Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2008

Open Access 01-12-2008 | Research

Cloning of somatolactin alpha, beta forms and the somatolactin receptor in Atlantic salmon: Seasonal expression profile in pituitary and ovary of maturing female broodstock

Authors: Susana Benedet, Björn Thrandur Björnsson, Geir Lasse Taranger, Eva Andersson

Published in: Reproductive Biology and Endocrinology | Issue 1/2008

Login to get access

Abstract

Background

Somatolactin (Sl) is a fish specific adenohypophyseal peptide hormone related to growth hormone (Gh). Some species, including salmonids, possess two forms: Sl alpha and Sl beta. The somatolactin receptor (slr) is closely related to the growth hormone receptor (ghr). Sl has been ascribed many physiological functions, including a role in sexual maturation. In order to clarify the role of Sl in the sexual maturation of female Atlantic salmon (Salmo salar), the full length cDNAs of slr, Sl alpha and Sl beta were cloned and their expression was studied throughout a seasonal reproductive cycle using real-time quantitative PCR (RTqPCR).

Methods

Atlantic salmon Sl alpha, Sl beta and slr cDNAs were cloned using a PCR approach. Gene expression of Sl alpha, SL beta and slr was studied using RTqPCR over a 17 month period encompassing pre-vitellogenesis, vitellogenesis, ovulation and post ovulation in salmon females. Histological examination of ovarian samples allowed for the classification according to the degree of follicle maturation into oil drop, primary, secondary or tertiary yolk stage.

Results

The mature peptide sequences of Sl alpha, Sl beta and slr are highly similar to previously cloned salmonid forms and contained the typical motifs. Phylogenetic analysis of Atlantic salmon Sl alpha and Sl beta shows that these peptides group into the two Sl clades present in some fish species. The Atlantic salmon slr grouped with salmonid slr amongst so-called type I ghr. An increase in pituitary Sl alpha and Sl beta transcripts before and during spawning, with a decrease post-ovulation, and a constant expression level of ovarian slr were observed. There was also a transient increase in Sl alpha and Sl beta in May prior to transfer from seawater to fresh water and ensuing fasting.

