Molecular cloning and localization of the luteinizing hormone β subunit and glycoprotein hormone α subunit from Japanese anchovy Engraulis japonicus

Journal of Fish Biology

Volumn 77, Issue 2, 2010, Pages 372-387

  Ohkubo, M ^a   Katayama, S ^a   Shimizu, A ^a  

^a FISHERIES RESEARCH AGENCY   (Japan)

Author keywords

Cloning; Clupeiformes; Gonadotroph; Gonadotropin; Immunocytochemistry; Japanese anchovy; Pituitary

Indexed keywords

COMPLEMENTARY DNA; FISH PROTEIN; LUTEINIZING HORMONE BETA SUBUNIT; ALPHA CHAIN;

ALPHA CHAIN; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; DNA SEQUENCE; FISH; GENETICS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; DNA, COMPLEMENTARY; FISH PROTEINS; FISHES; GLYCOPROTEIN HORMONES, ALPHA SUBUNIT; LUTEINIZING HORMONE, BETA SUBUNIT; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

ANGUILLIFORMES; CLUPEA PALLASI; CLUPEIFORMES; CYPRINIFORMES; ENGRAULIS JAPONICUS; PISCES; TELEOSTEI;

EID: 77955043024     PISSN: 00221112     EISSN: 10958649     Source Type: Journal    
DOI: 10.1111/j.1095-8649.2010.02683.x     Document Type: Article

References (58)

