Stress-induced regulation of steroidogenic acute regulatory protein expression in head kidney of Gilthead seabream (Sparus aurata)

Journal of Endocrinology

Volumn 196, Issue 2, 2008, Pages 313-322

  Castillo, Juan ^a   Castellana, Barbara ^b   Acerete, Laura ^a   Planas, Josep V ^b   Goetz, Frederick W ^c   Mackenzie, Simon ^a   Tort, Lluis ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; CORTICOTROPIN; HYDROCORTISONE; LIPOPOLYSACCHARIDE; MESSENGER RNA; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

ACUTE STRESS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHRONIC STRESS; CONTROLLED STUDY; DNA SEQUENCE; GENETIC TRANSCRIPTION; HYDROCORTISONE BLOOD LEVEL; IN VITRO STUDY; KIDNEY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEA BREAM; SEQUENCE ANALYSIS; SPARUS AURATA; STRESS;

ACUTE DISEASE; AMINO ACID SEQUENCE; ANIMALS; CELLS, CULTURED; CLONING, MOLECULAR; GENE EXPRESSION; GONADS; HYDROCORTISONE; KIDNEY; LIPOPOLYSACCHARIDES; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEINS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEA BREAM; STRESS; TIME FACTORS; TISSUE DISTRIBUTION;

EID: 39749178924     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1677/JOE-07-0440     Document Type: Article

References (65)

