Detection of the hyaluronan receptor CD44 in the bovine oviductal epithelium

Journal of Reproduction and Development

Volumn 51, Issue 4, 2005, Pages 445-453

  Bergqvist, Ann Sofi ^a,b   Yokoo, Masaki ^c   Båge, Renée ^a   Sato, Eimei ^c   Rodríguez Martínez, Heriberto ^a,b  

^a SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

^b Swedish University of Agricultural Sciences   (Sweden)

^c TOHOKU UNIVERSITY   (Japan)

Author keywords

Bovine; CD44; Hyaluronan; Oviduct

Indexed keywords

HERMES ANTIGEN; HYALURONIC ACID;

ANIMAL; ARTICLE; BIOSYNTHESIS; CATTLE; CHEMISTRY; CYTOLOGY; EPITHELIUM; EPITHELIUM CELL; ESTRUS CYCLE; FEMALE; IMMUNOHISTOCHEMISTRY; METABOLISM; OVIDUCT; UTERUS; WESTERN BLOTTING;

ANIMALS; ANTIGENS, CD44; BLOTTING, WESTERN; CATTLE; EPITHELIAL CELLS; EPITHELIUM; ESTROUS CYCLE; FEMALE; HYALURONIC ACID; IMMUNOHISTOCHEMISTRY; OVIDUCTS; UTERUS;

ANIMALIA; BOS TAURUS; BOVINAE;

EID: 25644438585     PISSN: 09168818     EISSN: 13484400     Source Type: Journal    
DOI: 10.1262/jrd.17010     Document Type: Article

References (56)

