Differential expression and cellular localization of somatolactin-1 and -2 during early development in the gilthead sea bream

General and Comparative Endocrinology

Volumn 132, Issue 1, 2003, Pages 77-87

  Herrero Turrión, M Javier ^a   Rodríguez, Raquel E ^a   Velasco, Almudena ^a   Aijón, José ^a   Lara, Juan M ^a  

^a UNIVERSITY OF SALAMANCA   (Spain)

Author keywords

Gilthead sea bream; Hypophysis; In situ hybridization; MRNA; RT PCR; SL1; SL2

Indexed keywords

HYPOPHYSIS HORMONE; ISOPROTEIN; MESSENGER RNA; SOMATOLACTIN 1; SOMATOLACTIN 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DEVELOPMENT; EMBRYO; GENE EXPRESSION; HATCHING; HYBRIDIZATION; HYPOPHYSIS INTERMEDIATE LOBE; LARVA; NEUROHYPOPHYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SEA BREAM;

SPARUS AURATA;

EID: 0038183932     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/S0016-6480(03)00054-6     Document Type: Article

References (82)

1. Agellon L.B., Davies S.L., Lin C.M., Chen T.T., Powers D.A. Rainbow trout has two genes for growth hormone. Mol. Reprod. Dev. 1:1988;11-17.
2. Amemiya Y., Sogabe Y., Nozaki M., Takahashi A., Kawauchi H. Somatolactin in the white sturgeon and African lungfish and its evolutionary significance. Gen. Comp. Endocrinol. 114:1999;181-190.
3. Astola A., Pendón C., Ortíz M., Valdivia M.M. Cloning and expression of somatolactin, a pituitary hormone related to growth hormone and prolactin from gilthead seabream, Sparus aurata. Gen. Comp. Endocrinol. 104:1996;330-336.
4. Ayson F.G., Kaneko T., Hasegawa S., Hirano T. Differential expression of two prolactin and growth hormone genes during early development of tilapia (Oreochromis mossambicus) in fresh water and seawater: implications for possible involvement in osmoregulation during early life stages. Gen. Comp. Endocrinol. 95:1994;143-152.
5. Balon E.K. Saltatory processes and altricial to precocial forms in the ontogeny of fishes. Am. Zool. 21:1981;573-596.
6. Borrelli E. Pitfalls during development: controlling differentiation of the pituitary gland. Trends Genet. 10:1994;222-224.
7. Borski R.J., Hansen M.U., Nishioka R.S., Grau E.G. Differential processing of the two prolactin of the tilapia (Oreochromis mossambicus) in relation to environmental salinity. J. Exp. Zool. 264:1992;46-54.
8. Cavari B., Funkenstein B., Kawauchi H. Cloning of a second variant of somatolactin-encoding cDNA from the gilthead seabream Sparus aurata. Fish Physiol. Biochem. 22:2000;145-150.
9. Chan Y.H., Cheng K.W., Yu K.L., Chan K.M. Identification of two prolactin cDNA sequences from a goldfish pituitary cDNA library. Biochim. Biophys. Acta. 1307:1996;8-12.
10. Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162:1987;156-159.
11. Company R., Calduch-Giner J.A., Mingarro M., Pérez-Sánchez J. cDNA cloning and sequence of European sea bass (Dicentrarchus labrax) somatolactin. Comp. Biochem. Physiol. B. 127:2000;183-192.
12. Duan C., Duguay S.J., Plisetskaya E.M. Insulin-like growth factor I (IGF-I) mRNA expression in coho salmon, Oncorhynchus kisutch: tissue distribution and effects of growth hormone/prolactin family proteins. Fish Physiol. Biochem. 11:1993;371-379.
13. Funkenstein B., Kawauchi H., Cavari B. Ontogeny of somatolactin mRNA in the gilthead sea bream Sparus aurata. Fish Physiol. Biochem. 17:1997;247-252.
14. García-Hernández M.P., García-Ayala A., Elbal M.T., Agulleiro B. The adenohypophysis of Mediterranean yellowtail, Seriola dumerilii (Risso, 1810): an immunocytochemical study. Tissue Cell. 28:1996;577-585.
