Up-regulation of gonadotropin mRNA-expression at the onset of gametogenesis in the roach (Rutilus rutilus): Evidence for an important role of brain-type aromatase (cyp19a1b) in the pituitary

General and Comparative Endocrinology

Volumn 178, Issue 3, 2012, Pages 529-538

  Trubiroha, Achim ^a   Kroupova, Hana ^b   Wuertz, Sven ^a,c   Kloas, Werner ^a,c  

^a LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c HUMBOLDT UNIVERSITY   (Germany)

Author keywords

FSH; LH; Oogenesis; Sex steroids; Spermatogenesis; Steroid receptors

Indexed keywords

11 OXOTESTOSTERONE; 17,20BETA DIHYDROXYPREGN 4 EN 3 ONE; ANDROGEN RECEPTOR; AROMATASE; ESTRADIOL; ESTROGEN RECEPTOR; FOLLITROPIN BETA SUBUNIT; GONADOTROPIN; LUTEINIZING HORMONE BETA SUBUNIT; MESSENGER RNA; TESTOSTERONE;

ANIMAL TISSUE; ARTICLE; FEMALE; FISH; GAMETOGENESIS; GERMANY; HYPOPHYSIS; MALE; NONHUMAN; OVARY FOLLICLE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTION; RUTILUS RUTILUS; SEASONAL VARIATION; SPAWNING; SPERMATOGONIUM; UPREGULATION; VITELLOGENESIS;

EID: 84864825110     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2012.07.002     Document Type: Article

References (57)

