Cholesterol-mediated conformational changes in the steroidogenic acute regulatory protein are essential for steroidogenesis

Biochemistry

Volumn 52, Issue 41, 2013, Pages 7242-7253

  Rajapaksha, Maheshinie ^a   Kaur, Jasmeet ^b   Bose, Mahuya ^c   Whittal, Randy M ^d   Bose, Himangshu S ^b  

^a MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MEMORIAL HEALTH UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMICAL CHAPERONE; CHOLESTEROL METABOLISM; CONFORMATIONAL CHANGE; INTERMEDIATE STATE; MITOCHONDRIAL IMPORT; PROTEIN FINGERPRINTING; STEROIDOGENIC ACUTE REGULATORY PROTEINS; TRANSFER CAPACITIES;

AMINO ACIDS; CONFORMATIONS; ENZYME ACTIVITY; MASS SPECTROMETRY; MITOCHONDRIA; PROTEINS; STARS;

CHOLESTEROL;

AMINO ACID; CHAPERONE; CHOLESTEROL; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN STRUCTURE; STEROIDOGENESIS;

BINDING SITES; CHOLESTEROL; HUMANS; KINETICS; MITOCHONDRIA; PHOSPHOPROTEINS; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 84886039339     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi401125v     Document Type: Article

References (67)

