Germ cell proliferation and apoptosis during different phases of swordfish (Xiphias gladius L.) spermatogenetic cycle

Journal of Fish Biology

Volumn 70, Issue 1, 2007, Pages 83-99

  Corriero, A ^a   Desantis, S ^a   Bridges, C R ^b   Kime, D E ^c   Megalofonou, P ^d   Santamaria, N ^a   Cirillo, F ^a   Ventriglia, G ^a   Di Summa, A ^a   Deflorio, M ^a   Campobasso, F ^a   De Metrio, G ^a  

^a UNIVERSITY OF BARI   (Italy)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

^d UNIVERSITY OF ATHENS   (Greece)

Author keywords

Apoptosis; Germ cells; Proliferation; Spermatogenetic cycle; Swordfish; Testis

Indexed keywords

ANTIBODY; ANTIGEN; APOPTOSIS; GERM CELL; PERCIFORM; REPRODUCTIVE CYCLE; SEASONAL VARIATION; TESTOSTERONE;

XIPHIAS GLADIUS;

EID: 33846089932     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2006.01257.x     Document Type: Article

References (56)

1. Billard, R., Jalabert, B. & Breton, B. (1972). Les cellules de Sertoli des poissons téléostéens. I. Étude ultrastructurale. Annales de Biologie Animale, Biochimie et Biophysique 12, 19-32.
2. Billard, R., Fostier, A., Weil, C. & Breton, B. (1982). Endocrine control of spermatogenesis in teleost fish. Canadian Journal of Fisheries and Aquatic Sciences 39, 65-79.
3. Blanco-Rodriguez, J. & Martinez-Garcia, C. (1996). Spontaneous germ cell death in the testis of the adult rat takes the form of apoptosis: re-evaluation of cell types that exhibit the ability to die during spermatogenesis. Cell Proliferation 29, 13-31.
4. Blottner, S., Hingst, O. & Meyer, H. H. D. (1995). Inverse relationship between testicular proliferation and apoptosis in mammalian seasonal breeders. Theriogenology 44, 320-328.
5. Blottner, S., Roelants, H., Wagner, A. & Wenzel, U. D. (1999). Testicular mitosis, meiosis and apoptosis in mink (Mustela vison) during breeding and non-breeding season. Animal Reproduction Sciences 57, 237-249.
6. Borg, B. (1994). Androgens in teleost fishes. Comparative Biochemistry and Physiology 109C, 219-245.
7. Callard, G. V., Jorgensen, J. C. & Redding, J. M. (1995). Biochemical analysis of programmed cell death during premeiotic stages of spermatogenesis in vivo and in vitro. Developmental Genetics 16, 140-147.
8. Cefali, A., Bruno, R. & Minniti, F. (1998). Intercellular bridges in the immature swordfish (Xiphias gladius L. 1758) testis. Biologia Marina Mediterranea 5, 670-673.
9. Cinquetti, R. & Dramis, L. (2003). Histological, histochemical and ultrastructural investigations of the testis of Padogobius martensi between annual breeding seasons. Journal of Fish Biology 63, 1402-1428.
10. Comeau, L. A., Campana, S. E., Chouinard, G. A. & Hanson, J. (2001). Timing of Atlantic cod Gadus morhua seasonal migrations in relation to serum levels of gonadal and thyroidal hormones. Marine Ecology Progress Series 221, 245-253.
11. Consten, D., Keuning, E. D., Bogerd, J., Zandbergen, M. A., Lambert, J. G. D., Komen, J. & Goos, H. J. Th. (2002). Sex steroids and their involvement in the cortisol-induced inhibition of pubertal development in male common carp, Cyprinus carpio L. Biology of Reproduction 67, 465-472.
12. Corriero, A., Acone, F., Desantis, S., Zubani, D., Deflorio, M., Ventriglia, G., Bridges, C. R., Labate, M., Palmieri, G., McAllister, B. G., Kime, D. E. & De Metrio, G. (2004). Histological and immunohistochemical investigation on ovarian development and plasma estradiol levels in the swordfish (Xiphias gladius L.). European Journal of Histochemistry 48, 413-422.