1. Amer M.A., Miura T., Miura C., Yamauchi K. Involvement of sex steroid hormones in the early stages of spermatogenesis in Japanese huchen (Hucho perryi). Biol. Reprod. 2001, 65:1057-1066.
2. Andersson E., Borg B., Lambert J.G.D. Aromatase-activity in brain and pituitary of immature and mature Atlantic salmon (Salmo salar L.) parr. Gen. Comp. Endocrinol. 1988, 72:394-401.
3. Ando H., Swanson P., Kitani T., Koide N., Okada H., Ueda H., Urano A. Synergistic effects of salmon gonadotropin-releasing hormone and estradiol-17beta on gonadotropin subunit gene expression and release in masu salmon pituitary cells in vitro. Gen. Comp. Endocrinol. 2004, 137:109-121.
4. Billard R. Spermatogenesis and spermatology of some teleost fish species. Reprod. Nutr. Dev. 1986, 26:877-920.
5. Callard G.V., Specker J.L., Knapp J., Nishioka R.S., Bern H.A. Aromatase is concentrated in the proximal pars-distalis of tilapia pituitary. Gen. Comp. Endocrinol. 1988, 71:70-79.
6. Celius T., Walther B.T. Oogenesis in Atlantic salmon (Salmo salar L.) occurs by zonagenesis preceding vitellogenesis in vivo and in vitro. J. Endocrinol. 1998, 158:259-266.
7. Diotel N., Page Y.L., Mouriec K., Tong S.K., Pellegrini E., Vaillant C., Anglade I., Brion F., Pakdel F., Chung B.C., Kah O. Aromatase in the brain of teleost fish: expression, regulation and putative functions. Front. Neuroendocrinol. 2010, 31:172-192.
8. Divers S.L., McQuillan H.J., Matsubara H., Todo T., Lokman P.M. Effects of reproductive stage and 11-ketotestosterone on LPL mRNA levels in the ovary of the shortfinned eel. J. Lipid Res. 2010, 51:3250-3258.
9. Driescher E., Behrendt H., Schellenberger G., Stellmacher R. Lake Mueggelsee and its environment - natural conditions and anthropogenic impacts. Int. Rev. Ges. Hydrobiol. 1993, 78:327-343.
10. Endo T., Todo T., Lokman P.M., Kudo H., Ijiri S., Adachi S., Yamauchi K. Androgens and very low density lipoprotein are essential for the growth of previtellogenic oocytes from Japanese Eel, Anguilla japonica, in vitro. Biol. Reprod. 2011, 84:816-825.
11. Geraudie P., Gerbron M., Hill E., Minier C. Roach (Rutilus rutilus) reproductive cycle: a study of biochemical and histological parameters in a low contaminated site. Fish Physiol. Biochem. 2010, 36:767-777.
12. Geraudie P., Gerbron M., Minier C. Seasonal variations and alterations of sex steroid levels during the reproductive cycle of male roach (Rutilus rutilus). Mar. Environ. Res. 2010, 69(Suppl):S53-S55.
13. Gomez J.M., Weil C., Ollitrault M., Le Bail P.Y., Breton B., Le Gac F. Growth hormone (GH) and gonadotropin subunit gene expression and pituitary and plasma changes during spermatogenesis and oogenesis in rainbow trout (Oncorhynchus mykiss). Gen. Comp. Endocrinol. 1999, 113:413-428.
14. Goos H.J.T., Vanderloo J.C.M., Smitvandijk W., Deleeuw R. Steroid aromatase, 2-hydroxylase and COMT activity in gonadotropic cells of the African catfish, Clarias gariepinus. Cell Biol. Int. Rep. 1985, 9:529.
15. Hermelink B., Wuertz S., Trubiroha A., Rennert B., Kloas W., Schulz C. Influence of temperature on puberty and maturation of pikeperch, Sander lucioperca. Gen. Comp. Endocrinol. 2011, 172:282-292.
16. Hotchkiss A.K., Rider C.V., Blystone C.R., Wilson V.S., Hartig P.C., Ankley G.T., Foster P.M., Gray C.L., Gray L.E. Fifteen years after " Wingspread" -environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go. Toxicol. Sci. 2008, 105:235-259.
17. Jafri S.I.H. Gametogenesis in roach, Rutilus rutilus (L.) (Cyprinidae: Teleostei), Pakistan. J. Zool. 1990, 22:361-377.
18. Jobling S., Beresford N., Nolan M., Rodgers-Gray T., Brighty G.C., Sumpter J.P., Tyler C.R. Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biol. Reprod. 2002, 66:272-281.
19. Katsu Y., Lange A., Urushitani H., Ichikawa R., Paull G.C., Cahill L.L., Jobling S., Tyler C.R., Iguchi T. Functional associations between two estrogen receptors, environmental estrogens, and sexual disruption in the roach (Rutilus rutilus). Environ. Sci. Technol. 2007, 41:3368-3374.