1. Acerete L, Balasch JC, Castellana B, Redruello B, Roher N, Canario AV, Planas JV, MacKenzie S & Tort L 2007 Cloning of the glucocorticoid receptor (GR) in gilthead seabream (Sparus aurata). Differential expression of GR and immune genes in gilthead seabream after an immune challenge. Comparative Biochemistry and Physiology. Part B, Biochemistry and Molecular Biology 148 32-43.
2. Aluru N, Renaud R, Leatherland JF & Vijayan MM 2005 Ah receptor-mediated impairment of interrenal steroidogenesis involves StAR protein and P450scc gene attenuation in rainbow trout. Toxicological Sciences 84 260-269.
3. Arakane F, Sugawara T, Nishino, H, Liu Z, Holt JA, Pain D, Stocco DM, Miller WL & Strauss JF 1996 Steroidogenic acute regulatory protein (StAR) retains activity in the absence of its mitochondrial import sequence: implications for the mechanism of StAR action. PNAS 93 13731-13736.
4. Arakane F, King SR, Du Y, Kallen CB, Walsh LP, Watari H, Stocco DM & Strauss JF 1997 Phosphorylation of steroidogenic acute regulatory protein (StAR) modulates its steroidogenic activity. Journal of Biological Chemistry 272 32656-32662.
5. Ariyoshi N, Kim YC, Artemenko I, Bhattacharyya KK & Jefcoate CR 1998 Characterization ofthe rat Star gene that encodes the predominant 3.5-kilobase pair mRNA. ACTH stimulation of adrenal steroids in vivo precedes elevation of Star mRNA and protein. Journal of Biological Chemistry 273 7610-7619.
6. Artemenko IP, Zhao D, Hales DB, Hales KH & Jefcoate CR 2001 Mitochondrial processing of newly synthesized steroidogenic acute regulatory protein (StAR), but not total StAR, mediates cholesterol transfer to cytochrome P450 side chain cleavage enzyme in adrenal cells. Journal of Biological Chemistry 276 46583-46596.
7. Balm PHM 1997 Immune-endocrine interactions. In Fish Stress and Health in Aquaculture, pp 195-221. Eds GK Iwama, AD Pickering, JP Sumpter, CB Schreck & NM Ruane. Cambridge, UK: Cambridge University Press.
8. Balm PHM, van Lieshout E, Lokate J & Wendelaar-Bonga SE 1995 Bacterial lipopolysaccharide (LPS) and interleukin 1 (IL-1) exert multiple physiological effects in the tilapia Oreochromis mossambicus (Teleostei). Journal of Comparative Physiology. B 165 85-92.
9. Bandeen A & Leatherland JF 1997 Transportation and handling stress of white suckers raised in cages. Aquaculture International 5 385-396.
10. Bauer MP, Bridgham JT, Langenau DM, Johnson AL & Goetz FW 2000 Conservation of steroidogenic acute regulatory (StAR) protein structure and expression in vertebrates. Molecular and Cellular Endocrinology 168 119-125.
11. Carsia RV & John-Alder H 2003 Seasonal alterations in adrenocortical cell function associated with stress-responsiveness and sex in the eastern fence lizard (Sceloporus undulatus). Hormones and Behavior 43 408-420.
12. Carsia RV, Scanes CG & Malamed S 1984 Self-suppression of corticosteroidogenesis: evidence for a role of adrenal 5 alpha-reductase. Endocrinology 115 2464-2472.
13. Clark BJ, Wells J, King SR & Stocco DM 1994 The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (StAR). Journal of Biological Chemistry 269 28314-28322.
14. Clark BJ, Soo SC, Caron KM, Ikeda Y, Parker KL & Stocco DM 1995 Hormonal and developmental regulation of the steroidogenic acute regulatory protein. Molecular Endocrinology 9 1346-1355.
15. Donaldson EM 1981 The pituitary-interrenal axis as an indicator of stress in fish. In Stress in Fish, pp 11-47. Ed. AD Pickering. New York: Academic Press Co.
16. Fleury A, Cloutier M, Ducharme L, Lefebvre A, LeHoux J & LeHoux JG 1996 Adrenocorticotropin regulates the level of the steroidogenic acute regulatory (StAR) protein mRNA in hamster adrenals. Endocrine Research 22 515-520.
17. Fleury A, Ducharme L & Lehoux JG 1998 In vivo effects of adrenocorticotrophin on the expression of the hamster steroidogenic acute regulatory protein. Journal of Molecular Endocrinology 21 131-139.
18. Ganga R, Tort L, Acerete L, Montero D & Izquierdo MS 2006 Modulation of ACTH-induced cortisol release by polyunsaturated fatty acids in interrenal cells from gilthead seabream, Sparus aurata. Journal of Endocrinology 190 39-45.
19. Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD & Bairoch A 2003 ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Research 31 3784-3788.
20. Geslin M & Auperin B 2004 Relationship between changes in mRNAs of the genes encoding steroidogenic acute regulatory protein and P450 cholesterol side chain cleavage in head kidney and plasma levels of cortisol in response to different kinds of acute stress in the rainbow trout (Oncorhynchus mykiss). General and Comparative Endocrinology 135 70-80.
