Effect of denervation on the regulation of mitochondrial transcription factor a expression in skeletal muscle

American Journal of Physiology - Cell Physiology

Volumn 309, Issue 4, 2015, Pages C228-C238

  Tryon, Liam D ^a,b   Crilly, Matthew J ^a,b   Hood, David A ^a,b  

^a YORK UNIVERSITY   (Canada)

^b YORK UNIVERSITY   (Canada)

Author keywords

Disuse; Mitochondrial biogenesis; Mitochondrial DNA; RNA stability; RNA binding protein

Indexed keywords

BINDING PROTEIN; CYTOCHROME C OXIDASE; MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL TRANSCRIPTION FACTOR A; RNA BINDING PROTEIN; DNA BINDING PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL LOSS; CELL ORGANELLE; CONTROLLED STUDY; DNA REPLICATION; DNA TRANSCRIPTION; DOWN REGULATION; ENZYME ACTIVITY; ENZYME REPRESSION; GENE ACTIVATION; GENE DOSAGE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HALF LIFE TIME; IN VIVO STUDY; MALE; MUSCLE ATROPHY; MUSCLE CELL; MUSCLE DENERVATION; MUSCLE MASS; MUSCLE MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RNA DEGRADATION; SARCOLEMMA; SKELETAL MUSCLE; TIBIALIS ANTERIOR MUSCLE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; ANIMAL; BIOSYNTHESIS; INNERVATION; METABOLISM; MITOCHONDRION; PROCEDURES; RANDOMIZATION; SPRAGUE DAWLEY RAT;

ANIMALS; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; MALE; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MUSCLE DENERVATION; MUSCLE, SKELETAL; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; TRANSCRIPTION FACTORS;

EID: 84939481460     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00266.2014     Document Type: Article

References (58)

