Fish Physiology and Biochemistry

, Volume 44, Issue 3, pp 983–995 | Cite as

Characterization and expression analyses of somatolactin-α and -β genes in rare minnows (Gobiocypris rarus) following waterborne cadmium exposure

  • Xiao-Hong Liu
  • Bi-Wen Xie
  • Zhi-Jian Wang
  • Yao-Guang Zhang


Using reverse transcription-polymerase chain reaction (RT-PCR) and RACE (rapid amplification of cDNA ends), somatolactin-α (rmSLα) and -β (rmSLβ) were identified from the pituitary gland of rare minnows (Gobiocypris rarus). The full-length cDNAs of these two genes were 1288 and 801 bp, encoding prepeptides of 250 and 228 amino acids residues, respectively. rmSLβ can be detected in the brain (including the pituitary), ovary, testis, and gill, while rmSLα was mainly expressed in the brain. On the other hand, rmSLα was expressed in all the fetal developmental stages; however, rmSLβ can just be detected in the stages since from 14 h post-fertilization (hpf). After exposure to acute waterborne cadmium (Cd), rmSLα was distinctly upregulated in juvenile rare minnows at all detected time points, from 24 to 96 h and 10 days, while rmSLβ was significantly altered only in 96 h or 10-day treatment groups. As for adults, acute Cd exposure caused alterations of both rmSLα and rmSLβ in the brain (containing the pituitary) at the 24 h; subchronic waterborne Cd treatment led to upregulation of rmSLα, while decrease of mSLβ in the brain. Alteration of rmSL transcripts following waterborne Cd exposure further confirmed the endocrine disruption of this heavy metal. Besides, exposure to as low as 5 μg/L Cd caused alteration of rmSLα, which suggested that rmSLα might be a potential biomarker for risk assessment of aquatic Cd.


Somatolactin Rare minnow Waterborne cadmium exposure Subfunctionalization 



This work was funded by the major program of science and technology commission foundation of Chongqing (cstc2014yykfc80001), China postdoctoral science foundation (2017M622949), and Chongqing postdoctoral science foundation special funded project (Xm2017071). We thank Dr. Qi Liu for helpful discussion, and we are grateful for the members in Zhang’s and Wang’s laboratory for fish raising and sample collection.

Supplementary material

10695_2018_487_MOESM1_ESM.eps (18.6 mb)
Figure S1 Three dimensional structure models of somatolactin-α (SLα) and (SLβ) genes predicted by Swiss-model Workspace. (EPS 19077 kb)
10695_2018_487_MOESM2_ESM.docx (50 kb)
ESM 2 (DOCX 48 kb)