Conclusion

The up-regulation of Sl alpha and Sl beta during vitellogenesis and spawning, with a subsequent decrease post-ovulation, supports a role for Sl during gonadal growth and spawning. Sl could also be involved in calcium/phosphate mobilization associated with vitellogenesis or have a role in energy homeostasis associated with lipolysis during fasting. The up-regulation of both Sl alpha and Sl beta prior to fasting and freshwater transfer, suggests a role for Sl linked to reproduction that may be independent of the maturation induced fasting.
Appendix
Available only for authorised users
Literature
1.
Ono M, Takayama Y, Rand-Weaver M, Sakata S, Yasunaga T, Noso T, Kawauchi H: cDNA cloning of SL, a pituitary protein related to growth hormone and prolactin. Proc Natl Acad Sci USA. 1990, 87: 4330-4334. 10.1073/pnas.87.11.4330.PubMedCentralCrossRefPubMed
2.
Rand-Weaver M, Noso T, Muramoto K, Kawauchi H: Isolation and characterization of SL, a new protein related to growth hormone and prolactin from Atlantic cod (Gadus morhua) pituitary glands. Biochem. 1991, 30: 1509-1515. 10.1021/bi00220a010.CrossRef
3.
Takayama Y, Ono M, Rand-Weaver M, Kawauchi H: Greater conservation of somatolactin, a presumed pituitary hormone of the growth hormone/prolactin family, than of growth hormone in teleost fish. Gen Comp Endocrinol. 1991, 83: 366-374. 10.1016/0016-6480(91)90141-R.CrossRefPubMed
4.
Zhu Y, Stiller JW, Shaner MP, Baldini A, Scemama JL, Capehart AA: Cloning of SL α and β cDNAs in zebrafish and phylogenetic analysis of two distinct SL subtypes in fish. J Endocrinol. 2004, 182: 509-518. 10.1677/joe.0.1820509.CrossRefPubMed
5.
Fukada H, Ozaki Y, Pierce AL, Adachi S, Yamauchi K, Hara A, Swanson P, Dickhoff WW: Identification of the salmon SL receptor, a new member of the cytokine receptor family. Endocrinol. 2005, 146: 2354-2361. 10.1210/en.2004-1578.CrossRef
6.
Saera-Vila A, Calduch-Giner JA, Pérez-Sánchez J: Duplication of growth hormone receptor (GHR) in fish genome: gene organization and transcriptional regulation of GHR type I and type II in gilthead sea bream (Sparus aurata). Gen Comp Endocrinol. 2005, 142: 193-203. 10.1016/j.ygcen.2004.11.005.CrossRefPubMed
7.
Rand-Weaver M, Swanson P, Kawauchi H, Dickhoff WW: SL, a novel pituitary protein: purification and plasma levels during reproductive maturation of coho salmon. J Endocrinol. 1992, 133: 393-403.CrossRefPubMed
8.
Rand-Weaver M, Swanson P: Plasma somatolactin levels in coho salmon (Oncorhynchus kisutch) during smoltification and sexual maturation. Fish Physiol Biochem. 1993, 11: 175-182. 10.1007/BF00004564.CrossRefPubMed
9.
Rand-Weaver M, Pottinger TG, Sumpter JP: Plasma somatolactin concentrations in salmonid fish are elevated by stress. J Endocrinol. 1993, 138: 509-515.CrossRefPubMed
10.
Rand-Weaver M, Pottinger TG, Sumpter JP: Pronounced seasonal rhythms in plasma somatolactin levels in rainbow trout. J Endocrinol. 1995, 146: 113-119.CrossRefPubMed
11.
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. 1999, 23: 189-198. 10.1677/jme.0.0230189.CrossRefPubMed
12.
Olivereau M, Rand-Weaver M: Immunoreactive somatolactin cells in the pituitary of young, migrating, spawning and spent chinook salmon, Oncorhynchus tshawytscha. Fish Physiol Biochem. 1994, 13: 141-151. 10.1007/BF00004339.CrossRefPubMed
13.
Olivereau M, Rand-Weaver M: Immunocytochemical study of the somatolactin cells in the pituitary of Pacific salmon, Oncorhynchus nerka, and O. keta at some stages of the reproductive cycle. Gen Comp Endocrinol. 1994, 93: 28-35. 10.1006/gcen.1994.1004.CrossRefPubMed
14.
Kakizawa S, Kaneko T, Ogasawara T, Hirano T: Changes in plasma somatolactin levels during spawning migration of chum salmon (Oncorhynchus keta). Fish Physiol Biochem. 1995, 14: 93-101. 10.1007/BF00002453.CrossRefPubMed
15.
Campbell B, Dickey J, Beckman B, Young G, Pierce A, Fukada H, Swanson P: Previtellogenic oocyte growth in salmon: Relationships among body growth, plasma insulin-like growth factor 1, estradiol-17 beta, follicle-stimulating hormone and expression of ovarian genes for insulin-like growth factors, steroidogenic acute regulatory protein and receptors for gonadotropins, growth hormone and SL. Biol Reprod. 2006, 75: 34-44. 10.1095/biolreprod.105.049494.CrossRefPubMed
