Distinct organ-specific up- and down-regulation of IGF-I and IGF-II mRNA in various organs of a GH-overexpressing transgenic Nile tilapia

Transgenic Research

Volumn 19, Issue 2, 2010, Pages 231-240

  Eppler, Elisabeth ^a   Berishvili, Giorgi ^a   Mazel, Peter ^a   Caelers, Antje ^a   Hwang, Gyulin ^b   Maclean, Norman ^b   Reinecke, Manfred ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Brain; Gills; Growth hormone; Heart; IGF I; IGF II; Intestine; Kidney; Liver; Muscle; Pituitary; Spleen; Transgenic

Indexed keywords

OREOCHROMIS NILOTICUS; TILAPIA;

MESSENGER RNA; SOMATOMEDIN B; SOMATOMEDIN C;

ANIMAL; ANTIBODY SPECIFICITY; ARTICLE; CICHLID; DOWN REGULATION; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIVER; MALE; METABOLISM; SKELETAL MUSCLE; TRANSGENIC ANIMAL; UPREGULATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CICHLIDS; DOWN-REGULATION; FEMALE; INSULIN-LIKE GROWTH FACTOR I; INSULIN-LIKE GROWTH FACTOR II; LIVER; MALE; MUSCLE, SKELETAL; ORGAN SPECIFICITY; RNA, MESSENGER; UP-REGULATION;

EID: 77952300339     PISSN: 09628819     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11248-009-9314-8     Document Type: Article

References (69)

