Mitochondrial metabolic regulation by GRP78

Science Advances

Volumn 3, Issue 2, 2017, Pages

  Prasad, Manoj ^a   Pawlak, Kevin J ^a   Burak, William E ^a,b   Perry, Elizabeth E ^c   Marshall, Brendan ^c   Whittal, Randy M ^d   Bose, Himangshu S ^a,b  

^a MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Memorial University   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; CHOLESTEROL; ENZYME ACTIVITY; MAMMALS; PROTEINS; STARS;

CHOLESTEROL TRANSPORT; CYTOPLASMIC PROTEINS; ENDOPLASMIC RETICULUM; INTERMEDIATE FOLDING; METABOLIC REGULATIONS; MITOCHONDRIAL PROTEIN; OUTER MITOCHONDRIAL MEMBRANES; STEROIDOGENIC ACUTE REGULATORY PROTEINS;

MITOCHONDRIA;

CHOLESTEROL; HEAT SHOCK PROTEIN; HSPA5 PROTEIN, RAT; PHOSPHOPROTEIN; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

ANIMAL; ENDOPLASMIC RETICULUM; MALE; METABOLISM; MITOCHONDRIAL MEMBRANE; MITOCHONDRION; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; CHOLESTEROL; ENDOPLASMIC RETICULUM; HEAT-SHOCK PROTEINS; MALE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PHOSPHOPROTEINS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 85026394487     PISSN: None     EISSN: 23752548     Source Type: Journal    
DOI: 10.1126/sciadv.1602038     Document Type: Article

References (37)

