Histological and stereological evaluation of zebrafish (Danio rerio) spermatogenesis with an emphasis on spermatogonial generations

Biology of Reproduction

Volumn 81, Issue 1, 2009, Pages 177-187

  Leal, Marcelo C ^a,b   Cardoso, Edson R ^a   Nóbrega, Rafael H ^a,b   Batlouni, Sergio R ^a   Bogerd, Jan ^b   França, Luiz R ^a   Schulz, Rüdiger W ^b,c  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b UTRECHT UNIVERSITY   (Netherlands)

^c INSTITUTE OF MARINE RESEARCH   (Norway)

Author keywords

Leydig cells; Sertoli cells; Spermatogenesis; Teleost fish; Testis

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BIOMETRY; CELL MATURATION; CELL PROLIFERATION; CELL STRUCTURE; CONTROLLED STUDY; HISTOLOGY; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; LEYDIG CELL; MALE; MEIOSIS; NONHUMAN; PRIORITY JOURNAL; SERTOLI CELL; SPERMATID; SPERMATOCYTE; SPERMATOGENESIS; SPERMATOGONIUM; STEREOLOGY; TESTIS; ZEBRA FISH;

ANIMALS; CELL COUNT; CELL DIFFERENTIATION; GERM CELLS; LEYDIG CELLS; MALE; MODELS, BIOLOGICAL; SERTOLI CELLS; SPERMATOGENESIS; SPERMATOGONIA; TESTIS; TIGHT JUNCTIONS; ZEBRAFISH;

DANIO RERIO; MAMMALIA; TELEOSTEI; VERTEBRATA;

EID: 67649662580     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.109.076299     Document Type: Article

References (78)