1. Bendtsen J D, Nielsen H, von Heijne G, Brunakm S. Improved prediction of signal peptides: SignalP 3.0. Journal of Molecular Biology 2004, 340:783-795.
2. Carolsfeld J, Powell J F, Park M, Fischer W H, Craig A G, Chang J P, Rivier J E, Sherwood N M. Primary structure and function of three gonadotropin-releasing hormones, including a novel form, from an ancient teleost, herring. Endocrinology 2000, 141:505-512.
3. Cerdà J, Chauvigne 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. General and Comparative Endocrinology 2008, 156:470-481.
4. Chang Y S, Huang C J, Huang F L, Lo T B. Primary structures of carp gonadotropin subunits deduced from cDNA nucleotide sequences. International Journal of Peptide and Protein Research 1988, 32:556-564.
5. Chang Y S, Huang C J, Huang F L, Liu C S, Lo T B. Purification, characterization, and molecular cloning of gonadotropin subunits of silver carp (Hypophthalmichthys molitrix). General and Comparative Endocrinology 1990, 78:23-33.
6. Copeland P A, Thomas P. Isolation of gonadotropin subunits and evidence for two distinct gonadotropins in Atlantic croaker (Micropogonias undulatus). General and Comparative Endocrinology 1993, 91:115-125.
7. Elizur A, Zmora N, Rosenfeld H, Meiri I, Hassin S, Gordin H, Zohar Y. Gonadotropins beta-GtHI and beta-GtHII from the gilthead seabream, Sparus aurata. General and Comparative Endocrinology 1996, 102:39-46.
8. Farbridge K J, Leatherland J F. A comparative immunohistochemical study of the pars distalis in six species of teleost fishes. Fish Physiology and Biochemistry 1986, 1:63-74.
9. Gen K, Okuzawa K, Senthilkumaran B, Tanaka H, Moriyama S, Kagawa H. Unique expression of gonadotropin-I and -II subunit genes in male and female red seabream (Pagrus major) during sexual maturation. Biology of Reproduction 2000, 63:308-319.
10. Grandi G, Colombo G, Chicca M. Immunocytochemical studies on the pituitary gland of Anguilla anguilla L., in relation to early growth stages and diet-induced sex differentiation. General and Comparative Endocrinology 2003, 131:66-76.
11. Han Y S, Liao I C, Huang Y S, Tzeng W N, Yu J Y. Profiles of PGH-alpha, GTH I-beta, and GTH II-beta mRNA transcript levels at different ovarian stages in the wild female Japanese eel Anguilla japonica. General and Comparative Endocrinology 2003, 133:8-16.
12. Hassin S, Elizur A, Zohar Y. Molecular cloning and sequence analysis of striped bass (Morone saxatilis) gonadotrophin-I and -II subunits. Journal of Molecular Endocrinology 1995, 15:23-35.
13. Hellqvist A, Bornestaf C, Borg B, Schmitz M. Cloning and sequencing of the FSH-beta and LH beta-subunit in the three-spined stickleback, Gasterosteus aculeatus, and effects of photoperiod and temperature on LH-beta and FSH-beta mRNA expression. General and Comparative Endocrinology 2004, 135:167-174.
14. Hellqvist A, Schmitz M, Mayer I, Borg B. Seasonal changes in expression of LH-beta and FSH-beta in male and female three-spined stickleback, Gasterosteus aculeatus. General and Comparative Endocrinology 2006, 145:263-269.
15. Ikeuchi T, Nagae M, Lokman P M, Adachi S, Yamauchi K. Specific antibodies against synthetic oligopeptides of eel GTH/TSH subunits. Fisheries Science 1999, 65:871-877.
16. Itoh H, Suzuki K, Kawauchi H. The complete amino acid sequences of beta-subunits of two distinct chum salmon GTHs. General and Comparative Endocrinology 1988, 71:438-451.
17. Jackson K, Goldberg D, Ofir M, Abraham M, Degani G. Blue gourami (Trichogaster trichopterus) gonadotropic beta subunits (I and II) cDNA sequences and expression during oogenesis. Journal of Molecular Endocrinology 1999, 23:177-187.
18. Kagawa H, Kawazoe I, Tanaka H, Okuzawa K. Immunocytochemical identification of two distinct gonadotropic cells (GTH I and GTH II) in the pituitary of bluefin tuna, Thunnus thynnus. General and Comparative Endocrinology 1998, 110:11-18.
19. Kajimura S, Yoshiura Y, Suzuki M, Utoh T, Horie N, Oka H, Aida K. Change in the level of mRNA coding for gonadotropin Iβ and IIβ subunits during vitellogenesis in the common Japanese conger Conger myriaster. Fisheries Science 2001a, 67:1053-1062.