1. C. A. Mannella, K. Buttle, B. K. Rath, M. Marko, Electron microscopic tomography of rat-liver mitochondria and their interaction with the endoplasmic reticulum. Biofactors 8, 225–228 (1998).
2. G. Csordás, C. Renken, P. Várnai, L. Walter, D. Weaver, K. F. Buttle, T. Balla, C. A. Mannella, G. Hajnóczky, Structural and functional features and significance of the physical linkage between ER and mitochondria. J. Cell Biol. 174, 915–921 (2006).
3. B. Kornmann, E. Currie, S. R. Collins, M. Schuldiner, J. Nunnari, J. S. Weissman, P. Walter, An ER-mitochondria tethering complex revealed by a synthetic biology screen. Science 325, 477–481 (2009).
4. J. E. Vance, Phospholipid synthesis in a membrane fraction associated with mitochondria. J. Biol. Chem. 265, 7248–7256 (1990).
5. M. Lebiedzinska, G. Szabadkai, A. W. E. Jones, J. Duszynski, M. R. Wieckowski, Interactions between the endoplasmic reticulum, mitochondria, plasma membrane and other subcellular organelles. Int. J. Biochem. Cell Biol. 41, 1805–1816 (2009).
6. C. M. Dobson, Protein folding and misfolding. Nature 426, 884–890 (2003).
7. R. R. Kopito, Aggregosomes, inclusion bodies and protein aggregation. Trends Cell Biol. 10, 524–530 (2000).
8. Z. Kostova, D. H. Wolf, For whom the bell tolls: Protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection. EMBO J. 22, 2309–2317 (2003).
9. B. Bukau, A. L. Horwich, The Hsp70 and Hsp60 chaperone machines. Cell 92, 351–366 (1998).
10. F. U. Hartl, M. Hayer-Hartl, Molecular chaperones in the cytosol: From nascent chain to folded protein. Science 295, 1852–1858 (2002).
11. Y. Ma, L. M. Hendershot, The role of the unfolded protein response in tumour development: Friend or foe? Nat. Rev. Cancer 4, 966–977 (2004).
12. D. M. Stocco, B. J. Clark, Regulation of the acute production of steroids in steroidogenic cells. Endocr. Rev. 17, 221–244 (1996).
13. H. S. Bose, T. Sugawara, J. F. Strauss III, W. L. Miller; International Congenital Lipoid Adrenal Hyperplasia Consortium, The pathophysiology and genetics of congenital lipoid adrenal hyperplasia. N. Engl. J. Med. 335, 1870–1879 (1996).
14. M. Bose, R. M. Whittal, W. L. Miller, H. S. Bose, Steroidogenic activity of StAR requires contact with mitochondrial VDAC1 and phosphate carrier protein. J. Biol. Chem. 283, 8837–8845 (2008).
15. H. S. Bose, Mechanistic sequence of mitochondrial cholesterol transport by StAR proteins. J. Proteins Proteom. 2, 1–9 (2011).
16. M. Prasad, J. Kaur, K. J. Pawlak, M. Bose, R. M. Whittal, H. S. Bose, Mitochondria-associated endoplasmic reticulum membrane (MAM) regulates steroidogenic activity via steroidogenic acute regulatory protein (StAR)-voltage-dependent anion channel 2 (VDAC2) interaction. J. Biol. Chem. 290, 2604–2616 (2015).
17. W. L. Miller, H. S. Bose, Early steps in steroidogenesis: Intracellular cholesterol trafficking. J. Lipid Res. 52, 2111–2135 (2011).
18. B. J. Clark, J. Wells, S. R. King, D. M. Stocco, 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). J. Biol. Chem. 269, 28314–28322 (1994).
19. W. L. Miller, R. J. Auchus, The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr. Rev. 32, 81–151 (2011).
20. V. R. Lingappa, J. R. Lingappa, R. Prasad, K. E. Ebner, G. Blobel, Coupled cell-free synthesis, segregation, and core glycosylation of a secretory protein. Proc. Natl. Acad. Sci. U.S.A. 75, 2338–2342 (1978).
21. C. P. Ponting, L. Aravind, START: A lipid-binding domain in StAR, HD-ZIP and signalling proteins. Trends Biochem. Sci. 24, 130–132 (1999).
22. E. London, How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells. Biochim. Biophys. Acta 1746, 203–220 (2005).
23. D. Marsh, Cholesterol-induced fluid membrane domains: A compendium of lipid-raft ternary phase diagrams. Biochim. Biophys. Acta 1788, 2114–2123 (2009).
24. K. Christinsen, H. S. Bose, F. M. Harris, W. L. Miller, J. D. Bell, Binding of steroidogenic acute regulatory protein to synthetic membranes suggests an active molten globule. J. Biol. Chem. 276, 17044–17051 (2001).
25. D. C. Yaworsky, B. Y. Baker, H. S. Bose, K. B. Best, L. B. Jensen, J. D. Bell, M. A. Baldwin, W. L. Miller, pH-dependent interactions of the carboxyl-terminal helix of steroidogenic acute regulatory protein with synthetic membranes. J. Biol. Chem. 280, 2045–2054 (2005).
26. H. S. Bose, R. M. Whittal, M. A. Baldwin, W. L. Miller, 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 (1999).
27. K.-S. C. Marriott, M. Prasad, V. Thapliyal, H. S. Bose, s-1 receptor at the mitochondrial-associated endoplasmic reticulum membrane is responsible for mitochondrial metabolic regulation. J. Pharmacol. Exp. Ther. 343, 578–586 (2012).
28. H. S. Bose, V. R. Lingappa, W. L. Miller, Rapid regulation of steroidogenesis by mitochondrial protein import. Nature 417, 87–91 (2002).
29. K. J. Pawlak, M. Prasad, J. L. Thomas, R. M. Whittal, H. S. Bose, Inner mitochondrial translocase Tim50 interacts with 3b-hydroxysteroid dehydrogenase type 2 to regulate adrenal and gonadal steroidogenesis. J. Biol. Chem. 286, 39130–39140 (2011).
30. A. Luria, V. Vegelyte-Avery, B. Stith, N. M. Tsvetkova, W. F. Wolkers, J. H. Crowe, F. Tablin, R. Nuccitelli, Detergent-free domain isolated from Xenopus egg plasma membrane with properties similar to those of detergent-resistant membranes. Biochemistry 41, 13189–13197 (2002).
31. J. L. Macdonald, L. J. Pike, A simplified method for the preparation of detergent-free lipid rafts. J. Lipid Res. 46, 1061–1067 (2005).
32. M. P. Schwartz, A. Matouschek, The dimensions of the protein import channels in the outer and inner mitochondrial membrane. Proc. Natl. Acad. Sci. U.S.A. 96, 13086–13090 (1999).
33. U. Dettmer, A. J. Newman, E. S. Luth, T. Bartels, D. Selkoe, In vivo cross-linking reveals principally oligomeric forms of a-synuclein and b-synuclein in neurons and non-neuronal cells. J. Biol. Chem. 288, 6371–6385 (2013).
34. M. Bose, D. Debnath, Y. Chen, H. S. Bose, Folding, activity and import of steroidogenic acute regulatory protein into mitochondria changed by nicotine exposure. J. Mol. Endocrinol. 39, 67–79 (2007).
35. K. J. Pawlak, M. Prasad, K. A. McKenzie, J. P. Wiebe, C. G. Gairola, R. M. Whittal, H. S. Bose, Decreased cytochrome c oxidase IV expression reduces steroidogenesis. J. Pharmacol. Exp. Ther. 338, 598–604 (2011).
36. M. Prasad, J. L. Thomas, R. M. Whittal, H. S. Bose, Mitochondrial 3b-hydroxysteroid dehydrogenase enzyme activity requires a reversible pH-dependent conformational change at the intermembrane space J. Biol. Chem. 287, 9534–9546 (2012).
37. M. Rajapaksha, J. Kaur, M. Prasad, K. J. Pawlak, B. Marshall, E. W. Perry, R. M. Whittal, H. S. Bose, An outer mitochondrial translocase, Tom22, is crucial for inner mitochondrial steroidogenic regulation in adrenal and gonadal tissues. Mol. Cell. Biol. 36, 1032–1047 (2016).