15. Herrero-Turrión M.J., Velasco A., Rodríguez R.E., Aijón J., Lara J.M. Co-expression of somatolactin mRNAs in the pituitary gland of gilthead sea bream. Anat. Embryol. 205:2002;407-416.
16. Ichikawa T. Histological observations in the pituitary gland and the glomerular body of the larvae of the marine teleost Hexagrammos otakii. Z. Zellforsch. 141:1973;493-503.
17. Iraqi F., Gong Z., Hew C.L. Isolation and characterization of somatolactin genes from cold water marine teleost lumpfish (Cyclopterus lumpus) and habilut (Hippoglossus hippoglossus). Mol. Mar. Biol. Biotechnol. 2:1993;96-103.
18. Jackson L.F., Swanson P., Duan C., Fruchtman S., Sullivan C.V. Purification, characterization, and bioassay of prolactin and growth hormone from temperate basses, genus morone. Gen. Comp. Endocrinol. 117:2000;138-150.
19. Johnson L.L., Norberg B., Willis M.L., Zebroski H., Swanson P. Isolation, characterization, and radioimmunoassay of Atlantic halibut somatolactin and plasma levels during stress and reproduction in flatfish. Gen. Comp. Endocrinol. 105:1997;194-209.
20. Kakizawa S., Kaneko T., Hasegawa S., Hirano T. Activation of somatolactin cells in the pituitary of the rainbow trout Oncorhynchus mykiss by low environmental calcium. Gen. Comp. Endocrinol. 91:1993;298-306.
21. Kakizawa S., Kaneko T., Hasegawa S., Hirano T. Effects of feeding, fasting, background adaptation, acute stress, and exhaustive exercise on the plasma somatolactin concentrations in rainbow trout. Gen. Comp. Endocrinol. 98:1995;137-146.
22. Kakizawa S., Kaneko T., Ogasawara T., Hirano T. Changes in plasma somatolactin levels during spawing migration of chum salmon. Fish Physiol. Biochem. 14:1995;93-101.
23. Kakizawa S., Kaneko T., Hirano T. Elevation of plasma somatolactin concentrations during acidosis in rainbow trout. J. Exp. Biology. 199:1996;1043-1051.
24. Kakizawa S., Ishimatsu A., Takeda T., Kaneko T., Hirano T. Possible involvement of somatolactin in the regulation of plasma bicarbonate for the compensation of acidosis in rainbow trout. J. Exp. Biol. 200:1997;2675-2683.
25. Kaneko T., Hirano T. Role of prolactin and somatolactin in calcium regulation in fish. J. Exp. Biol. 184:1993;31-45.
26. Kaneko T., Kakizawa S., Yada T. Pituitary of "cobalt" variant of rainbow trout separated from the hypothalamus lack most pars intermedial and neurohypophysial tissue. Gen. Comp. Endocrinol. 92:1993;31-40.
27. Kaneko T. Cell biology of somatolactin. Int. Rev. Cytol. 169:1996;1-24.
28. Llewellyn L., Ramsurn V.P., Sweeney G.E., Wigham T., Santos C.R., Power D.M. Cloning and characterisation of a fish aldolase B gene. Biochim. Biophys. Acta. 1263:1995;75-78.
29. Lu M., Swanson P., Renfro J.L. Effect of somatolactin and related hormones on transport by flounder renal tubule primary cultures. Am. J. Physiol. 268:1995;R577-R582.
30. Magliulo C., Schreibman M.P., Blum V. The distribution of immunoreactive FMRF-amide, neurotensin, and galanin in the brain and pituitary gland of three species of Xiphophorus from birth to sexual maturity. Gen. Comp. Endocrinol. 92:1993;269-280.
31. Mahmoud S.S., Moloney M.M., Habibi H.R. Cloning and sequencing of the goldfish growth hormone cDNA. Gen. Comp. Endocrinol. 101:1996;139-144.
32. Moons L., Cambré M., Ollevier F., Vandesande F. Immunocytochemical demonstration of close relationships between neuropeptidergic nerve fibers and hormone-producing cell types in the adenohypophysis of the sea bass (Dicentrarchus labrax). Gen. Comp. Endocrinol. 73:1989;270-283.
