Expression of hyaluronan synthase 1 and distribution of hyaluronan during follicular atresia in pig ovaries

Biology of Reproduction

Volumn 80, Issue 2, 2009, Pages 249-257

  Miyake, Yuko ^a,b   Sakurai, Masahiro ^b   Tanaka, Sachi ^b   Tunjung, Woro Anindito Sri ^b   Yokoo, Masaki ^b   Matsumoto, Hiromichi ^b,c   Aso, Hisashi ^b   Yamaguchi, Takahiro ^b   Sato, Eimei ^b  

^a TAKEDA PHARMACEUTICAL COMPANY LIMITED   (Japan)

^b TOHOKU UNIVERSITY   (Japan)

^c UTSUNOMIYA UNIVERSITY   (Japan)

Author keywords

Apoptosis; Atresia; Follicle; Hyaluronan; Ovary

Indexed keywords

HERMES ANTIGEN; HYALURONAN SYNTHASE 1; HYALURONAN SYNTHASE 2; HYALURONAN SYNTHASE 3; HYALURONIC ACID; HYALURONIC ACID BINDING PROTEIN; MESSENGER RNA; N ACETYLGLUCOSAMINYLTRANSFERASE; POLYCLONAL ANTIBODY; SYNTHETASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; IMMUNOHISTOCHEMISTRY; MACROPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY FOLLICLE ATRESIA; OVARY FOLLICLE FLUID; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEQUENCE ANALYSIS; SWINE; THECA CELL; WESTERN BLOTTING;

ANIMALS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FEMALE; FOLLICULAR ATRESIA; FOLLICULAR FLUID; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCURONOSYLTRANSFERASE; HYALURONIC ACID; MACROPHAGES; OVARY; RNA, MESSENGER; SWINE; TISSUE DISTRIBUTION;

SUIDAE; SUS SCROFA;

EID: 59949084220     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.108.067694     Document Type: Article

References (48)