  1. Agustsson T, Sundell K, Sakamoto T et al (2003) Pituitary gene expression of somatolactin, prolactin, and growth hormone during Atlantic salmon parr-smolt transformation. Aquaculture 222(1):229–238CrossRefGoogle Scholar
  2. Amemiya Y, Sogabe Y, Nozaki M, Takahashi A, Kawauchi H (1999) Somatolactin in the white sturgeon and African lungfish and its evolutionary significance. Gen Comp Endocrinol 114(2):181–190CrossRefPubMedGoogle Scholar
  3. Astola A, Pendon C, Ortiz M et al (1996) Cloning and expression of somatolactin, a pituitary hormone related to growth hormone and prolactin from gilthead seabream, Sparus aurata. Gen Comp Endocrinol 104(3):330–336CrossRefPubMedGoogle Scholar
  4. Benedet S, Bjornsson BT, Taranger GL et al (2008) Cloning of somatolactin alpha, beta forms and the somatolactin receptor in Atlantic salmon: seasonal expression profile in pituitary and ovary of maturing female broodstock. Reprod Biol Endocrinol 6:42CrossRefPubMedPubMedCentralGoogle Scholar
  5. Biasini M, Bienert S, Waterhouse A et al (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42(Web Server issue):W252–W258CrossRefPubMedPubMedCentralGoogle Scholar
  6. Brzoska MM, Moniuszko-Jakoniuk J (2001) Interactions between cadmium and zinc in the organism. Food Chem Toxicol 39(10):967–980CrossRefPubMedGoogle Scholar
  7. Canepa MM, Pandolfi M, Maggese MC et al (2006) Involvement of somatolactin in background adaptation of the cichlid fish Cichlasoma dimerus. J Exp Zool A Comp Exp Biol 305(5):410–419CrossRefPubMedGoogle Scholar
  8. Company R, Astola A, Pendon C et al (2001) Somatotropic regulation of fish growth and adiposity: growth hormone (GH) and somatolactin (SL) relationship. Comp Biochem Physiol C Toxicol Pharmacol 130(4):435–445CrossRefPubMedGoogle Scholar
  9. Daza DO, Larhammar D (2018) Evolution of the growth hormone, prolactin, prolactin 2 and somatolactin family. Gen Comp Endocrinol.
  10. Dolci GS, Vey LT, Schuster AJ, Roversi K, Roversi K, Dias VT, Pase CS, Barcelos RCS, Antoniazzi CTD, Golombieski JI, Glanzner WG, Anezi Junior PA, Gonçalves PBD, Nunes MAG, Dressler VL, Baldisserotto B, Burger ME (2014) Hypoxia acclimation protects against oxidative damage and changes in prolactin and somatolactin expression in silver catfish (Rhamdia quelen) exposed to manganese. Aquat Toxicol 157:175–185CrossRefPubMedGoogle Scholar
  11. Ferrandino I, Favorito R, Grimaldi MC (2010) Cadmium induces changes on ACTH and PRL cells in Podarcis sicula lizard pituitary gland. Eur J Histochem 54(4):e45CrossRefPubMedPubMedCentralGoogle Scholar
  12. Fukamachi S, Meyer A (2007) Evolution of receptors for growth hormone and somatolactin in fish and land vertebrates: lessons from the lungfish and sturgeon orthologues. J Mol Evol 65(4):359–372CrossRefPubMedGoogle Scholar
  13. Harvey S, Martinez-Moreno CG, Luna M et al (2015) Autocrine/paracrine roles of extrapituitary growth hormone and prolactin in health and disease: an overview. Gen Comp Endocrinol 220:103–111CrossRefPubMedGoogle Scholar
  14. Honji RM, Nobrega RH, Pandolfi M et al (2013) Immunohistochemical study of pituitary cells in wild and captive Salminus hilarii (Characiformes: Characidae) females during the annual reproductive cycle. Spring 2:460. CrossRefGoogle Scholar
  15. Imaoka T, Matsuda M, Mori T (2000) Extrapituitary expression of the prolactin gene in the goldfish, African clawed frog and mouse. Zool Sci 17(6):791–796CrossRefGoogle Scholar
  16. Jarup L, Berglund M, Elinder CG et al (1998) Health effects of cadmium exposure—a review of the literature and a risk estimate. Scand J Work Environ Health 24(Suppl 1):1–51PubMedGoogle Scholar
  17. Jiang Q, Wong AOL (2013) Signal transduction mechanisms for autocrime/paracrine regulation of somatolactin-a serection and synthesis in carp pituitary cells by somatolactin-ɑ and -β. Am J Physiol Endocrinol Metab 304:E176–E186CrossRefPubMedGoogle Scholar
  18. Jiang Q, He M, Wang X, Wong AOL (2008a) Grass carp somatolactin: II. Pharmacological study on postreceptor signaling mechanisms for PACAP-induced somatolactin-alpha and -beta gene expression. Am J Physiol Endocrinol Metab 295(2):E477–E490CrossRefPubMedGoogle Scholar
  19. Jiang Q, Ko WK, Lerner EA et al (2008b) Grass carp somatolactin: I. Evidence for PACAP induction of somatolactin-alpha and -beta gene expression via activation of pituitary PAC-I receptors. Am J Physiol Endocrinol Metab 295(2):E463–E476CrossRefPubMedGoogle Scholar
  20. Jones I, Kille P, Sweeney G (2001) Cadmium delays growth hormone expression during rainbow trout development. J Fish Bio 59(4):1015–1022CrossRefGoogle Scholar