33. Mousa M.A., Mousa S.A. Immunocytochemical study on the localization and distribution of the somatolactin cells in the pituitary gland and the brain of Oreochromis niloticus (Teleostei, cichlidae). Gen. Comp. Endocrinol. 113:1999;197-211.
34. Mousa M.A., Mousa S.A. Implication of somatolactin in the regulation of sexual maturation and spawning of Mugil cephalus. J. Exp. Zool. 287:2000;62-73.
35. Olivereau M., Olivereau J., Vandesande F. Localization of growth hormone-releasing factor-like immunoreactivity in the hypothalamo-hypophysial system of some teleost species. Cell Tissue Res. 259:1990;73-80.
36. Olivereau M., Rand-Weaver M. Immunocytochemical study of the somatolactin cells in the pituitary of Pacific salmon, Oncorhynchus nerca, and O. keta at some stages of the reproductive cycle. Gen. Comp. Endocrinol. 93:1994;28-35.
37. Olivereau M., Rand-Weaver M. Inmunoreactive somatolactin cells in the pituitary young, migrating, spawing and spent chinook salmon, Oncorhynchus tshawytscha. Gen. Comp. Endocrinol. 13:1994;141-151.
38. Ono M., Takayama Y., Rand-Weaver M., Sakata S., Yasunaga T., Noso T., Kawauchi H. cDNA cloning of somatolactin, a pituitary protein related to growth hormone and prolactin. Proc. Natl. Acad. Sci. USA. 87:1990;4330-4334.
39. Ono M., Harigai T., Kaneko T., Sato Y., Ihara S., Kawauchi H. Pit-1/GH factor-1 involvement in the gene expression of somatolactin. Mol. Endocrinol. 8:1994;109-115.
40. Pandolfi M., Paz D.A., Maggese C., Ravaglia M., Vissio P. Ontogeny of immunoreactive somatolactin, prolactin and growth hormone secretory cells in the developing pituitary gland of Cichlasoma dimerus (Teleostei, Perciformes). Anat. Embryol. 203:2001;461-468.
41. Parhar I.S., Iwata M. Gonadotropin releasing hormone (GnRH) neurons project to growth hormone and somatolactin cells in the steelhead trout. Histochemistry. 102:1994;195-203.
42. Parhar I.S., Iwata M., Pfaff D.W., Schwanzel-Fukuda M. Embryonic development of gonadotropin-releasing hormone neurons in the sockeye salmon. J. Comp. Neurol. 362:1995;256-270.
43. Parhar I.S. GnRH in tilapia. Parhar I.S., Sakuma Y. GnRH in Tilapia. 1997;99-102 Brain Shuppan Publishers, Tokyo.
44. Pendón C., Martínez-Barberá J.P., Pérez-Sánchez J., Rodríguez R.B., Grenett H., Valdivia M.M. Cloning of the sole (Solea senegalensis) growth hormone-encoding cDNA. Gene. 145:1994;237-240.
45. Pendón C., Astola A., Pérez-Sánchez J., Valdivia M.M. Release of glycosylated and non-glycosylated forms of somatolactin by fish pituitary culture in vitro. Ann. NY Acad. Sci. 839:1998;478-479.
46. Planas J.V., Swanson P., Rand-Weaver M., Dickhoff W.W. Somatolactin stimulates in vitro gonadal steroidogenesis in coho salmon, Oncorhynchus kisutch. Gen. Comp. Endocrinol. 87:1992;1-5.
47. Power D.M., Canario A.V. Immunocytochemistry of somatotrophs, gonadotrophs, prolactin and adrenocorticotropin cells in larval sea bream (Sparus auratus) pituitaries. Cell Tissue Res. 269:1992;341-346.
48. Rand-Weaver M., Baker B.J., Kawauchi H. Cellular localization of somatolactin in the pars intermedia of some teleost fishes. Cell Tissue Res. 263:1991;207-215.
49. Rand-Weaver M., Noso T., Kawauchi H. The complete amino acid sequences of two variants of growth hormone from Atlantic cod. Gen. Comp. Endocrinol. 81:1991;39-50.
50. Rand-Weaver M., Swanson P., Kawauchi H., Dickhoff W.W. Somatolactin, a novel pituitary protein: purification and plasma levels during reproductive maturation of coho salmon. J. Endocrinol. 133:1992;393-403.