1. Tsafriri A, Braw RH. Experimental approaches to atresia in mammals. Oxf Rev Reprod Biol 1984; 6:226-265.
2. Hirshfield AN. Development of follicles in the mammalian ovary. Int Rev Cytol 1991; 124:43-101.
3. Alonso-Pozos I, Rosales-Torres A, Avalos-Rodriguez A, Vergara-Onofre M, Rosado-Garcia A. Mechanism of granulosa cell death during follicular atresia depends on follicular size. Therigenology 2003; 60:1071-1081.
4. Manabe N, Imai Y, Ohno H, Takahagi Y, Sugimoto M, Miyamoto H. Apoptosis occurs in granulosa cells but not cumulus cells in the atretic antral follicles in pig ovaries. Experientia 1996; 52:647-651.
5. Miyake Y, Matsumoto H, Yokoo M, Miyazawa K, Kimura N, Tunjung WAS, Shimizu T, Sasada H, Aso H, Yamaguchi T, Sato E. Expression and glycosylation with polylactosamine of CD44 antigen on macrophages during follicular atresia in pig ovaries. Biol Reprod 2006; 74:501-510.
6. Vachon E, Martin R, Plumb J, Kwok V, Vandivier W, Glogauer M, Kapus A, Wang X, Chow CW, Grinstein S, Downey GP. CD44 is a phagocytic receptor. Blood 2006; 107:4149-4158.
7. Vachon E, Martin R, Kwok V, Cherepanov V, Chow CW, Doerschuk CM, Plumb J, Grinstein G, Downey GP. CD44-mediated phagocytosis induces inside-out activation of complement receptor-3 in murine macrophages. Blood 2007; 110:4492-4502.
8. Vivers S, Heasman SJ, Hart SP, Dransfield I. Divalent cation-independent augmentation of macrophage phagocytosis of apoptotic neutrophils by CD44 antibody. Clin Exp Immunol 2004; 138:447-452.
9. Teder P, Vandivier RW, Jiang D, Liang J, Cohn L, Purè E, Henson PM, Noble PW. Resolution of lung inflammation by CD44. Science 2002; 296:155-158.
10. Weigel PH, Hascall VC, Tammi M. Hyaluronan synthases. J Biol Chem 1997; 272:13997-14000.
11. DeAngelis PL. Hyaluronan synthases: fascinating glycosyltransferases from vertebrates, bacterial pathogens, and algal viruses. Cell Mol Life Sci 1999; 56:670-682.
12. Salustri A, Camaioni A, Di Giacomo M, Fulop C, Hascall VC. Hyaluronan and proteoglycans in ovarian follicles. Hum Reprod Update 1999; 5:293-301.
13. Stock AE, Bouchard N, Brown K, Spicer AP, Underhill CB, Doré M, Sirois J. Induction of hyaluronan synthase 2 by human chorionic gonadotropin in mural granulosa cells of equine preovulatory follicles. Endocrinology 2002; 143:4375-4384.
14. Fraser JR, Laurent TC, Laurent UB. Hyaluronan: in nature, distribution, functions and turnover. J Intern Med 1997; 242:27-33.
15. Kobayashi H, Sun GW, Terao T. Immunolocalization of hyaluronic acid and inter-alpha-trypsin inhibitor in mice. Cell Tissue Res 1999; 296:587-597.
16. Irving-Rodgers HF, Rodgers RJ. Extracellular matrix in ovarian follicular development and disease. Cell Tissue Res 2005; 322:89-98.
17. Tammi MI, Day AJ, Turley EA. Hyaluronan and homeostasis: a balancing act. J Biol Chem 2002; 277:4851-4854.
18. Day AJ, Prestwich GD. Hyaluronan-binding proteins: trying up the giant. J Biol Chem 2002; 277:4585-4588.
19. Turley EA, Noble PW, Bourguignon LY. Signaling properties of hyaluronan receptors. J Biol Chem 2002; 277:4589-4592.
20. Toole BP. Hyaluronan in morphogenesis. Semin Cell Dev Biol 2001; 12: 79-87.
21. Chen WY, Abatangelo G. Functions of hyaluronan in wound repair. Wound Repair Regen 1999; 7:79-89.
22. Gerdin B, Hallgren R. Dynamic role of hyaluronan(HYA) in connective tissue activation and inflammation. J Intern Med 1997; 242:49-55.
23. Laurent TC, Fraser JR, Laurent UB, Engstrom-Laurent A. Hyaluronan in inflammatory joint disease. Acta Orthop Scand Suppl 1995; 266:116-120.
24. Sun LK, Beck-Schimmer B, Oertli B, Wuthrich RP. Hyaluronan-induced cyclooxygenase-2 expression promotes thromboxane A2 production by renal cells. Kidney Int 2001; 59:190-196.
25. Kosaki R, Watanabe K, Yamaguchi Y. Overproduction of hyaluronan by expression of the hyaluronan synthase Has2 enhances anchorage- independent growth and tumorigenicity. Cancer Res 1999; 59:1141-1145.
26. Simpson MA, Wilson CM, Furcht LT, Spicer AP, Oegema TR Jr, McCarthy JB. Manipulation of hyaluronan synthase expression in prostate adenocarcinoma cells alters pericellular matrix retention and adhesion to bone marrow endothelial cells. J Biol Chem 2002; 277:10050-10057.