1. Anfinsen, C. B. (1973) Principles that govern the folding of protein chains Science 181, 222-225
2. Record, S. E., Dobson, C. M., and Evans, P. A. (1992) The folding of hen lysozyme involves partially structured intermediates and multiple pathways Nature 358, 302-307
3. Zimmerman, S. B. and Minton, A. P. (1993) Macromolecular crowding: Biochemical, biophysical and physiological consequences Annu. Rev. Biomol. Struct. 22, 27-75
4. Han, J. and Herzfeld, J. (1993) Macromolecular diffusion in crowded solutions Biophys. J. 65, 1155-1161
5. Minton, A. P. (2000) Implications of macromolecular crowding as protein assembly Curr. Opin. Struct. Biol. 10, 34-39
6. Minton, A. P. (2000) Effect of a concentrated "insert" macromolecule consolute on the stability of a globular protein with respect to denaturation by heat and by chaperones: A statistical thermodynamic model Biophys. J. 78, 101-109
7. Miller, W. L. and Bose, H. S. (2011) Early steps in steroidogenesis: Intracellular cholesterol trafficking J. Lipid Res. 52, 2111-2135
8. Ponting, C. P. and Aravind, L. (1999) START: A lipid-binding domain in StAR, HD-ZIP and signalling proteins Trends Biochem. Sci. 24, 130-132
9. Lin, D., Sugawara, T., Strauss, J. F., III, Clark, B. J., Stocco, D. M., Saenger, P., Rogol, A., and Miller, W. L. (1995) Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis Science 267, 1828-1831
10. Hauffa, B. P., Miller, W. L., Grumbach, M. M., Conte, F. A., and Kaplan, S. L. (1985) Congenital adrenal hyperplasia due to deficient cholesterol side-chain cleavage activity (20,22 desmolase) in a patient treated for 18 years Clin. Endocrinol. 23, 481-493
11. Bose, H. S., Sugawara, T., Strauss, J. F., III, and Miller, W. L. (1996) The pathophysiology and genetics of congenital lipoid adrenal hyperplasia N. Engl. J. Med. 335, 1870-1878
12. Bose, H. S. (2011) Folding of START-domain proteins for cholesterol transport Journal of Proteins and Proteomics 2, 1-9
13. Miller, W. L. and Auchus, R. J. (2011) The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders Endocr. Rev. 32, 81-151
14. Caron, K. M., Soo, S. C., Wetsel, W. C., Stocco, D. M., Clark, B. J., and Parker, K. L. (1997) Targeted disruption of the mouse gene encoding steroidogenic acute regulatory protein provides insights into congenital lipoid adrenal hyperplasia Proc. Natl. Acad. Sci. U.S.A. 94, 11540-11546
15. Soccio, R. E. and Breslow, J. L. (2003) StAR-related lipid transfer (START) proteins: Mediators of intracellular lipid metabolism J. Biol. Chem. 278, 22183-22186
16. Soccio, R. E., Adams, R. M., Maxwell, K. N., and Breslow, J. L. (2005) Differential gene regulation of StarD4 and StarD5 cholesterol transfer proteins. Activation of StarD4 by sterol regulatory element-binding protein-2 and StarD5 by endoplasmic reticulum stress J. Biol. Chem. 280, 19410-19418
17. Bose, H. S., Whittal, R. M., Ran, Y., Bose, M., Baker, B. Y., and Miller, W. L. (2008) StAR-like activity and molten globule behavior of StARD6, a male germ-line protein Biochemistry 47, 2277-2288
18. Clark, B. J. (2012) The mammalian START domain protein family in lipid transport in health and disease J. Endocrinol. 212, 257-275
19. Watari, H., Arakane, F., Moog-Lutz, C., Callen, C. B., Tomasetto, C., Gerton, G. L., Rio, M. C., Baker, M. E., and Strauss, J. F., III (1997) MLN64 contains a domain with homology to the steroidogenic acute regulatory protein (StAR) that stimulates steroidogenesis Proc. Natl. Acad. Sci. U.S.A. 94, 8462-8467
20. Bose, H. S., Whittal, R. M., Huang, M. C., Baldwin, M. A., and Miller, W. L. (2000) N-218 MLN64, a protein with StAR-like steroidogenic activity is folded and cleaved similarly to StAR Biochemistry 39, 11722-11731
21. Roderick, S. L., Chan, W. W., Agate, D. S., Olsen, L. R., Vetting, M. W., Rajashankar, K. R., and Cohen, D. E. (2002) Structure of human phosphatidylcholine transfer protein in complex with its ligand Nat. Struct. Biol. 9, 507-511
22. Rodriguez-Agudo, D., Ren, S., Hylemon, P. B., Redford, K., Natarajan, R., Del Castillo, A., Gil, G., and Pandak, W. M. (2005) Human StARD5, a cytosolic StAR-related binding protein J. Lipid Res. 46, 1615-1623
23. Rodriguez-Agudo, D., Ren, S., Wong, E., Marques, D., Redford, K., Gil, G., Hylemon, P. B., and Pandak, W. M. (2008) Intracellular transporter StARD4 binds cholesterol and increases cholesteryl ester formation J. Lipid Res. 49, 1409-1419
24. Horibata, Y. and Sugimoto, H. (2010) StarD7 mediates the intracellular trafficking of phosphatidylcholine to mitochondria J. Biol. Chem. 285, 7358-7365
25. Rena, V., Flores-Martín, J., Angeletti, S., Panzetta-Dutari, G. M., and Genti-Raimondi, S. (2011) StarD7 gene expression in trophoblast cells: Contribution of SF-1 and Wnt-catenin signaling Mol. Endocrinol. 25, 1364-1375