1. Alho AM, Underhill CB. The hyaluronate receptor is preferentially expressed on proliferating epithelial cells. J Cell Biol 1989; 108: 1557-1565.
2. Lee CN, Ax RL. Concentrations and compositions of glycosaminoglycans in the bovine female reproductive tract. J Dairy Sci 1984; 67: 2006-2009.
3. Toole BP. Hyaluronan and its binding proteins, the hyaladherins. Curr Opin Cell Biol 1990; 2: 839-844.
4. Underhill C. CD44: the hyaluronan receptor. J Cell Sci 1992; 103: 292-298.
5. Turley EA. Hyaluronan and cell locomotion. Cancer Metastasis Rev 1992; 11: 21-30.
6. Hunnicutt GR, Primakoff P, Myles DG. Sperm surface protein PH-20 is bifunctional: one activity is a hyaluronidase and a second, distinct activity is required in secondary sperm-zona binding. Biol Reprod 1996; 55: 80-86.
7. Aruffo A, Stamenkovic I, Melnick M, Underhill CB, Seed B. CD44 is the principal cell surface receptor for hyaluronate. Cell 1990; 61: 1303-1313.
8. Ponta H, Wianwright D, Herrlich P. The CD44 protein family. J Biochem Cell Biol 1998; 30: 299-305.
9. Culty M, Nguyen HA, Underhill CB. The hyaluronan receptor (CD44) participates in the uptake and degradation of hyaluronan. J Cell Biol 1992; 116: 1055-1062.
10. Thomas L, Byers HR, Vink J, Stamenkovic I. CD44H regulates tumor cell migration on hyaluronate-coated substrate. J Cell Biol 1992; 118: 971-977.
11. Woerner SM, Givehchian M, Durst M, Schneider A, Costa S, Melsheimer P, Lacroix J, Zoller M, Doeberitz MK. Expression of CD44 splice variants in normal, dysplastic, and neoplastic cervical epithelium. Clin Cancer Res 1995; 1: 1125-1132.
12. Borland G, Ross JA, Guy K. Forms and functions of CD44. Immunol 1998; 93: 139-148.
13. Saegusa M, Hashimura M, Okayasu I. CD44 expression in normal, hyperplastic, and malignant endometrium. J Pathol 1998; 184: 297-306.
14. Kaneko T, Saito H, Toya M, Satio T, Nakahara K, Hiroi M. Hyalronic acid inhibits apoptosis in granulose cells via CD44. J Assist Reprod Genet 2000; 17: 162-167.
15. Knudson W, Chow G, Knudson CB. CD44-mediated uptake and degradation of hyaluronan. Matrix Biol 2002; 21: 15-23.
16. Turley EA, Nobie PW, Bourguignon YW. Signalling properties of hyaluronan receptors. J Biol Chem 2002; 277: 4589-4592.
17. Behzad F, Seif MW, Campbell S, Aplin JD. Expression of two isoforms of CD44 in human endometrium. Biol Reprod 1994; 51: 739-747.
18. Albers A, Thie M, Hohn HP, Denker HW. Differential expression and localization of integrins and CD44 in the membrane domains of human uterine epithelial cells during the menstrual cycle. Acta Anat 1995; 153: 12-19.
19. Ohta N, Saito H, Kaneko T, Yoshida M, Takahashi T, Saito T, Nakahara, K, Hiroi M. Soluble CD44 in human ovarian follicular fluid. J Assist Reprod Genet 2001; 18: 21-25.
20. Goshen R, Ariel I, Shuster S, Hochberg A, Vlodavsky I, de Groot N, Ben-Rafael Z, Stern R. Hyaluronan, CD44 and its variant exons in human trophoblast invasion and placental angiogenesis. Mol Hum Reprod 1996; 2: 685-691.
21. Aplin JD. Adhesion molecules in implantation. Rev Reprod 1997; 2: 84-93.
22. Marzioni D, Crescimanno C, Zaccheo D, Coppari R, Underhill CB, Castellucci M. Hyaluronate and CD44 expression in the human placenta throughout pregnancy. Eur J Histochem 2001; 45: 131-140.
23. Furnus CC, Valcarcel A, Dulout FN, Errecalde AL. The hyaluronic acid receptor (CD44) is expressed in bovine oocytes and early stage embryos Theriogenology 2003; 60: 1633-1644.
24. Ball GD, Bellin, ME Ax, RL, First NL. Glycosaminoglycans in bovine cumulus-oocyte complexes; morphology and chemistry. Mol Cell Endocrinol 1982; 28: 113-122.
25. Schoenfelder M, Einspanier R. Expression of hyaluronan synthases and corresponding hyaluronan receptors is differentially regulated during oocyte maturation in cattle. Biol Reprod 2003; 69: 269-277.
26. 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.
27. Yokoo M, Miyahayashi Y, Naganuma T, Kimura N, Hiroshi S, Sato E. Identification of hyaluronic acid-binding proteins and their expression in porcine cumulus-oocyte complexes during in vitro maturation. Biol Reprod 2002; 67: 1165-1171.
28. Yokoo M, Tienthai P, Kimura N, Niwa K, Sato E, Rodriguez-Martinez H. Localisation of the hyaluronan receptor CD44 in porcine cumulus cells during in vivo and in vitro maturation. Zygote 2002; 10: 317-326.
29. Eppig JJ. FSH stimulates hyaluronic acid synthesis by oocyte-cumulus cell complexes from mouse preovulatory follicles. Nature 1979; 281: 483-484.
30. Ohta N, Sairo H, Kuzumkai T, Takahashi T, Ito NM, Saito T, Nakahara K, Hiroi M. Expression of CD44 in human cumulus and mural granulosa cells of individual patients in in-vitro fertilization programmes. Mol Hum Reprod 1999; 5: 22-28.
31. Ranganathan S, Ganguly AK, Datta K. Evidence for presence of hyaluronan binding protein on spermatozoa and its possible involvement in sperm function. Mol Reprod Dev 1994; 38: 69-76.