13. Cuisset, B., Pradelles, P., Kime, D. E., Kühn, E. R., Babin, P., Davail, S. & Le Menn, F. (1994). Enzyme immonoassay for 11-ketotestosterone using acetylcholinesterase as label: application to the measurement of 11-ketotestosterone in plasma of Siberian sturgeon. Comparative Biochemistry and Physiology C 108, 229-241.
14. De Metrio, G., Desantis, S., Santamaria, N., Labate, M., Acone, F., Sanna, L. & Palmieri, G. (1996). Osservazioni in TEM sui tubuli seminiferi del testicolo di giovani di pesce spada (Xhiphias gladius L.). Biologia Marina Mediterranea 3, 365-369.
15. De Metrio, G., Cacucci, M., Corriero, A., Santamaria, N. & Spedicato, D. (1998). Investigation on the fishing activities and on the biology of large pelagic fish (Thunnus thynnus L., Thunnus alalunga Bonn., Sarda sarda Bloch, Xiphias gladius L., Auxis rochei Risso) in the northern Ionian Sea from 1990 to 1997. Biologia Marina Mediterranea 5, 215-228.
16. De Metrio, G., Corriero, A., Desantis, S., Zubani, D., Cirillo, F., Deflorio, M., Bridges, C. R., Eicker, J., de la Serna, J. M., Megalofonou, P. & Kime, D. E. (2003). Evidence of a high percentage of intersex in the Mediterranean swordfish. Marine Pollution Bulletin 46, 358-361.
17. Dunkel, L., Hirvonen, V. & Erkkila, K. (1997). Clinical aspect of male germ cell apoptosis during testis development and spermatogenesis. Cell Death and Differentiation 4, 171-179.
18. Grier, H. J. (1993). Comparative organization of Sertoli cells including the Sertoli cell barrier. In The Sertoli Cell (Russel, L. D. & Griswold, M. D., eds), pp. 704-739. Clearwater, FL: Chace River Press.
19. Grier, H. J., Linton, J. R., Leatherland, J. F. & DeVlaming, V. L. (1980). Structural evidence for two different testicular types in teleost fishes. The American Journal of Anatomy 159, 331-345.
20. Harmin, S. A., Crim, L. W. & Wiegand, M. D. (1995). Isolation, partial characterization, induction, and the occurrence in plasma of the major vitelline envelope proteins in the Atlantic halibut (Hippoglossus hippoglossus) during sexual maturation. Canadian Journal of Fisheries and Aquatic Sciences 51, 1700-1707.
21. Jespersen, Å. (1984). Spermatozoans from a parasitic dwarf male of Neoceratias spinifer Pappenheim, 1914. Videnskabelige Meddelelser Dansk naturhistorisk Forening 145, 37-42.
22. Kime, D. A. & Manning, N. J. (1982). Seasonal patterns of free and conjugated androgens in the brown trout Salmo trutta. General and Comparative Endocrinology 48, 222-231.
23. Koya, Y., Soyano, K., Yamamoto, K., Obana, H. & Matsubara, T. (2002). Testicular development and serum profiles of steroid hormone levels in captive male Pacific herring Cuplea pallasii during their first maturational cycle. Fisheries Sciences 68, 1099-1105.
24. Lahnsteiner, F. & Patzner, R. A. (1990). Spermiogenesis and structure of mature spermatozoa in blenniid fishes (Pisces, Blenniidae). Journal of Submicroscopic Cytology and Pathology 22, 565-576.
25. LeGrand, E. K. (1997). An adaptationist view of apoptosis. Quarterly Review of Biology 72, 135-147.
26. Liu, H. W., Stickney, R. R. & Dickhoff, W. W. (1991). Changes in plasma concentrations of sex steroids in adult Pacific halibut, Hippoglossus stenolepis. Journal of the World Aquaculture Society 22, 30-35.