1. Agius C, Roberts RJ (2003) Melano-macrophage centres and their role in fish pathology. J Fish Dis 26: 499-509.
2. Ayson FG, de Jesus EG, Moriyama S, Hyodo S, Funkenstein B, Gertler A, Kawauchi H (2002) Differential expression of insulin-like growth factor I and II mRNAs during embryogenesis and early larval development in rabbitfish, Siganus guttatus. Gen Comp Endocrinol 126: 165-174.
3. Berishvili G, D'Cotta H, Baroiller J-F, Segner H, Reinecke M (2006a) Differential expression of IGF-I mRNA and peptide in the male and female gonad during early development of a bony fish, the tilapia Oreochromis niloticus. Gen Comp Endocrinol 146: 204-210.
4. Berishvili G, Shved N, Eppler E, Clota F, Baroiller J-F, Reinecke M (2006b) Organ-specific expression of IGF-I during early development of bony fish as revealed in the tilapia, Oreochromis niloticus, by in situ hybridisation and immunohistochemistry: indication for the particular importance of local IGF-I. Cell Tissue Res 325: 287-301.
5. Biga PR, Schelling GT, Hardy RW, Cain KD, Overturf K, Ott TL (2004) The effects of recombinant bovine somatotropin (rbST) on tissue IGF-I, IGF-I receptor, and GH mRNA levels in rainbow trout, Oncorhynchus mykiss. Gen Comp Endocrinol 135: 324-333.
6. Bowden TJ (2008) Modulation of the immune system of fish by their environment. Fish Shellfish Immunol 25: 373-383.
7. Caelers A, Schmid AC, Hrusovsky A, Reinecke M (2003) Insulin-like growth factor II mRNA is expressed in neurones of the brain of the bony fish Oreochromis mossambicus, the tilapia. Eur J Neurosci 18: 355-363.
8. Caelers A, Berishvili G, Meli ML, Eppler E, Reinecke M (2004) Establishment of a real-time RT-PCR for the determination of absolute amounts of IGF-I and IGF-II gene expression in liver and extrahepatic sites of the tilapia. Gen Comp Endocrinol 137: 196-204.
9. Caelers A, Maclean N, Hwang G, Eppler E, Reinecke M (2005) Expression of endogenous and exogenous growth hormone (GH) in a GH-transgenic tilapia (Oreochromis niloticus). Transgenic Res 14: 95-104.
10. Calduch-Giner JA, Pérez-Sánchez J (1999) Expression of growth hormone gene in the head kidney of gilthead sea bream (Sparus aurata). J Exp Zool 283: 326-330.
11. Calduch-Giner JA, Sitjà-Bobadilla A, Alvarez-Pellitero P, Pérez-Sánchez J (1997) Growth hormone is a phagocyte-activating factor in the gilthead sea bream (Sparus aurata). Cell Tissue Res 287: 535-540.
12. Cao YB, Chen XQ, Wang S, Chen XC, Wang YX, Chang JP, Du JZ (2009) Growth hormone and insulin-like growth factor of naked carp (Gymnocypris przewalskii) in Lake Qinghai: expression in different water environments. Gen Comp Endocrinol 161: 400-406.
13. Chen JY, Tsai HL, Chang CY, Wang JI, Shen SC, Wu JL (1998) Isolation and characterization of tilapia (Oreochromis mossambicus) insulin-like growth factors gene and proximal promoter region. DNA Cell Biol 17: 359-376.
14. Codina M, García de la Serrana D, Sánchez-Gurmaches J, Montserrat N, Chistyakova O, Navarro I, Gutiérrez J (2008) Metabolic and mitogenic effects of IGF-II in rainbow trout (Oncorhynchus mykiss) myocytes in culture and the role of IGF-II in the PI3 K/Akt and MAPK signalling pathways. Gen Comp Endocrinol 157: 116-124.
15. Collet C, Candy J, Richardson N, Sara V (1997) Organisation, sequence and expression of the gene encoding IGFII from barramundi (Teleosteii; Lates calcarifer). Biochem Genet 35: 211-224.
16. Devlin RH, Vesaki TY, Donaldson EM, Hew CL (1995) Transmission and phenotopic effects of an antifreeze/GH gene construct in coho salmon (Oncorhynchus kisutch). Aquaculture 137: 161-167.
17. Devlin RH, Swanson P, Clarke WC, Plisetskaya E, Dickhoff W, Moriyama S, Yesaki TY, Hew C-L (2000) Seawater adaptability and hormone levels in growth-enhanced transgenic coho salmon, Oncorhynchus kisutch. Aquaculture 191: 367-385.
