinization. Recent Prog Horm Res 57:195-220
35. 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
36. Liu J, Park ES, Jo M 2009 Runt-related transcription factor 1 regulates luteinized hormone-induced prostaglandin-endoperoxide synthase 2 expression in rat periovulatory granulosa cells. Endocrinology 150:3291-3300
37. Li F, Liu J, Park ES, Jo M, Curry Jr TE 2009 The B cell translocation gene (BTG) family in the rat ovary: hormonal induction, regulation, and impact on cell cycle kinetics. Endocrinology 150:3894-3902
38. Peluso JJ 2003 Progesterone as a regulator of granulosa cell viability. J Steroid Biochem Mol Biol 85:167-173
39. Quirk SM, Cowan RG, Harman RM 2004 Progesterone receptor and the cell cycle modulate apoptosis in granulosa cells. Endocrinology 145:5033-5043
40. Svensson EC, Markström E, Andersson M, Billig H 2000 Progesterone receptor-mediated inhibition of apoptosis in granulosa cells isolated from rats treated with human chorionic gonadotropin. Biol Reprod 63:1457-1464
41. Russell DL, Salustri A 2006 Extracellular matrix of the cumulusoocyte complex. Semin Reprod Med 24:217-227
42. Camaioni A, Salustri A, Yanagishita M, Hascall VC 1996 Proteoglycans and proteins in the extracellular matrix of mouse cumulus cell-oocyte complexes. Arch Biochem Biophys 325:190-198
43. Lydon JP, DeMayo FJ, Funk CR, Mani SK, Hughes AR, Montgomery Jr CA, Shyamala G, Conneely OM, O'Malley BW 1995 Mice lacking progesterone receptor exhibit pleiotropic reproductive abnormalities. Genes Dev 9:2266-2278
44. Lim H, Paria BC, Das SK, Dinchuk JE, Langenbach R, Trzaskos JM, Dey SK 1997 Multiple female reproductive failures in cyclooxygenase 2-deficient mice. Cell 91:197-208
45. Hizaki H, Segi E, Sugimoto Y, Hirose M, Saji T, Ushikubi F, Matsuoka T, Noda Y, Tanaka T, Yoshida N, Narumiya S, Ichikawa A 1999 Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP(2). Proc Natl Acad Sci USA 96:10501-10506
46. Hsieh M, Lee D, Panigone S, Horner K, Chen R, Theologis A, Lee DC, Threadgill DW, Conti M 2007 Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol 27:1914-1924
47. Fan HY, Liu Z, Shimada M, Sterneck E, Johnson PF, Hedrick SM, Richards JS 2009 MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 324:938-941
48. Sirois J, Richards JS 1993 Transcriptional regulation of the rat prostaglandin endoperoxide synthase 2 gene in granulosa cells. Evidence for the role of a cis-acting C/EBP β promoter element. J Biol Chem 268:21931-21938 (Pubitemid 23320698)
49. Gutierrez S, Javed A, Tennant DK, van Rees M, Montecino M, Stein GS, Stein JL, Lian JB 2002 CCAAT/enhancer-binding proteins (C/EBP) β and δ activate osteocalcin gene transcription and synergize with Runx2 at the C/EBP element to regulate bone-specific expression. J Biol Chem 277:1316-1323
50. Zhang DE, Hetherington CJ, Meyers S, Rhoades KL, Larson CJ, Chen HM, Hiebert SW, Tenen DG 1996 CCAAT enhancer-binding protein (C/EBP) and AML1 (CBF α2) synergistically activate the macrophage colony-stimulating factor receptor promoter. Mol Cell Biol 16:1231-1240
51. Braw RH, Bar-Ami S, Tsafriri A 1981 Effect of hypophysectomy on atresia of rat preovulatory follicles. Biol Reprod 25:989-996
52. Uilenbroek JT, Woutersen PJ, van der Schoot P 1980 Atresia of preovulatory follicles: gonadotropin binding and steroidogenic activity. Biol Reprod 23:219-229
53. Chun SY, Billig H, Tilly JL, Furuta I, Tsafriri A, Hsueh AJ 1994 Gonadotropin suppression of apoptosis in cultured preovulatory follicles: mediatory role of endogenous insulin-like growth factor I. Endocrinology 135:1845-1853
54. Lee J, Park HJ, Choi HS, Kwon HB, Arimura A, Lee BJ, Choi WS, Chun SY 1999 Gonadotropin stimulation of pituitary adenylate cyclase-activating polypeptide (PACAP) messenger ribonucleic acid in the rat ovary and the role of PACAP as a follicle survival factor. Endocrinology 140:818-826
55. Porter DA, Harman RM, Cowan RG, Quirk SM 2001 Susceptibility of ovarian granulosa cells to apoptosis differs in cells isolated before or after the preovulatory LH surge. Mol Cell Endocrinol 176:13-20
56. Kaneko T, Saito H, Toya M, Satio T, Nakahara K, Hiroi M 2000 Hyaluronic acid inhibits apoptosis in granulosa cells via CD44. J Assist Reprod Genet 17:162-167
57. Saito H, Kaneko T, Takahashi T, Kawachiya S, Saito T, Hiroi M 2000 Hyaluronan in follicular fluids and fertilization of oocytes. Fertil Steril 74:1148-1152
58. Ghatak S, Misra S, Toole BP 2005 Hyaluronan constitutively regulates ErbB2 phosphorylation and signaling complex formation in carcinoma cells. J Biol Chem 280:8875-8883
59. Misra S, Ghatak S, Toole BP 2005 Regulation of MDR1 expression and drug resistance by a positive feedback loop involving hyaluronan, phosphoinositide 3-kinase, and ErbB2. J Biol Chem 280:20310-20315
60. Cattaruzza S, Schiappacassi M, Kimata K, Colombatti A, Perris R 2004 The globular domains of PG-M/versican modulate the proliferation- apoptosis equilibrium and invasive capabilities of tumor cells. FASEB J 18:779-781
61. 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
62. Park ES, Choi S, Muse KN, Curry Jr TE, Jo M 2008 Response gene to complement 32 expression is induced by the luteinizing hormone (LH) surge and regulated by LH-induced mediators in the rodent ovary. Endocrinology 149:3025-3036