27. Mattei, X., Siau, Y., Thiaw, O. T. & Thiam, D. (1993). Peculiarities in the organization of testis of Ophiodon sp. (Pisces Teleostei). Evidence for two types of spermatogenesis in teleost fish. Journal of Fish Biology 43, 931-937.
28. Megalofonou, P., Dean, J. M., Metrio, G., Wilson, C. & Berkeley, S. (1995). Age and growth of juvenile swordfish, Xiphias gladius Linnaeus, from the Mediterranean Sea. Journal of Experimental Marine Biology and Ecology 188, 79-88.
29. Minniti, F., Bruno, R., Labate, M., Desantis, S., De Metrio, G. & Mauceri, A. (2005). Ultrastructural features of germ cells in immature swordfish Xiphias gladius (Teleostei, Xiphidae). Italian Journal of Zoology 72, 217-221.
30. Miura, T., Yamauchi, K., Takahashi, H. & Nagahama, Y. (1991). Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Proceedings of the National Academy of Sciences USA 88, 5774-5778.
31. Nandi, S., Banerjee, P. P. & Zirkin, B. R. (1999). Germ cell apoptosis in the testes of Sprague Dawley rats following testosterone withdrawal by ethane 1,2-dimethanesulfonate administration: relationship to Fas? Biology of Reproduction 61, 70-75.
32. Nash, J. P., Davail-Cuisset, B., Bhattacharyya, S., Suter, H., Le Menn, F. & Kime, D. E. (2000). An enzyme linked immunosorbant assay (ELISA) for testosterone, 17β-estradiol, and 17α,20β-dihydroxy-4-pregnen-3- one using acetylcholinesterase as tracer: application to measurement of diel patterns in rainbow trout (Oncorhynchus mykiss). Fish Physiology and Biochemistry 22, 355-363.
33. Nonclercq, D., Reverse, D., Toubeau, G., Beckers, J. F., Sulon, J., Laurent, G., Zanen, J. & Heuson-Stiennon, J. A. (1996). In situ demonstration of germinal cell apoptosis during diethylstilbestrol-induced testis regression in adult male Syrian hamsters. Biology of Reproduction 55, 1368-1376.
34. Orsi Relini, L., Palandri, G., Garibaldi, F. & Cima, C. (1996). Swordfish maturity and growth. New observations in the Ligurian Sea. Biologia Marina Mediterranea 3, 352-359.
35. Patterson, D. A., MacDonald, J. S., Hinch, S. G., Healey, M. C. & Farrell, A. P. (2004). The effect of exercise and captivity on energy partitioning, reproductive maturation and fertilization success in adult sockeye salmon. Journal of Fish Biology 64, 1039-1059.
36. Potoschi, A., Cavallaro, G., Sturiale, P. & Lo Duca, G. (1994). Eggs and larvae of swordfish, tuna and albacore caught in the Ionian Sea. Biologia Marina Mediterranea 1, 119-124.
37. Prisco, M., Liguoro, A., Comitato, R., Cardone, A., D'Onghia, B., Ricchiari, L., Angelini, F. & Andreucci, P. (2003). Apoptosis during spermatogenesis in the spotted ray Torpedo marmorata. Molecular Reproduction and Development 64, 341-348.
38. Rodriguez, I., Ody, C., Araki, K., Garcia, I. & Vassalli, P. (1997). An early and massive wave of germinal cell apoptosis is required for the development of functional spermatogenesis. EMBO Journal 16, 2262-2270.
39. Scott, A. P., Bye, V. J., Baynes, S. M. & Springate, J. C. R. (1980). Seasonal variation in plasma concentration of 11-ketotestosterone and testosterone in male rainbow trout, Salmo gairdnerii Richardson. Journal of Fish Biology 17, 495-505.
40. de la Serna, J. M., Ortiz de Urbina, J. M. & Macias, D. (1996). Observations on sex-ratio, maturity and fecundity by length-class for swordfish (Xiphias gladius) captured with surface longline in the western Mediterranean. ICCAT Collective Volume of Scientific Papers 45, 115-139.
