Transcriptional activation of LON Gene by a new form of mitochondrial stress: A role for the nuclear respiratory factor 2 in StAR overload response (SOR)

Molecular and Cellular Endocrinology

Volumn 408, Issue , 2015, Pages 62-72

  Bahat, Assaf ^a   Perlberg, Shira ^a   Melamed Book, Naomi ^a   Isaac, Sara ^a   Eden, Amir ^a   Lauria, Ines ^b   Langer, Thomas ^b   Orly, Joseph ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^b UNIVERSITY OF COLOGNE   (Germany)

Author keywords

LON transcription; Mitochondrial proteases; StAR degradation

Indexed keywords

ENDOPEPTIDASE LA; GA BINDING PROTEIN; PHOSPHOPROTEIN; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

ANIMAL; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGICAL STRESS; TRANSCRIPTION INITIATION;

ANIMALS; BASE SEQUENCE; GA-BINDING PROTEIN TRANSCRIPTION FACTOR; HUMANS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PHOSPHOPROTEINS; PROTEASE LA; STRESS, PHYSIOLOGICAL; TRANSCRIPTIONAL ACTIVATION;

EID: 84939938548     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2015.02.022     Document Type: Review

References (123)

1. Aldridge J.E., Horibe T., Hoogenraad N.J. Discovery of genes activated by the mitochondrial unfolded protein response (mtUPR) and cognate promoter elements. PLoS ONE 2007, 2:e874.
2. Almajan E.R., Richter R., Paeger L., Martinelli P., Barth E., Decker T., et al. AFG3L2 supports mitochondrial protein synthesis and Purkinje cell survival. J. Clin. Invest 2012, 122:4048.
3. Anand R., Langer T., Baker M. Proteolytic control of mitochondrial function and morphogenesis. Biochim. Biophys. Acta 2012, 1833(1):195-204.
4. Anuka E., Yivgi-Ohana N., Eimerl S., Garfinkel B., Melamed-Book N., Chepurkol E., et al. Infarct-induced steroidogenic acute regulatory protein: a survival role in cardiac fibroblasts. Mol. Endocrinol 2013, 27:1502-1517.
5. Arakane F., Sugawara T., Nishino H., Liu Z., Holt J.A., Pain D., et al. Steroidogenic acute regulatory protein (StAR) retains activity in the absence of its mitochondrial import sequence: implications for the mechanism of StAR action. PNAS 1996, 93:13731-13736.
6. Ariyoshi N., Kim Y.-C., Artemenko I., Bhattacharyya K.K., 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 1998, 273:7610-7619.
7. Artemenko I.P., Zhao D., Hales D.B., Hales K.H., Jefcoate C.R. 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. J. Biol. Chem 2001, 276:46583-46596.
8. Atorino L., Silvestri L., Koppen M., Cassina L., Ballabio A., Marconi R., et al. Loss of m-AAA protease in mitochondria causes complex I deficiency and increased sensitivity to oxidative stress in hereditary spastic paraplegia. J. Cell Biol 2003, 163:777-787.
9. Augustin S., Nolden M., Müller S., Hardt O., Arnold I., Langer T. Characterization of peptides released from mitochondria evidence for constant proteolysis and peptide efflux. J. Biol. Chem 2005, 280:2691-2699.
10. Bahat A., Perlberg S., Melamed-Book N., Lauria I., Langer T., Orly J. StAR enhances transcription of genes encoding the mitochondrial proteases involved in its own degradation. Mol. Endocrinol 2013, 28:208-224.
11. Baker M.J., Tatsuta T., Langer T. Quality control of mitochondrial proteostasis. Cold Spring Harb. Perspect. Biol 2011, 3:a007559.
12. Baker M.J., Lampe P.A., Stojanovski D., Korwitz A., Anand R., Tatsuta T., et al. Stress-induced OMA1 activation and autocatalytic turnover regulate OPA1-dependent mitochondrial dynamics. EMBO J. 2014, 33:578-593.
13. Banfi S., Bassi M.T., Andolfi G., Marchitiello A., Zanotta S., Ballabio A., et al. Identification and characterization of AFG3L2, a novel paraplegin-related gene. Genomics 1999, 59:51-58.
