Stage-specific gene expression during fish spermatogenesis as determined by laser-capture microdissection and quantitative-PCR in sea bass (Dicentrarchus labrax) gonads

Biology of Reproduction

Volumn 79, Issue 4, 2008, Pages 738-747

  Viñas, Jordi ^a   Piferrer, Francesc ^a  

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

Author keywords

11 hydroxylase; Androgen receptor; Aromatase; Estradiol receptor; Estrogen receptors; Gene expression patterns; Igf1; Laser capture microdissection; Sea bass; Sox17; Spermatogenesis; Steroid hormones; Testis; Vasa

Indexed keywords

ANDROGEN RECEPTOR; ANDROGEN RECEPTOR BETA; AROMATASE; BIOLOGICAL MARKER; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROGEN RECEPTOR BETA 1; ESTROGEN RECEPTOR BETA 2; PROTEIN VASA; SOMATOMEDIN C; STEROID 11BETA MONOOXYGENASE; TRANSCRIPTION FACTOR SOX17; UNCLASSIFIED DRUG;

ANDROGEN METABOLISM; ANDROGEN SYNTHESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; ESTROGEN METABOLISM; EUROPEAN SEA BASS; GENE EXPRESSION; GERM CELL; GONAD; HORMONE ACTION; LASER CAPTURE MICRODISSECTION; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPERMATID; SPERMATOGENESIS; SPERMATOGONIUM; SPERMATOZOON; TELEOST;

ANIMALS; AROMATASE; BASS; DEAD-BOX RNA HELICASES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GONADS; INSULIN-LIKE GROWTH FACTOR I; LASER THERAPY; MALE; MICRODISSECTION; RECEPTORS, ANDROGEN; RECEPTORS, ESTROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEX-DETERMINING REGION Y PROTEIN; SPERMATOGENESIS; STEROID 11-BETA-HYDROXYLASE;

DICENTRARCHUS LABRAX; SERRANIDAE; TELEOSTEI;

EID: 53349118112     PISSN: 00063363     EISSN: None     Source Type: Journal    
DOI: 10.1095/biolreprod.108.069708     Document Type: Article

References (69)