20. Kestemont P., Rinchard J., Feys V., Fostier A. Spawning migrations, sexual maturity and sex steroid levels in female roach Rutilus rutilus from the river Meuse. Aquat. Sci. 1999, 61:111-121.
21. Kitahashi T., Ogawa S., Soga T., Sakuma Y., Parhar I. Sexual maturation modulates expression of nuclear receptor types in laser-captured single cells of the Cichlid (Oreochromis niloticus) pituitary. Endocrinology 2007, 148:5822-5830.
22. Kloas W., Urbatzka R., Opitz R., Wurtz S., Behrends T., Hermelink B., Hofmann F., Jagnytsch O., Kroupova H., Lorenz C., Neumann N., Pietsch C., Trubiroha A., Van Ballegooy C., Wiedemann C., Lutz I. Endocrine disruption in aquatic vertebrates. Ann. N.Y. Acad. Sci. 2009, 1163:187-200.
23. Kortner T.M., Rocha E., Arukwe A. Previtellogenic oocyte growth and transcriptional changes of steroidogenic enzyme genes in immature female Atlantic cod (Gadus morhua L.) after exposure to the androgens 11-ketotestosterone and testosterone. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2009, 152:304-313.
24. Kroupova H., Trubiroha A., Wuertz S., Kloas W. Stage-dependent differences in RNA composition and content affect the outcome of expression profiling in roach (Rutilus rutilusx) ovary. Comp. Biochem. Physiol. A: Mol. Integr. Physiol. 2011, 159:141-149.
25. Lange A., Katsu Y., Ichikawa R., Paull G.C., Chidgey L.L., Coe T.S., Iguchi T., Tyler C.R. Altered sexual development in roach (Rutilus rutilus) exposed to environmental concentrations of the pharmaceutical 17alpha-ethinylestradiol and associated expression dynamics of aromatases and estrogen receptors. Toxicol. Sci. 2008, 106:113-123.
26. Lange A., Paull G.C., Hamilton P.B., Iguchi T., Tyler C.R. Implications of persistent exposure to treated wastewater effluent for breeding in wild roach (Rutilus rutilus) populations. Environ. Sci. Technol. 2011, 45:1673-1679.
27. Le Page Y., Menuet A., Kah O., Pakdel F. Characterization of a cis-acting element involved in cell-specific expression of the zebrafish brain aromatase gene. Mol. Reprod. Dev. 2008, 75:1549-1557.
28. Levavi-Sivan B., Biran J., Fireman E. Sex steroids are involved in the regulation of gonadotropin-releasing hormone and dopamine D2 receptors in female tilapia pituitary. Biol. Reprod. 2006, 75:642-650.
29. Levavi-Sivan B., Bogerd J., Mananos E.L., Gomez A., Lareyre J.J. Perspectives on fish gonadotropins and their receptors. Gen. Comp. Endocrinol. 2010, 165:412-437.
30. Lubzens E., Young G., Bobe J., Cerda J. Oogenesis in teleosts: how eggs are formed. Gen. Comp. Endocrinol. 2010, 165:367-389.
31. Martyniuk C.J., Kroll K.J., Porak W.F., Steward C., Grier H.J., Denslow N.D. Seasonal relationship between gonadotropin, growth hormone, and estrogen receptor mRNA expression in the pituitary gland of largemouth bass. Gen. Comp. Endocrinol. 2009, 163:306-317.
32. Miura C., Higashino T., Miura T. A progestin and an estrogen regulate early stages of oogenesis in fish. Biol. Reprod. 2007, 77:822-828.
33. Miura T., Miura C., Ohta T., Nader M.R., Todo T., Yamauchi K. Estradiol-17beta stimulates the renewal of spermatogonial stem cells in males. Biochem. Biophys. Res. Commun. 1999, 264:230-234.
34. Mouriec K., Gueguen M.M., Manuel C., Percevault F., Thieulant M.L., Pakdel F., Kah O. Androgens upregulate cyp19a1b (aromatase B) gene expression in the brain of zebrafish (Danio rerio) through estrogen receptors. Biol. Reprod. 2009, 80:889-896.
35. Nagahama Y., Yamashita M. Regulation of oocyte maturation in fish. Dev. Growth Differ. 2008, 50(Suppl 1):S195-S219.
36. Noaksson E., Tjarnlund U., Bosveld A.T., Balk L. Evidence for endocrine disruption in perch (Perca fluviatilis) and roach (Rutilus rutilus) in a remote Swedish lake in the vicinity of a public refuse dump. Toxicol. Appl. Pharmacol. 2001, 174:160-176.
37. Nolan M., Jobling S., Brighty G., Sumpter J.P., Tyler C.R. A histological description of intersexuality in the roach. J. Fish Biol. 2001, 58:160-176.