18. Duan C (1998) Nutritional and developmental regulation of insulin-like growth factors in fish. J Nutr 128: 306S-314S.
19. Duguay SJ, Swanson P, Dickhoff WW (1994) Differential expression and hormonal regulation of alternatively spliced IGF-I mRNA transcripts in salmon. J Mol Endocrinol 12: 25-37.
20. Duguay SJ, Lai-Zhang J, Steiner DF, Funkenstein B, Chan SJ (1996) Developmental and tissue regulated expression of IGF-I and IGF-II mRNAs in Sparus aurata. J Mol Endocrinol 16: 123-132.
21. Eppler E, Caelers A, Shved N, Hwang G, Rahman AM, Maclean N, Zapf J, Reinecke M (2007a) Insulin-like growth factor I (IGF-I) in a growth-enhanced transgenic (GH-overexpressing) bony fish, the tilapia (Oreochromis niloticus): indication for a higher impact of autocrine/paracrine than of endocrine IGF-I. Transgenic Res 16: 479-489.
22. Eppler E, Shved N, Moret O, Reinecke M (2007b) IGF-I is distinctly located in the bony fish pituitary as revealed for Oreochromis niloticus, the Nile tilapia, using real-time RT-PCR, in situ hybridisation and immunohistochemistry. Gen Comp Endocrinol 150: 87-95.
23. Fryer JN (1979) Prolactin-binding sites in tilapia (Sarotherodon mossambicus) kidney. Gen Comp Endocrinol 39: 397-403.
24. Funkenstein B, Almuly R, Chan SJ (1997) Localization of IGF-I and IGF-I receptor mRNA in Sparus aurata larvae. Gen Comp Endocrinol 107: 291-303.
25. Gahr SA, Vallejo RL, Weber GM, Shepherd BS, Silverstein JT, Rexroad CEIII (2008) Effects of short-term growth hormone treatment on liver and muscle transcriptomes in rainbow trout (Oncorhynchus mykiss). Physiol Genomics 32: 380-392.
26. Hernández O, Guillén I, Estrada MP, Cabrera E, Pimintel R, Piña JC, Abad Z, Sánchez V, Hidalgo Y, Martínez R, Lleonart R, de la Fuente J (1997) Characterization of transgenic tilapia lines with different ectopic expression of tilapia growth hormone. Mol Mar Biol Biotech 6: 364-375.
27. Hwang GL, Azizur MA, Abdul RS, Sohm F, Farahmand H, Smith A, Brooks C, Maclean N (2003) Isolation and characterisation of tilapia beta-actin promoter and comparison of its activity with carp beta-actin promoter. Biochim Biophys Acta 1625: 11-18.
28. Jhingan E, Devlin RH, Iwama GK (2003) Disease resistance and effects of triploidy in growth hormone transgenic coho salmon. J Fish Biol 63: 806-823.
29. Kajimura S, Uchida K, Yada T, Riley LG, Byatt JC, Collier RJ, Aida K, Hirano T, Grau EG (2001) Stimulation of insulin-like growth factor-I production by recombinant bovine growth hormone in Mozambique tilapia, Oreochromis mossambicus. Fish Physiol Biochem 25: 221-230.
30. Kajita Y, Sakai M, Kobayashi M, Kawauchi H (1992) Enhancement of non-specific cytotoxic activity of leucocytes in rainbow trout Oncorhynchus mykiss injected with growth hormone. Fish Shellfish Immunol 2: 155-157.
31. Le Gac F, Ollitrault M, Loir M, Le Bail PY (1992) Evidence for binding and action of growth hormone in trout testis. Biol Reprod 46: 949-957.
32. Leung LY, Kwong AK, Man AK, Woo NY (2008) Direct actions of cortisol, thyroxine and growth hormone on IGF-I mRNA expression in sea bream hepatocytes. Comp Biochem Physiol A 151: 705-710. doi: 10. 1016/j. cbpa. 2008. 08. 023.
33. Loffing-Cueni D, Schmid AC, Reinecke M (1999) Molecular cloning and tissue expression of insulin-like growth factor II prohormone in the bony fish Cottus scorpius. Gen Comp Endocrinol 113: 32-37.
34. Maclean N, Rahman MA, Sohm F, Hwang G, Iyengar A, Ayad H, Smith A, Farahmand H (2002) Transgenic tilapia and the tilapia genome. Gene 295: 265-277.
35. Mori T, Devlin RH (1999) Transgenic and host growth hormone expression in pituitary and nonpituitary tissues of normal and growth hormone transgenic salmon. Mol Cell Endocrinol 149: 129-139.
