The effect of glycosaminoglycans on rat gametes in vitro and the associated signal pathway

Reproduction

Volumn 135, Issue 3, 2008, Pages 311-319

  Borg, Neil ^a   Holland, Michael ^a  

^a HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BALANCED SALT SOLUTION; BICARBONATE; CELL PROTEIN; CHONDROITIN SULFATE; GLYCOSAMINOGLYCAN; HERMES ANTIGEN; HYALURONIC ACID; MESSENGER RNA; RINGER SOLUTION;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; CUMULUS OOPHORUS; EMBRYO; FERTILIZATION IN VITRO; GAMETE; INCUBATION TIME; MALE; METAPHASE; NONHUMAN; OOCYTE DEVELOPMENT; OOCYTE MATURATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROBE; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD44; BLOTTING, WESTERN; CELLS, CULTURED; CHONDROITIN SULFATES; CULTURE MEDIA; FEMALE; FERTILIZATION IN VITRO; GLYCOSAMINOGLYCANS; HYALURONIC ACID; MALE; OOCYTES; OOGENESIS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERUM ALBUMIN, BOVINE; SIGNAL TRANSDUCTION;

RATTUS;

EID: 40949141800     PISSN: 14701626     EISSN: None     Source Type: Journal    
DOI: 10.1530/REP-07-0267     Document Type: Article

References (91)

1. Alho AM & Underhill CB 1989 The hyaluronate receptor is preferentially expressed on proliferating epithelial cells. Journal of Cell Biology 108 1557-1565.
2. Archibong AE, Petters RM & Johnson BH 1989 Development of porcine embryos from one- and two-cell stages to blastocysts in culture medium supplemented with porcine oviductal fluid. Biology of Reproduction 41 1076-1083.
3. Ax RL & Ryan RJ 1979 The porcine ovarian follicle. IV. Mucopolysaccharides at different stages of development. Biology of Reproduction 20 1123-1132.
4. Bajorath J 2000 Molecular organization, structural features, and ligand binding characteristics of CD44, a highly variable cell surface glycoprotein with multiple functions. Proteins 39 103-111.
5. Bendahmane M, Zeng HT & Tulsiani DR 2002 Assessment of acrosomal status in rat spermatozoa: studies on carbohydrate and non-carbohydrate agonists. Archives of Biochemistry and Biophysics 404 38-47.
6. Borland G, Ross JA & Guy K 1998 Forms and functions of CD44. Immunology 93 139-148.
7. Bose N & Masellis AM 2005 Secretory products of breast cancer cells upregulate hyaluronan production in a human osteoblast cell line. Clinical and Experimental Metastasis 22 629-642.
8. Bourguignon LY, Gilad E, Rothman K & Peyrollier K 2005 Hyaluronan-CD44 interaction with IQGAP1 promotes Cdc42 and ERK signaling, leading to actin binding, Elk-1/estrogen receptor transcriptional activation, and ovarian cancer progression. Journal of Biological Chemistry 280 11961-11972.
9. 2+ signaling, and cytoskeleton modification in head and neck squamous cell carcinoma cells. Journal of Biological Chemistry 281 14026-14040.
10. Camaioni A, Hascall VC, Yanagishita M & Salustri A 1993 Effects of exogenous hyaluronic acid and serum on matrix organization and stability in the mouse cumulus cell-oocyte complex. Journal of Biological Chemistry 268 20473-20481.
11. Camenisch TD, Schroeder JA, Bradley J, Klewer SE & McDonald JA 2002 Heart-valve mesenchyme formation is dependent on hyaluronan-augmented activation of ErbB2-ErbB3 receptors. Nature Medicine 8 850-855.
12. Cherr GN, Yudin AI, Li MW, Vines CA & Overstreet JW 1999 Hyaluronic acid and the cumulus extracellular matrix induce increases in intracellular calcium in macaque sperm via the plasma membrane protein PH-20. Zygote 7 211-222.
13. Cohen DJ, Rochwerger L, Ellerman DA, Morgenfeld MM, Busso D & Cuasnicu PS 2000 Relationship between the association of rat epididymal protein 'DE' with spermatozoa and the behavior and function of the protein. Molecular Reproduction and Development 56 180-188.
14. Cuasnicu PS, Conesa D & Rochwerger L 1990 Potential contraceptive use of an epididymal protein that participates in fetilization. In Gamete Interaction: Prospects for Immunocontraception, pp 143-153. Eds NJ Alexander, D Griffin, JM Spieler & GMH Waites. New York: Wiley-Liss.