16.
Planas JV, Swanson P, Rand-Weaver M, Dickhoff WW: Somatolactin stimulates in vitro gonadal steroidogenesis in coho salmon, Oncorhynchus kisutch. Gen Comp Endocrinol. 1992, 87: 1-5. 10.1016/0016-6480(92)90142-7.CrossRefPubMed
17.
Oguri M: On the Enlarged Liver in "Cobalt" Variant of Rainbow Trout. Bull Jpn Soc Sci Fish. 1976, 42: 823-830.CrossRef
18.
Kaneko T, Kakizawa S, Yada T: Pituitary of "cobalt" variant of the rainbow trout separated from the hypothalamus lacks most pars intermedial and neurohypophysial tissue. Gen Comp Endocrinol. 1993, 92: 31-40. 10.1006/gcen.1993.1140.CrossRefPubMed
19.
Yada T, Moriyama S, Suzuki Y, Azuma T, Takahashi A, Hirose S, Naito N: Relationships between obesity and metabolic hormones in the "cobalt" variant of rainbow trout. Gen Comp Endocrinol. 2002, 128: 36-43. 10.1016/S0016-6480(02)00047-3.CrossRefPubMed
20.
Fukamachi S, Yada T, Mitani H: Medaka receptors for SL and growth hormone: phylogenetic paradox among fish growth hormone receptors. Genetics. 2005, 171: 1875-1883. 10.1534/genetics.105.048819.PubMedCentralCrossRefPubMed
21.
Yang BY, Arab M, Chen TT: Cloning and characterization of rainbow trout (Oncorhynchus mykiss) SL cDNA and its expression in pituitary and nonpituitary tissues. Gen Comp Endocrinol. 1997, 106: 271-280. 10.1006/gcen.1996.6880.CrossRefPubMed
22.
Yang BY, Chen TT: Identification of a new growth hormone family protein, SL-like protein, in the rainbow trout (Oncorhynchus mykiss) pituitary gland. Endocrinology. 2003, 144: 850-857. 10.1210/en.2002-221005.CrossRefPubMed
23.
Thompson JD, Higgins DG, Gibson TJ: CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994, 22: 4673-4680. 10.1093/nar/22.22.4673.PubMedCentralCrossRefPubMed
24.
25.
Dahle R, Taranger GL, Karlsen Ø, Kjesbu OS, Norberg B: Gonadal development and associated changes in liver size and sexual steroids during the reproductive cycle of captive male and female Atlantic cod (Gadus morhua L.). Comp Biochem Physiol A Mol Integr Physiol. 2003, 136 (3): 641-653. 10.1016/S1095-6433(03)00215-0.CrossRefPubMed
26.
Bogerd J, Blomenröhr M, Andersson E, Putten van der HHAGM, Tensen CP, Vischer H, Granneman JCM, Janssen-Dommerholt C, Goos HJTh, Schulz RW: Discrepancy between molecular structure and ligand selectivity of a testicular gonadotropin receptor of the African catfish (Clarias gariepinus). Biol Reprod. 2001, 64: 1633-1643. 10.1095/biolreprod64.6.1633.CrossRefPubMed
27.
Taranger GL, Haux C, Hansen T, Stefansson SO, Björnsson BT, Walther BT, Kryvi H: Mechanisms underlying photoperiodic effects on age at sexual maturity in Atlantic salmon, Salmo salar. Aquaculture. 1999, 177: 47-60. 10.1016/S0044-8486(99)00068-X.CrossRef
28.
Amemiya Y, Sogabe Y, Nozaki M, Takahashi A, Kawauchi H: SL in the white sturgeon and African lungfish and its evolutionary significance. Gen Comp Endocrinol. 1999, 114: 181-199. 10.1006/gcen.1998.7250.CrossRefPubMed
29.
Vega-Rubín de Celis S, Gómez P, Calduch-Giner JA, Médale F, Pérez-Sánchez J: Expression and characterization of European sea bass (Dicentrarchus labrax) SL: Assessment of in vivo metabolic effects. Mar Biotechnol. 2003, 5: 92-101. 10.1007/s10126-002-0053-6.CrossRefPubMed
30.
Ingleton PM, Power DM, Canario AVM, Martin TJ, Danks JA: Parathyroid hormone-related protein and somatolactin in sea bream (Sparus aurata) brain and pituitary. Ann NY Acad Sci. 1998, 839: 370-371. 10.1111/j.1749-6632.1998.tb10800.x.CrossRef
31.
Abbink W, Bevelander GS, Hang X, Lu W, Guerreiro PM, Spanings T, Canario AVM, Flik G: PTHrP regulation and calcium balance in sea bream (Sparus auratus L.) under calcium constraint. J Exp Biol. 2006, 209: 3550-3557. 10.1242/jeb.02399.CrossRefPubMed
32.
Guerreiro PM, Renfro L, Power DM, Canario AVM: The parathyroid hormone family of peptides: structure, tissue distribution, regulation, and potential functional roles in calcium and phosphate balance in fish. Am J Physiol Regul Integr Comp Physiol. 2007, 292: R679-R696.CrossRefPubMed