14. Blesa J.R., Prieto-Ruiz J.A., Hernández J.M., Hernández-Yago J. NRF-2 transcription factor is required for human TOMM20 gene expression. Gene 2007, 391:198-208.
15. Bose H.S., Sugawara T., Strauss J.F., Miller W.L. The pathophysiology and genetics of congenital lipoid adrenal hyperplasia. NEJM 1996, 335:1870-1879.
16. Bose H.S., Lingappa V.R., Miller W.L. Rapid regulation of steroidogenesis by mitochondrial protein import. Nature 2002, 417:87-91.
17. Bose M., Whittal R.M., Miller W.L., Bose H.S. Steroidogenic activity of StAR requires contact with mitochondrial VDAC1 and phosphate carrier protein. J. Biol. Chem 2008, 283:8837-8845.
18. Bota D.A., Davies K.J. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol 2002, 4:674-680.
19. Bota D.A., Ngo J.K., Davies K.J. Downregulation of the human Lon protease impairs mitochondrial structure and function and causes cell death. Free Radic. Biol. Med 2005, 38:665-677.
20. Bruni F., Polosa P.L., Gadaleta M.N., Cantatore P., Roberti M. Nuclear respiratory factor 2 induces the expression of many but not all human proteins acting in mitochondrial DNA transcription and replication. J. Biol. Chem 2010, 285:3939-3948.
21. Bulteau A.L., Bayot A. Mitochondrial proteases and cancer. Biochim. Biophys. Acta 2011, 1807:595-601.
22. Caron K.M., Soo S.C., Parker K.L. Targeted disruption of StAR provides novel insights into congenital adrenal hyperplasia. Endocr. Res 1998, 24:827-834.
23. Casari G., De Fusco M., Ciarmatori S., Zeviani M., Mora M., Fernandez P., et al. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell 1998, 93:973-983.
24. Cherradi N., Capponi A.M. The acute regulation of mineralocorticoid biosynthesis: scenarios for the StAR system. Trends Endocrinol. Metab 1998, 9:412-418.
25. Christenson L.K., Strauss J.F. Steroidogenic acute regulatory protein: an update on its regulation and mechanism of action. Arch. Med. Res 2001, 32:576-586.
26. Clark B.J., Wells J., King S.R., Stocco D.M. 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 1994, 269:28314-28322.
27. Collins P.J., Kobayashi Y., Nguyen L. The ets-related transcription factor GABP directs bidirectional transcription. PLoS Genet 2007, 3:e208.
28. Coppola M., Pizzigoni A., Banfi S., Bassi M.T., Casari G., Incerti B. Identification and characterization of YME1L1, a novel paraplegin-related gene. Genomics 2000, 66:48-54.
29. Ćurčić D., Glibetić M., Larson D.E., Sells B.H. GA-binding protein is involved in altered expression of ribosomal protein L32 gene. J. Cell. Biochem 1997, 65:287-307.
30. Di Bella D., Lazzaro F., Brusco A., Plumari M., Battaglia G., Pastore A., et al. Mutations in the mitochondrial protease gene AFG3L2 cause dominant hereditary ataxia SCA28. Nat. Genet 2010, 42:313-321.
31. Duarte A., Castillo A.F., Podestá E.J., Poderoso C. Mitochondrial fusion and ERK activity regulate steroidogenic acute regulatory protein localization in mitochondria. PLoS ONE 2014, 9:e100387.
32. Erjavec N., Bayot A., Gareil M., Camougrand N., Nystrom T., Friguet B., et al. Deletion of the mitochondrial Pim1/Lon protease in yeast results in accelerated aging and impairment of the proteasome. Free Radic. Biol. Med 2013, 56:9-16.
33. Ferreirinha F., Quattrini A., Pirozzi M., Valsecchi V., Dina G., Broccoli V., et al. Axonal degeneration in paraplegin-deficient mice is associated with abnormal mitochondria and impairment of axonal transport. J. Clin. Invest 2004, 113:231-242.
34. Fromm L., Burden S.J. Neuregulin-1-stimulated phosphorylation of GABP in skeletal muscle cells. Biochemistry 2001, 40:5306-5312.