36. Mori T, Hiraka I, Kurata Y, Kawauchi H, Mano N, Devlin RH, Nagoya H, Araki K (2007) Changes in hepatic gene expression related to innate immunity, growth and iron metabolism in GH-transgenic amago salmon (Oncorhynchus masou) by cDNA subtraction and microarray analysis, and serum lysozyme activity. Gen Comp Endocrinol 151: 42-54.
37. Moriyama S, Ayson FG, Kawauchi H (2000) Growth regulation by insulin-like growth factor-I in fish. Rev Biosci Biotechnol Biochem 64: 1553-1562.
38. Moriyama S, Yamaguchi K, Takasawa T, Chiba H, Kawauchi H (2008) Identification of two insulin-like growth factor IIs in the Japanese eel, Anguilla japonica: cloning, tissue distribution, and expression after growth hormone treatment and seawater acclimation. Comp Biochem Physiol B 149: 47-57.
39. Patruno M, Sivieri S, Poltronieri C, Sacchetto R, Maccatrozzo L, Martinello T, Funkenstein B, Radaelli G (2008) Real-time polymerase chain reaction, in situ hybridization and immunohistochemical localization of insulin-like growth factor-I and myostatin during development of Dicentrarchus labrax (Pisces: Osteichthyes). Cell Tissue Res 331: 643-658.
40. Perrot V, Funkenstein B (1999) Cellular distribution of insulin-like growth factor II (IGF-II) mRNA and hormonal regulation of IGF-I and IGF-II mRNA expression in rainbow trout testis (Oncorhynchus mykiss). Fish Physiol Biochem 20: 219-229.
41. Perrot V, Moiseeva EB, Gozes Y, Chan SJ, Funkenstein B (2000) Insulin-like growth factor receptors and their ligands in gonads of a hermaphroditic species, the gilthead seabream (Sparus aurata): expression and cellular localization. Biol Reprod 63: 229-241.
42. Peterson BC, Small BC, Bilodeau L (2007) Effects of GH on immune and endocrine responses of channel catfish challenged with Edwardsiella ictaluri. Comp Biochem Physiol A 146: 47-53.
43. Pierce AL, Fukada H, Dickhoff WW (2005) Metabolic hormones modulate the effect of growth hormone (GH) on insulin-like growth factor-I (IGF-I) mRNA level in primary culture of salmon hepatocytes. J Endocrinol 184: 341-349.
44. Ponce M, Infante C, Funes V, Manchado M (2008) Molecular characterization and gene expression analysis of insulin-like growth factors I and II in the redbanded seabream, Pagrus auriga: transcriptional regulation by growth hormone. Comp Biochem Physiol B 150: 418-426.
45. Radaelli G, Poltronieri C, Bertotto D, Funkenstein B, Simontacchi C (2008) Cellular localization of insulin-like growth factor-II protein in the sea bass (Dicentrarchus labrax) from hatching to adult. Histol Histopathol 23: 523-530.
46. Rahman MA, Mak R, Ayad H, Smith A, Maclean N (1998) Expression of a novel piscine growth hormone gene results in growth enhancement in transgenic tilapia (Oreochromis niloticus). Transgenic Res 7: 357-369.
47. Raven PA, Uh M, Sakhrani D, Beckman BR, Cooper K, Pinter J, Leder E, Silverstein J, Devlin RH (2008) Endocrine effects of growth hormone overexpression in transgenic coho salmon. Gen Comp Endocrinol 159: 26-37.
48. Reinecke M, Collet C (1998) The phylogeny of the insulin-like growth factors. Int Rev Cytol 183: 1-94.
49. Reinecke M, Schmid A, Ermatinger R, Loffing-Cueni D (1997) Insulin-like growth factor I in the teleost Oreochromis mossambicus, the tilapia: gene sequence, tissue expression, and cellular localization. Endocrinology 138: 3613-3619.
50. Reinecke M, Bjornsson BT, Dickhoff WW, McCormick SD, Navarro I, Power DM, Gutierrez J (2005) Growth hormone and insulin-like growth factors in fish: where we are and where to go. Gen Comp Endocrinol 142: 20-24.
51. Sakai M, Kobayashi M, Kawauchi H (1996) In vitro activation of fish phagocytic cells by GH, prolactin and somatolactin. J Endocrinol 151: 113-158.
52. Sakai M, Kajita Y, Kobayashi M, Kawauchi H (1997) Immunostimulating effect of growth hormone: in-vivo administration of growth hormone in rainbow trout enhances resistance to Vibrio anguillarum infection. Vet Immunol Immunopathol 57: 147-152.