1. Callard IP, Callard GV, Lance V, Bolaffi JL, Rosset JS. Testicular regulation in non-mammalian vertebrates. Biol Reprod 1978; 18:16-43.
2. Callard G. Reproduction in male Elasmobranch fishes. In: Kinne RKH (ed.), Oogenesis, Spermatogenesis and Reproduction, vol. 10. Basel, Switzerland: Karger; 1991:104-154.
3. Schulz RW, Miura T. Spermatogenesis and its endocrine regulation. Fish Physiol Biochem 2002; 26:43-56.
4. Miura T, Miura CI. Molecular control mechanisms of fish spermatogenesis. Fish Physiol Biochem 2003; 28:181-186.
5. O'Donnell L, McLachlan RI, Wreford NG, de Kretser DM, Robertson DM. Testosterone withdrawal promotes stage-specific detachment of round spermatids from the rat seminiferous epithelium. Biol Reprod 1996; 55:895-901.
6. Sharpe RM, Maddocks S, Millar M, Kerr JB, Saunders PT, McKinnell C. Testosterone and spermatogenesis. Identification of stage-specific, androgen-regulated proteins secreted by adult rat seminiferous tubules. J Androl 1992; 13:172-184.
7. Sluka P, O'Donnell L, Stanton PG. Stage-specific expression of genes associated with rat spermatogenesis: characterization by laser-capture microdissection and real-time polymerase chain reaction. Biol Reprod 2002; 67:820-828.
8. Bremner WJ, Millar MR, Sharpe RM, Saunders PTK. Immunohistochemical localization of androgen receptors in the rat testis - evidence for stage-dependent expression and regulation by androgens. Endocrinology 1994; 135:1227-1234.
9. Nakamura N, Shibata H, O'Brien DA, Mori C, Eddy EM. Spermatogenic cell-specific type 1 hexokinase is the predominant hexokinase in sperm. Mol Reprod Dev 2008; 75:632-640.
10. Harvey S, Baudet ML, Murphy A, Luna M, Hull KL, Aramburo C. Testicular growth hormone (GH): GH expression in spermatogonia and primary spermatocytes. Gen Comp Endocrinol 2004; 139:158-167.
11. Bittman EL, Doherty L, Huang LY, Paroskie A. Period gene expression in mouse endocrine tissues. Am J Physiol Regul Integr Comp Physiol 2003; 285:R561-R569.
12. Yao JJ, Chiba T, Sakai J, Hirose K, Yamamoto M, Hada A, Kuramoto K, Higuchi K, Mori M. Mouse testis transcriptome revealed using serial analysis of gene expression. Mamm Genome 2004; 15:433-451.
13. Chan WY, Lee TL, Wu SM, Ruszczyka L, Alba D, Baxendale V, Rennert OM. Transcriptome analyses of male germ cells with serial analysis of gene expression (SAGE). Mol Cell Endocrinol 2006; 250:8-19.
14. Loir M. Spermatogonia of rainbow trout: II. In vitro study of the influence of pituitary hormones, growth factors and steroids on mitotic activity. Mol Reprod Dev 1999; 53:434-442.
15. Thomas KH, Wilkie TM, Tomashefsky P, Bellve AR, Simon MI. Differential gene expression during mouse spermatogenesis. Biol Reprod 1989; 41:729-739.
16. Bonner RF, Emmert-Buck M, Cole K, Pohida T, Chuaqui R, Goldstein S, Liotta LA. Cell sampling: laser capture microdissection: molecular analysis of tissue. Science 1997; 278:1481-1483.
17. Emmert-Buck MR, Bonner RF, Smith PD, Chuaqui RF, Zhuang Z, Goldstein SR, Weiss RA, Liotta LA. Laser capture microdissection. Science 1996; 274:998-1001.
18. Fend F, Specht K, Kremer M, Quintanilla-Martínez L. Laser capture microdissection in pathology. Laser Capture Mic Microdissec 2002; 356:196-206.
19. Suárez-Quian CA, Goldstein SR, Bonner RF. Laser capture microdissection: a new tool for the study of spermatogenesis. J Androl 2000; 21:601-608.
20. Sluka P, O'Donnell L, McLachlan RI, Stanton PG. Application of laser-capture microdissection to analysis of gene expression in the testis. Prog Histochem Cytoc 2008; 42:173-201.
21. Liang G, Zhang XD, Wang LJ, Sha YS, Zhang JC, Miao SY, Zong SD, Wang LF, Koide SS. Identification of differentially expressed genes of primary spermatocyte against round spermatid isolated from human testis using the laser capture microdissection technique. Cell Res 2004; 14:507-512.
22. Grier HJ. Comparative organization of Sertoli cells including the Sertoli cell barrier. In: Russell LD, Griswold MD (eds.), The Sertoli Cell. Clearwater, FL: Cache River Press; 1993:704-730.
23. Parenti LR, Grier HJ. Evolution and phylogeny of gonad morphology in bony fishes. Integr Comp Biol 2004; 44:333-348.
24. Loir M, Sourdaine P, Mendis-Handagama SM, Jégou B. Cell-cell interactions in the testis of teleosts and elasmobranchs. Micros Res Tech 1995; 32:533-552.
25. Nagahama Y. Endocrine regulation of gametogenesis in fish. Int J Dev Biol 1994; 38:217-229.