15. Culty M, Miyake K, Kincade PW, Sikorski E, Butcher EC & Underhill C 1990 The hyaluronate receptor is a member of the CD44 (H-CAM) family of cell surface glycoproteins. Journal of Cell Biology 111 2765-2774.
16. Dekel N & Phillips DM 1979 Maturation of the rat cumulus oophorus. A scanning electron microscopic study. Biology of Reproduction 21 9-18.
17. Entwistle J, Hall CL & Turley EA 1996 HA receptors: regulators of signalling to the cytoskeleton. Journal of Cellular Biochemistry 61 569-577.
18. Eppig JJ 1979 FSH stimulates hyaluronic acid synthesis by oocyte-cumulus cell complexes from mouse preovulatory follicles. Nature 281 483-484.
19. 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.
20. Eriksen GV, Malmstrom A, Uldbjerg N & Huszar G 1994 A follicular fluid chondroitin sulfate proteoglycan improves the retention of motility and velocity of human spermatozoa. Fertility and Sterility 62 618-623.
21. Fulop C, Salustri A & Hascall VC 1997 Coding sequence of a hyaluronan synthase homologue expressed during expansion of the mouse cumulus-oocyte complex. Archives of Biochemistry and Biophysics 337 261-266.
22. Furnus CC, Valcarcel A, Dulout FN & Errecalde AL 2003 The hyaluronic acid receptor (CD44) is expressed in bovine oocytes and early stage embryos. Theriogenology 60 1633-1644.
23. Goh HH, Yang XF, Tain CF, Liew LP & Ratnam SS 1992 Oogenesis, fertilisation and early embryonic development in rats. II: Dose-dependent effects of human chorionic gonadotrophin. Annals of the Academy of Medicine of Singapore 21 451-458.
24. Gotoh M, Sato T, Akashima T, Iwasaki H, Kameyama A, Mochizuki H, Yada T, Inaba N, Zhang Y, Kikuchi N et al. 2002a Enzymatic synthesis of chondroitin with a novel chondroitin sulfate N-acetylgalactosaminyl-transferase that transfers N-acetylgalactosamine to glucuronic acid in initiation and elongation of chondroitin sulfate synthesis. Journal of Biological Chemistry 277 38189-38196.
25. Gotoh M, Yada T, Sato T, Akashima T, Iwasaki H, Mochizuki H, Inaba T, Togayachi A, Kudo T, Watanabe H et al. 2002b Molecular cloning and characterization of a novel chondroitin sulfate glucuronyltransferase that transfers glucuronic acid to N-acetylgalactosamine. Journal of Biological Chemistry 277 38179-38188.
26. Green SJ, Tarone G & Underhill CB 1988a Aggregation of macrophages and fibroblasts is inhibited by a monoclonal antibody to the hyaluronate receptor. Experimental Cell Research 178 224-232.
27. Green SJ, Tarone G & Underhill CB 1988b Distribution of hyaluronate and hyaluronate receptors in the adult lung. Journal of Cell Science 90 145-156.
28. Hamamah S, Wittemer C, Barthelemy C, Richet C, Zerimech F, Royere D & Degand P 1996 Identification of hyaluronic acid and chondroitin sulfates in human follicular fluid and their effects on human sperm motility and the outcome of in vitro fertilization. Reproduction, Nutrition, Development 36 43-52.
29. Hamashima N 1982 Effect of hyaluronic acid on the pre-implantation development of mouse embryo in vitro. Development, Growth and Differentiation 24 353-357.
30. Isacke CM 1994 The role of the cytoplasmic domain in regulating CD44 function. Journal of Cell Science 107 2353-2359.
31. Itano N, Atsumi F, Sawai T, Yamada Y, Miyaishi O, Senga T, Hamaguchi M & Kimata K 2002 Abnormal accumulation of hyaluronan matrix diminishes contact inhibition of cell growth and promotes cell migration. PNAS 99 3609-3614.
32. Jang G, Lee BC, Kang SK & Hwang WS 2003 Effect of glycosaminoglycans on the preimplantation development of embryos derived from in vitro fertilization and somatic cell nuclear transfer. Reproduction, Fertility, and Development 15 179-185.
33. Jensen CE & Zachariae F 1958 Studies on the mechanism of ovulation: isolation and analysis of acid mucopolysaccharicles in bovine follicular fluid. Acta Endocrinologica 27 356-368.
34. Josefsberg LB, Galiani D, Lazar S, Kaufman O, Seger R & Dekel N 2003 Maturation-promoting factor governs mitogen-activated protein kinase activation and interphase suppression during meiosis of rat oocytes. Biology of Reproduction 68 1282-1290.
