Steroidogenic acute regulatory protein in white sturgeon (Acipenser transmontanus): cDNA cloning, sites of expression and transcript abundance in corticosteroidogenic tissue after an acute stressor

General and Comparative Endocrinology

Volumn 162, Issue 2, 2009, Pages 233-240

  Kusakabe, Makoto ^a   Zuccarelli, Micah D ^b   Nakamura, Ikumi ^a   Young, Graham ^a,c  

^a UNIVERSITY OF WASHINGTON   (United States)

^b UNIVERSITY OF IDAHO   (United States)

^c WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Actinopterygii; Acute stress; StAR; White sturgeon; Yellow corpuscles

Indexed keywords

COMPLEMENTARY DNA; CORTICOSTEROID; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

ACIPENSER TRANSMONTANUS; ACUTE STRESS; AMINO ACID SEQUENCE; ANIMAL TISSUE; ARTICLE; BRAIN; CONTROLLED STUDY; FISH; GONAD; IN SITU HYBRIDIZATION; KIDNEY; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SPLEEN; STEROIDOGENESIS;

EID: 67349205124     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2009.02.007     Document Type: Article

References (54)

1. Aluru N., Renaud R., Leatherland J.F., and Vijayan M.M. Ah Receptor-mediated impairment of interrenal steroidogenesis involves StAR protein and P450scc gene attenuation in rainbow trout. Toxicol. Sci. 84 (2005) 260-269
2. Arakane F., King S.R., Du Y., Kallen C.B., Walsh L.P., Watari H., Stocco D.M., and Strauss III J.F. Phosphorylation of steroidogenic acute regulatory protein (StAR) modulates its steroidogenic activity. J. Biol. Chem. 272 (1997) 32656-32662
3. Arakane F., Sugawara T., Nishino H., Liu Z., Holt J.A., Pain D., Stocco D.M., Miller W.L., and Strauss III J.F. Steroidogenic acute regulatory protein (StAR) retains activity in the absence of its mitochondrial import sequence: Implications for the mechanism of StAR action. Proc. Natl. Acad. Sci. USA 93 (1996) 13731-13736
4. Ariyoshi N., Kim Y.C., Artemenko I., Bhattacharyya K.K., and Jefcoate C.R. Characterization of the 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. J. Biol. Chem. 273 (1998) 7610-7619
5. Arukwe A. Modulation of brain steroidogenesis by affecting transcriptional changes of steroidogenic acute regulatory (StAR) protein and cholesterol side chain cleavage (P450scc) in juvenile Atlantic salmon (Salmo salar) is a novel aspect of nonylphenol toxicity. Environ. Sci. Technol. 39 (2005) 9791-9798
6. Baker B.Y., Yaworsky D.C., and Miller W.L. A pH-dependent molten globule transition is required for activity of the steroidogenic acute regulatory protein, StAR. J. Biol. Chem. 280 (2005) 41753-41760
7. Barton B.A., Bollig H., Hauskins B.L., and Jansen C.R. Juvenile pallid (Scaphirhynchus albus) and hybrid pallid x shovelnose (Salbus x platorynchus) sturgeons exhibit low physiological responses to acute handling and severe confinement. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 126 (2000) 125-134
8. Bauer M.P., Bridgham J.T., Langenau D.M., Johnson A.L., and Goetz F.W. Conservation of steroidogenic acute regulatory (StAR) protein structure and expression in vertebrates. Mol. Cell. Endocrinol. 168 (2000) 119-125
9. Bayunova L., Barannikova I., and Semenkova T. Sturgeon stress reactions in aquaculture. J. Appl. Ichthyol. 18 (2002) 397-404
10. Bose H.S., Lingappa V.R., and Miller W.L. The steroidogenic acute regulatory protein, StAR, works only at the outer mitochondrial membrane. Endocr. Res. 28 (2002) 295-308
11. Bose H.S., Sato S., Aisenberg J., Shalev S.A., Matsuo N., and Miller W.L. Mutations in the steroidogenic acute regulatory protein (StAR) in six patients with congenital lipoid adrenal hyperplasia. J. Clin. Endocrinol. Metab. 85 (2000) 3636-3639
12. Caron K.M., Soo S.C., Wetsel W.C., Stocco D.M., Clark B.J., and Parker K.L. Targeted disruption of the mouse gene encoding steroidogenic acute regulatory protein provides insights into congenital lipoid adrenal hyperplasia. Proc. Natl. Acad. Sci. USA 94 (1997) 11540-11545
13. Castillo J., Castellana B., Acerete L., Planas J.V., Goetz F.W., Mackenzie S., and Tort L. Stress-induced regulation of steroidogenic acute regulatory protein expression in head kidney of Gilthead seabream (Sparus aurata). J. Endocrinol. 196 (2008) 313-322
14. Chen X., Baker B.Y., Abduljabbar M.A., and Miller W.L. A genetic isolate of congenital lipoid adrenal hyperplasia with atypical clinical findings. J. Clin. Endocrinol. Metab. 90 (2005) 835-840