26. LeGac F, Loir M, LeBail PY, Ollitrault M. Insulin-like growth factor (IGF-I) mRNA and IGF-I receptor in trout testis and in isolated spermatogenic and Sertoli cells. Mol Reprod Dev 1996; 44:23-35.
27. Miura T, Yamauchi K, Nagahama Y, Takahashi H. Induction of spermatogenesis in male Japanese eel, Anguilla japonica, by a single injection of human chorionic-gonadotropin. Zool Sci 1991; 8:63-73.
28. Miura T, Miura C. Japanese eel: a model for analysis of spermatogenesis. Zool Sci 2001; 18:1055-1063.
29. Chaves-Pozo E, Liarte S, Vargas-Chacoff L, García-López A, Mulero V, Meseguer J, Mancera JM, García-Ayala A. 17Beta-estradiol triggers postspawning in spermatogenically active gilthead seabream (Sparus aurata L.) males. Biol Reprod 2007; 76:142-148.
30. Zanuy S, Carrillo M, Felip A, Rodríguez L, Blázquez M, Ramos J, Piferrer F. Genetic, hormonal and environmental approaches for the control of reproduction in the European sea bass (Dicentrarchus labrax L.). Aquaculture 2001; 202:187-203.
31. Piferrer F, Blázquez M, Navarro L, González A. Genetic, endocrine, and environmental components of sex determination and differentiation in the European sea bass (Dicentrarchus labrax L.). Gen Comp Endocrinol 2005; 142:102-110.
32. Rodríguez L, Zanuy S, Carrillo M. Influence of daylength on the age at first maturity and somatic growth in male sea bass (Dicentrarchus labrax, L.). Aquaculture 2001; 196:159-175.
33. Olsen LC, Aasland R, Fjose A. A vasa-like gene in zebrafish identifies putative primordial germ cells. Mech Dev 1997; 66:95-105.
34. Dalla Valle L, Lunardi L, Colombo L, Belvedere P. European sea bass (Dicentrarchus labrax L.) cytochrome P450arom: cDNA cloning, expression and genomic organization. J Steroid Biochem Mol Biol 2002; 80:25-34.
35. Socorro S, Martins RS, Deloffre L, Mylonas CC, Canario AVM. A cDNA for European sea bass (Dicentrachus labrax) 11 beta-hydroxylase: gene expression during the thermosensitive period and gonadogenesis. Gen Comp Endocrinol 2007; 150:164-173.
36. Miguel-Queralt S, Avvakumov GV, Blázquez M, Piferrer F, Hammond GL. Sea bass (Dicentrarchus labrax) sex hormone binding globulin: molecular and biochemical properties and phylogenetic comparison of its orthologues in multiple fish species. Mol Cell Endocrinol 2005; 229:21-29.
37. Halm S, Martínez-Rodríguez G, Rodríguez L, Prat F, Mylonas CC, Carrillo M, Zanuy S. Cloning, characterisation, and expression of three oestrogen receptors (ERalpha, ERbeta1 and ERbeta2) in the European sea bass, Dicentrarchus labrax. Mol Cell Endocrinol 2004; 223:63-75.
38. Blázquez M, Piferrer F. Sea bass (Dicentrarchus labrax) androgen receptor: cDNA cloning, tissue-specific expression, and mRNA levels during early development and sex differentiation. Mol Cell Endocrinol 2005; 237:37-48.
39. Wang R, Cheng HH, Xia LX, Guo YQ, Huang X, Zhou RJ. Molecular cloning and expression of Sox17 in gonads during sex reversal in the rice field eel, a teleost fish with a characteristic of natural sex transformation. Biochem Biophys Res Commun 2003; 303:452-457.
40. Galay-Burgos M, Llewellyn L, Mylonas CC, Canario AV, Zanuy S, Sweeney GE. Analysis of the Sox gene family in the European sea bass (Dicentrarchus labrax). Comp Biochem Physiol B Comp Biochem 2004; 137:279-284.
41. Grier HJ, Taylor RG. Testicular maturation and regression in the common snook. J Fish Biol 1998; 53:521-542.
42. Zanuy S, Carrillo M, Mateos J, Trudeau V, Kah O. Effects of sustained administration of testosterone in pre-pubertal sea bass (Dicentrarchus labrax L). Aquaculture 1999; 177:21-35.
43. Felip A, Piferrer F, Carrillo M, Zanuy S. Comparison of the gonadal development and plasma levels of sex steroid hormones in diploid and triploid sea bass, Dicentrarchus labrax L. J Exp Zool 2001; 290:384-395.
44. Schuitze K, Lahr G. Identification of expressed genes by laser-mediated manipulation of single cells. Nat Biotech 1998; 16:737-742.
45. Muller PY, Janovjak H, Miserez AR, Dobbie Z. Processing of gene expression data generated by quantitative real-time RT PCR. BioTechniques 2002; 33:514-514.
46. Elvers D, Remer L, Arnold N, Bauerle D. Laser microdissection of biological tissues: process optimization. Appl Phys Mat Sci Proc 2005; 80:55-59.
47. Miguel-Queralt S, Blázquez M, Piferrer F, Hammond GL. Sex hormonebinding globulin expression in sea bass (Dicentrarchus labrax L.) throughout development and the reproductive season. Mol Cell Endocrinol 2007; 276:55-62.
