Sex-specific changes in the expression of kisspeptin, kisspeptin receptor, gonadotropins and gonadotropin receptors in the Senegalese sole (Solea senegalensis) during a full reproductive cycle

Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology

Volumn 162, Issue 4, 2012, Pages 364-371

  Mechaly, Alejandro S ^a,b   Viñas, Jordi ^a,c   Piferrer, Francesc ^a  

^a INSTITUT DE CIÈNCIES DEL MAR   (Spain)

^b UNIVERSITY OF SYDNEY   (Australia)

^c UNIVERSITY OF GIRONA   (Spain)

Author keywords

Fish; Fsh ; Gpr54; Kiss2; Kiss2r; Lh ; Puberty; Reproduction

Indexed keywords

11 OXOTESTOSTERONE; ESTRADIOL; FOLLITROPIN BETA SUBUNIT; FOLLITROPIN RECEPTOR; G PROTEIN COUPLED RECEPTOR 54; GONADOTROPIN; GONADOTROPIN RECEPTOR; KISSPEPTIN; KISSPEPTIN 2; KISSPEPTIN 2 RECEPTOR; LUTEINIZING HORMONE BETA SUBUNIT; LUTEINIZING HORMONE RECEPTOR; TESTOSTERONE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; AUTUMN; ENZYME LINKED IMMUNOSORBENT ASSAY; ESTRADIOL BLOOD LEVEL; FEMALE; FISH; FOREBRAIN; GONAD; HISTOLOGY; HYPOPHYSIS; MALE; MESENCEPHALON; NONHUMAN; NUCLEOTIDE SEQUENCE; OVARY CYCLE; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEASONAL VARIATION; SEX DIFFERENCE; SOLEA SENEGALENSIS; SPAWNING; SPRING; TESTOSTERONE BLOOD LEVEL; WINTER;

ANIMALIA; SOLEA SENEGALENSIS; VERTEBRATA;

EID: 84861529525     PISSN: 10956433     EISSN: 15314332     Source Type: Journal    
DOI: 10.1016/j.cbpa.2012.04.003     Document Type: Article

References (53)