15. Doroshov S.I., Moberg G.P., and Van Eenennaam J.P. Observation on the reproductive cycle of cultured white sturgeon, Acipenser transmontanus. Environ. Biol. Fish. 48 (1997) 265-278
16. Farkash Y., Timberg R., and Orly J. Preparation of antiserum to rat cytochrome P-450 cholesterol side chain cleavage, and its use for ultrastructural localization of the immunoreactive enzyme by protein A-gold technique. Endocrinology 118 (1986) 1353-1365
17. Fleury A., Ducharme L., and LeHoux J.G. In vivo effects of adrenocorticotrophin on the expression of the hamster steroidogenic acute regulatory protein. J. Mol. Endocrinol. 21 (1998) 131-139
18. Flück C.E., Maret A., Mallet D., Portrat-Doyen S., Achermann J.C., Leheup B., Theintz G.E., Mullis P.E., and Morel Y. A novel mutation L260P of the steroidogenic acute regulatory protein gene in three unrelated patients of Swiss ancestry with congenital lipoid adrenal hyperplasia. J. Clin. Endocrinol. Metab. 90 (2005) 5304-5308
19. Furukawa A., Miyatake A., Ohnishi T., and Ichikawa Y. Steroidogenic acute regulatory protein (StAR) transcripts constitutively expressed in the adult rat central nervous system: Colocalization of StAR, cytochrome P-450scc (CYP XIA1), and 3β-hydroxysteroid dehydrogenase in the rat brain. J. Neurochem. 71 (1998) 2231-2238
20. Geslin M., and Auperin B. 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). Gen. Comp. Endocrinol. 135 (2004) 70-80
21. Goetz F.W., Norberg B., McCauley L.A., and Iliev D.B. Characterization of the cod (Gadus morhua) steroidogenic acute regulatory protein (StAR) sheds light on StAR gene structure in fish. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 137 (2004) 351-362
22. Hagen I.J., Kusakabe M., and Young G. Effects of ACTH and cAMP on steroidogenic acute regulatory protein and P450 11β-hydroxylase messenger RNAs in rainbow trout interrenal cells: relationship with in vitro cortisol production. Gen. Comp. Endocrinol. 145 (2006) 254-262
23. Idler D.R., and O'Halloran M.J. Steroids of a chondrostean: identification of interrenal tissue in the American Atlantic sturgeon, Acipenser oxyrhynchus Mitchill, by histological and histochemical methods. J. Endocrinol. 48 (1970) 621-626
24. Idler D.R., and Sangalang G.B. Steroids of a chondrostean: in-vitro steroidogenesis in yellow bodies isolated from kidneys and along the posterior cardinal veins of the American Atlantic sturgeon, Acipenser oxyrhynchus Mitchill. J. Endocrinol. 48 (1970) 627-637
25. Inoue J.G., Miya M., Tsukamoto K., and Nishida M. Basal actinopterygian relationship: a mitogenomic perspective on the phylogeny of the "ancient fish". Mol. Phylogenet. Evol. 26 (2003) 110-120
26. Ivell R., Tillmann G., Wang H., Nicol M., Stewart P.M., Bartlick B., Walther N., Mason J.I., and Morley S.D. Acute regulation of the bovine gene for the steroidogenic acute regulatory protein in ovarian theca and adrenocortical cells. J. Mol. Endocrinol. 24 (2000) 109-118
27. Kusakabe M., Todo T., McQuillan H.J., Goetz F.W., and Young G. Characterization and expression of steroidogenic acute regulatory protein and MLN64 cDNAs in trout. Endocrinology 143 (2002) 2062-2070
28. Kusakabe M., Kobayashi T., Todo T., Lokman P.M., Nagahama Y., and Young G. Molecular cloning and expression during spermatogenesis of a cDNA encoding testicular 11β-hydroxylase (P45011β) in rainbow trout (Oncorhynchus mykiss). Mol. Reprod. Dev. 62 (2002) 456-469
29. Lecointre G., and Le Guyader H. The Tree of Life (2006), The Belknap Press of Harvard University Press, Massachusetts, London, England pp. 325-527
30. Lehoux J.G., Fleury A., and Ducharme L. The acute and chronic effects of adrenocorticotropin on the levels of messenger ribonucleic acid and protein of steroidogenic enzymes in rat adrenal in vivo. Endocrinology 139 (1998) 3913-3922
31. Li Y.Y., Inoue K., and Takei Y. Steroidogenic acute regulatory protein in eels: cDNA cloning and effects of ACTH and seawater transfer on its mRNA expression. Zool. Sci. 20 (2003) 211-219
32. Lin D., Sugawara T., Strauss III J.F., Clark B.J., Stocco D.M., Saenger P., Rogol A., and Miller W.L. Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. J. Endocrinol. 267 (1995) 1828-1831