35. Gerdes F., Tatsuta T., Langer T. Mitochondrial AAA proteases - towards a molecular understanding of membrane-bound proteolytic machines. Biochim. Biophys. Acta 2012, 1823:49-55.
36. Gerstein M.B., Kundaje A., Hariharan M., Landt S.G., Yan K.-K., Cheng C., et al. Architecture of the human regulatory network derived from ENCODE data. Nature 2012, 489:91-100. 10.1038/nature11245.
37. Gleyzer N., Vercauteren K., Scarpulla R.C. Control of mitochondrial transcription specificity factors (TFB1M and TFB2M) by nuclear respiratory factors (NRF-1 and NRF-2) and PGC-1 family coactivators. Mol. Cell. Biol 2005, 25:1354-1366.
38. Granot Z., Silverman E., Friedlander R., Melamed-Book N., Eimerl S., Timberg R., et al. The life cycle of the steroidogenic acute regulatory (StAR) protein: from transcription through proteolysis. Endocr. Res 2002, 28:375-386.
39. Granot Z., Geiss-Friedlander R., Melamed-Book N., Eimerl S., Timberg R., Weiss A.M., et al. Proteolysis of normal and mutated steroidogenic acute regulatory proteins in the mitochondria: the fate of unwanted proteins. Mol. Endocrinol 2003, 17:2461-2476.
40. Granot Z., Kobiler O., Melamed-Book N., Eimerl S., Bahat A., Lu B., et al. Turnover of mitochondrial steroidogenic acute regulatory (StAR) protein by Lon protease: the unexpected effect of proteasome inhibitors. Mol. Endocrinol 2007, 21:2164-2177.
41. Granot Z., Melamed-Book N., Bahat A., Orly J. Turnover of StAR protein: roles for the proteasome and mitochondrial proteases. Mol. Cell. Endocrinol 2007, 265:51-58.
42. Gugneja S., Virbasius J.V., Scarpulla R.C. Four structurally distinct, non-DNA-binding subunits of human nuclear respiratory factor 2 share a conserved transcriptional activation domain. Mol. Cell. Biol 1995, 15:102-111.
43. Handschin C., Kobayashi Y.M., Chin S., Seale P., Campbell K.P., Spiegelman B.M. PGC-1α regulates the neuromuscular junction program and ameliorates Duchenne muscular dystrophy. Genes Dev 2007, 21:770-783.
44. Haynes C.M., Ron D. The mitochondrial UPR-protecting organelle protein homeostasis. J. Cell Sci 2010, 123:3849-3855.
45. Haynes C.M., Petrova K., Benedetti C., Yang Y., Ron D. ClpP mediates activation of a mitochondrial unfolded protein response in C. elegans. Dev. Cell 2007, 13:467-480.
46. Herndon C.A., Fromm L. Neuregulin-1 induces acetylcholine receptor transcription in the absence of GABPα phosphorylation. J. Neurosci. Res 2008, 86:982-991.
47. Higgins J.J., Pucilowska J., Lombardi R.Q., Rooney J.P. A mutation in a novel ATP-dependent Lon protease gene in a kindred with mild mental retardation. Neurology 2004, 63:1927-1931.
48. Hoffmeyer A., Avots A., Flory E., Weber C.K., Serfling E., Rapp U.R. The GABP-responsive element of the interleukin-2 enhancer is regulated by JNK/SAPK-activating pathways in T lymphocytes. J. Biol. Chem 1998, 273:10112-10119.
49. Hori O., Ichinoda F., Tamatani T., Yamaguchi A., Sato N., Ozawa K., et al. Transmission of cell stress from endoplasmic reticulum to mitochondria enhanced expression of Lon protease. J. Cell Biol 2002, 157:1151-1160.
50. Ishii T., Hasegawa T., Pai C.-I., Yvgi-Ohana N., Timberg R., Zhao L., et al. The roles of circulating high-density lipoproteins and trophic hormones in the phenotype of knockout mice lacking the steroidogenic acute regulatory protein. Mol. Endocrinol 2002, 16:2297-2309.