1. Agulleiro M.J., Anguis V., Cañavate J.P., Martínez-Rodríguez G., Mylonas C.C., Cerdà J. Induction of spawning of captive-reared Senegal sole (Solea senegalensis) using different administration methods for gonadotropin-releasing hormone agonist. Aquaculture 2006, 257:511-524.
2. Akazome Y., Kanda S., Okubo K., Oka Y. Functional and evolutionary insights into vertebrate kisspeptin systems from studies of fish brain. J. Fish Biol. 2010, 76:161-182.
3. Amano M., Pham K.X., Amiya N., Yamanome T., Yamamori K. Changes in brain seabream GnRH mRNA and pituitary seabream GnRH peptide levels during ovarian maturation in female barfin flounder. Gen. Comp. Endocrinol. 2008, 158:168-172.
4. Anguis V., Cañavate J.P. Spawning of captive Senegal sole (Solea senegalensis) under a naturally fluctuating temperature regime. Aquaculture 2005, 243:133-145.
5. Beirão J., Cabrita E., Soares F., Herraez M.P., Dinis M.T. Cellular damage in spermatozoa from wild-captured Solea senegalensis detected with comet analysis and annexin-V. J. Appl. Ichthyol. 2008, 24:508-513.
6. Biran J., Ben-Dor S., Levavi-Sivan B. Molecular identification and functional characterization of the kisspeptin/kisspeptin receptor system in lower vertebrates. Biol. Reprod. 2008, 79:776-786.
7. Cabrita E., Soares F., Dinis M.T. Characterization of Senegal sole, Solea senegalensis, male broodstock in terms of sperm production and quality. Aquaculture 2006, 261:967-975.
8. Cerdà J., Chauvigné F., Agulleiro M.J., Marin E., Halm S., Martínez-Rodríguez G., Prat F. Molecular cloning of Senegalese sole (Solea senegalensis) follicle-stimulating hormone and luteinizing hormone subunits and expression pattern during spermatogenesis. Gen. Comp. Endocrinol. 2008, 156:470-481.
9. Chauvigné F., Tingaud-Sequeira A., Agulleiro M.J., Calusinska M., Gómez M., Finn R.N., Cerdà J. Functional and evolutionary analysis of flatfish gonadotropin receptors reveals cladal- and lineage-level divergence of the teleost glycoprotein receptor family. Biol. Reprod. 2010, 82:1088-1102.
10. de Roux N., Genin E., Carel J.C., Matsuda F., Chaussain J.L., Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:10972-10976.
11. Dinis M.T., Ribeiro L., Soares F., Sarasquete C. A review on the cultivation potential of Solea senegalensis in Spain and in Portugal. Aquaculture 1999, 176:27-38.
12. Falcón J., Migaud H., Muñoz-Cueto J.A., Carrillo M. Current knowledge on the melatonin system in teleost fish. Gen. Comp. Endocrinol. 2010, 165:469-482.
13. Felip A., Zanuy S., Pineda R., Pinilla L., Carrillo M., Tena-Sempere M., Gómez A. Evidence for two distinct KiSS genes in non-placental vertebrates that encode kisspeptins with different gonadotropin-releasing activities in fish and mammals. Mol. Cell. Endocrinol. 2009, 312:61-71.
14. Filby A.L., van Aerle R., Duitman J., Tyler C.R. The kisspeptin/gonadotropin releasing hormone pathway and molecular signaling of puberty in fish. Biol. Reprod. 2008, 78:278-289.
15. Forné I., Agulleiro M.J., Asensio E., Abián J., Cerdà J. 2-D DIGE analysis of Senegalese sole (Solea senegalensis) testis proteome in wild-caught and hormone-treated F1 fish. Proteomics 2009, 9:2171-2181.
16. García-López A., Anguis V., Couto E., Canario A.V.M., Cañavate J.P., Sarasquete C., Martínez-Rodríguez G. Non-invasive assessment of reproductive status and cycle of sex steroid levels in a captive wild broodstock of Senegalese sole Solea senegalensis (Kaup). Aquaculture 2006, 254:583-593.
17. García-López A., Fernández-Pasquier V., Couto E., Canario A.V.M., Sarasquete C., Martínez-Rodríguez G. Testicular development and plasma sex steroid levels in cultured male Senegalese sole Solea senegalensis Kaup. Gen. Comp. Endocrinol. 2006, 147:343-351.
18. García-López A., Couto E., Canario A.V.M., Sarasquete C., Martínez-Rodríguez G. Ovarian development and plasma sex steroid levels in cultured female Senegalese sole Solea senegalensis. Comp. Biochem. Physiol. A 2007, 146:342-354.