41. Sharpe, R. M. (1994). Regulation of spermatogenesis. In The Physiology of Reproduction (Knobil, E. & Neill, J. D., eds), pp. 1363-1434. New York: Raven Press.
42. Sinha Hikim, A. P. & Swerdloff, R. S. (1999). Hormonal and genetic control of germ cell apoptosis in the testis. Reviews of Reproduction 4, 38-47.
43. Sol, S. Y., Olson, O. P., Lomaz, D. P. & Johnson, L. L. (1998). Gonadal development and associated changes in plasma reproductive steroids in English sole, Pleuronectes vetulus, from Puget Sound, Washington. Fisheries Bulletin 96, 859-870.
44. Štrbenc, M., Fazarinc, G., Bavdek, V. & Pogačnik, A. (2003). Apoptosis and proliferation during seasonal testis regression in the brown hare (Lupus europaeus L.). Anatomia Histologia Embryologia 32, 48-53.
45. Tserpes, G., Peristeraki, P. & Somarakis, S. (2001). On the reproduction of swordfish (Xiphias gladius L.) in the eastern Mediterranean. ICCAT Collective Volume of Scientific Papers 52, 740-744.
46. Uchida, D., Yamashita, M., Kitano, T. & Iguchi, T. (2002). Oocyte apoptosis during the transition from ovary-like tissue to testes during sex differentiation of juvenile zebrafish. The Journal of Experimental Biology 205, 711-718.
47. Vaux, D. L. & Strausser, A. (1996). The molecular biology of apoptosis. Proceedings of the National Academy of Sciences USA 93, 2239-2244.
48. Weber, L. P., Kiparissis, Y., Hwang, G. S., Niimi, A. J., Janz, D. M. & Metcalfe, C. D. (2002). Increased cellular apoptosis after chronic aqueous exposure to nonylphenol and quercetin in adult medaka (Oryzias latipes). Comparative Biochemistry and Physiology 131, 51-59.
49. Weltzien, F.-A., Taranger, G. L., Karlsen, Ø. & Norberg, B. (2002). Spermatogenesis and related androgen levels in Atlantic halibut (Hippoglossus hippoglossus L.). Comparative Biochemistry and Physiology A 132, 567-575.
50. Woods, A. L., Hall, P. A., Shepherd, N. A., Hanby, A. M., Waseem, N. H., Lane, D. P. & Levison, D. A. (1991). The assessment of proliferating cell nuclear antigen (PCNA) immunostaining in primary gastrointestinal lymphomas and its relationship to histological grade, S+G2+M phase fraction (flow cytometric analysis) and prognosis. Histopathology 19, 21-27.
51. Woolveridge, I., de Boer-Brouwer, M., Taylor, F., Teerds, K. J., Wu, F. C. W. & Morris, I. D. (1999). Apoptosis in the rat spermatogenic epithelium following androgen withdrawal: changes in apoptosis-related genes. Biology of Reproduction 60, 461-470.
52. Yin, Y., Stahl, B. C., DeWolf, W. C. & Morgentaler, A. (1998). p53-mediated germ cell quality control in spermatogenesis. Developmental Biology 204, 165-171.
53. Young, K. A. & Nelson, R. J. (2001). Mediation of seasonal testicular regression by apoptosis. Reproduction 122, 677-685.
54. Young, K. A., Zirkin, B. R. & Nelson, R. J. (1999). Short photoperiod induces testicular apoptosis in the white-footed mouse (Peromyscus leucopus). Endocrinology 140, 1331-1339.
55. Yoneda, M., Tokimura, M., Fujita, H., Takeshita, N., Takeshita, K., Matsuyama, M. & Matsuura, S. (1998). Reproductive cycle and sexual maturity of the anglerfish Lophiomus setigerus in the East China Sea with a note on specialized spermatogenesis. Journal of Fish Biology 52, 164-178.
56. Yu, C., Hall, P. A., Fletcher, C. D., Camplejohn, R. S., Waseem, N. H., Lane, D. P. & Levison, D. A. (1991). Haemangiopericytomas: the prognostic value of immunohistochemical staining with a monoclonal antibody to proliferating cell nuclear antigen (PCNA). Histopathology 19, 29-33.