35. Kano K, Miyano T & Kato S 1998 Effects of glycosaminoglycans on the development of in vitro-matured and -fertilized porcine oocytes to the blastocyst stage in vitro. Biology of Reproduction 58 1226-1232.
36. Kawakami E, Arai T, Oishi I, Hori T & Tsutsui T 2000 Induction of dog sperm capacitation by glycosaminoglycans and glycosaminoglycan amounts of oviductal and uterine fluids in bitches. Journal of Veterinary Medical Science 62 65-68.
37. Kim KS, Foster JA & Gerton GL 2001 Differential release of guinea pig sperm acrosomal components during exocytosis. Biology of Reproduction 64 148-156.
38. Kim HS, Lee GS, Hyun SH, Nam DH, Lee SH, Jeong YW, Kim S, Kim JH, Kang SK, Lee BC et al. 2005 Embryotropic effect of glycosaminoglycans and receptors in development of porcine pre-implantation embryos. Theriogenology 63 1167-1190.
39. Kimura N, Konno Y, Miyoshi K, Matsumoto H & Sato E 2002 Expression of hyaluronan synthases and CD44 messenger RNAs in porcine cumulus-oocyte complexes during in vitro maturation. Biology of Reproduction 66 707-717.
40. Kitagawa H, Uyarna T & Sugahara K 2001 Molecular cloning and expression of a human chondroitin synthase. Journal of Biological Chemistry 276 38721-38726.
41. Kobayashi H, Suzuki M, Kanayama N, Nishida T, Takigawa M & Terao T 2002 CD44 stimulation by fragmented hyaluronic acid induces upregulation of urokinase-type plasminogen activator and its receptor and subsequently facilitates invasion of human chondrosarcoma cells. International Journal of Cancer 102 379-389.
42. Kon J, Ooe H, Oshima H, Kikkawa Y & Mitaka T 2006 Expression of CD44 in rat hepatic progenitor cells. Journal of Hepatology 45 90-98.
43. Kosaki R, Watanabe K & Yamaguchi Y 1999 Overproduction of hyaluronan by expression of the hyaluronan synthase Has2 enhances anchorage-independent growth and tumorigenicity. Cancer Research 59 1141-1145.
44. Lee CN & Ax RL 1984 Concentrations and composition of glycosaminoglycans in the female bovine reproductive tract. Journal of Dairy Science 67 2006-2009.
45. Lee CN, Clayton MK, Bushmeyer SM, First NL & Ax RL 1986 Glycosaminoglycans in ewe reproductive tracts and their influence on acrosome reactions in bovine spermatozoa in vitro. Journal of Animal Science 63 861-867.
46. Legg JW, Lewis CA, Parsons M, Ng T & Isacke CM 2002 A novel PKC-regulated mechanism controls CD44 ezrin association and directional cell motility. Nature Cell Biology 4 399-407.
47. Lenz RW, Ball GD, Lohse JK, First NL & Ax RL 1983 Chondroitin sulfate facilitates an acrosome reaction in bovine spermatozoa as evidenced by light microscopy, electron microscopy and in vitro fertilization. Biology of Reproduction 28 683-690.
48. Lesley J & Hyman R 1998 CD44 structure and function. Frontiers in Bioscience 3 d616-d630.
49. Lesley J, Hyman R & Kincade PW 1993 CD44 and its interaction with extracellular matrix. Advance Immunology 54 271-335.
50. Liu D, Liu T, Li R & Sy MS 1998 Mechanisms regulating the binding activity of CD44 to hyaluronic acid. Frontiers in Bioscience 3 d631-d636.
51. Lu DP, Tian L, O'Neill C & King NJ 2002 Regulation of cellular adhesion molecule expression in murine oocytes, peri-implantation and post-implantation embryos. Cell Research 12 373-383.
52. Lugli A, Zlobec I, Gunthert U, Minoo P, Baker K, Tomillo L, Terracciano L & Jass JR 2006 Overexpression of the receptor for hyaluronic acid mediated motility is an independent adverse prognostic factor in colorectal cancer. Modern Pathology 19 1302-1309.
53. Marchal R, Caillaud M, Martoriati A, Gerard N, Mermillod P & Goudet G 2003 Effect of growth hormone (GH) on in vitro nuclear and cytoplasmic oocyte maturation, cumulus expansion, hyaluronan synthases, and connexins 32 and 43 expression, and GH receptor messenger RNA expression in equine and porcine species. Biology of Reproduction 69 1013-1022.
54. Marhaba R, Bourouba M & Zoller M 2005 CD44v6 promotes proliferation by persisting activation of MAP kinases. Cell Signalling 17 961-973.