51. Rand-Weaver M., Swanson P. Plasma somatolactin levels in coho salmon (Oncorhyncus kitsutch) during smoltification and sexual maturation. Fish Physiol. Biochem. 11:1993;175-182.
52. Rand-Weaver M., Pottinger T.G., Sumpter J.P. Plasma somatolactin concentrations in salmonid fish are elevated by stress. J. Endocrinol. 138:1993;509-515.
53. Rand-Weaver M., Pottinger T.G., Guest A., Martin P., Smal J., Sumpter J.P. Somatolactin and growth hormone are differentially correlated to various metabolic parameters in trout. Neth. J. Zool. 45:1995;129-131.
54. Rentier-Delrue F., Swennen D., Prunet P., Lion M., Martial J.A. Tilapia prolactin: molecular cloning of two cDNAs and expression in Escherichia coli. DNA. 8:1989;261-270.
55. Rodríguez-Gómez F.J., Rendón-Unceta M.C., Piñuela C., Muñoz-Cueto J.A., Jimenez-Tenorio N., Sarasquete C. Immunocytohistochemical characterization of pituitary cells of the bluefin tuna, Thunnus thynnus L. Histol. Histopathol. 16:2001;443-451.
56. Ruijter J.M. Development and aging of the teleost pituitary: qualitative and quantitative observations in the annual cyprinodont Cynolebias whitei. Anat. Embryol. 175:1987;379-386.
57. Saga T., Yamaki K., Doi Y., Yoshizuka M. Chronological study of the appearance of adenohypophysial cells in the ayu (Plecoglossus altivelis). Anat. Embryol. 200:1999;469-475.
58. Santos C.R., Brinca L., Ingleton P.M., Power D.M. Cloning, expression, and tissue localisation of prolactin in adult sea bream (Sparus aurata). Gen. Comp. Endocrinol. 114:1999;57-66.
59. Sato N., Watanabe K., Murata K., Sakaguchi M., Kariya Y., Kimura S., Nonaka M., Kimura A. Molecular cloning and nucleotide sequence of tuna growth hormone cDNA. Biochim. Biophys. Acta. 949:1988;35-42.
60. Schoots A.F.M., Ruijter J.M., van Kemenade J.A.M., Denuce J.M. Immunoreactive prolactin in the pituitary gland of cyprinidont fish at the time of hatching. Cell Tissue Res. 233:1983;611-618.
61. Schreibman M.P., Margolis-Kazan H., Halpern-Sebold L. Immunoreactive gonadotropin and luteinizing hormone releasing hormone in the pituitary of neonatal platyfish. Gen. Comp. Endocrinol. 47:1982;385-391.
62. Shepherd B.S., Sakamoto T., Nishioka R.S., Richman III N.H., Mori I., Madsen S.S., Chen T.T., Hirano T., Bern H.A., Grau E.G. Somatotropic actions of the homologous growth hormone and prolactins in the euryhaline teleost, the tilapia, Oreochromis mossambicus. Proc. Natl. Acad. Sci. USA. 94:1997;2068-2072.
63. Shepherd B.S., Sakamoto T., Hyodo S., Nishioka R.S., Ball C., Bern H.A., Grau E.G. Is the primitive regulation of pituitary prolactin (tPRL177 and tPRL188) secretion and gene expression in the euryhaline tilapia (Oreochromis mossambicus) hypothalamic or environmental? J. Endocrinol. 161:1999;121-129.
64. Song S., Trinh K.Y., Hew C.L., Hwang S.J., Belkhode S., Idler D.R. Molecular cloning and expression of salmon prolactin cDNA. Eur. J. Biochem. 172:1988;279-285.
65. Specker J.L., King D.S., Nishioka R.S., Shirahata K., Yamaguchi K., Bern H.A. Isolation and partial characterization of a pair of prolactins released in vitro by the pituitary of a cichlid fish, Oreochromis mossambicus. Proc. Natl. Acad. Sci. USA. 82:1985;7490-7494.
66. Stefano A.V., Vissio P.G., Paz D.A., Somoza G.M., Maggese M.C., Barrantes G.E. Colocalization of GnRH binding sites with gonadotropin-, somatotropin-, somatolactin-, and prolactin-expressing pituitary cells of the pejerrey, Odontesthes bonariensis, in vitro. Gen. Comp. Endocrinol. 116:1999;133-139.