27. Toole BP, Wight TN, Tammi MI. Hyaluronan-cell interactions in cancer and vascular disease. J Biol Chem 2002; 277:4593-4596.
28. Spicer AP, McDonald JA. Characterization and molecular evolution of a vertebrate hyaluronan synthase gene family. J Biol Chem 1998; 273:1923-1932.
29. Spicer AP, McDonald JA. Eukaryotic hyaluronan synthases. World Wide Web(URL:http://www.glycoforum.gr.jp/science/hyaluronan/HA07/ HA07E.html)(September 15, 1998).
30. Jacobson A, Brinck J, Briskin MJ, Spicer AP, Heldin P. Expression of human hyaluronan synthases in response to external stimuli. Biochem J 2000; 348:29-35.
31. Spicer AP, Seldin MF, Olsen AS, Brown N, Wells DE, Doggett NA, Itano N, Kimata K, Inazawa J, McDonald JA. Chromosomal localization of the human and mouse hyaluronan synthase genes. Genomics 1997; 41:493-497.
32. Itano N, Sawai T, Yoshida M, Lenas P, Yamada Y, Imagawa M, Shinomura T, Hamaguchi M, Yoshida Y, Ohnuki Y, Miyauchi S, Spicer AP, et al. Three isoforms of mammalian hyaluronan synthases have distinct enzymatic properties. J Biol Chem 1999; 274:25085-25092.
33. Pienimaki JP, Rilla K, Fulop C, Sironen RK, Karvinen S, Pasonen S, Lammi MJ, Tammi R, Hascall VC, Tammi MI. Epidermal growth factor activates hyaluronan synthase 2 in epidermal keratinocytes and increases pericellular and intracellular hyaluronan. J Biol Chem 2001; 276:20428-20435.
34. Sayo T, Sugiyama Y, Takahashi Y, Ozawa N, Sakai S, Ishikawa O, Tamura M, Inoue S. Hyaluronan synthase 3 regulates hyaluronan synthesis in cultured human keratinocytes. J Invest Dermatol 2002; 118:43-48.
35. Kimura N, Konno Y, Miyoshi K, Matsumoto H, Sato E. Expression of hyaluronan synthases and CD44 messenger RNAs in porcine cumulus- oocyte complexes during in vitro maturation. Biol Reprod 2002; 66:707-717.
36. Yokoo M, Miyahayashi Y, Naganuma T, Kimura N, Sasada H, Sato E. Identification of hyaluronic acid-binding proteins and their expressions in porcine cumulus-oocyte complexes during in vitro maturation. Biol Reprod 2002; 67:1165-1171.
37. Yokoo M, Kimura N, Shimizu T, Naganuma T, Matsumoto H, Sasada H, Sato E. Induction of porcine oocyte maturation by hyaluronan-CD44 system. J Fertil Implant 2003; 20:33-36.
38. Yokoo M, Sato E. Cumulus-oocyte complex interactions during oocyte maturation. Int Rev Cytol 2004; 235:251-291.
39. Takayanagi Y, Yoshida M, Bielsky IF, Ross HE, Kawamata M, Onaka T, Yanagisawa T, Kimura T, Matzuk MM, Young LY, Nishimori K. Pervasive social deficits, but normal parturition in oxytocin receptor deficient mice. Proc Natl Acad Sci U S A 2005; 44:16096-16101.
40. Itano N, Kimata K. Molecular cloning of human hyaluronan synthase. Biochem Biophys Res Comm 1996; 222:816-820.
41. Spicer AP, Augustine ML, McDonald JA. Molecular cloning and characterization of a putative mouse hyaluronan synthase. J Biol Chem 1996; 271:23400-23405.
42. Miyazawa K, Aso H, Honda M, Kido T, Minashima T, Kanaya T, Watanabe K, Ohwada S, Rose MT, Yamaguchi T. Identification of bovine dendritic cell phenotype from bovine peripheral blood. Res Vet Sci 2006; 81:40-45.
43. + T cell subsets of calves. Vet Immuno Immunopathol 2007; 118:84-91.
44. Li L, Asteriou T, Bernert B, Heldin CH, Heldin P. Growth factor regulation of hyaluronan synthesis and degradation in human dermal fibroblasts: importance of hyaluronan for the mitogenic response of PDGF-BB. Biochem J 2007; 404:327-336.
45. Rodgers RJ, Irving-Rodgers HF, Russell DL. Extracellular matrix of the developing ovarian follicle. Reproduction 2003; 126:415-424.
46. Irving-Rodgers HF, Rodgers RJ. Extracellular matrix of the developing ovarian follicle. Semin Reprod Med 2006; 24:195-220.
47. Orimoto AM, Dumaresq-Doiron K, Jiang JY, Tanphaichitr N, Tsang BK, Carmona E. Mammalian hyaluronidase induces ovarian granulosa cell apoptosis and is involved in follicular atresia. Endocrinology 2008; 149:5835-5847.
48. Minge CE, Ryan NK, Van Der Hoek KH, Robker RL, Norman RJ. Troglitazone regulates peroxisome proliferator-activated receptors and inducible nitric oxide synthase in murine ovarian macrophages. Biol Reprod 2006; 74:153-160.