  21. Kaneko T, Hirano T (1993) Role of prolactin and somatolactin in calcium regulation in fish. J Exp Biol 184:31–45Google Scholar
  22. Kroupova H, Trubiroha A, Wuertz S, Frank SN, Sures B, Kloas W (2012) Nutritional status and gene expression along the somatotropic axis in roach (Rutilus rutilus) infected with the tapeworm Ligula intestinalis. Gen Comp Endocrinol 177(2):270–277CrossRefPubMedGoogle Scholar
  23. Li P, Li ZH (2015) Physiological responses in Chinese rare minnow larvae following exposure to low-dose tributyltin. Bull Environ Contam Toxicol 95(5):588–592CrossRefPubMedGoogle Scholar
  24. Li ZH, Chen L, Wu YH, Li P, Li YF, Ni ZH (2014) Effects of waterborne cadmium on thyroid hormone levels and related gene expression in Chinese rare minnow larvae. Comp Biochem Physiol C Toxicol Pharmacol 161:53–57CrossRefPubMedGoogle Scholar
  25. Liu XH, Xie BW, Wang ZJ, Jin L, Zhang YG (2016) The secretion, synthesis, and metabolism of cortisol and its downstream genes in the H-P-I axis of rare minnows (Gobiocypris rarus) are disrupted by acute waterborne cadmium exposure. Comp Biochem Physiol C Toxicol Pharmacol 185-186:112–121CrossRefPubMedGoogle Scholar
  26. Liu XH, Wang ZJ, Jin L, Huang J, Pu DY, Wang DS, Zhang YG (2017) Effects of subchronic exposure to waterborne cadmium on H-P-I axis hormones and related genes in rare minnows (Gobiocypris rarus). Comp Biochem Phsiol C Toxicol Pharmacol 202:1–11CrossRefGoogle Scholar
  27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25(4):402–408CrossRefPubMedGoogle Scholar
  28. Lopez M, Nica G, Motte P, Martial JA, Hammerschmidt M, Muller M (2006) Expression of the somatolactin beta gene during zebrafish embryonic development. Gene Expr Patterns 6(2):156–161CrossRefPubMedGoogle Scholar
  29. Lynn SG, Shepherd BS (2007) Molecular characterization and sex-specific tissue expression of prolactin, somatolactin and insulin-like growth factor-I in yellow perch (Perca flavescens). Comp Biochem Physiol B Biochem Mol Biol 147(3):412–427CrossRefPubMedGoogle Scholar
  30. Malekpouri P, Moshaghie AA, Kazemian M et al (2011) Protective effect of zinc on related parameters to bone metabolism in common carp fish (Cyprinus carpio L.) intoxified with cadmium. Fish Physiol Biochem 37(1):187–196CrossRefPubMedGoogle Scholar
  31. Marins LF, Levy JA, Folch JM et al (2003) A growth hormone-based phylogenetic analysis of euteleostean fishes including a representative species of the Atheriniformes order, Odontesthes argentinensis. Genet Mol 26(3):295–300Google Scholar
  32. May D, Todd CM, Rand-Weaver M (1997) cDNA cloning of eel (Anguilla anguilla) somatolactin. Gene 188(1):63–67CrossRefPubMedGoogle Scholar
  33. McKay SJ, Trautner J, Smith MJ et al (2004) Evolution of duplicated growth hormone genes in autotetraploid salmonid fishes. Genome 47(4):714–723CrossRefPubMedGoogle Scholar
  34. Nguyen N, Sugimoto M, Zhu Y (2006) Production and purification of recombinant somatolactin beta and its effects on melanosome aggregation in zebrafish. Gen Comp Endocrinol 145(2):182–187CrossRefPubMedGoogle Scholar
  35. Okocha RC, Adedeji OB (2011) Overview of cadmium toxicity in fish. J Appl Sci Res 7:1195–1207Google Scholar
  36. Olsson PE (1998) Disorders associated with heavy metal pollution. In: Leatherland JE, Woo PTK (eds) Fish diseases and disorders volume 2 (non-infectious disorders). CABI International, UK, pp 105–131Google Scholar
  37. Ono M, Takayama Y, Rand-Weaver M, Sakata S, Yasunaga T, Noso T, Kawauchi H (1990) cDNA cloning of somatolactin, a pituitary protein related to growth hormone and prolactin. Proc Natl Acad Sci U S A 87(11):4330–4334CrossRefPubMedPubMedCentralGoogle Scholar
  38. Peng JP, Lian AJ, Jiang Q (2016) Production and purification of recombinant somatolactin and its effects on insulin-like growth factors gene expression in tilapia hepatocytes. Fish Aquac J 7:166CrossRefGoogle Scholar
  39. Qin F, Wang L, Liu S, Wang Z (2013) Characterization of reference genes in rare minnow, Gobiocypris rarus (Actinopterygii: Cypriniformes: Cyprinidae), in early postembryonic development and in response to EDCs treatment. Acta Ichthyol Piscat 43(2):127–138CrossRefGoogle Scholar
  40. Rand-Weaver M, Noso T, Muramoto K, Kawauchi H (1991) Isolation and characterization of somatolactin, a new protein related to growth hormone and prolactin from Atlantic cod (Gadus morhua) pituitary glands. Biochemistry 30(6):1509–1515CrossRefPubMedGoogle Scholar
  41. Rhee JS, Kim BM, SOO Seo J et al (2012) Cloning of growth hormone, somatolactin, and their receptor mRNAs, their expression in organs, during development, and on salinity stress in the hermaphroditic fish, Kryptolebias marmoratus. Comp Biochem Physiol A Mol Integr Physiol 161(4):436–442CrossRefPubMedGoogle Scholar