26. Arakane, F., Sugawara, T., Nishino, H., Liu, Z., Holt, J. A., Pain, D., Stocco, D. M., Miller, W. L., and Strauss, J. F., III (1996) Steroidogenic acute regulatory protein (StAR) retains activity in the absence of its mitochondrial targeting sequence: Implications for the mechanism of StAR action Proc. Natl. Acad. Sci. U.S.A. 93, 13731-13736
27. Bose, H. S., Lingappa, V. R., and Miller, W. L. (2002) Rapid regulation of steroidogenesis by mitochondrial protein import Nature 417, 87-91
28. Riegelhaupt, J. J., Waase, M. P., Garbarino, J., Cruz, D. E., and Breslow, J. L. (2010) Targeted disruption of steroidogenic acute regulatory protein D4 leads to modest weight reduction and minor alterations in lipid metabolism J. Lipid Res. 51, 1134-1143
29. Tsujishita, Y. and Hurley, J. H. (2000) Structure and lipid transport mechanism of a StAR-related domain Nat. Struct. Biol. 7, 408-414
30. Mathieu, A. P., Fleury, A., Duchame, L., Lavigme, P., and LeHoux, J. G. (2002) Insights into steroidogenic acute regulatory protein (StAR)-dependent cholesterol transfer in mitochondria: Evidence from molecular modeling and structure-based thermodynamics supporting the existence of partially unfolded states of StAR J. Mol. Endocrinol. 29, 327-345
31. Romanowski, M. J., Soccio, R. E., Breslow, J. L., and Burley, S. K. (2002) Crystal structure of the Mus musculus cholesterol-regulated START protein 4 (StarD4) containing a StAR-related lipid transfer domain Proc. Natl. Acad. Sci. U.S.A. 99, 6949-6954
32. Bose, H. S., Whittal, R. W., Bose, M., and Debnath, D. (2009) Hydrophopbic core of the steroidogenic acute regulatory protein for cholesterol transport Biochemistry 48, 1198-1209
33. Bose, H. S., Whittal, R. M., Baldwin, M. A., and Miller, W. L. (1999) The active form of the steroidogenic acute regulatory protein, StAR, appears to be a molten globule Proc. Natl. Acad. Sci. U.S.A. 96, 7250-7255
34. Christinsen, K., Bose, H. S., Harris, F. M., Miller, W. L., and Bell, J. D. (2001) Binding of StAR to synthetic membranes suggests an active molten globule J. Biol. Chem. 276, 17044-17051
35. Murcia, M., Faraldo-Gomez, J. D., Maxfield, F. R., and Roux, B. (2006) Modelling the structure of the StART domains of MLN64 and StAR proteins in complex with cholesterol J. Lipid Res. 47, 2614-2630
36. Roostaee, A., Barbar, E., Lehoux, J. G., and Lavigne, P. (2008) Cholesterol binding is a prerequisite for the activity of the steroidogenic acute regulatory protein (StAR) Biochem. J. 412, 553-562
37. Arakane, F., Kallen, C. B., Watari, H., Foster, J. A., Sepuri, N. B. V., Pain, D., Stayrook, S. E., Lewis, M., Gerton, G. L., and Strauss, J. F., III (1998) The mechanism of action of steroidogenic acute regulatory protein (StAR): StAR acts on the outside of mitochondria to stimulate steroidogenesis J. Biol. Chem. 273, 16339-16345
38. Bose, H. S., Baldwin, M. A., and Miller, W. L. (1998) Incorrect folding of steroidogenic acute regulatory protein (StAR) in congenital lipoid adrenal hyperplasia Biochemistry 37, 9768-9775
39. Gill, S. C. and von Hippel, P. H. (1989) Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182, 319-326
40. Rosenfeld, J., Capdeville, J., Guillemot, J. C., and Ferrara, P. (1992) In-gel digestion of proteins for internal sequence analysis after one- or two-dimensional electrophoresis Anal. Biochem. 203, 173-179
41. Santolini, J., Haraux, F., Sigalat, C., Moal, G., and Andre, F. (1999) Kinetic analysis of tentoxin binding chloroplast F1-ATPase J. Biol. Chem. 274, 849-858
42. Bose, M., Adams, B. P., Whittal, R. M., and Bose, H. S. (2008) Identification of unknown protein complex members by radiolocalization and analysis of low-abundance complexes resolved using native PAGE Electrophoresis 29, 753-760
43. Bose, M., Debnath, D., Chen, Y., and Bose, H. S. (2007) Folding, activity and import of steroidogenic acute regulatory protein (StAR) into mitochondria changed by nicotine exposure J. Mol. Endocrinol. 39, 67-79
44. Schwartz, M. P. and Matouschek, A. (1999) The dimensions of the protein import channels in the outer and inner mitochondrial membrane Proc. Natl. Acad. Sci. U.S.A. 96, 13086-13090
45. Rajapaksha, M., Prasad, M., Thomas, J. L., Whittal, R. M., and Bose, H. S. (2013) 3β-Hydroxysteroid dehydrogenase2 (3βHSD2) requires chaperone-assisted folding for steroidogenic activity ACS Chem. Biol. 8, 1000-1008
46. Hanson, M., Cherezov, V., Griffith, M., Roth, C., Jaakola, V.-P., Chien, E., Velasquez, J., Kuhn, P., and Stevens, R. (2008) A specific cholesterol binding site is established by the 2.8 Å structure of the human β2-adrenergic receptor Structure 16, 897-905