20. Kajimura S, Yoshiura Y, Suzuki M, Aida K. cDNA cloning of two gonadotropin beta subunits (GTH-Ibeta and -IIbeta) and their expression profiles during gametogenesis in the Japanese flounder (Paralichthys olivaceus). General and Comparative Endocrinology 2001b, 122:117-129.
21. Kato Y, Gen K, Maruyama O, Tomizawa K, Kato T. Molecular cloning of cDNAs encoding two gonadotrophin beta subunits (GTH-I beta and -II beta) from the masu salmon, Oncorhynchus masou: rapid divergence of the GTH-I beta gene. Journal of Molecular Endocrinology 1993, 11:275-282.
22. Ko H, Park W, Kim D J, Kobayashi M, Sohn Y C. Biological activities of recombinant Manchurian trout FSH and LH: their receptor specificity, steroidogenic and vitellogenic potencies. Journal of Molecular Endocrinology 2007, 38:99-111.
23. Laiz-Carrión R, del Mar Segura-Noguera M, del Pilar Martín del Río M, Mancera J M. Ontogeny of adenohypophyseal cells in the pituitary of the American shad (Alosa sapidissima). General and Comparative Endocrinology 2003, 132:454-464.
24. Licht P, Papkoff H, Farmer S W, Muller C H, Tsui H W, Crews D. Evolution of gonadotropin structure and function. Recent Progress in Hormone Research 1967, 33:169-248.
25. Lin Y W, Rupnow B A, Price D A, Greenberg R M, Wallace R A. Fundulus heteroclitus gonadotropins. 3. Cloning and sequencing of gonadotropic hormone (GTH) I and II beta-subunits using the polymerase chain reaction. Molecular and Cellular Endocrinology 1992, 85:127-139.
26. Liu Z, Kim S, Karsi A. Channel catfish follicle-stimulating hormone and luteinizing hormone: complementary DNA cloning and expression during ovulation. Marine Biotechnology 2001, 3:590-599.
27. Mateos J, Mañanós E, Martínez-Rodríguez G, Carrillo M, Querat B, Zanuy S. Molecular characterization of sea bass gonadotropin subunits (alpha, FSHbeta, and LHbeta) and their expression during the reproductive cycle. General and Comparative Endocrinology 2003, 133:216-232.
28. Miura T, Yamauchi K, Takahashi H, Nagahama Y. Human chorionic gonadotropin induces all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). Developmental Biology 1991, 146:258-262.
29. Nagahama Y. Histo-physiological studies on the pituitary gland of some teleost fishes, with special reference to the classification of hormone-producing cells in the adenohypophysis. Memoirs of the Faculty of Fisheries Hokkaido University 1973, 21:1-63.
30. Nielsen H, Engelbrecht J, Brunak S, von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Engineering 1997, 10:1-6.
31. Nozaki M, Naito N, Swanson P, Dickhoff W W, Nakai Y, Suzuki K, Kawauchi H. Salmonid pituitary gonadotrophs. II. Ontogeny of GTH I and GTH II cells in the rainbow trout (Salmo gairdneri irideus). General and Comparative Endocrinology 1990, 77:358-367.
32. Olivereau M, Nagahama Y. Immunocytochemistry of gonadotropic cells in the pituitary of some teleost species. General and Comparative Endocrinology 1983, 50:252-260.
33. Pierce J G, Parsons T F. Glycoprotein hormones: structure and function. Annual Review of Biochemistry 1981, 50:465-495.
34. Power M E, Carolsfield J, Wallis G P, Sherwood N M. Isolation and characterization of a cDNA for gonadotropin II-beta of Pacific herring, an ancient teleost. Journal of Fish Biology 1997, 50:315-323.
35. Prat F, Sumpter J P, Tyler C R. Validation of radioimmunoassays for two salmon gonadotropins (GTH I and GTH II) and their plasma concentrations throughout the reproductive cycle in male and female rainbow trout (Oncorhynchus mykiss). Biology of Reproduction 1996, 54:1375-1382.
36. Querat B, Sellouk A, Salmon C. Phylogenetic analysis of the vertebrate glycoprotein hormone family including new sequences of sturgeon (Acipenser baeri) beta subunits of the two gonadotropins and the thyroid-stimulating hormone. Biology of Reproduction 2000, 63:222-228.
37. Rebers F E M, Tensen C P, Schulz R W, Goos H J T, Bogerd J. Modulation of glycoprotein hormone α- and gonadotropin IIβ-subunit mRNA levels in the pituitary gland of mature male African catfish, Clarias gariepinus. Fish Physiology and Biochemistry 1997, 17:99-108.
38. Rosenfeld H, Levavi-Sivan B, Levavi-Sivan B, Melamed P, Yaron Z, Elizur A. The GTH β subunits of tilapia: gene cloning and expression. Fish Physiology and Biochemistry 1997, 17:85-92.