1. Adhihetty PJ, O’Leary MF, Chabi B, Wicks KL, Hood DA. Effect of denervation on mitochondrially mediated apoptosis in skeletal muscle. J Appl Physiol 3: 1143–1151, 2007.
2. Amirouche A, Tadesse H, Lunde JA, Bélanger G, Côté J, Jasmin BJ. Activation of p38 signaling increases utrophin A expression in skeletal muscle via the RNA-binding protein KSRP and inhibition of AU-rich element-mediated mRNA decay: implications for novel DMD therapeutics. Hum Mol Genet 22: 3093–3111, 2013.
3. Argadine HM, Hellyer NJ, Mantilla CB, Zhan W, Sieck GC. The effect of denervation on protein synthesis and degradation in adult rat diaphragm muscle. J Appl Physiol 107: 438–444, 2009.
4. Bizeau ME, Willis WT, Hazel JR. Differential responses to endurance training in subsarcolemmal and intermyofibrillar mitochondria. J Appl Physiol 85: 1279–1284, 1998.
5. Brault JJ, Jespersen JG, Goldberg AL. Peroxisome proliferator-activated receptor- γ coactivator-1 α or -1 β overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J Biol Chem 285: 19460–19471, 2010.
6. Briata P, Forcales SV, Ponassi M, Corte G, Chen CY, Karin M, Puri PL, Gherzi R. p38-dependent phosphorylation of the mRNA decaypromoting factor KSRP controls the stability of select myogenic transcripts. Mol Cell 20: 891–903, 2005.
7. Chen CY, Shyu AB. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20: 465–470, 1995.
8. Cogswell AM, Stevens RJ, Hood DA. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol 264: C383–C389, 1993.
9. Connor MK, Takahashi M, Hood DA. Tissue-specific stability of nuclear and mitochondrially encoded mRNAs. Arch Biochem Biophys 333: 103–108, 1996.
10. Csibi A, Leibovitch MP, Cornille K, Tintignac LA, Leibovitch SA. MAFbx/atrogin-1 controls the activity of the initiation factor eIF3-f in skeletal muscle atrophy by targeting multiple C-terminal lysines. J Biol Chem 284: 4413–4421, 2009.
11. D’souza D, Lai RY, Shuen M, Hood DA. mRNA stability as a function of striated muscle oxidative capacity. Am J Physiol Regul Integr Comp Physiol 303: R408–R417, 2012.
12. Donà M, Sandri M, Rossini K, Dell’Aica I, Podhorska-Okolow M, Carraro U. Functional in vivo gene transfer into the myofibers of adult skeletal muscle. Biochem Biophys Res Commun 312: 1132–1138, 2003.
13. Ekstrand MI, Falkenberg M, Rantanen A, Park CB, Gaspari M, Hultenby K, Rustin P, Gustafsson CM, Larsson NG. Mitochondrial transcription factor A regulates mtDNA copy number in mammals. Hum Mol Genet 13: 935–944, 2004.
14. Falkenberg M, Larsson NG, Gustafsson CM. DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem 76: 679–699, 2007.
15. Figueroa A, Cuadrado A, Fan J, Atasoy U, Muscat GE, Muñoz- Canoves P, Muñoz A. Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Mol Cell Biol 23: 4991–5004, 2003.
16. Finol HJ, Lewis DM, Owens R. The effects of denervation on contractile properties of rat skeletal muscle. J Physiol 319: 81–92, 1981.
17. Freyssenet D, Connor MK, Takahashi M, Hood DA. Cytochrome c transcriptional activation and mRNA stability during contractile activity in skeletal muscle. Am J Physiol Endocrinol Metab 277: E26–E32, 1999.
18. Furuno K, Goodman M, Goldberg AL. Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J Biol Chem 265: 8550–8557, 1990.
19. Gherzi R, Lee KY, Briata P, Wegmüller D, Moroni C, Karin M, Chen CY. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol Cell 14: 571–583, 2004.
20. Gordon JW, Rungi AA, Inagaki H, Hood DA. Effects of contractile activity on mitochondrial transcription factor A expression in skeletal muscle. J Appl Physiol 90: 389–396, 2001.
21. Handschin C, Spiegelman BM. Peroxisome proliferator-activated receptor- γ coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27: 728–735, 2006.
22. Hindi SM, Mishra V, Bhatnagar S, Tajrishi MM, Ogura Y, Yan Z, Burkly LC, Zheng TS, Kumar A. Regulatory circuitry of TWEAK-Fn14 system and PGC-1α in skeletal muscle atrophy program. FASEB J 28: 1398–1411, 2014.
23. Klemperer HG. Lowered proportion of polysomes and decreased amino acid incorporation from denervation muscle. FEBS Lett 28: 169–172, 1972.
24. Koves TR, Noland RC, Bates AL, Henes ST, Muoio DM, Cortright RN. Subsarcolemmal and intermyofibrillar mitochondria play distinct roles in regulating skeletal muscle fatty acid metabolism. Am J Physiol Cell Physiol 288: C1074–C1082, 2005.
25. Kukat C, Larsson NG. mtDNA makes a U-turn for the mitochondrial nucleoid. Trends Cell Biol 23: 457–463, 2013.
26. Kukat C, Wurm CA, Spåhr H, Falkenberg M, Larsson NG. Superresolution microscopy reveals that mammalian mitochondrial nucleoids have a uniform size and frequently contain a single copy of mtDNA. Proc Natl Acad Sci USA 108: 13534–13539, 2011.
27. Lagirand-Cantaloube J, Offner N, Csibi A, Leibovitch MP, Batonnet- Pichon S, Tintignac LA, Segura CT, Leibovitch SA. The initiation factor eIF3-f is a major target for atrogin1/MAFbx function in skeletal muscle atrophy. EMBO J 27: 1266–1276, 2008.
28. Lai RY, Ljubicic V, D’souza D, Hood DA. Effect of chronic contractile activity on mRNA stability in skeletal muscle. Am J Physiol Cell Physiol 299: C155–C163, 2010.
29. Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, Gorospe M. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 23: 3092–3102, 2004.