53. Schmid AC, Naef E, Kloas W, Reinecke M (1999) IGF-II and IGF-II in the ovary of a bony fish Oreochromis mossambicus, the tilapia: in situ hybridisation, immunohistochemical localisation, Northern Blot and cDNA sequences. Mol Cell Endocrinol 156: 141-149.
54. Schmid AC, Reinecke M, Kloas W (2000) Primary cultured hepatocytes of the bony fish, Oreochromis mossambicus, the tilapia: a valid tool for physiological studies on IGF-I expression in liver. J Endocrinol 166: 265-273.
55. Schmid AC, Lutz I, Kloas W, Reinecke M (2003) Thyroid hormone stimulates hepatic IGF-I mRNA expression in a bony fish, the tilapia Oreochromis mossambicus, in vitro and in vivo. Gen Comp Endocrinol 130: 129-134.
56. Segner H, Eppler E, Reinecke M (2006) The impact of environmental hormonally active substances on the endocrine and immune system of fish. Review. In: Reinecke M, Zaccone G, Kapoor BG (eds) Fish Endocrinology 2006, vol 2. Science Publishers, Enfield (NH), pp 809-865.
57. Shamblott MJ, Chen TT (1993) Age-related and tissue-specific levels of five forms of insulin-like growth factor mRNA in a teleost. Mol Mar Biol Biotechnol 2: 351-361.
58. Shamblott MJ, Cheng CM, Bolt D, Chen TT (1995) Appearance of insulin-like growth factor mRNA in the liver and pyloric caeca of a teleost in response to exogenous growth hormone. Proc Natl Acad Sci USA 92: 6943-6949.
59. Shepherd BS, Drennon K, Johnson J, Nichols JW, Playle RC, Singer TD, Vijayan MM (2005) Salinity acclimation affects the somatotropic axis in rainbow trout. Am J Physiol Integr Comp Physiol 288: R1385-R1395.
60. Shved N, Berishvili G, Baroiller J-F, Segner H, Eppler E, Reinecke M (2007) Ethinylestradiol differentially interferes with the IGF-I system in the tilapia, Oreochromis niloticus. J Endocrinol 195: 513-523.
61. Shved N, Berishvili G, Häusermann E, D'Cotta H, Baroiller J-F, Eppler E (2009) Challenge with 17α-ethinylestradiol (EE2) during early development persistently impairs growth, differentiation, and local expression of IGF-I and IGF-II in immune organs of tilapia. Fish Shellfish Immunol 26: 524-530.
62. Sitjà-Bobadilla A, Calduch-Giner J, Saera-Vila A, Palenzuela O, Álvarez-Pellitero P, Pérez-Sanchez J (2008) Chronic exposure to the parasite Enteromyxum leei (Myxozoa: Myxosporea) modulates the immune response and the expression of growth, redox and immune relevant genes in gilthead sea bream, Sparus aurata L. Fish Shellfish Immunol 24: 610-619.
63. Sundström LF, Lohmus M, Johnsson JI, Devlin RH (2004) Growth hormone transgenic salmon pay for growth potential with increased predation mortality. Proc Biol Sci 271(Suppl. 5): S350-S352.
64. Tse MCL, Vong QP, Cheng CHK, Chan KM (2002) PCR-cloning and gene expression studies in common carp (Cyprinus carpio) insulin-like growth factor-II. Biochim Biophys Acta 1575: 63-74.
65. Vong QP, Chan KM, Cheng CH (2003) Quantification of common carp (Cyprinus carpio) IGF-I and IGF-II mRNA by real-time PCR: differential regulation of expression by GH. J Endocrinol 178: 513-521.
66. Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243: 215-285.
67. Yada T, Azuma T, Takagi Y (2001) Stimulation of non-specific immune functions in seawater-acclimated rainbow trout, Oncorhynchus mykiss, with reference to the role of growth hormone. Comp Biochem Physiol B 129: 695-701.
68. Yada T, Uchida K, Kajimura S, Azuma T, Hirano T, Grau EG (2002) Immunomodulatory effects of prolactin and growth hormone in the tilapia, Oreochromis mossambicus. J Endocrinol 173: 483-492.
69. Yada T, Misumi I, Muto K, Azuma T, Schreck CB (2004) Effects of prolactin and growth hormone on proliferation and survival of cultured trout leucocytes. Gen Comp Endocrinol 136: 298-306.