51. Jenkinson E.M., Rehman A.U., Walsh T., Clayton-Smith J., Lee K., Morell R.J., et al. Perrault syndrome is caused by recessive mutations in CLPP, encoding a mitochondrial ATP-dependent chambered protease. Am. J. Hum. Genet 2013, 92(4):605-613.
52. Katayama Y., Gottesman S., Pumphrey J., Rudikoff S., Clark W.P., Maurizi M. The two-component, ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component. J. Biol. Chem 1988, 263:15226-15236.
53. Kim T.Y., Wang D., Kim A.K., Lau E., Lin A.J., Liem D.A., et al. Metabolic labeling reveals proteome dynamics of mouse mitochondria. Mol. Cell. Proteomics 2012, 11:1586-1594.
54. King S.R., Ronen-Fuhrmann T., Timberg R., Clark B.J., Orly J., Stocco D.M. Steroid production after in vitro transcription, translation, and mitochondrial processing of protein products of complementary deoxyribonucleic acid for steroidogenic acute regulatory protein. Endocrinology 1995, 136:5165-5176.
55. King S.R., Liu Z., Soh J., Eimerl S., Orly J., Stocco D.M. Effects of disruption of the mitochondrial electrochemical gradient on steroidogenesis and the steroidogenic acute regulatory (StAR) protein. J. Steroid Biochem. Mol. Biol 1999, 69:143-154. 10.1016/S0960-0760(98)00152-6.
56. Kiriakidou M., McAllister J., Sugawara T., Strauss J. Expression of steroidogenic acute regulatory protein (StAR) in the human ovary. J. Clin. Endocrinol. Metab 1996, 81:4122-4128.
57. Kondadi A.K., Wang S., Montagner S., Kladt N., Korwitz A., Martinelli P., et al. Loss of the m-AAA protease subunit AFG3L2 causes mitochondrial transport defects and tau hyperphosphorylation. EMBO J. 2014, 33:1011-1026.
58. Koppen M., Metodiev M.D., Casari G., Rugarli E.I., Langer T. Variable and tissue-specific subunit composition of mitochondrial m-AAA protease complexes linked to hereditary spastic paraplegia. Mol. Cell. Biol 2007, 27:758-767.
59. Lau E., Wang D., Zhang J., Yu H., Lam M.P., Liang X., et al. Substrate-and isoform-specific proteome stability in normal and stressed cardiac mitochondria. Circ. Res 2012, 110:1174-1178.
60. Lavigne P., Najmanivich R., LeHoux J.-G. Mammalian StAR-Related Lipid Transfer (START) Domains with Specificity for Cholesterol: Structural Conservation and Mechanism of Reversible Binding, Cholesterol Binding and Cholesterol Transport Proteins 2010, 425-437. Springer.
61. Leonhard K., Herrmann J., Stuart R., Mannhaupt G., Neupert W., Langer T. AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J. 1996, 15:4218.
62. Leonhard K., Guiard B., Pellecchia G., Tzagoloff A., Neupert W., Langer T. Membrane protein degradation by AAA proteases in mitochondria: extraction of substrates from either membrane surface. Mol. Cell 2000, 5:629-638.
63. Levine R.L. Commentary on "Downregulation of the human Lon protease impairs mitochondrial structure and function and causes cell death" by D.A. Bota, J.K. Ngo, and K.J.A. Davies. Free Radic. Biol. Med 2005, 38:1445-1446.
64. Lin D., Sugawara T., Strauss J.R., Clark B.J., Stocco D.M., Saenger P., et al. Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis. Science 1995, 267:1828-1831.
65. Lin J., Handschin C., Spiegelman B.M. Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab 2005, 1:361-370.
66. Lu B., Yadav S., Shah P.G., Liu T., Tian B., Pukszta S., et al. Roles for the human ATP-dependent Lon protease in mitochondrial DNA maintenance. J. Biol. Chem 2007, 282:17363-17374.
67. + lon protease. Mol. Cell 2013, 49:121-132.
68. Maillard R.A., Chistol G., Sen M., Righini M., Tan J., Kaiser C.M., et al. ClpX (P) generates mechanical force to unfold and translocate its protein substrates. Cell 2011, 145:459-469.