55. Oh SH, Miyoshi K & Funahashi R 1998 Rat oocytes fertilized in modified rat 1-cell embryo culture medium containing a high sodium chloride concentration and bovine serum albumin maintain developmental ability to the blastocyst stage. Biology of Reproduction 59 884-889.
56. Ohta N, Saito H, Kaneko T, Yoshida M, Takahashi T, Saito T, Nakahara K & Hiroi M 2001 Soluble CD44 in human ovarian follicular fluid. Journal of Assisted Reproduction and Genetics 18 21-25.
57. Roscic-Mrkic B, Fischer M, Leemann C, Manrique A, Gordon CJ, Moore JP, Proudfoot AE & Trkola A 2003 RANTES (CCL5) uses the proteoglycan CD44 as an auxiliary receptor to mediate cellular activation signals and HIV-1 enhancement. Blood 102 1169-1177.
58. Ruoslahti E & Yamaguchi Y 1991 Proteoglycans as modulators of growth factor activities. Cell 64 867-869.
59. Sakai K, Kimata K, Sato T, Gotoh M, Narimatsu H, Shinomiya K & Watanabe H 2007 Chondroitin sulfate N-acetylgalactosaminyltransferase-1 plays a critical role in chondroitin sulfate synthesis in cartilage. Journal of Biological Chemistry 282 4152-4162.
60. Salustri A, Yanagishita M & Hascall VC 1989 Synthesis and accumulation of hyaluronic acid and proteoglycans in the mouse cumulus cell-oocyte complex during follicle-stimulating hormone-induced mucification. Journal of Biological Chemistry 264 13840-13847.
61. Salustri A, Ulisse S, Yanagishita M & Hascall VC 1990 Hyaluronic acid synthesis by mural granulosa cells and cumulus cells in vitro is selectively stimulated by a factor produced by oocytes and by transforming growth factor-beta. Journal of Biological Chemistry 265 19517-19523.
62. Salustri A, Yanagishita M, Underhill CB, Laurent TC & Hascall VC 1992 Localization and synthesis of hyaluronic acid in the cumulus cells and mural granulosa cells of the preovulatory follicle. Developmental Biology 151 541-551.
63. Sato E, Ishibashi T & Koide SS 1987 Prevention of spontaneous degeneration of mouse oocytes in culture by ovarian glycosaminoglycans. Biology of Reproduction 37 371-376.
64. Sato E, Kawamura N & Ishibashi T 1988 Chemicals influencing maturation, activation, and degeneration of bovine oocytes in culture. Journal of Dairy Science 71 3482-3488.
65. Sato E, Inoue M, Takahashi Y & Toyoda Y 1994 Glycosaminoglycans prevent induction of fragmentation of porcine oocytes stimulated by dibutyryl cyclic adenosine 3′,5′-monophosphate in culture. Cell Structure and Function 19 29-36.
66. Sato T, Gotoh M, Kiyohara K, Kameyama A, Kubota T, Kikuchi N, Ishizuka Y, Iwasaki H, Togoyachi A, Kudo T et al. 2003 Molecular cloning and characterization of a novel human beta 1,4-N-acetylgalactosaminyltransferase, beta 4GalNAc-T3, responsible for the synthesis of N,N'-diacetyllactosediamine, galNAc beta 1-4GlcNAc. Journal of Biological Chemistry 278 47534-47544.
67. Schoenfelder M & Einspanier R 2003 Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle. Biology of Reproduction 69 269-277.
68. Screaton GR, Bell MV, Jackson DG, Cornelis FB, Gerth U & Bell JI 1992 Genomic structure of DNA encoding the lymphocyte homing receptor CD44 reveals at least 12 alternatively spliced exons. PNAS 89 12160-12164.
69. Shi M, Dennis K, Peschon JJ, Chandrasekaran R & Mikecz K 2001 Antibody-induced shedding of CD44 from adherent cells is linked to the assembly of the cytoskeleton. Journal of Immunology 167 123-131.
70. Shi X, Leng L, Wang T, Wang W, Du X, Li J, McDonald C, Chen Z, Murphy JW, Lolis E et al. 2006 CD44 is the signaling component of the macrophage migration inhibitory factor-CD74 receptor complex. Immunity 25 595-606.
71. Silbert JE & Freilich LS 1980 Biosynthesis of chondroitin sulphate by a Golgi-apparatus-enriched preparation from cultures of mouse mastocytoma cells. Biochemical Journal 190 307-313.
72. Singh R, Subramanian S, Rhodes JM & Campbell BJ 2006 Peanut lectin stimulates proliferation of colon cancer cells by interaction with glycosylated CD44v6 isoforms and consequential activation of c-Met and MAPK: functional implications for disease-associated glycosylation changes. Glycobiology 16 594-601.