19. Guzmán J.M., Ramos J., Mylonas C.C., Mañanós E. Spawning performance and plasma levels if GnRHa and sex steroids in cultured female Senegalese sole (Solea senegalensis) treated with different GnRHa-delivery systems. Aquaculture 2009, 291:200-209.
20. Guzmán J.M., Rubio M., Ortiz-Delgado J., Klenke U., Kight K., Cross I., Sánchez-Ramos I., Riaza A., Reborditos L., Sarasquete C., Zohar Y., Mañanós E. Comparative gene expression of gonadotropins (FSH and LH) and peptide levels of gonadotropin-releasing hormones (GnRHs) in the pituitary of wild and cultured Senegalese sole (Solea senegalensis) broodstocks. Comp. Biochem. Physiol. A 2009, 153:266-277.
21. Guzmán J.M., Cal R., García-López A., Chereguini O., Kight K., Olmedo M., Sarasquete C., Mylonas C.C., Peleteiro J.B., Zohar Y., Mañanós E.L. Effects of in vivo treatment with the dopamine antagonist pimozide and gonadotropin-releasing hormone agonist (GnRHa) on the reproductive axis of Senegalese sole (Solea senegalensis). Comp. Biochem. Physiol. A 2011, 158(2):235-245.
22. Imsland A.K., Foss A., Conceicão L.E.C., Dinis M.T., Delbare D., Schram E., Kamstra A., Rema P., White P. A review of the culture potential of Solea solea and S. senegalensis. Rev. Fish Biol. Fish. 2003, 13:379-407.
23. Kanda S., Akazome Y., Matsunaga T., Yamamoto N., Yamada S., Tsukamura H., Maeda K., Oka Y. Identification of KiSS-1 product kisspeptin and steroid-sensitive sexually dimorphic kisspeptin neurons in medaka (Oryzias latipes). Endocrinology 2008, 149:2467-2476.
24. Kitahashi T., Ogawa S., Parhar I.S. Cloning and expression of kiss2 in the zebrafish and medaka. Endocrinology 2009, 150:821-831.
25. Lee Y.R., Tsunekawa K., Moon M.J., Um H.N., Hwang J.I., Osugi T., Otaki N., Sunakawa Y., Kim K., Vaudry H., Kwon H.B., Seong J.Y., Tsutsui K. Molecular evolution of multiple forms of kisspeptins and GPR54 receptors in vertebrates. Endocrinology 2009, 150:2837-2846.
26. Li S., Zhang Y., Liu Y., Huang X., Huang W., Lu D., Zhu P., Shi Y., Cheng C.H., Liu X., Lin H. Structural and functional multiplicity of the kisspeptin/GPR54 system in goldfish (Carassius auratus). J. Endocrinol. 2009, 201:407-418.
27. Maugars G., Schmitz M. Expression of gonadotropin and gonadotropin receptor genes during early sexual maturation in male Atlantic salmon parr. Mol. Reprod. Dev. 2008, 75:403-413.
28. Mechaly A.S., Viñas J., Piferrer J. Identification of two isoforms of the Kisspeptin-1 receptor (kiss1r) generated by alternative splicing in a modern teleost, the Senegalese sole (Solea senegalensis). Biol. Reprod. 2009, 80:60-69.
29. Mechaly A.S., Viñas J., Murphy C., Reith M., Piferrer F. Gene structure of the Kiss1 receptor-2 (Kiss1r-2) in the Atlantic halibut: insights into the evolution and regulation of Kiss1r genes. Mol. Cell. Endocrinol. 2010, 317:78-89.
30. Mechaly A.S., Viñas J., Piferrer J. Gene structure analysis of kisspeptin-2 (Kiss2) in the Senegalese sole (Solea senegalensis): characterization of two splice variants of Kiss2, and novel evidence for metabolic regulation of kisspeptin signaling in non-mammalian species. Mol. Cell. Endocrinol. 2011, 339:14-24.
31. Mittelholzer C., Andersson E., Taranger G.L., Consten D., Hirai T., Senthilkumaran B., Nagahama Y., Norberg B. Molecular characterization and quantification of the gonadotropin receptors FSH-R and LH-R from Atlantic cod (Gadus morhua). Gen. Comp. Endocrinol. 2009, 160:47-58.
32. Mohamed J.S., Benninghoff A.D., Holt G.J., Khan I.A. Developmental expression of the G protein-coupled receptor 54 and three GnRH mRNAs in the teleost fish cobia. J. Mol. Endocrinol. 2007, 38:235-244.
33. Nocillado J.N., Levavi-Sivan B., Carrick F., Elizur A. Temporal expression of G-protein-coupled receptor 54 (GPR54) gonadotropin-releasing hormones (GnRH), and dopamine receptor D2 (drd2) in pubertal female grey mullet, Mugil cephalus. Gen. Comp. Endocrinol. 2007, 150:278-287.
34. Oakley A.E., Clifton D.K., Steiner R.A. Kisspeptin signaling in the brain. Endocr. Rev. 2009, 30:713-743.