69. Maltecca F., Aghaie A., Schroeder D.G., Cassina L., Taylor B.A., Phillips S.J., et al. The mitochondrial protease AFG3L2 is essential for axonal development. J. Neurosci 2008, 28:2827-2836.
70. Maltecca F., De Stefani D., Cassina L., Consolato F., Wasilewski M., Scorrano L., et al. Respiratory dysfunction by AFG3L2 deficiency causes decreased mitochondrial calcium uptake via organellar network fragmentation. Hum. Mol. Genet 2012, 21:3858-3870.
71. Matsushima Y., Kaguni L.S. Matrix proteases in mitochondrial DNA function. Biochim. Biophys. Acta 2012, 1819:1080-1087.
72. Meier R.K., Clark B.J. Angiotensin II-dependent transcriptional activation of human steroidogenic acute regulatory protein gene by a 25-kDa cAMP-responsive element modulator protein isoform and Yin Yang 1. Endocrinology 2012, 153:1256-1268.
73. Merkwirth C., Dargazanli S., Tatsuta T., Geimer S., Löwer B., Wunderlich F.T., et al. Prohibitins control cell proliferation and apoptosis by regulating OPA1-dependent cristae morphogenesis in mitochondria. Genes Dev 2008, 22:476-488.
74. Miller W.L. Congenital lipoid adrenal hyperplasia: the human gene knockout for the steroidogenic acute regulatory protein. J. Mol. Endocrinol 1997, 19:227-240.
75. Miller W.L. Mechanism of StAR's regulation of mitochondrial cholesterol import. Mol. Cell. Endocrinol 2007, 265:46-50.
76. Miller W.L., Auchus R.J. The molecular biology, biochemistry, and physiology of human steroidogenesis and its disorders. Endocr. Rev 2011, 32:81-151.
77. Miller W.L., Strauss J.F. Molecular pathology and mechanism of action of the steroidogenic acute regulatory protein, StAR Proceedings of Xth International Congress on Hormonal Steroids, Quebec, Canada, 17-21 June 1998. J. Steroid Biochem. Mol. Biol 1999, 69:131-141.
78. Mogk A., Dougan D., Weibezahn J., Schlieker C., Turgay K., Bukau B. Broad yet high substrate specificity: the challenge of AAA+ proteins. J. Struct. Biol 2004, 146:90-98.
79. Morohaku K., Phuong N.S., Selvaraj V. Developmental expression of translocator protein/peripheral benzodiazepine receptor in reproductive tissues. PLoS ONE 2013, 8:e74509.
80. Nakae J., Tajima T., Sugawara T., Arakane F., Hanaki K., Hotsubo T., et al. Analysis of the steroidogenic acute regulatory protein (StAR) gene in Japanese patients with congenital lipoid adrenal hyperplasia. Hum. Mol. Genet 1997, 6:571-576.
81. Neupert W., Brunner M. The protein import motor of mitochondria. Nat. Rev. Mol. Cell Biol 2002, 3:555-565.
82. Ngo J.K., Davies K.J. Importance of the lon protease in mitochondrial maintenance and the significance of declining lon in aging. Ann. N. Y. Acad. Sci 2007, 1119:78-87.
83. Ngo J.K., Davies K.J. Mitochondrial Lon protease is a human stress protein. Free Radic. Biol. Med 2009, 46:1042-1048.
84. Ngo J.K., Pomatto L.C., Bota D.A., Koop A.L., Davies K.J. Impairment of lon-induced protection against the accumulation of oxidized proteins in senescent wi-38 fibroblasts. J. Gerontol. A. Biol Sci. Med Sci 2011, 66:1178-1185.
85. Ngo J.K., Pomatto L.C., Davies K.J. Upregulation of the mitochondrial Lon Protease allows adaptation to acute oxidative stress but dysregulation is associated with chronic stress, disease, and aging. Redox Biol 2013, 1:258-264.
86. Ondrovičová G., Liu T., Singh K., Tian B., Li H., Gakh O., et al. Cleavage site selection within a folded substrate by the ATP-dependent lon protease. J. Biol. Chem 2005, 280:25103-25110.