73. Spicer AP, Olson JS & McDonald JA 1997a Molecular cloning and characterization of a cDNA encoding the third putative mammalian hyaluronan synthase. Journal of Biological Chemistry 272 8957-8961.
74. Spicer AP, Seldin MF et al. 1997b Chromosomal localization of the human and mouse hyaluronan synthase genes. Genomics 41 493-497.
75. Suchanek E, Simunic V, Juretic D & Grizelj V 1994 Follicular fluid contents of hyaluronic acid, follicle-stimulating hormone and steroids relative to the success of in vitro fertilization of human oocytes. Fertility and Sterility 62 347-352.
76. Therien I, Bergeron A, Bousquet D & Manjunath P 2005 Isolation and characterization of glycosaminoglycans from bovine follicular fluid and their effect on sperm capacitation. Molecular Reproduction and Development 71 97-106.
77. Tolg C, Hofmann M, Herrlich P & Ponta H 1993 Splicing choice from ten variant exons establishes CD44 variability. Nucleic Acids Research 21 1225-1229.
78. Toyoda Y & Chang MC 1974 Fertilization of rat eggs in vitro by epididymal spermatozoa and the development of eggs following transfer. Journal of Reproduction and Fertility 36 9-22.
79. Toyokawa K, Harayama H & Miyake M 2005 Exogenous hyaluronic acid enhances porcine parthenogenetic embryo development in vitro possibly mediated by CD44. Theriogenology 64 378-392.
80. Uyama T, Kitagawa H, Tamura Ji J & Sugahara K 2002 Molecular cloning and expression of human chondroitin N-acetylgalactosaminyltransferase: the key enzyme for chain initiation and elongation of chondroitin/dermatan sulfate on the protein linkage region tetrasaccharide shared by heparin/heparan sulfate. Journal of Biological Chemistry 277 8841-8846.
81. Wade MA, Roman SD, Jones RC & Aitken RJ 2003 Adenylyl cyclase isoforms in rat testis and spermatozoa from the cauda epididymidis. Cell and Tissue Research 314 411-419.
82. Watanabe K & Yamaguchi Y 1996 Molecular identification of a putative human hyaluronan synthase. Journal of Biological Chemistry 271 22945-22948.
83. Weigel PH, Hascall VC & Tammi M 1997 Hyaluronan synthases. Journal of Biological Chemistry 272 13997-14000.
84. Whittingham DG 1971 Culture of mouse ova. Journal of Reproduction and Fertility 14 (Supplement) 7-21.
85. Yada T, Gotoh M, Sato T, Shionyu M, Go M, Kaseyama H, Iwasaki H, Kikuchi N, Kwon YD, Togayachi A et al. 2003a Chondroitin sulfate synthase-2. Molecular cloning and characterization of a novel human glycosyltransferase homologous to chondroitin sulfate glucuronyltransferase, which has dual enzymatic activities. Journal of Biological Chemistry 278 30235-30247.
86. Yada T, Sato T, Kaseyama H, Gotoh M, Iwasaki H, Kikuchi N, Kwon YD, Togayachi A, Kudo T, Watanabe H et al. 2003b Chondroitin sulfate synthase-3. Molecular cloning and characterization. Journal of Biological Chemistry 278 39711-39725.
87. Yanagishita M & Hascall VC 1979 Biosynthesis of proteoglycans by rat granulosa cells cultured in vitro. Journal of Biological Chemistry 254 12355-12364.
88. Yanagishita M, Rodbard D & Hascall VC 1979 Isolation and characterization of proteoglycans from porcine ovarian follicular fluid. Journal of Biological Chemistry 254 911-920.
89. Yokoo M, Miyahayashi Y, Naganuma T, Kimura N, Sasada H & Sato E 2002a Identification of hyaluronic acid-binding proteins and their expressions in porcine cumulus-oocyte complexes during in vitro maturation. Biology of Reproduction 67 1165-1171.
90. Yokoo M, Tientha P, Kimura N, Niwa K, Sato E & Rodriguez-Martinez H 2002b Localisation of the hyaluronan receptor CD44 in porcine cumulus cells during in vivo and in vitro maturation. Zygote 10 317-326.
91. Yokoo M, Shimizu T, Kimura N, Tunjung WA, Matsumoto H, Abe H, Sasada H, Rodriguez-Martinez H & Sato E 2007 Role of the hyaluronan receptor CD44 during porcine oocyte maturation. Journal of Reproduction and Development 53 263-270.