Stage-specific degeneration of germ cells in the seminiferous tubules of non-obese diabetic mice

International Journal of Andrology

Volumn 20, Issue 4, 1997, Pages 243-254

  Sainio Pollanen S ^a   Henriksen K ^a   Parvinen, M ^a   Simell, O ^a   Pollanen P ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

Apoptosis; Infertility; Spermatogenesis; Testis

Indexed keywords

DNA FRAGMENT; PHOSPHATIDYLSERINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; AUTOIMMUNITY; AUTORADIOGRAPHY; CELL DEGENERATION; CELL LABELING; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DIABETES MELLITUS; ETIOLOGY; GERM CELL; MALE; MALE INFERTILITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEMINIFEROUS TUBULE; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM;

EID: 0030733290     PISSN: 01056263     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2605.1997.00061.x     Document Type: Article

References (49)

1. Allan, D. J., Harmon, B. V. & Kerr, J. F. R. (1987) Cell death in spermatogenesis. In: Perspectives on Mammalian Cell Death (ed. C. S. Potten CS), pp. 229-258. Oxford University Press, London.
2. Allan, D. J., Harmon, B. V. & Roberts, S. A. (1992) Spermatogonial apoptosis has three morphologically recognizable phases and shows no circadian rhythm during normal spermatogenesis in the rat. Cell Proliferation, 25, 241-250.
3. Billig, H., Furuta, I. & Hsueh, J. W. (1995a) Gonadotropin-releasing hormone directly induces apoptotic cell death in the rat ovary: biochemical and in situ detection of deoxyribonucleic acid fragmentation in granulosa cells. Endocrinology, 134, 245-251.
4. Billig, H., Furuta, I., Rivier, C., Tapanainen, J., Parvinen, M. & Hsueh, A. J. (1995b) Apoptosis in testis germ cells: developmental changes in gonadotropin dependence and localization to selective tubule stages. Endocrinology, 136, 5-12.
5. Brinkworth, M. H., Weinbauer, G. F., Schlatt, S. & Nieschlag, E. (1995) Identification of male germ cells undergoing apoptosis in adult rats. Journal of Reproduction and Fertility, 105, 25-33.
6. Bursch, W., Kleine, L. & Tenniswood, M (1990) The biochemistry of cell death by apoptosis. Biochemistry and Cell Biology, 68, 1071-1074.
7. Bursch, W., Taper, H. S., Lauer, B. & Schulte-Hermann, R. (1985) Quantitative histological and histochemical studies on the occurrence and stages of controlled cell death (apoptosis) during regression of rat liver hyperplasia. Virchows Archives B of Cellular Pathology Including Molecular Pathology, 50, 153-166.
8. Callard, G. V., Jorgensen, J. C. & Redding, J. M. (1985) Biochemical analysis of programmed cell death during premeiotic stages of spermatogenesis in vivo and in vitro. Developmental Genetics, 16, 140-147.
9. Cameron, D. F., Murray, F. T. & Drylie, D. D. (1985) Interstitial compartment pathology and spermatogenic disruption in testes from impotent diabetic men. Anatomical Record, 213, 53-62.
10. Cameron, D. F., Rountree, J., Schultz, R. E., Repetta, D. & Muray, F. T. (1990) Sustained hyperglycaemia results in testicular dysfunction and reduced fertility potential in BBWOR diabetic rats. American Journal of Physiology, 259, E881-889.
11. Casciola-Rosen, L. A., Anhalt, G. J. & Rosen, A. (1995) DNA-dependent protein kinase is one of a subset of autoantigens specifically cleaved early during apoptosis. Journal of Experimental Medicine, 182, 1625-1634.
12. Creasy, D. M., Flynn, J. C., Gray, T. J. B. & Butler, W. H. (1985) A quantitative study of stage-specific spermatocyte damage following administration of ethylene glycol monomethyl ether in the rat. Experimental Molecular Pathology, 43, 321-336.
13. Duvall, E., Wyllie, A. H. & Morris, R. G. (1985) Macrophage recognition of cells undergoing programmed cell death (apoptosis). Immunology, 56, 351-358.