1. Engeszer RE, Patterson LB, Rao AA, Parichy DM. Zebrafish in the wild: a review of natural history and new notes from the field. Zebrafish 2007; 4:21-40. (Pubitemid 46657947)
2. McGonnell IM, Fowkes RC. Fishing for gene function-endocrine modeling in the zebrafish. J Endocrinol 2006; 189:425-439. (Pubitemid 43919221)
3. Briggs JP. The zebrafish: a new model organism for integrative physiology. Am J Physiol Regul Integr Comp Physiol 2002; 282:R3-R9. (Pubitemid 34663905)
4. Aleström P, Holter JL, Nourizadeh-Lillabadi R. Zebrafish in functional genomics and aquatic biomedicine. Trends Biotechnol 2006; 24:15-21. (Pubitemid 43017746)
5. Dahm R, Geisler R. Learning from small fry: the zebrafish as a genetic model organism for aquaculture fish species. Mar Biotechnol (NY) 2006; 8:329-345. (Pubitemid 44221541)
6. Hess RA, França LR. Structure of the Sertoli cell. In: Skinner MK, Griswold MD (eds.), Sertoli Cell Biology. San Diego, CA: Elsevier Academic Press; 2005:19-40.
7. De Rooij DG, Russell LD. All you wanted to know about spermatogonia but were afraid to ask. J Androl 2000; 21:776-798. (Pubitemid 30808061)
8. De Rooij DG. Regulation of spermatogonial stem cell behavior in vivo and in vitro. Anim Reprod 2006; 3:130-134.
9. Ehmcke J, Wistuba J, Schlatt S. Spermatogonial stem cells: questions, models and perspectives. Hum Reprod Update 2006; 12:275-282.
10. Pudney J. Comparative cytology of the non-mammalian vertebrate Sertoli cell. In: Russell LD, Griswold MD (eds.), The Sertoli Cell. Clearwater, FL: Cache River Press; 1993:612-657.
11. Pudney J. Comparative cytology of the Leydig cell. In: Payne AH, Hardy MP, Russell LD (eds.), The Leydig Cell. Vienna, IL: Cache River Press; 1996:98-142.
12. Loir M, Sourdaine P, Mendis-Handagama SM, Jégou B. Cell-cell interactions in the testis of teleost and elasmobranchs. Micr Res Tech 1995; 32:533-552.
13. Jones RC, Lin M. Spermatogenesis in birds. Oxf Rev Reprod Biol 1993; 15:233-264.
14. Gribbins KM, Elsey RM, Gist DH. Cytological evaluation of the germ cell development strategy within the testis of the American alligator, Alligator mississippiensis. Acta Zool (Stockholm) 2006; 87:59-69.
15. Nóbrega RH, Batlouni SR, França LR. An overview of functional and stereological evaluation of spermatogenesis and germ cell transplantation in fish. Fish Physiol Biochem 2009; 35:197-206.
16. Nash JP, Kime DE, Van der Ven LT, Wester PW, Brion F, Maack G, Stahlschmidt-Allner P, Tyler CR. Long-term exposure to environmental concentrations of the pharmaceutical ethynylestradiol causes reproductive failure in fish. Environ Health Perspect 2004; 112:1725-1733. (Pubitemid 40017295)
17. Van den Hurk R, Schoonen WG, van Zoelen GA, Lambert JG. The biosynthesis of steroid glucuronides in the testis of the zebrafish, Brachydanio rerio, and their pheromonal function as ovulation inducers. Gen Comp Endocrinol 1987; 68:179-188.
18. Vilela DAR, Silva SGB, Peixoto MTD, Godinho HP, França LR. Spermatogenesis in teleost: insights from the Nile tilapia (Oreochromis niloticus) model. Fish Physiol Biochem 2003; 28:187-190. (Pubitemid 39530384)
19. Schulz RW, Menting S, Bogerd J, França LR, Vilela DAR, Godinho HP. Sertoli cell proliferation in the adult testis-evidence from two fish species belonging to different orders. Biol Reprod 2005; 73:891-898. (Pubitemid 41507491)
20. Matta SLP, Vilela DAR, Godinho HP, França LR. The goitrogen 6-npropyl-2-thiouracil (PTU) given during testis development increases Sertoli and germ cell numbers per cyst in fish: the tilapia (Oreochromis niloticus) model. Endocrinology 2002; 143:970-978. (Pubitemid 34164045)
21. Braat AK, van de Water S, Goos H, Bogerd J, Zivkovic D. Vasa protein expression and localization in the zebrafish. Mech Dev 2000; 95:271-274. (Pubitemid 30440820)
22. Houwing S, Kamminga LM, Berezikov E, Cronembold D, Girard A, van den Elst H, Filippov DV, Blaser H, Raz E, Moens CB, Plasterk RH, Hannon GJ, et al. A role for Piwi and piRNAs in germ cell maintenance and transposon silencing in zebrafish. Cell 2007; 129:69-82. (Pubitemid 46509793)
23. Essers J, Theil AF, Baldeyron C, van Cappellen WA, Houtsmuller AB, Kanaar R, Vermeulen W. Nuclear dynamics of PCNA in DNA replication and repair. Mol Cell Biol 2005; 25:9350-9359. (Pubitemid 41507836)
24. Miura C, Miura T, Yamashita M. PCNA protein expression during spermatogenesis of the Japanese eel (Anguilla japonica). Zool Sci 2002; 19:87-91. (Pubitemid 34881823)