48. Miguel-Queralt S, Knowlton M, Avvakumov GV, Al-Nouno R, Kelly GM, Hammond GL. Molecular and functional characterization of sex hormone binding globulin in zebrafish. Endocrinology 2004; 145:5221-5230.
49. Schulz RW, Menting S, Bogerd J, Franca 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.
50. Knaut H, Pelegri F, Bohmann K, Schwarz H, Nusslein-Volhard C. Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J Cell Biol 2000; 149:875-888.
51. Xu HY, Gui JF, Hong YH. Differential expression of vasa RNA and protein during spermatogenesis and oogenesis in the gibel carp (Carassius auratus gibelio), a bisexually and gynogenetically reproducing vertebrate. Dev Dyn 2005; 233:872-882.
52. Kobayashi T, Kajiura-Kobayashi H, Nagahama Y. Differential expression of vasa homologue gene in the germ cells during oogenesis and spermatogenesis in a teleost fish, tilapia, Oreochromis niloticus. Mech Dev 2000; 99:139-142.
53. Kusakabe M, Kobayashi T, Todo T, Lokman PM, Nagahama Y, Young G. Molecular cloning and expression during spermatogenesis of a cDNA encoding testicular 11 beta-hydroxylase (P450 11beta) in rainbow trout (Oncorhynchus mykiss). Mol Reprod Dev 2002; 62:456-469.
54. Maguire SM, Tribley WA, Griswold MD. Follicle-stimulating hormone (FSH) regulates the expression of FSH receptor messenger ribonucleic acid in cultured Sertoli cells and in hypophysectomized rat testis. Biol Reprod 1997; 56:1106-1111.
55. Ohta T, Miyake H, Miura C, Kamei H, Aida K, Miura T. Follicle-stimulating hormone induces spermatogenesis mediated by androgen production in Japanese eel, Anguilla japonica. Biol Reprod 2007; 77:970-977.
56. Kusakabe M, Nakamura I, Evans J, Swanson P, Young G. Changes in mRNAs encoding steroidogenic acute regulatory protein, steroidogenic enzymes and receptors for gonadotropins during spermatogenesis in rainbow trout testes. J Endocrinol 2006; 189:541-554.
57. Ikeuchi T, Todo T, Kobayashi T, Nagahama Y. Two subtypes of androgen and progestogen receptors in fish testes. Comp Biochem Physiol B Comp Biochem 2001; 129:449-455.
58. Takeo J, Yamashita S. Immunohistochemical localization of rainbow trout androgen receptors in the testis. Fish Sci 2001; 67:518-523.
59. Arenas MI, Royuela M, Lobo MVT, Alfaro JM, Fraile B, Paniagua R. Androgen receptor (AR), estrogen receptor-alpha (ER-alpha) and estrogen receptor-beta (ER-beta) expression in the testis of the newt, Triturus marmoratus marmoratus during the annual cycle. J Anat 2001; 199:465-472.
60. O'Donnell L, Robertson KM, Jones ME, Simpson ER. Estrogen and spermatogenesis. Endocr Rev 2001; 22:289-318.
61. Akingbemi BT. Estrogen regulation of testicular function. Reprod Biol Endocrinol 2005; 3:51-64.
62. Carreau S, Bourguiba S, Lambard S, Galeraud-Denis I, Genissel C, Bilinska B, Benahmed M, Levallet J. Aromatase expression in male germ cells. J Steroid Biochem Mol Biol 2001; 79:203-208.
63. Bilinska B, Schmalz-Fraczek B, Kotula M, Carreau S. Photoperiod-dependent capability of androgen aromatization and the role of estrogens in the bank vole testis visualized by means of immunohistochemistry. Mol Cell Endocrinol 2001; 178:189-198.
64. Betka M, Callard GV. Negative feedback control of the spermatogenic progression by testicular oestrogen synthesis: insights from the shark testis model. Apmis 1998; 106:252-257.
65. Blázquez M, Zanuy S, Carrillo M, Piferrer F. Structural and functional effects of early exposure to estradiol-17 beta and 17 alpha-ethynylestradiol on the gonads of the gonochoristic teleost Dicentrarchus labrax. Fish Physiol Biochem 1998; 18:37-47.
66. Kanai Y, Kanai-Azuma M, Noce T, Saido TC, Shiroishi T, Hayashi Y, Yazaki K. Identification of two Sox17 messenger RNA isoforms, with and without the high mobility group box region, and their differential expression in mouse spermatogenesis. J Cell Biol 1996; 133:667-681.
67. Berishvili G, D'Cotta H, Baroiller JF, Segner H, Reinecke M. Differential expression of IGF-I mRNA and peptide in the male and female gonad during early development of a bony fish, the tilapia Oreochromis niloticus. Gen Comp Endocrinol 2006; 146:204-210.
68. Dubois W, Callard GV. Culture of intact sertoli germ-cell units and isolated Sertoli cells from Squalus-testis. 2. Stimulatory effects of insulin and Igf-I on DNA-synthesis in premeiotic stages. J Exp Zool 1993; 267:233-244.
69. Eisen MB, Spellman PT, Brown PO, Botstein D. Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 1998; 95:14863-14868.