14. French, L. E., Hahne, M., Viard, I., Radlgruber, G., Zanone, R. J., Becker, K., Müller, C. & Tschopp, J. (1996) Fas and Fas ligand in embryos and adult mice: ligand expression in several immune-privileged tissues and coexpression in adult tissues characterized by apoptotic cell turnover. Cell Biology, 133, 335-343.
15. Furuta, I., Porkka-Heiskanen, T., Scarbrough, K., Tapanainen, J., Turek, F. W. & Hsueh, A. J. (1994) Photoperiod regulates testis cell apoptosis in Djungarian hamsters. Biology of Reproduction, 51, 1315-1321.
16. Fushimi, H., Horie, H., Inoue, T., Kameyama, M., Kanao, K., Ishihara, S., Isujimura, T., Nunotani, H., Minami, T. & Okazaki, Y. (1989) Low testosterone levels in diabetic men and animals: a possible role in testicular impotence. Diabetes Research and Clinical Practice, 6, 297-301.
17. Garchon, H. J., Luan, J. J., Eloy, L., Bedossa, P. & Bach, J. F. (1994) Genetic analysts of immune dysfunction in non-obese diabetic (NOD) mice: mapping of a susceptibility locus close to the Bcl-2 gene correlates with increased resistance of NOD T cells to apoptosis induction. European Journal Immunology, 24, 380-384.
18. Gavrieli, Y., Sherman, Y. & Ben-Sasson, S. A. (1992) Identification of programmed cell death in situ via specific labelling of nuclear DNA fragmentation. Journal of Cell Biology, 119, 493-501.
19. Gondos, B. & Bevier, W. (1995) Effect of insulin on testicular alterations in the nonobese diabetic mouse. Annals of Clinical and Laboratory Science, 25, 272-277.
20. Gross-Bellard, M., Oudet, P. & Chambon, P. (1973) Isolation of high molecular-weight DNA from mammalian cells. European Journal of Biochemistry, 36, 32-38.
21. Henriksén, K., Hakovirta, H & Parvinen, M. (1995a) In situ quantification of stage-specific apoptosis in the rat seminiferous epithelium: effects of short-term experimental cryptorchidism. International Journal of Andrology, 18, 256-262.
22. Henriksén, K., Hakovirta, H. & Parvinen, M. (1995b) Testosterone inhibits and induces apoptosis in rat seminiferous tubules in a stage-specific manner: in situ quantification in squash preparations after administration of ethane dimethane sulphonate. Endocrinology, 136, 3285-3291.
23. Henriksén, K., Kulmala, J., Toppari, J., Mehrotra, K. & Parvinen M (1996) Stage-specific apoptosis in the rat seminiferous epithelium: quantification of irradiation effects. Journal of Andrology, in press.
24. Hikim, A. P., Wang, C., Leung, A. & Swerdloff, R. S. (1995) Involvement of apoptosis in the induction of germ cell degeneration in adult rats after gonadotrophin-releasing hormone antagonist treatment. Endocrinology, 136, 2770-2775.
25. Huckins, C. (1978) The morphology and kinetics of spermatogonial degeneration in normal adult rats: an analysis using a simplified classification of the germinal epithelium. Anatomical Record, 190, 905-926.
26. Kerr, J. B. (1992) Spontaneous degeneration of germ cells in normal rat testis. Assessment of cell types and frequency during the spermatogenic cycle. Journal of Reproduction and Fertility, 95, 825-830.
27. Koopman, G., Reutelingsperger, C. P. M., Kuijten, G. A. M., Keehnen, R. M. J., Pals, S. T. & van Oers, M. H. J. (1994) Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood, 84, 1415-1420.
28. Ku, W. W., Wine, R. N., Chae, B. Y., Ghanayem, B. I. & Chapin, R. E. (1995) Spermatocyte toxicity of 2-methoxyethanol (ME) in rats and guinea pigs: evidence for the induction of apoptosis. Toxicology and Applied Pharmacology, 134, 100-110.
29. Kühn-Velten, N., Codjambopoulo, P., Herberg, L., Kley, H. K. & Staib, W. (1985) In-vitro studies of the development of pituitary and testicular functions in diabetes (C57Bl/KsJ-db/db) mutant mice. Hormone and Metabolic Research, 17, 576-579.
30. Martin, S. J., Reutelingsperger, C. P., McGahon, A. J., Rader, J. A., van Schie, R. C., LaFace, D. M., Green, D. R. (1995) Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 and Abl. Journal of Experimental Medicine 182, 1545-1556.