  42. Rogalska J, Pilat-Marcinkiewica B, Brzoska MM (2011) Protective effect of zinc against cadmium hepatotoxicity depends on this bioelement intake and level of cadmium exposure: a study in a rat model. Chem Biol Interact 193(3):191–203CrossRefPubMedGoogle Scholar
  43. Sasano Y, Yoshimura A, Fukamachi S (2012) Reassessment of the function of somatolactin alpha in lipid metabolism using medaka mutant and transgenic strains. BMC Genet 13:64CrossRefPubMedPubMedCentralGoogle Scholar
  44. Sinha YN (1995) Structural variants of prolactin: occurrence and physiological significance. Endocr Rev 16(3):354–369CrossRefPubMedGoogle Scholar
  45. Takayama Y, Rand-Weaver M, Kawauchi H, Ono M (1991) Gene structure of chum salmon somatolactin, a presumed pituitary hormone of the growth hormone/prolactin family. Mol Endocrinol 5(6):778–786CrossRefPubMedGoogle Scholar
  46. Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30(12):2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  47. Uchida K, Moriyama S, Breves JP, Fox BK, Pierce AL, Borski RJ, Hirano T, Gordon Grau E (2009) cDNA cloning and isolation of somatolactin in Mozambique tilapia and effects of seawater acclimation, confinement stress and fasting on its pituitary expression. Gen Comp Endocrinol 161(2):162–170CrossRefPubMedGoogle Scholar
  48. Valenzuela G, Perez A, Navarro M et al (2012) Somatolactin expression is modulated by estrogen in pituitary of Cyprinus carpio. Avances en endocrinologia comparada VIGoogle Scholar
  49. Valenzuela GE, Perez A, Navarro M, Romero A, Figueroa J, Kausel G (2015) Differential response of two somatolactin genes to zinc or estrogen in pituitary of Cyprinus carpio. Gen Comp Endocrinol 215:98–105CrossRefPubMedGoogle Scholar
  50. Wang B, Du YL (2013) Cadmium and its neurotoxic effects. Oxid Med Cell Long, 1–12Google Scholar
  51. Wang H, Liang Y, Li S, Chang J (2013) Acute toxicity, respiratory reaction, and sensitivity of three cyprinid fish species caused by exposure to four heavy metals. PLoS One 8(6):e65282CrossRefPubMedPubMedCentralGoogle Scholar
  52. Waye A, Trudeau VL (2011) Neuroendocrine disruption: more than hormones are upset. J Toxicol Environ Health B Crit Rev 14(5–7):270–291CrossRefPubMedPubMedCentralGoogle Scholar
  53. Wunderink YS, de Vrieze E, Metz JR, Halm S, Martínez-Rodríguez G, Flik G, Klaren PHM, Mancera JM (2012) Subfunctionalization of POMC paralogues in Senegalese sole (Solea senegalensis). Gen Comp Endocrinol 175(3):407–415CrossRefPubMedGoogle Scholar
  54. Yang BY, Chen TT (2003) Identification of a new growth hormone family protein, somatolactin-like protein, in the rainbow trout (Oncorhyncus mykiss) pituitary gland. Endocrinology 144(3):850–857CrossRefPubMedGoogle Scholar
  55. Yang BY, Arab M, Chen TT (1997) Cloning and characterization of rainbow trout (Oncorhynchus mykiss) somatolactin cDNA and its expression in pituitary and nonpituitary tissues. Gen Comp Endocrinol 106(2):271–280CrossRefPubMedGoogle Scholar
  56. Yang O, Kim HL, Weon JI, Seo YR (2015) Endocrine-disrupting chemicals: review of toxicological mechanisms ssing molecular pathway analysis. J Cancer Prev 20(1):12–24CrossRefPubMedPubMedCentralGoogle Scholar
  57. Yuan C, Zhang YY, Hu GJ, Li M, Zheng Y, Gao J, Yang Y, Zhou Y, Wang Z (2013) Expression of two zona pellucida genes is regulated by 17α-ethinylestradiol in adult rare minnow Gobiocypris rarus. Comp Biochem Physiol C Toxicol Pharmacol 158(1):1–9CrossRefPubMedGoogle Scholar
  58. Zhu Y, Yoshiura Y, Kikuchi K, Aida K, Thomas P (1999) Cloning and phylogenetic relationship of red drum somatolactin cDNA and effects of light on pituitary somatolactin mRNA expression. Gen Comp Endocrinol 113(1):69–79CrossRefPubMedGoogle Scholar
  59. Zhu Y, Stiller JW, Shaner MP, Baldini A, Scemama JL, Capehart AA (2004) Cloning of somatolactin alpha and beta cDNAs in zebrafish and phylogenetic analysis of two distinct somatolactin subtypes in fish. J Endocrinol 182(3):509–518CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Xiao-Hong Liu
    • 1
  • Bi-Wen Xie
    • 2
  • Zhi-Jian Wang
    • 1
  • Yao-Guang Zhang
    • 1
  1. 1.Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), Key Laboratory of Aquatic Science of ChongqingSouthwest University School of Life SciencesChongqingChina
  2. 2.Conservation and Utilization of Fishes Resources in the Upper Reaches of the Yangtze River Key Laboratory of Sichuan ProvinceNeijiang Normal University, School of Life ScienceNeijiangChina

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