35. Oliveira C., Dinis M.T., Soares F., Cabrita E., Pousão-Ferreira P., Sánchez-Vázquez F.J. Lunar and daily spawning rhythms of Senegal sole Solea senegalensis. J. Fish Biol. 2009, 75:61-74.
36. Oliveira C., Duncan N.A., Pousão-Ferreira P., Mañanós E., Sánchez-Vázquez F.J. Influence of the lunar cycle on plasma melatonin, vitellogenin and sex steroids rhythms in Senegal sole, Solea senegalensis. Aquaculture 2010, 306:343-347.
37. Parhar I.S., Ogawa S., Sakuma Y. Laser-captured single digoxigenin-labeled neurons of gonadotropin-releasing hormone types reveal a novel G protein coupled receptor (Gpr54) during maturation in cichlid fish. Endocrinology 2004, 145:3613-3618.
38. Richard N., Corvaisier S., Camacho E., Kottler M.L. KiSS-1 and GPR54 at the pituitary level: overview and recent insights. Peptides 2009, 30:123-129.
39. Roa J., Aguilar E., Dieguez C., Pinilla L., Tena-Sempere M. New frontiers in kisspeptin/GPR54 physiology as fundamental gatekeepers of reproductive function. Front. Neuroendocrinol. 2008, 29:48-69.
40. Roseweir A.K., Millar R.P. The role of kisspeptin in the control of gonadotrophin secretion. Hum. Reprod. Update 2009, 15:203-212.
41. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative CT method. Nat. Protoc. 2008, 3:1101-1108.
42. Seminara S.B., Messager S., Chatzidaki E.E., Thresher R.R., Acierno J.S., Shagoury J.K., Bo-Abbas Y., Kuohung W., Schwinof K.M., Hendrick A.G., Zahn D., Dixon J., Kaiser U.B., Slaugenhaupt S.A., Gusella J.F., O'Rahilly S., Carlton M.B., Crowley W.F., Aparicio S.A., Colledge W.H. The GPR54 gene as a regulator of puberty. N. Engl. J. Med. 2003, 349:1614-1627.
43. Servili A., Le Page Y., Leprince J., Caraty A., Escobar S., Parhar E.S., Seong J.Y., Vaudry H., Kah O. Organization of two independent kisspeptin systems derived from evolutionary-ancient kiss genes in the brain of zebrafish. Endocrinology 2011, 152:1527-1540.
44. Shahjahan M., Motohashi E., Doi H., Ando H. Elevation of Kiss2 and its receptor gene expression in the brain and pituitary of grass puffer during the spawning season. Gen. Comp. Endocrinol. 2010, 169:48-57.
45. Shimizu Y., Tomikawa J., Hirano K., Nanikawa Y., Akazome Y., Kanda S., Kazeto Y., Okuzawa K., Uenoyama Y., Ohkura S., Tsukamura H., Maeda K.I., Gen K., Oka Y., Yamamoto N. Central distribution of kiss2 neurons and peri-pubertal changes in their expression in the brain of male and female red seabream Pagrus major. Gen. Comp. Endocrinol. 2012, 175:432-442.
46. 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.
47. Tena-Sempere M. Kisspeptin signaling in the brain: recent developments and future challenges. Mol. Cell. Endocrinol. 2010, 314:164-169.
48. Tena-Sempere M., Felip A., Gómez A., Zanuy S., Carrillo M. Comparative insights of the kisspeptin/kisspeptin receptor system: lessons from non-mammalian vertebrates. Gen. Comp. Endocrinol. 2012, 175:234-243.
49. Um H.N., Han J.M., Hwang J.I., Hong S.I., Vaudry H., Seong J.Y. Molecular coevolution of kisspeptins and their receptors from fish to mammals. Ann. N. Y. Acad. Sci. 2010, 1200:67-74.
50. Weltzien F.A., Taranger G.L., Karlsen O., Norberg B. Spermatogenesis and related plasma androgen levels in Atlantic halibut (Hippoglossus hippoglossus L.). Comp. Biochem. Physiol. A 2002, 132:567-575.
51. Yang B., Jiang Q., Chan T., Ko W.K., Wong A.O. Goldfish kisspeptin: molecular cloning, tissue distribution of transcript expression, and stimulatory effects on prolactin, growth hormone and luteinizing hormone secretion and gene expression via direct actions at the pituitary level. Gen. Comp. Endocrinol. 2010, 165:60-71.
52. Zhang D., Xiong H., Mennigen J.A., Popesku J.T., Marlatt V.L., Martyniuk C.J., Crump K., Cossins A.R., Xia X., Trudeau V.L. Defining global neuroendocrine gene expression patterns associated with reproductive seasonality in fish. PLoS One 2009, 4:e5816.
53. Zohar Y., Muñoz-Cueto J.A., Elizur A., Kah O. Neuroendocrinology of reproduction in teleost fish. Gen. Comp. Endocrinol. 2010, 165:438-455.