31. Miething, A. (1992) Germ cell death during prespermatogenesis in the testis of the golden hamster. Cell and Tissue Research, 267, 583-590.
32. Murray, F. T., Cameron, D. F., Orth, J. M. & Katovich, M. J. (1985) Gonadal dysfunction in the spontaneously diabetic BB rat: alterations of testes morphology, serum testosterone and LH. Hormone and Metabolic Research, 17, 495-501.
33. Oakberg, E. (1956) A description of spermatogenesis in the mouse and its use in analysis of the cycle of seminiferous epithelium and germ cell renewal. American Journal of Anatomy, 99, 391-413.
34. Oldstone, M. B. A., Nerenberg, M., Southern, P., Price, J. & Lewicki, H. (1991) Virus infection triggers insulin-dependent diabetes mellitus in a transgenic model: role of the anti-self (virus) immune response. Cell, 65, 319-331.
35. Parvinen, M. & Hecht, N. B. (1981) Identification of living spermatogenic cells of the mouse by transillumination-phase contrast microscopic techique for 'in situ' analyses of DNA polymerase activities. Histochemistry, 71, 567-579.
36. Robitaille, P., Dessureault, J., Letarte, J. & O'Regan, S. (1979) Antibodies to sperm-specific nuclear antigens in juvenile diabetics. Annales Immunologie (Paris), 130, 809-813.
37. Russell, L. D. & Clermont, Y. (1977) Degeneration of germ cells in normal, hypophysectomized and hormone treated hypophysectomized rats. Anatomical Record, 187, 347-366.
38. Saari, T., Jahnukainen, K. & Pöllänen P (1996) Autoantigenicity of the basal compartment of seminiferous tubules in the rat. Journal of Reproductive Immunology, 31, 65-80.
39. Sainio-PÖllänen, S., Saari, T., Simell, O. & PÖllänen, P. (1996) CD28-CD80/CD86 interactions in testicular immunoregulation. Journal of Reproductive Immunology, 31, 145-163.
40. Shikone, T., Billig, H. & Hsueh, A. J. (1994) Experimentally induced cryptorchidism increases apoptosis in rat testis. Biology of Reproduction, 51, 865-872.
41. Suda, T., Takahashi, T., Golstein, P. & Nagata, S. (1993) Molecular cloning and expression of the Fas ligand, a novel member of the tumor necrosis factor family. Cell, 75, 1169-1178.
42. Tapanainen, J. S., Tilly, J. L., Vihko, K. K. & Hsueh, A. J. (1993) Hormonal control of apoptotic cell death in the testis: gonadotropins and androgens as testicular cell survival factors. Molecular Endocrinology, 7, 643-650.
43. Tilly, J. T. & Hsueh, A. J. W. (1993) A microscale autoradiographic method for the qualitative and quantitative analysis of apoptotic DNA fragmentation. Journal of Cell Physiology, 154, 519-526.
44. Troiano, L., Fustini, M. F., Lovato, E., Frasoldati, A., Malorni, W., Capri, M., Grassilli, E., Mamma, P. & Franceschi, C. (1994) Apoptosis and spermatogenesis: evidence from an in vivo model of testosterone withdrawal in the adult rat. Biochemical and Biophysical Research Communications, 202, 1315-1321.
45. von Herrath, M. G., Dockter, J., Lewicki, H. & Oldstone, M. B. A. (1994) How virus induces a rapid and slow onset IDDM in a transgenic model. Immunity, 1, 231-242.
46. Watanabe-Fukunaga, R., Brannan, C. I., Itoh, N., Yonehara, S., Copeland, N. G., Jenkins, N. A. & Nagata, S. (1992) The cDNA structure, expression and chromosomal assignment of the mouse Fas antigen. Journal of Immunology, 148, 1274-1279.
47. Wyllie, A. H., Morris, R. G., Smith, A. L. & Dunlop, D. (1984) Chromatin cleavage in apoptosis: association with condensed chromatin morphology and dependence on macromolecular synthesis. Journal of Pathology, 142, 67-77.
48. Wyllie, A. H. (1980) Glucocorticoid-induced thymocyte apoptosis is associated with endogenous endonuclease activation. Nature, 284, 555-556.
49. Yule, T. D., Montoya, G. D., Russell, L. D., Williams, T. M. & Tung, K. S. K. (1988) Autoantigenic germ cells exist outside the blood-testis barrier. Journal of Immunology, 141, 1161-1167.