25. Van de Kant HJG, de Rooij DG. Periodic acid incubation can replace hydrochloric acid hydrolysis and trypsin digestion in immunogold-silver staining of bromodeoxyuridine incorporation in plastic sections and allows the PAS reaction. Histochem J 1992; 24:170-175.
26. Miura T. Spermatogenic cycle in fish. In: Knobil E, Neill JD (eds.), Encyclopedia of Reproduction. San Diego: Academic Press; 1999: 4:571-578.
27. Grier HJ, Linton JR, Leatherland JF, De Vlaming VL. Structural evidence for two different testicular types in teleost fishes. Am J Anat 1980; 159:331-345. (Pubitemid 11155327)
28. Grier HJ. Cellular organization of the testis and spermatogenesis in fishes. Am Zool 1981; 21:345-357.
29. Parenti LR, Grier HJ. Evolution and phylogeny of gonad morphology in bony fishes. Integr Comp Biol 2004; 44:333-348. (Pubitemid 40112742)
30. Almeida FFL, Kristoffersen C, Taranger GL, Schulz RW. Spermatogenesis in Atlantic cod (Gadus morhua): a novel model of cystic germ cell development. Biol Reprod 2008; 78:27-34.
31. Garcia-Lopez A, Martinez-Rodriguez G, Sarasquete C. Male reproductive system in Senegalese sole Solea senegalensis (Kaup): anatomy, histology and histochemistry. Histol Histopathol 2005; 20:1179-1189. (Pubitemid 41489163)
32. Petersen C, Soder O. The Sertoli cell-a hormonal target and 'super' nurse for germ cells that determines testicular size. Horm Res 2006; 66:153-161. (Pubitemid 44413275)
33. Billard R. La spermatogenèse de Poecilia reticulata. I-estimation du nombre de générations goniales et rendement de la spermatogenèse. Ann Biol Anim Biochim Biophys 1969; 9:251-271.
34. Van den Hurk R, Peute J, Vermeij JAJ. Ultrastructural study of the testis of the black molly (Mollienisia latipinna) I. The intratesticular efferent duct system. Proc Kon Ned Akad Wet Ser 1974; 77:460-469.
35. Leal MC, Feitsma H, Cuppen E, França LR, Schulz RW. Completion of meiosis in male zebrafish (Danio rerio) despite lack of DNA mismatch repair gene mlh1. Cell Tissue Res 2008; 332:133-139.
36. Sharpe RM. Regulation of spermatogenesis. In: Knobil E, Neill JD (eds.), The Physiology of Reproduction. New York: Raven Press; 1994:1363-1434.
37. França LR, Russell LD. The testis of domestic animals. In: Martínez-García F, Regadera J (eds.), Male Reproduction: A Multidisciplinary Overview. Madrid: Churchill Communications; 1998:198-219.
38. Baum JS, St George JP, McCall K. Programmed cell death in the germ line. Semin Cell Dev Biol 2005; 16:245-259. (Pubitemid 40432126)
39. Ewing HH. Spermatogenesis in the zebrafish, Brachydanio rerio. Anat Rec 1972; 172:308.
40. Ando N, Miura T, Nader MR, Miura C, Yamauchi K. A method for estimating the number of mitotic divisions in fish testes. Fisheries Sci 2000; 66:299-303.
41. Billard R. A quantitative analysis of spermatogenesis in the trout, Salmo trutta fario. Cell Tiss Res 1983; 230:495-502.
42. Lo Nostro FL, Grier H, Meijide FJ, Guerrero GA. Ultrastructure of the testis in Synbranchus marmoratus (Teleostei, Synbranchidae): the germinal compartment. Tissue Cell 2003; 35:121-132. (Pubitemid 36636886)
43. Quagio-Grassiotto I, Carvalho ED. The ultrastructure of Sorubim lima (Teleostei, Siluriformes, Pimelodidae) spermatogenesis: premeiotic and meiotic periods. Tissue Cell 1999; 31:561-567.
44. Billard R. Ultrastructural changes in the spermatogonia and spermatocytes of Poecilia reticulata during spermatogenesis. Cell Tissue Res 1984; 237:219-226.
45. Selman K, Wallace RA. Gametogenesis in Fundulus heteroclitus. Am Zool 1986; 26:173-192.
46. Chiarini-Garcia H, Meistrich ML. High-resolution light microscopic characterization of spermatogonia. In: Hou SX, Singh SR (eds.), Germline Stem Cells. Methods in Molecular Biology. Totowa, NJ: Humana Press, Springer Science; 2008; 450:95-107.
47. Chiarini-Garcia H, Russell LD. Characterization of mouse spermatogonia by transmission electron microscopy. Reproduction 2002; 123:567-577. (Pubitemid 34303158)
48. Lacerda SMSN, Batlouni SR, Silva SBG, Homem CSP, França LR. Germ cells transplantation in fish: the Nile-tilapia model. Anim Reprod 2006; 3:146-159.
49. Shikina S, Ihara S, Yoshizaki G. Culture conditions for maintaining the survival and mitotic activity of rainbow trout transplantable type A spermatogonia. Mol Reprod Dev 2008; 75:529-537. (Pubitemid 351214155)
50. Fuller MT, Spradling AC. Male and female Drosophila germline stem cells: two versions of immortality. Science 2007; 316:402-404. (Pubitemid 46651479)