39. Saga T, Oota Y, Nozaki M, Swanson P. Salmonid pituitary gonadotrophs. III. Chronological appearance of GTH I and other adenohypophysial hormones in the pituitary of the developing rainbow trout (Oncorhynchus mykiss irideus). General and Comparative Endocrinology 1993, 92:233-241.
40. Sekine S, Saito A, Itoh H, Kawauchi H, Itoh S. Molecular cloning and sequence analysis of chum salmon gonadotropin cDNAs. Proceedings of the National Academy of Science of the United States of America 1989, 86:8645-8649.
41. Shimizu A, Yamashita M. Purification of mummichog (Fundulus heteroclitus) gonadotropins and their subunits, using an immunochemical assay with antisera raised against synthetic peptides. General and Comparative Endocrinology 2002, 125:79-91.
42. Shimizu A, Tanaka H, Kagawa H. Immunocytochemical applications of specific antisera raised against synthetic fragment peptides of mummichog GtH subunits: examining seasonal variations of gonadotrophs (FSH cells and LH cells) in the mummichog and applications to other acanthopterygian fishes. General and Comparative Endocrinology 2003, 132:35-45.
43. Shimizu A, Hamaguchi M, Ito H, Ohkubo M, Udagawa M, Fujii K, Kobayashi T, Nakamura M. Appearances and chronological changes of mummichog Fundulus heteroclitus FSH cells and LH cells during ontogeny, sexual differentiation, and gonadal development. General and Comparative Endocrinology 2008, 156:312-322.
44. So W K, Kwok H F, Ge W. Zebrafish gonadotropins and their receptors: II. Cloning and characterization of zebrafish follicle-stimulating hormone and luteinizing hormone subunits - their spatial-temporal expression patterns and receptor specificity. Biology of Reproduction 2005, 72:1382-1396.
45. Sohn Y C, Yoshiura Y, Kobayashi M, Aida K. Seasonal changes in mRNA levels of gonadotropin and thyrotropin subunits in the goldfish, Carassius auratus. General and Comparative Endocrinology 1999, 113:436-444.
46. Suzuki K, Nagahama Y, Kawauchi H. Steroidogenic activities of two distinct salmon gonadotropins. General and Comparative Endocrinology 1988a, 71:452-458.
47. Suzuki K, Kanamori A, Nagahama Y, Kawauchi H. Development of salmon GTH I and GTH II radioimmunoassays. General and Comparative Endocrinology 1988b, 71:459-467.
48. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 2007, 24:1596-1599.
49. Thompson J D, Higgins D G, Gibson T J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 1994, 22:4673-4680.
50. Tyler C R, Sumpter J P, Kawauchi H, Swanson P. Involvement of gonadotropin in the uptake of vitellogenin into vitellogenic oocytes of the rainbow trout, Oncorhynchus mykiss. General and Comparative Endocrinology 1991, 84:291-299.
51. Ulloa-Aguirre A, Timossi C, Damián-Matsumura P, Dias J A. Role of glycosylation in function of follicle-stimulating hormone. Endocrine 1999, 11:205-215.
52. Vischer H F, Teves A C, Ackermans J C, van Dijk W, Schulz R W, Bogerd J. Cloning and spatiotemporal expression of the follicle-stimulating hormone beta subunit complementary DNA in the African catfish (Clarias gariepinus). Biology of Reproduction 2003, 68:1324-1332.
53. Watanabe Y. Latitudinal variation in the recruitment dynamics of small pelagic fishes in the western North pacific. Journal of Sea Research 2007, 58:46-58.
54. Wong T T, Zohar Y. Novel expression of gonadotropin subunit genes in oocytes of the gilthead seabream (Sparus aurata). Endocrinology 2004, 145:5210-5220.
55. Xia H, Chen F, Puett D. A region in the human glycoprotein hormone alpha-subunit important in holoprotein formation and receptor binding. Endocrinology 1994, 134:1768-1770.
56. Yoshiura Y, Kobayashi M, Kato Y, Aida K. Molecular cloning of the cDNAs encoding two gonadotropin beta subunits (GTH-I-beta and -II-beta) from the goldfish, Carassius auratus. General and Comparative Endocrinology 1997, 105:379-389.
57. Yoshiura Y, Suetake H, Aida K. Duality of gonadotropin in a primitive teleost, Japanese eel (Anguilla japonica). General and Comparative Endocrinology 1999, 114:121-131.
58. Zenkevics H, Vose V, Vosekalne I, Bũcena A. Partial deglycosylation of alpha subunit modifies sturgeon gonadotropin function. Acta Biochimica Polonica 2000, 47:815-819.