21. Girard C, Brodeur JC & Hontela A 1998 Responsiveness of the interrenal tissue of yellow perch (Perca flavescens) from contaminated sites to an ACTH challenge test in vivo. Canadianjournal of Fisheries and Aquatic Sciences 55 438-450.
22. Goetz FW, Norberg B, McCauley L & Iliev DB 2004 Characterization of the cod (Gadus morhua) steroidogenic acute regulatory protein (StAR) sheds light on StAR gene structure in fish. Comparative Biochemistry and Physiology, Part B 137 351-362.
23. Grinevich V, Ma XM, Herman JP, Jezova D, Akmayev I & Aguilera G 2001 Effect of repeated lipopolysaccharide administration on tissue cytokine expression and hypothalamic-pituitary-adrenal axis activity in rats. Journal of Neuroendocrinology 13 711-723.
24. Hagen IJ, Kusakabe M & Young G 2006 Effects ofACTH and cAMP on steroidogenic acute regulatory protein and P450 11beta-hydroxylase messenger RNAs in rainbow trout interrenal cells: relationship with in vitro cortisol production. General and Comparative Endocrinology 145 254-262.
25. Hall TA 1999 BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41 95-98.
26. Hoglund E, Balm PH & Winberg S 2000 Skin darkening, a potential social signal in subordinate arctic charr (Salvelinus alpinus): the regulatory role of brain monoamines and pro-opiomelanocortin-derived peptides. Journal of Experimental Biology 203 1711-1721.
27. Holland JW, Pottinger TG & Secombes CJ 2002 Recombinant interleukin -1β activates the hypothalamic-pituitary-interrenal aids in rainbow trout, Oncorhynchus mykiss. Journal of Endocrinology 175 261-267.
28. Ivell R, Tillman G, Wang H, Nicol M, Stewart PM, Bardick B, Walther N, Mason JL & Morley SD 2000 Acute regulation of the bovine gene for the steroidogenic acute regulatory protein in ovarian theca and adrenocortical cells. Journal of Molecular Endocrinology 24 109-118.
29. Kallen CB, Arakane F, Christenson LK, Watari H, Devoto L & Strauss JF 1998 Unveiling the mechanism of action and regulation of the steroidogenic acute regulatory protein. Molecular and Cellular Endocrinology 145 39-45.
30. King SR, Manna PR, Ishii T, Syapin PJ, Ginsberg SD, Wilson K, Walsh LP, Parker KL, Stocco DM, Smith RG et al. 2002 An essential component in steroid synthesis, the steroidogenic acute regulatory protein, is expressed in discrete regions of the brain. Journal of Neuroscience 22 10613-10620.
31. Klingbeil CK 1985 Corticosterone and aldosterone dose-dependent responses to ACTH and angiotensin II in the duck (Anas platyrhynchos). General and Comparative Endocrinology 59 382-390.
32. Kusakabe M, Todo T, McQuillan HJ, Goetz FW & Young G 2002 Characterization and expression of steroidogenic acute regulatory protein and MLN64 cDNAs in trout. Endocrinology 143 2062-2070.
33. Lehoux JG, Fleury A & Ducharne L 1998 The acute and chronic stress effects of adrenocorticotropin on the levels of messenger ribonucleic acid and protein of steroidogenic enzymes in rat adrenal in vivo. Endocrinology 139 3913-3922.
34. Lehoux JG, Mathieu A, Lavigne P & Fleury A 2003 Adrenocorticotropin regulation of steroidogenic acute regulatory protein. Microscopy Research and Technique 15 288-299.
35. Li CH, Chung D, Yamashiro D & Lee CY 1978 Isolation, characterization and synthesis of a corticotrophin-inhibiting peptide from human pituitary glands. PNAS 75 4306-4309.
36. Li YY, Inoue K & Takei Y 2003 Steroidogenic acute regulatory protein in eels: cDNA cloning and effects of ACTH and seawater transfer on its mRNA expression. Zoological Science 20 211-219.
37. Liu J, Heikkila P, Kahri AI & Voutilainen R 1996 Expression of the steroidogenic acute regulatory protein mRNA in adrenal tumors and cultured adrenal cells. Journal of Endocrinology 150 43-50.
38. Mackenzie S, Planas JV & Goetz FW 2003 LPS-stimulated expression of a tumor necrosis factor-alpha mRNA in primary trout monocytes and in vitro differentiated macrophages. Developmental and Comparative Immunology 27 393-400.
39. Mackenzie S, Iliev D, Liarte C, Koskinnen H, Planas JV, Goetz FW, Molsa H, Krasnov A & Tort L 2005 Transcriptional analysis of LPS-stimulated activation of trout (Oncorhynchus mykiss) monocyte/macrophage cells in primary culture treated with cortisol. Molecular Immunology 43 1340-1348.
40. Miller WL 1988 Molecular biology of steroid hormone synthesis. Endocrine Reviews 9 295-318.
41. Miller WL & Strauss JF 1999 Molecular pathology and mechanism of action of the steroidogenic acute regulatory, StAR. Journal of Steroid Biochemistry and Molecular Biology 69 131-141.
42. Netchitailo F, Lihrmann I & Vaudry H 1984 Lack of effect of dexamethasone on corticosteroid production in the amphibian. Journal of Steroid Biochemistry 21 727-731.