30. Larsson NG, Wang J, Wilhelmsson H, Oldfors A, Rustin P, Lewandowski M, Barsh GS, Clayton DA. Mitochondrial transcription factor A is necessary for mt DNA maintenance and embryogenesis in mice. Nature 18: 231–236, 1998.
31. Lee JE, Lee JY, Wilusz J, Tian B, Wilusz CJ. Systematic analysis of cis-elements in unstable mRNAs demonstrates that CUGBP1 is a key regulator of mRNA decay in muscle cells. PLos One 5: e11201, 2010.
32. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP. Peroxisome proliferator-activated receptor-γ coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest 106: 847–856, 2000.
33. Machida M, Takeda K, Yokono H, Ikemune S, Taniguchi Y, Kiyosawa H, Takemasa T. Reduction of ribosome biogenesis with activation of the mTOR pathway in denervated atrophic muscle. J Cell Physiol 227: 1569–1576, 2012.
34. Maniura-Weber K, Goffart S, Garstka HL, Montoya J, Wiesner RJ. Transient overexpression of mitochondrial transcription factor A (TFAM) is sufficient to stimulate mitochondrial DNA transcription, but not sufficient to increase mtDNA copy number in cultured cells. Nucleic Acids Res 32: 6015–6027, 2004.
35. Metafora S, Felsani A, Cotrufo R, Tajana GF, Di Iorio G, Del Rio A, De Prisco PP, Esposito V. Neural control of gene expression in the skeletal muscle fibre: the nature of the lesion in the muscular proteinsynthesizing machinery following denervation. Proc R Soc Lond Ser B Biol Sci 209: 239–255, 1980.
36. Moraes KC, Wilusz CJ, Wilusz J. CUG-BP binds to RNA substrates and recruits PARN deadenylase. RNA 12: 1084–1091, 2006.
37. Ngo HB, Kaiser JT, Chan DC. The mitochondrial transcription and packaging factor Tfam imposes a U-turn on mitochondrial DNA. Nat Struct Mol Biol 18: 1290–1296, 2011.
38. O’Leary MF, Hood DA. Effect of prior chronic contractile activity on mitochondrial function and apoptotic protein expression in denervated muscle. J Appl Physiol 105: 114–120, 2008.
39. O’Leary MF, Hood DA. Denervation-induced oxidative stress and autophagy signaling in muscle. Autophagy 5: 230–231, 2009.
40. O’Leary MF, Vainshtein A, Carter HN, Zhang Y, Hood DA. Denervation- induced mitochondrial dysfunction and autophagy in skeletal muscle of apoptosis-deficient animals. Am J Physiol Cell Physiol 303: C447– C454, 2012.
41. Peng SS, Chen CY, Xu N, Shyu AB. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J 17: 3461–3470, 1998.
42. Rattenbacher B, Beisang D, Wiesner DL, Jeschke JC, von Hohenberg M, St Louis-Vlasova IA, Bohjanen PR. Analysis of CUGBP1 targets identifies GU-repeat sequences that mediate rapid mRNA decay. Mol Cell Biol 30: 3970–3980, 2010.
43. Rubio-Cosials A, Sidow JF, Jiménez-Menéndez N, Fernández-Millán P, Montoya J, Jacobs HT, Coll M, Bernadó P, Solà, M. Human mitochondrial transcription factor A induces a U-turn structure in the light strand promoter. Nat Struct Mol Biol 18: 1281–1289, 2011.
44. Sacheck JM, Hyatt JP, Raffaello A, Jagoe RT, Roy RR, Edgerton VR, Lecker SH, Goldberg AL. Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21: 140–155, 2007.
45. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH, Goldberg AL, Spiegelman BM. PGC-1α protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 103: 16260–16265, 2006.
46. Scarpulla RC. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 88: 611–638, 2008.
47. Shi Y, Dierckx A, Wanrooij PH, Wanrooij S, Larsson NG, Wilhelmsson LM, Falkenberg M, Gustafsson CM. Mammalian transcription factor A is a core component of the mitochondrial transcription machinery. Proc Natl Acad Sci USA 109: 16510–16515, 2012.
48. Singh K, Hood DA. Effect of denervation-induced muscle disuse on mitochondrial protein import. Am J Physiol Cell Physiol 300: C138–C145, 2011.
49. Taylor AB, Smith BS, Kitada S, Kojima K, Miyaura H, Otwinowski Z, Ito A, Deisenhofer J. Crystal structures of mitochondrial processing peptidase reveal the mode for specific cleavage of import signal sequences. Structure 9: 615–625, 2001.
50. Vainshtein A, Desjardins EM, Armani A, Sandri M, Hood DA. PGC-1α modulates denervation-induced mitophagy in skeletal muscle. Skelet Muscle 5: 1–17, 2015.
51. Virbasius JV, Scarpulla RC. Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proc Natl Acad Sci USA 91: 1309–1313, 1994.
52. Vlasova IA, Tahoe NM, Fan D, Larsson O, Rattenbacher B, Sternjohn JR, Vasdewani J, Karypis G, Reilly CS, Bitterman PB, Bohjanen PR. Conserved GU-rich elements mediate mRNA decay by binding to CUGbinding protein 1. Mol Cell 29: 263–270, 2008.
53. Wagatsuma A, Kotake N, Mabuchi K, Yamada S. Expression of nuclear-encoded genes involved in mitochondrial biogenesis and dynamics in experimentally denervated muscle. J Physiol Biochem 67: 359–370, 2011.
54. Wicks KL, Hood DA. Mitochondrial adaptations in denervated muscle: relationship to muscle performance. Am J Physiol Cell Physiol 260: C841–C850, 1991.
55. Wredenberg A, Wibom R, Wilhelmsson H, Graff C, Wiener HH, Burden SJ, Oldfors A, Westerblad H, Larsson NG. Increased mitochondrial mass in mitochondrial myopathy mice. Proc Natl Acad Sci USA 99: 15066–15071, 2002.
56. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115–124, 1999.
57. Yakubovskaya E, Guja KE, Eng ET, Choi WS, Mejia E, Beglov D, Lukin M, Kozakov D, Garcia-Diaz M. Organization of the human mitochondrial transcription initiation complex. Nucleic Acids Res 42: 4100–4112, 2014.
58. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 6: 472–483, 2007