33. Liu J., Heikkilä P., Kahri A.I., and Voutilainen R. Expression of the steroidogenic acute regulatory protein mRNA in adrenal tumors and cultured adrenal cells. J. Endocrinol. 150 (1996) 43-50
34. Melcangi R.C., Garcia-Segura L.M., and Mensah-Nyagan A.G. Neuroactive steroids: state of the art and new perspectives. Cell. Mol. Life Sci. 65 (2008) 777-797
35. Modi D., Shah C., Sachdeva G., Gadkar S., Bhartiya D., and Puri C. Ontogeny and cellular localization of SRY transcripts in the human testes and its detection in spermatozoa. Reproduction 130 (2005) 603-613
36. Nunez B.S., Piermarini P.M., Evans A.N., and Applebaum S.L. Cloning and characterization of cDNAs encoding steroidogenic acute regulatory protein from freshwater stingrays (Potamotrygon spp.). J. Mol. Endocrinol. 35 (2005) 557-569
37. Nunez B.S., and Evans A.N. Hormonal regulation of the steroidogenic acute regulatory protein (StAR) in gonadal tissues of the Atlantic croaker (Micropogonias undulatus). Gen. Comp. Endocrinol. 150 (2007) 495-504
38. Pollack S.E., Furth E.E., Kallen C.B., Arakane F., Kiriakidou M., Kozarsky K.F., and Strauss J.F.3rd. Localization of the steroidogenic acute regulatory protein in human tissues. J. Clin. Endocrinol. Metab. 82 (1997) 4243-4251
39. Ronquist F., and Huelsenbeck J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19 (2003) 1572-1574
40. Le Roy C., Li J.Y., Stocco D.M., Langlois D., and Saez J.M. Regulation by adrenocorticotropin (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, cytochrome P450c17, and 3β-hydroxysteroid dehydrogenase. Endocrinology 141 (2000) 1599-1607
41. Sandhoff T.W., Hales D.B., Hales K.H., and McLean M.P. Transcriptional regulation of the rat steroidogenic acute regulatory protein gene by steroidogenic factor 1. Endocrinology 139 (1998) 4820-4831
42. Semenkova T.B., Bayunova L.V., Boev A.A., and Dyubin V.P. Effects of stress on serum cortisol levels of sturgeon in aquaculture. J. Appl. Ichthyol. 15 (1999) 270-272
43. Stocco D.M. Clinical disorders associated with abnormal cholesterol transport: mutations in the steroidogenic acute regulatory protein. Mol. Cell. Endocrinol. 191 (2002) 19-25
44. Sugawara T., Holt J.A., Driscoll D., Strauss III J.F., Lin D., Miller W.L., Patterson D., Clancy K.P., Hart I.M., Clark B.J., and Stocco D.M. 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. Proc. Natl. Acad. Sci. USA 92 (1995) 4778-4782
45. Sumpter J.P., Dye H.M., and Benfey T.J. The effects of stress on plasma ACTH, alpha-MSH, and cortisol levels in salmonid fishes. Gen. Comp. Endocrinol. 62 (1986) 377-385
46. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
47. Tomasetto C., Regnier C., Moog-Lutz C., Mattei M.G., Chenard M.P., Lidereau R., Basset P., and Rio M.C. Identification of four novel human genes amplified and overexpressed in breast carcinoma and localized to the q11-q21.3 region of chromosome 17. Genomics 28 (1995) 367-376
48. Tsujishita Y., and Hurley J.H. Structure and lipid transport mechanism of a StAR-related domain. Nat. Struct. Biol. 7 (2000) 408-414
49. Villeneuve D.L., Blake L.S., Brodin J.D., Greene K.J., Knoebl I., Miracle A.L., Martinovic D., and Ankley G.T. Transcription of key genes regulating gonadal steroidogenesis in control and ketoconazole- or vinclozolin-exposed fathead minnows. Toxicol. Sci. 98 (2007) 395-407
50. Weherenberg U., Prange-Kiel J., and Rune G.M. Steroidogenic factor-1 expression in marmoset and rat brain hippocampus: co-localization with StAR and aromatase. J. Neurochem. 76 (2001) 1879-1886
51. Wendelaar Bonga S.E. The stress response in fish. Physiol. Rev. 77 (1997) 591-625
52. Yaworsky D.C., Baker B.Y., Bose H.S., Best K.B., Jensen L.B., Bell J.D., Baldwin M.A., and Miller W.L. pH-dependent Interactions of the carboxyl-terminal helix of steroidogenic acute regulatory protein with synthetic membranes. J. Biol. Chem. 280 (2005) 2045-2054
53. Youson J.H., and Butler D.G. The andrenocortical homolog in the lake sturgeon, Acipenser fulvescens rafinesque. Am. J. Anat. 145 (1976) 207-223
54. Zuccarelli M.D., Kusakabe M., Nakamura I., Prentice E.F., Young G., and Ingermann R.L. Acute stress response of endangered Kootenai River white sturgeon, Acipenser transmontanus, reflected in peritoneal fluid and blood plasma. J. Fish Biol. 72 (2008) 1831-1840