43. Nichols DJ & Weisbart M 1984 Plasma cortisol concentrations in Atlantic salmon, Salmo salar: episodic variations, diurnal change, and short term response to adrenocorticotrophic hormone. General and Comparative Endocrinology 56 169-176.
44. Nishikawa T, Sasano H, Omura M & Suematsu S 1996 Regulation of expression of the steroidogenic acute regulatory (StAR) protein by ACTH in bovine adrenal fasciculata cells. Biochemical and Biophysical Research Communications 223 12-18.
45. Nunez BS & Evans AN 2007 Hormonal regulation of the steroidogemc acute regulatory protein (StAR) in gonadal tissues of the Atlantic croaker (Micropogomas undulatus). General and Comparative Endocrinology 150 495-504.
46. Nunez BS, Piermarini PM, Evans AN & Applebaum SL 2005 Cloning and characterization of cDNAs encoding steroidogenic acute regulatory protein from freshwater stingrays (Potamotrygon spp). Journal of Molecular Endocrinology 35 557-569.
47. Patino R, Redding JM & Schreck CB 1987 Interrenal secretion of corticosteroids and plasma cortisol and cortisone concentrations after acute stress and during seawater acclimation in juvenile coho salmon (Oncorhynchus kisutch). General and Comparative Endocrinology 68 431-439.
48. Pickering AD, Pottinger TG & Christie P 1982 Recovery of the brown trout, Salmo salar L., from acute handling stress: a time-course study. Journal of Fish Biology 20 229-244.
49. Pottinger TG & Carrick TR 2001 ACTH does not mediate divergent stress responsiveness in rainbow trout. Comparative Biochemistry and Physiology 129A 399-404.
50. Rotllant J, Balm PH, Perez-Sanchez J, Wendelaar-Bonga SE & Tort L 2001 Pituitary and interrenal function in gilthead seabream (Sparus aurata L., Teleostei) after handling and confinement stress. General and Comparative Endocrinology 121 333-342.
51. Le Roy C, Li JY, Stocco DM, Langlois D & Saez JM 2000 Regulation of adenocorticotropin (ACTH), angiotensin II, transforming growth factor-β and insulin-like growth factor I of bovine adrenal cell steroidogenic capacity and expression of ACTH receptor, steroidogenic acute regulatory protein, cyrochrome P450c17, and 3b-hydroxysteroid dehydrogenase. Endocrinology 141 1599-1607.
52. Sandhoff TW, Hales DB, Hales KH & McLean MP 1998 Transcriptional regulation of the rat steroidogenic acute regulatory protein gene by steroidogenic factor 1. Endocrinology 139 4820-4831.
53. Schreck CB & Bradford CS 1990 Interrenal corticosteroid production: potential regulation by the immune system in the salmonid. Progress in Clinical and Biological Research 342 480-486.
54. Sewer MB & Waterman MR 2003 ACTH modulation of transcription factors responsible for steroid hydroxylase gene expression in the adrenal cortex. Microscopy Research and Technique 61 300-307.
55. Stocco DM 1999 Steroidogenic acute regulatory (StAR) protein: what's new? BioEssays 9 768-775.
56. Stocco DM 2002 Clinical disorders associated with abnormal cholesterol transport: mutations in the steroidogenic acute regulatory protein. Molecular and Cellular Endocrinology 191 19-25.
57. Strauss JE Kallen CB, Christenson LK, Watari H, Devoto L, Arakane F, Kiriakidou M & Sugawara T 1999 The steroidogenic acute regulatory protein (StAR): a window into the complexities of intracellular cholesterol trafficking. Recent Progress in Hormone Research 54 369-394.
58. Sugawara T, Holt JA, Driscoll D, Strauss JF, Lin D, Miller WL, Patterson D, Clancy KP, Hart IM, Clark BJ et al. 1995 Human steroidogenic acute regulatory protein: functional activity in COS-1 cells, tissue-specific expression, and mapping of the structural gene to 8p11.2 and a pseudogene to chromosome 13. PNAS 92 4778-4782.
59. Sugawara T, Saito M & Fujimoto S 2000 Sp1 and SF-1 interact and cooperate in the regulation of human steroidogenic acute regulatory protein gene expression. Endocrinology 141 2895-2903.
60. Thompson JD, Higgins DG & Gibson TJ 1994 CLUSTALW: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22 4673-4680.
61. Tsujishita Y & Hurley JH 2000 Structure and lipid transport mechanism of a StAR-related domain. Nature Structural Biology 7 408-414.
62. Witari H, Arakane F, Moog-Lutz C, Kallen CB, Tomasetto C, Gerton GL, Rio MC, Baker ME & Strauss JF 1997 MLN64 contains a domain with homology to the steroidogenic acute regulatory protein (StAR) that stimulates steroidogenesis. PNAS 94 8462-8467.
63. Wendelaar Bonga SE 1997 The stress response in fish. Physiological Reviews 77 591-625.
64. Weyts FAA, Cohen N, Flik G & Verburg-van Kemenade BML 1999 Interactions between the immune system and the hypothalamo-pituitary-interrenal axis in fish. Fish and Shellfish Immunology 9 1-20.
65. Winberg S & Lepage O 1998 Elevation of brain 5-HT activity, POMC expression, and plasma cortisol in socially subordinate rainbow trout. American Journal of Physiology 274 R645-R654.