67. Takayama Y., Rand-Weaver M., Kawauchi H., Ono M. Gene structure of chum salmon somatolactin, a presumed pituitary hormone of the growth hormone/prolactin family. Mol. Endocrinol. 5:1991;778-786.
68. Taniyama S., Kitahashi T., Ando H., Ban M., Ueda H., Urano A. Changes in the levels of mRNAs for GH/prolactin/somatolactin family and Pit-1/GHF-1 in the pituitaries of pre-spawning chum salmon. J. Mol. Endocrinol. 23:1999;189-198.
69. Venkatesh B., Brenner S. Genomic structure and sequence of the pufferfish (Fugu rubripes) growth hormone-encoding gene: a comparative analysis of teleost growth hormone genes. Gene. 187:1997;211-215.
70. Villaplana M., García Ayala A., García Hernández M.P., Agulleiro B. Ontogeny of immunoreactive somatolactin cells in the pituitary of gilthead sea bream (Sparus aurata L., Teleostei). Anat. Embryol. 196:1997;227-234.
71. Villaplana M., García-Ayala A., Chaves-Pozo E., Agulleiro B. Identification of mammosomatotropes, growth hormone cells and prolactin cells in the pituitary gland of the gilthead sea bream (Sparus aurata L., Teleostei) using light immunocytochemical methods: an ontogenic study. Anat. Embryol. 202:2000;421-429.
72. Villaplana M., García Ayala A., García-Hernández M.P., Agulleiro B. Immunocytochemical and ultrastructural characterization of somatolactin cells from the gilthead sea bream (Sparus aurata L., Teleostei): an ontogenic study (from newly hatched to adults). Anat. Embryol. 203:2001;449-460.
73. Xiong F., Chin R.A., Hew C.L. A gene encoding chinook salmon (Oncorhynchus tschawytscha) prolactin: gene structure and potential cis-acting regulatory elements. Mol. Mar. Biol. Biotechnol. 1:1992;155-164.
74. Yang B.Y., Arab M., Chen T.T. Cloning and characterization of rainbow trout (Oncorhynchus mykiss) somatolactin cDNA and its expression in pituitary and nonpituitary tissue. Gen. Comp. Endocrinol. 106:1997;271-280.
75. Yang B.Y., Greene M., Chen T.T. Early embryonic expression of the growth hormone family protein genes in the developing rainbow trout, Oncorhynchus mykiss. Mol. Reprod. Dev. 53:1999;127-134.
76. Yasuda A., Itoh H., Kawauchi H. Primary structure of chum salmon prolactins: occurrence of highly conserved regions. Arch. Biochem. Biophys. 244:1986;528-541.
77. Yasuda A., Yamaguchi K., Noso T., Papkoff H., Polenov A.L., Nicoll C.S., Kawauchi H. The complete amino acid sequence of growth hormone from sturgeon (Acipencer guldenstadti). Biochim. Biophys. Acta. 1120:1992;297-304.
78. Zhu Y., Thomas P. Red drum somatolactin: development of a homologous radioimmunoassay and plasma levels after exposure to stressors or various backgrounds. Gen. Comp. Endocrinol. 99:1995;275-288.
79. Zhu Y., Thomas P. Elevations of somatolactin in plasma and pituitaries and increased alpha-MSH cell activity in red drum exposed to black background and decreased illumination. Gen. Comp. Endocrinol. 101:1996;21-31.
80. Zhu Y., Thomas P. Effects of somatolactin on melanosome aggregation in the melanophores of red drum (Sciaenops ocellatus) scales. Gen. Comp. Endocrinol. 105:1997;127-133.
81. Zhu Y., Thomas P. Effects of light on plasma somatolactin levels in red drum (Sciaenops ocellatus). Gen. Comp. Endocrinol. 111:1998;76-82.
82. Zhu Y., Yoshiura Y., Kikuchi K., Aida K., Thomas P. Cloning and phylogenetic relationship of red drum somatolactin cDNA and effects of light on pituitary somatolactin mRNA expression. Gen. Comp. Endocrinol. 113:1999;69-79.