87. Ongwijitwat S., Wong-Riley M.T. Is nuclear respiratory factor 2 a master transcriptional coordinator for all ten nuclear-encoded cytochrome c oxidase subunits in neurons?. Gene 2005, 360:65-77.
88. Papa L., Germain D. Estrogen receptor mediates a distinct mitochondrial unfolded protein response. J. Cell Sci 2011, 124:1396-1402.
89. Pellegrino M.W., Nargund A.M., Haynes C.M. Signaling the mitochondrial unfolded protein response. Biochim. Biophys. Acta 2013, 1833:410-416.
90. Pellegrino M.W., Nargund A.M., Kirienko N.V., Gillis R., Fiorese C.J., Haynes C.M. Mitochondrial UPR-regulated innate immunity provides resistance to pathogen infection. Nature 2014, 516:414-417.
91. Piantadosi C.A., Suliman H.B. Transcriptional control of mitochondrial biogenesis and its interface with inflammatory processes. Biochim. Biophys. Acta 2012, 1820:532-541.
92. Pierson T.M., Adams D., Bonn F., Martinelli P., Cherukuri P.F., Teer J.K., et al. Whole-exome sequencing identifies homozygous AFG3L2 mutations in a spastic ataxia-neuropathy syndrome linked to mitochondrial m-AAA proteases. PLoS Genet 2011, 7:e1002325.
93. Pinti M., Gibellini L., De Biasi S., Nasi M., Roat E., O'Connor J.-E., et al. Functional characterization of the promoter of the human Lon protease gene. Mitochondrion 2011, 11:200-206.
94. Priya A., Johar K., Wong-Riley M.T. Nuclear respiratory factor 2 regulates the expression of the same NMDA receptor subunit genes as NRF-1: both factors act by a concurrent and parallel mechanism to couple energy metabolism and synaptic transmission. Biochim. Biophys. Acta 2013, 1833:48-58.
95. Puigserver P., Spiegelman B.M. Peroxisome proliferator-activated receptor-γ coactivator 1α (PGC-1α): transcriptional coactivator and metabolic regulator. Endocr. Rev 2003, 24:78-90.
96. Quirós P.M., et al. ATP-Dependent Lon Protease Controls Tumor Bioenergetics by Reprogramming Mitochondrial Activity. Cell Reports 2014, 8:542-556.
97. Rath E., Berger E., Messlik A., Nunes T., Liu B., Kim S.C., et al. Induction of dsRNA-activated protein kinase links mitochondrial unfolded protein response to the pathogenesis of intestinal inflammation. Gut 2012, 61:1269-1278.
98. Rone M.B., Midzak A.S., Issop L., Rammouz G., Jagannathan S., Fan J., et al. Identification of a dynamic mitochondrial protein complex driving cholesterol import, trafficking, and metabolism to steroid hormones. Mol. Endocrinol 2012, 26:1868-1882.
99. Ronen-Fuhrmann T., Timberg R., King S.R., Hales K.H., Hales D.B., Stocco D.M., et al. Spatio-temporal expression patterns of steroidogenic acute regulatory protein (StAR) during follicular development in the rat ovary 1. Endocrinology 1998, 139:303-315.
100. Rosmarin A.G., Resendes K.K., Yang Z., McMillan J.N., Fleming S.L. GA-binding protein transcription factor: a review of GABP as an integrator of intracellular signaling and protein-protein interactions. Blood Cells Mol. Dis 2004, 32:143-154.
101. Ryan M.T., Hoogenraad N.J. Mitochondrial-nuclear communications. Annu. Rev. Biochem 2007, 76:701-722.
102. Sauer R.T., Bolon D.N., Burton B.M., Burton R.E., Flynn J.M., Grant R.A., et al. Sculpting the proteome with AAA+ proteases and disassembly machines. Cell 2004, 119:9-18.
103. Scarpulla R.C. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol. Rev 2008, 88:611-638.
104. Scarpulla R.C. Nucleus-encoded regulators of mitochondrial function: integration of respiratory chain expression, nutrient sensing and metabolic stress. Biochim. Biophys. Acta 2012, 1819:1088-1097.