38. Pasmanik M., Callard G.V. Changes in brain aromatase and 5 alpha-reductase activities correlate significantly with seasonal reproductive cycles in goldfish (Carassius auratus). Endocrinology 1988, 122:1349-1356.
39. Pasmanik M., Schlinger B.A., Callard G.V. In vivo steroid regulation of aromatase and 5-alpha-reductase in goldfish brain and pituitary. Gen. Comp. Endocrinol. 1988, 71:175-182.
40. Paull G.C., Lange A., Henshaw A.C., Tyler C.R. Ontogeny of sexual development in the roach (Rutilus rutilus) and its interrelationships with growth and age. J. Morphol. 2008, 269:884-895.
41. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
42. Piferrer F., Blazquez M. Aromatase distribution and regulation in fish. Fish Physiol. Biochem. 2005, 31:215-226.
43. Pottinger T.G., Yeomans W.E., Carrick T.R. Plasma cortisol and 17beta-oestradiol levels in roach exposed to acute and chronic stress. J. Fish Biol. 1999, 54:525-532.
44. Rebers F.E.M., Hassing G.A.M., Zandbergen M.A., Goos H.J.T., Schulz R.W. Regulation of steady-state luteinizing hormone messenger ribonucleic acid levels, de novo synthesis, and release by sex steroids in primary pituitary cell cultures of male African catfish, Clarias gariepinus. Biol. Reprod. 2000, 62:864-872.
45. Rinchard J., Kestemont P. Comparative study of reproductive biology in single- and multiple-spawner cyprinid fish. 1. Morphological and histological features. J. Fish Biol. 1996, 49:883-894.
46. Rinchard J., Kestemont P., Heine R. Comparative study of reproductive biology in single and multiple-spawner cyprinid fish. 2. Sex steroid and plasma protein phosphorus concentrations. J. Fish Biol. 1997, 50:169-180.
47. Schulz R.W., de Franca L.R., Lareyre J.J., Le G.F., Chiarini-Garcia H., Nobrega R.H., Miura T. Spermatogenesis in fish. Gen. Comp. Endocrinol. 2010, 165:390-411.
48. Scott A.P., Sumpter J.P., Stacey N. The role of the maturation-inducing steroid, 17,20beta-dihydroxypregn-4-en-3-one, in male fishes: a review. J. Fish Biol. 2010, 76:183-224.
49. Shimizu A. Effect of photoperiod and temperature on gonadal activity and plasma steroid levels in a reared strain of the mummichog (Fundulus heteroclitus) during different phases of its annual reproductive cycle. Gen. Comp. Endocrinol. 2003, 131:310-324.
50. Sohn Y.C., Yoshiura Y., Kobayashi M., Aida K. Seasonal changes in mRNA levels of gonadotropin and thyrotropin subunits in the goldfish, Carassius auratus. Gen. Comp. Endocrinol. 1999, 113:436-444.
51. Taranger G.L., Carrillo M., Schulz R.W., Fontaine P., Zanuy S., Felip A., Weltzien F.A., Dufour S., Karlsen O., Norberg B., Andersson E., Hansen T. Control of puberty in farmed fish. Gen. Comp. Endocrinol. 2010, 165:483-515.
52. Trubiroha A., Wuertz S., Frank S.N., Sures B., Kloas W. Expression of gonadotropin subunits in roach (Rutilus rutilus, Cyprinidae) infected with plerocercoids of the tapeworm Ligula intestinalis (Cestoda). Int. J. Parasitol. 2009, 39:1465-1473.
53. Trubiroha A., Kroupova H., Wuertz S., Frank S.N., Sures B., Kloas W. Naturally-induced endocrine disruption by the parasite Ligula intestinalis (Cestoda) in roach (Rutilus rutilus). Gen. Comp. Endocrinol. 2010, 166:234-240.
54. Tyler C.R., Lange A., Paull G.C., Katsu Y., Iguchi T. The roach (Rutilus rutilus) as a sentinel for assessing endocrine disruption. Environ. Sci. 2007, 14:235-253.
55. Vainikka A., Jokinen E.I., Kortet R., Taskinen J. Gender- and season-dependent relationships between testosterone, oestradiol and immune functions in wild roach. J. Fish Biol. 2004, 64:227-240.
56. Wuertz S., Nitsche A., Jastroch M., Gessner J., Klingenspor M., Kirschbaum F., Kloas W. The role of the IGF-I system for vitellogenesis in maturing female sterlet, Acipenser ruthenus Linnaeus, 1758. Gen. Comp. Endocrinol. 2007, 150:140-150.
57. Zohar Y., Munoz-Cueto J.A., Elizur A., Kah O. Neuroendocrinology of reproduction in teleost fish. Gen. Comp. Endocrinol. 2010, 165:438-455.