47. Boesze-Battaglia, K., Fliesler, S., and Albert, A. (1989) Cholesterol heterogeneity in bovine rod outer segment disk membranes J. Biol. Chem. 264, 18867-18870
48. Straume, M., Mitchell, D., Miller, J., and Litman, B. (1990) Interconversion of metarhodopsins I and II: A branched photointermediate decay model Biochemistry 29, 9135-9142
49. Bose, M., Whittal, R. M., Miller, W. L., and Bose, H. S. (2008) Steroidogenic activity of StAR requires contact with mitochondrial VDAC1 and phosphate carrier protein J. Biol. Chem. 283, 8837-8845
50. Chung, B., Matteson, K. J., Voutilainen, R., Mohandas, T. K., and Miller, W. L. (1986) Human cholesterol side-chain cleavage enzyme, P450scc: cDNA cloning, assignment of the gene to chromosome 15, and expression in the placenta Proc. Natl. Acad. Sci. U.S.A. 83, 8962-8966
51. Mukhopadhyay, A., Heard, T., Wen, X., Hammen, P., and Weiner, H. (2003) Location of the actual signal in the negatively charged leader sequence involved in the import into mitochondrial matrix space J. Biol. Chem. 278, 13712-13718
52. Fons, R. D., Bogert, B. A., and Hegde, R. S. (2003) Substrate-specific function of the translocaon-associated protein complex during translocation across the ER membrane J. Cell Biol. 160, 529-539
53. Thorsell, A. G., Lee, W. H., Persson, C., Siponen, M. I., Nilsson, M., Busam, R. D., Kotenyova, T., Schüler, H., and Lethio, L. (2011) Comparative structural analysis of lipid binding START domains PLoS One 6, e19521
54. Létourneau, D., Lorin, A., Lefebvre, A., Frappier, V., Gaudreault, F., Najmanovich, R., Lavigne, P., and LeHoux, J. G. (2012) StAR-related lipid transfer domain protein 5 binds primary bile acids J. Lipid Res. 53, 2677-2689
55. Zhang, L., Yan, F., Zhang, S., Lei, D., Charles, M. A., Cavigiolio, G., Oda, M., Krauss, R. M., Weisgraber, K. H., Rye, K. A., Pownall, H. J., Qiu, X., and Ren, G. (2012) Structural basis of transfer between lipoproteins by cholesteryl ester transfer protein Nat. Chem. Biol. 8, 342-349
56. Baker, B. Y., Yaworsky, D. C., and Miller, W. L. (2005) A pH-dependent molten globule transition is required for activity of the steroidogenic acute regulatory protein, StAR J. Biol. Chem. 280, 41753-41760
57. Baker, B. Y., Epand, R. F., Epand, R. M., and Miller, W. L. (2007) Cholesterol binding does not predict activity of the steroidogenic acute regulatory protein J. Biol. Chem. 282, 10223-10232
58. Camats, N., Pandey, A. V., Fernández-Cancio, M., Fernández, J. M., Ortega, A. M., Udhane, S., Andaluz, P., Audí, L., and Flück, C. F. (2013) STAR splicing mutations cause the severe phenotype of lipoid CAH: Insights from a novel splice mutation and review of reported cases Clin. Endocrinol. 10.1111/cen.12293
59. Tee, M. K., Lin, D., Sugawara, T., Holt, J. A., Guiguen, Y., Buckingham, B., Strauss, J. F., III, and Miller, W. L. (1995) T → A transversion 11 bp from a splice acceptor site in the gene for steroidogenic acute regulatory protein causes congenital lipoid adrenal hyperplasia Hum. Mol. Genet. 4, 2299-2305
60. Caron, K. M., Soo, S.-C., Wetsel, W. C., Stocco, D. M., Clark, B. J., and Parker, K. L. (1997) Targeted disruption of the mouse gene encoding steroidogenic acute regulatory protein provides insights into congenital lipoid adrenal hyperplasia Proc. Natl. Acad. Sci. U.S.A. 94, 11540-11545
61. Bose, H. S., Whittal, R. W., Debnath, D., and Bose, M. (2009) Steroidogenic acute regulatory protein has a more open conformation than the independently folded domains Biochemistry 48, 11630-11639
62. Prasad, M., Thomas, J. L., Whittal, R. M., and Bose, H. S. (2012) Mitochondrial 3β-hydroxysteroid dehydrogenase enzyme activity requires a reversible pH-dependent conformational change at the intermembrane space J. Biol. Chem. 287, 9534-9546
63. Jefcoate, C. (2002) High-flux mitochondrial cholesterol trafficking, a specialized function of the adrenal cortex J. Clin. Invest. 110, 881-890
64. Colombini, M. (2012) VDAC structure, selectivity, and dynamics Biochim. Biophys. Acta 1818, 1457-1465
65. Marriott, K. C., Prasad, M., Thapliyal, V., and Bose, H. S. (2012) Sigma-1 receptor at the mitochondrial associated ER-membrane is responsible for mitochondrial metabolic regulation J. Pharmacol. Exp. Ther. 343, 578-586
66. Cunningham, E. L. and Agard, D. A. (2003) Interdependent folding of the N- and C-terminal domains defines the cooperative folding of α-lytic protease Biochemistry 42, 13212-13219
67. Maity, H., Maity, M., Krishna, M. M., Mayne, L., and Englander, S. W. (2005) Protein folding: The stepwise assembly of folding units Proc. Natl. Acad. Sci. U.S.A. 102, 4741-4746