51. De Rooij DG. Proliferation and differentiation of spermatogonial stem cells. Reproduction 2001; 121:347-354. (Pubitemid 32243678)
52. Nakagawa T, Nabeshima Y, Yoshida S. Functional identification of the actual and potential stem cell compartments in mouse spermatogenesis. Dev Cell 2007; 2:195-206.
53. Grier HJ. Sperm development in the teleost Oryzias latipes. Cell Tissue Res 1976; 168:419-431.
54. Sprando RL, Heidinger RC, Russell LD. Spermiogenesis in the bluegill (Lepomis macrochirus): a study of cytoplasmic events including cell volume changes and citoplasmic elimination. J Morphol 1988; 198:165-177.
55. Lunstra DD, Schanbacher BD. Testicular function and Leydig cell ultraestructure in long-term bilateral cryptorchid rams. Biol Reprod 1988; 38:211-220.
56. Almeida FFL, Leal MC, França LR. Testis morphometry, duration of spermatogenesis and spermatogenic efficiency in the wild boar (Sus scrofa scrofa). Biol Reprod 2006; 75:792-799. (Pubitemid 44720400)
57. Johnson L, Neaves WB. Age related changes in the Leydig cell population, seminiferous tubules and sperm population in stallions. Biol Reprod 1981; 24:703-712. (Pubitemid 11081268)
58. Leal MC, França LR. The seminiferous epithelium cycle length in the black tufted-ear marmoset (Callithrix penicillata) is similar to humans. Biol Reprod 2006; 74:616-624.
59. Egami N, Hyodo-Taguchi Y. An autoradiographic examination of rate of spermatogenesis at different temperatures in the fish, Oryzias latipes. Exp Cell Res 1967; 47:665-667.
60. Billard R. Influence de la température sur la durée et l'efficacé de la spermatogenèse du guppy, Poecilia reticulata. C R Acad (Paris) 1968; 206:2287-2290.
61. De Felice DA, Rasch EM. Chronology of spermatogenesis and spermiogenesis in Poeciliid fishes. J Exp Zool 1969; 171:191-208.
62. Silva M, Godinho HP. Timing of some events of the gametogenesis in the male Nile tilapia, Sarotherodon niloticus. Arch Anat Microsc Morphol Exp 1983; 72:231-237.
63. Sinha GM, Mondal SK, Ghosal SK. Meiosis and spermiogenesis in a freshwater teleost fish, Channa punctatus (Bloch): an estimation of their duration by autoradiographic method. Cytol 1983; 48:87-93.
64. França LR, Ogawa T, Avarbock MR, Brinster RL, Russell LD. Germ cell genotype controls cell cycle during spermatogenesis in the rat. Biol Reprod 1998; 59:1371-1377. (Pubitemid 28549851)
65. Sinha GM, Mondal SK, Midya T, Ghosal SK. Chronology of meiosis and spermiogenesis in a fresh-water teleost fish, Colisa fasciata (Bloch and Schneider). Z Mikrosk Anat Forsch 1979; 93:442-448.
66. Billard R. Spermatogenesis and spermatology of some teleost fish species. Reprod Nutr Dev 1986; 26:877-920.
67. Licht P, Basu SL. Influence of temperature on lizard testes. Nature 1967; 213:672-674.
68. Setchell BP. The blood-testicular fluid barrier in sheep. J Physiol 1967; 189:63-65.
69. Dym M, Fawcett DW. The blood-testis barrier in the rat and the physiological compartimentation of the seminiferous epithelium. Biol Reprod 1970; 3:308-326.
70. Fawcett DW, Leak LV, Heidger PM Jr. Electron microscopic observations on the structural components of the blood-testis barrier. J Reprod Fertil Suppl 1970; 10:105-122.
71. Ross MH. Sertoli-Sertoli junctions and Sertoli-spermatid junctions after efferent ductule ligation and lanthanum treatment. Am J Anat 1977;148:49-55. (Pubitemid 8034348)
72. Bergmann M, Schindelmeiser J. Development of the blood testis barrier in the domestic fowl (Gallus domesticus). Int J Androl 1987; 10:482-488. (Pubitemid 17074070)
73. Baccetti B, Bigliardi E, Vegni Talluri M, Burrini AG. The Sertoli cell in lizards. J Ultrastruct Res 1983; 85:11-23. (Pubitemid 14159697)
74. Franchi E, Camatini M, de Curtis I. Morphological evidence of a permeability barrier in urodele testis. J Ultrastruct Res 1982; 80:253-263.
75. Abraham M, Rahamim E, Tibika H, Golenser E, Kieselskin M. The bloodtestis barrier in Aphanius dispar (Teleostei). Cell Tissue Res 1980; 211:207-214. (Pubitemid 11255441)
76. Silva S, Godinho HP. Barreira hemotesticular em Oreochromis niloticus (peixe-teleósteo). Rev Bras Ciênc Morfol 1989; 6:9-13.
77. Billard R. La spermatogenèse de Poecilia reticulata III. Ultrastructure des cellules de Sertoli. Ann Biol Anim Biochim Biophys 1970; 10:37-50.
78. Abraham M. The male germ cell protective barrier along phylogenesis. Int Rev Cytol 1991; 130:111-190.