32. Hunter RH. The Fallopian tubes: their role in fertility and infertility. In: The Fallopian Tubes, Chapter IV. New York: Springer-Verlag, 1988; 53-74.
33. Hunter RH, Flechon B, Flechon JE. Distribution, morphology and epithelial interactions of bovine spermatozoa in the oviduct before and after ovulation: a scanning electron microscope study. Tissue Cell 1991; 23: 641-656.
34. Lefebvre R, Chenoweth PJ, Drost M, LeClear CT, MacCubbin M, Dutton JT, Suarez SS. Characterization of the oviductal sperm reservoir in cattle. Biol Reprod 1995; 53: 1066-1074.
35. Pollard JW, Plante C, King WA, Hansen PJ, Betteridge KJ, Suarez SS. Fertilizing capacity of bovine sperm may be maintained by binding to oviductal epithelial cells. Biol Reprod 1991; 44: 102-107.
36. Lefebvre R, Suarez SS. Effect of capacitation on bull sperm binding to homologous oviductal epithelium. Biol Reprod 1996; 54: 575-582.
37. Fazeli A, Duncan AE, Watson PF, Holt WV. Sperm - oviduct interaction: induction of capacitation and preferential binding of uncapacitated spermatozoa to oviductal epithelial cells in porcine species. Biol Reprod 1999; 60: 879-886.
38. Rodriguez-Martinez H, Tienthai P, Suzuki K, Funahashi H, Ekwall H, Johannisson A. Involvement of oviduct in sperm capacitation and oocyte development in pigs. Reproduction 200; 58 (suppl): 129-145.
39. Parrish JJ, Susko-Parrish JL, Handrow RR, Sims MM, First ML. Capacitation of bovine spermatozoa by oviduct fluid. Biol Reprod 1989; 40: 1020-1025.
40. Huszar G, Willetts M, Corrales M. Hyaluronic acid (Sperm Select) improves retention of sperm motility and velocity in normospermic and oligospermic specimens. Fertil Steril 1990; 54: 1127-1134.
41. Kawakami E, Hori T, Tsutsui T. Induction of dog sperm capacitation by oviductal fluid. J Vet Med Sci 1998; 60: 197-202.
42. Suzuki K, Asano A, Eriksson B, Niwa K, Nagai T, Rodriguez-Martinez H. Capacitation status and in vitro fertility of boar spermatozoa: effects of seminal plasma, cumulus-oocyte-complexes-conditioned medium and hyaluronan. Inter J Androl 2002; 25: 84-93.
43. Bergqvist A-S, Rodríguez-Martínez H. Distribution of hyaluronan in the bovine oviduct. In: IETS Proceedings; 2003; Auckland, New Zeeland. Theriogenology 59; Abstract 467.
44. Tienthai P, Kjellén L, Pertoft H, Suzuki K, Rodríguez- Martínez H. Localization and quantitation of hyaluronan and sulphated glycosaminglycans in the tissues and intraluminal fluid of the pig oviduct. Reprod Fertil Develop 2000; 12: 173-182.
45. Tienthai P, Yokoo M, Kimura N, Heldin P, Sato E, Rodriguez-Martinez H. Immunohistochemical localization and expression of the hyaluronan receptor CD44 in the epithelium of the pig oviduct during oestrus. Reproduction 2003; 13: 119-132.
46. Bains R, Adeghe J, Carson RJ. Human sperm cells express CD44. Fertil Steril 2002; 78: 307-312.
47. Duchens M, Rodriguez-Martinez H, Forsberg M, Gustafsson H. Ultrastructure of bovine ovarian follicles induced to extended growth by perioestrous suprabasal progesterone levels. Acta Vet Scand 1996; 37: 239-250.
48. Hirano H, Watanbe T. Microsequencing of protein electrotransferred onto immobilizing matrices from polyacrylamide gel electrophoresis; application of insoluble protein. Electrophor 1990; 11: 573-580.
49. Laurent C, Hellström S, Engström-Laurent A, Wells AF, Bergh A. Localization and quantity of hyaluronan in urogenital organs of male and female rats. Cell Tissue Res 1995; 279: 241-248.
50. Edelstam G, Lundkvist Ö, Wells A, Laurent T. Localization of hyaluronan in regions of the human female reproductive tract. J Histochem Cytochem 1991; 39: 1131-1135.
51. Stamenkovic I, Aruffo A, Amiot M, Seed B. The hematopoietic and epithelial forms of CD44 are distinct polypeptides with different adhesion potentials for hyaluronate-bearing cells. EMBO J 1991; 10: 343-348.
52. Bartolazzi A, Nocks A, Aruffo A, Spring F, Stamenkovic I. Glycosylation of CD44 is implicated in CD44-mediated cell adhesion to hyaluronan. J Cell Biol 1996; 1322: 1199-1208.
53. Jalkanen S, Jalkanen M, Bargatze R, Tammi M, Butcher EC. Biochemical properties of glycoproteins involved in lymphocyte recognition of high endothelial venules in man. J Immunol 1988; 141: 1615-1623.
54. Terpe HJ, Stark H, Prehm P, Gunthert U. CD44 variant isoforms are preferentially expressed in basal epithelial of non-malignant human fetal and adult tissues. Histochem 1994; 101: 79-89.
55. Ulbrich SE, Schoenfelder M, Thoene S, Einspanier R. Hyaluronan in the bovine oviduct-modulation of synthases and receptors during the estrous cycle. Mol Cell Endocrin 2004; 214: 9-18.
56. Ghosh I, Bharadwaj A, Datta K. Reduction in the level of hyaluronan binding protein 1 (HABP1) is associated with loss of sperm motility. J Reprod Immunol 2002; 53: 45-54.