33.
Fukamachi S, Meyer A: Evolution of receptors for growth hormone and somatolactin in fish and land vertebrates: lessons from the lungfish and sturgeon orthologues. J Mol Evol. 2007, 65: 359-372. 10.1007/s00239-007-9035-7.CrossRefPubMed
34.
Nguyen N, Sugimoto M, Zhu Y: Production and purification of recombinant SLβ and its effects on melanosome aggregation in zebrafish. Gen Comp Endocrinol. 2006, 145: 182-187. 10.1016/j.ygcen.2005.09.015.CrossRefPubMed
35.
Kakizawa S, Kaneko T, Hirano T: Effects of hypothalamic factors on somatolactin secretion from the organ-cultured pituitary of rainbow trout. Gen Comp Endocrinol. 1997, 105: 71-78. 10.1006/gcen.1996.6799.CrossRefPubMed
36.
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. 1995, 99: 275-288. 10.1006/gcen.1995.1111.CrossRefPubMed
37.
Fukamachi S, Sugimoto M, Mitani H, Shima A: SL selectively regulates proliferation and morphogenesis of neural-crest derived pigment cells in medaka. Proc Natl Acad Sci USA. 2004, 101: 10661-10666. 10.1073/pnas.0401278101.PubMedCentralCrossRefPubMed
38.
Martín Canepa M, Pandolfi M, Maggese MC, Vissio PG: Involvement of SL in background adaptation of the cichlid fish Cichlasoma dimerus. J Exp Zool. 2006, 305A: 410-419. 10.1002/jez.a.273.CrossRef
39.
Fukamachi S, Wakamatsu Y, Mitani H: Medaka double mutants for color interfere and leucophore free: characterization of the xantophore-somatolactin relationship using the leucophore free gene. Dev Genes Evol. 2006, 216: 152-157. 10.1007/s00427-005-0040-9.CrossRefPubMed
40.
Mingarro M, Vega-Rubín de Celis S, Astola A, Pendón C, Martínez Valdivia M, Pérez-Sánchez J: Endocrine mediators of seasonal growth in gilthead sea bream (Sparus aurata): the growth hormone and SL paradigm. Gen Comp Endocrinol. 2002, 128: 102-111. 10.1016/S0016-6480(02)00042-4.CrossRefPubMed
41.
Kakizawa S, Kaneko T, Hirano T: Elevation of plasma somatolactin concentrations during acidosis in rainbow trout (Oncorhynchus mykiss). J Exp Biol. 1996, 199: 1043-1051.PubMed
42.
Lu M, Swanson P, Renfro JL: Effect of somatolactin and related hormones on phosphate transport by flounder renal tubule primary cultures. Am J Physiol. 1995, 268 (3 Pt 2): 577-582.
43.
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. 1993, 91: 298-306. 10.1006/gcen.1993.1130.CrossRefPubMed
44.
Calduch-Giner JA, Pendón C, Valdivia MM, Pérez-Sánchez J: Recombinant somatolactin as a stable and bioactive protein in a cell culture bioassay: development and validation of a sensitive and reproducible radioimmunoassay. J Endocrinol. 1998, 156: 441-447. 10.1677/joe.0.1560441.CrossRefPubMed
45.
Cheng KW, Chan YH, Chen YD, Yu KL, Chan KM: Sequence of a cDNA clone encoding a novel somatolactin in goldfish, Carassius auratus. Biochem Biophys Res Commun. 1997, 232: 282-287. 10.1006/bbrc.1997.6271.CrossRefPubMed
46.
Allan GJ, Shand JH, Beattie J, Flint DJ: Identification of novel sites in the ovine growth hormone receptor involved in binding hormone and conferring species specificity. Eur J Biochem. 1999, 261: 555-561. 10.1046/j.1432-1327.1999.00306.x.CrossRefPubMed
47.
Fukada H, Ozaki Y, Pierce AL, Adachi S, Yamauchi K, Hara A, Swanson P, Dickhoff WW: Salmon growth hormone receptor: molecular cloning, ligand specificity, and response to fasting. Gen Comp Endocrinol. 2004, 139: 61-71. 10.1016/j.ygcen.2004.07.001.CrossRefPubMed
48.
Benedet S, Johansson V, Sweeney G, Galay-Burgos M, Björnsson BTh: Cloning of two Atlantic salmon growth hormone receptor isoforms and in vitro ligand-binding response. Fish Physiol Biochem. 2005, 31: 315-329. 10.1007/s10695-005-2524-y.CrossRef
49.
Very NM, Kittilson JD, Norbeck LA, Sheridan MA: Isolation, characterization, and distribution of two cDNAs encoding for growth hormone receptor in rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol B. 2005, 140: 615-628. 10.1016/j.cbpc.2004.12.008.CrossRefPubMed
50.
Jiao B, Huang X, Chan CB, Zhang L, Wang D, Cheng CHK: The co-existence of two growth hormone receptors in teleost fish and their differential signal transduction, tissue distribution and hormonal regulation of expression in seabream. J Mol Endocrinol. 2006, 36: 23-40. 10.1677/jme.1.01945.CrossRefPubMed