105. Scarpulla R.C., Vega R.B., Kelly D.P. Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol. Metab 2012, 23:459-466.
106. Simpson E.R., Waterman M.R. Regulation by ACTH of steroid hormone biosynthesis in the adrenal cortex. Can. J. Biochem. Cell Biol 1983, 61:692-707.
107. Sowa Y., Shiio Y., Fujita T., Matsumoto T., Okuyama Y., Kato D., et al. Retinoblastoma binding factor 1 site in the core promoter region of the human RB gene is activated by hGABP/E4TF1. Cancer Res 1997, 57:3145-3148.
108. Stocco D.M. The role of PBR/TSPO in steroid biosynthesis challenged. Endocrinology 2014, 155:6-9.
109. Stocco D.M., Clark B.J. Regulation of the acute production of steroids in steroidogenic cells. Endocr. Rev 1996, 17:221-244.
110. Sunesen M., Huchet-Dymanus M., Christensen M.O., Changeux J.-P. Phosphorylation-elicited quaternary changes of GA binding protein in transcriptional activation. Mol. Cell. Biol 2003, 23:8008-8018.
111. Suzuki C.K., Suda K., Wang N., Schatz G. Requirement for the yeast gene LON in intramitochondrial proteolysis and maintenance of respiration. Science 1994, 264:273-276.
112. Tatsuta T., Augustin S., Nolden M., Friedrichs B., Langer T. m-AAA protease-driven membrane dislocation allows intramembrane cleavage by rhomboid in mitochondria. EMBO J. 2007, 26:325-335.
113. Tsujishita Y., Hurley J.H. Structure and lipid transport mechanism of a StAR-related domain. Nat. Struct. Mol. Biol 2000, 7:408-414.
114. Tu L.N., Morohaku K., Manna P.R., Pelton S.H., Butler W.R., Stocco D.M., et al. Peripheral benzodiazepine receptor/translocator protein global knock-out mice are viable with no effects on steroid hormone biosynthesis. J. Biol. Chem 2014, 289:27444-27454.
115. van Dyck L., Neupert W., Langer T. The ATP-dependent PIM1 protease is required for the expression of intron-containing genes in mitochondria. Genes Dev 1998, 12:1515-1524.
116. Villena J., Vinas O., Mampel T., Iglesias R., Giralt M., Villarroya F. Regulation of mitochondrial biogenesis in brown adipose tissue: nuclear respiratory factor-2/GA-binding protein is responsible for the transcriptional regulation of the gene for the mitochondrial ATP synthase β subunit. Biochem. J. 1998, 331:121-127.
117. Virbasius J.V., Virbasius C.A., Scarpulla R.C. Identity of GABP with NRF-2, a multisubunit activator of cytochrome oxidase expression, reveals a cellular role for an ETS domain activator of viral promoters. Genes Dev 1993, 7:380-392.
118. Wang N., Gottesman S., Willingham M.C., Gottesman M.M., Maurizi M.R. A human mitochondrial ATP-dependent protease that is highly homologous to bacterial Lon protease. PNAS 1993, 90:11247-11251.
119. Wu Z., Puigserver P., Andersson U., Zhang C., Adelmant G., Mootha V., et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 1999, 98:115-124.
120. Wu Z., Huang X., Feng Y., Handschin C., Feng Y., Gullicksen P.S., et al. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1α transcription and mitochondrial biogenesis in muscle cells. PNAS 2006, 103:14379-14384.
121. Yang S.J., Liang H.L., Ning G., Wong-Riley M.T. Ultrastructural study of depolarization-induced translocation of NRF-2 transcription factor in cultured rat visual cortical neurons. Eur. J. Neurosci 2004, 19:1153-1162.
122. Yu S., Cui K., Jothi R., Zhao D.-M., Jing X., Zhao K., et al. GABP controls a critical transcription regulatory module that is essential for maintenance and differentiation of hematopoietic stem/progenitor cells. Blood 2011, 117:2166-2178.
123. Zhao Q., Wang J., Levichkin I.V., Stasinopoulos S., Ryan M.T., Hoogenraad N.J. A mitochondrial specific stress response in mammalian cells. EMBO J. 2002, 21:4411-4419.