51.
Phillips R, Ráb P: Chromosome evolution in the Salmonidae (Pisces): an update. Biol Rev Camb Philos Soc. 2001, 76: 1-25. 10.1017/S1464793100005613.CrossRefPubMed
52.
Johnson LL, Norberg B, Willis ML, Zebroski H, Swanson P: Isolation, characterization, and radioimmunoassay of Atlantic halibut somatolactin and plasma levels during stress and reproduction in flatfishes. Gen Comp Endocrinol. 1997, 105: 194-209. 10.1006/gcen.1996.6821.CrossRefPubMed
53.
Mousa MA, Mousa SA: Implication of somatolactin in the regulation of sexual maturation and spawning of Mugil cephalus. J Exp Zool. 2000, 287: 62-73. 10.1002/1097-010X(20000615)287:1<62::AID-JEZ8>3.0.CO;2-0.CrossRefPubMed
54.
Persson P, Sundell K, Björnsson BTh, Lundqvist H: Calcium metabolism and osmoregulation during sexual maturation of river running Atlantic salmon. J Fish Biol. 1998, 52: 334-349. 10.1111/j.1095-8649.1998.tb00801.x.CrossRef
55.
Norberg B, Björnsson BT, Brown CL, Wichardt UP, Deftos L, Haux C: Changes in plasma vitellogenin, sex steroids, calcitonin, and thyroid hormones related to sexual maturation in female brown trout (Salmo trutta). Gen Comp Endocrinol. 1989, 75: 316-26. 10.1016/0016-6480(89)90085-3.CrossRefPubMed
56.
Fuentes J, Guerreiro PM, Modesto T, Rotlant J, Canario AVM, Power DM: A PTH/PTHrP receptor antagonist blocks the hypercalcemic response to estradiol-17 β. Am J Physiol Regul Integr Comp Physiol. 2007, 293: R956-R960.CrossRefPubMed
57.
Bevelander GS, Hang X, Abbink W, Spanings T, Canario AVM, Flik G: PTHrP potentiating estradiol-induced vitellogenesis in sea bream (Sparus auratus, L.). Gen Comp Endocrinol. 2006, 149: 159-165.CrossRefPubMed
58.
Company R, Astola A, Pendón C, Valdivia MM, Pérez-Sánchez J: Somatotropic regulation of fish growth and adiposity: growth hormone (GH) and somatolactin (SL) relationship. Comp Biochem Physiol C. 2001, 130: 435-445. 10.1016/S1096-4959(01)00408-0.CrossRef
59.
Vega-Rubín de Celis S, Gómez-Requeni P, Pérez-Sánchez J: Production and characterization of recombinantly derived peptides and antibodies for accurate determinations of somatolactin, growth hormone and insulin-like growth factor-I in European sea bass (Dicentrarchus labrax). Gen Comp Endocrinol. 2004, 139: 266-277. 10.1016/j.ygcen.2004.09.017.CrossRefPubMed
60.
Vega-Rubín de Celis S, Rojas P, Gómez-Requeni P, Albalat A, Gutiérrez J, Médale F, Kaushik S, Navarro I, Pérez-Sánchez J: Nutritional assessment of somatolactin function in gilthead sea bream (Sparus aurata): concurrent changes in somatotropic axis and pancreatic hormones. Comp Biochem Physiol A. 2004, 138: 533-542. 10.1016/j.cbpb.2004.06.007.CrossRef
61.
Kadri S, Thorpe JE, Metcalfe NB: Anorexia in one-sea-winter Atlantic salmon (Salmo salar) during summer, associated with sexual maturation. Aquaculture. 1997, 151: 405-409. 10.1016/S0044-8486(96)01495-0.CrossRef
Metadata
Title
Cloning of somatolactin alpha, beta forms and the somatolactin receptor in Atlantic salmon: Seasonal expression profile in pituitary and ovary of maturing female broodstock
Authors
Susana Benedet
Björn Thrandur Björnsson
Geir Lasse Taranger
Eva Andersson
Publication date
01-12-2008
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2008
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/1477-7827-6-42

Other articles of this Issue 1/2008

Reproductive Biology and Endocrinology 1/2008 Go to the issue

Research

Influence of pregnancy and labor on the occurrence of nerve fibers expressing the capsaicin receptor TRPV1 in human corpus and cervix uteri

Review

Regulatory RNAs and chromatin modification in dosage compensation: A continuous path from flies to humans?

Research

Level set segmentation of bovine corpora lutea in ex situ ovarian ultrasound images

Research

Prostasome-like vesicles stimulate acrosome reaction of pig spermatozoa

Research

The glycoprotein-hormones activin A and inhibin A interfere with dendritic cell maturation

Research

Assessment of the biopotency of follitropin alfa and lutropin alfa combined in one injection: a comparative trial in Sprague-Dawley rats