Molecular characterization of skeletal muscle atrophy in the R6/2 mouse model of Huntington's disease

American Journal of Physiology - Endocrinology and Metabolism

Volumn 301, Issue 1, 2011, Pages

  She, Pengxiang ^a   Zhang, Zhiyou ^a   Marchionini, Deanna ^b   Diaz, William C ^c   Jetton, Thomas J ^c   Kimball, Scot R ^a   Vary, Thomas C ^a   Lang, Charles H ^a   Lynch, Christopher J ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b CHDI Management Inc   (United States)

^c UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 METHYLHISTIDINE; AUTOPHAGY PROTEIN 5; AUTOPHAGY PROTEIN 7; BECLIN 1; CASPASE; CASPASE 3; CASPASE 7; CASPASE 8; CASPASE 9; CYTOCHROME C; F BOX PROTEIN; FAS ANTIGEN; FAS ASSOCIATED DEATH DOMAIN PROTEIN; LC3B I PROTEIN; LC3B II PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MUSCLE PROTEIN; MUSCLE RING FINGER 1 PROTEIN; PROTEIN; PROTEIN KINASE B; UNCLASSIFIED DRUG;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; AUTOPHAGY; BODY COMPOSITION; BODY MASS; CATABOLISM; DIET RESTRICTION; ENERGY EXPENDITURE; ENZYME ACTIVITY; FEMALE; FOOD INTAKE; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; HUNTINGTON CHOREA; LOCOMOTION; MALE; MOLECULAR MECHANICS; MOUSE; MUSCLE ATROPHY; NONHUMAN; OBESITY; ORGAN WEIGHT; OXYGEN CONSUMPTION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; REFEEDING; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TRANSGENIC MOUSE; UPREGULATION; URINARY EXCRETION; WEIGHT REDUCTION;

ADIPOSITY; AGE FACTORS; ANIMALS; BODY WEIGHT; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; FEMALE; HUNTINGTON DISEASE; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUSCULAR ATROPHY; SIGNAL TRANSDUCTION;

EID: 79959589571     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00630.2010     Document Type: Article

References (73)

1. Almeida S, Sarmento-Ribeiro AB, Januario C, Rego AC, Oliveira CR. Evidence of apoptosis and mitochondrial abnormalities in peripheral blood cells of Huntington's disease patients. Biochem Biophys Res Commun 374: 599-603, 2008.
2. Argiles JM, Lopez-Soriano FJ, Busquets S. Apoptosis signalling is essential and precedes protein degradation in wasting skeletal muscle during catabolic conditions. Int J Biochem Cell Biol 40: 1674-1678, 2008.
3. Attaix D, Aurousseau E, Combaret L, Kee A, Larbaud D, Ralliere C, Souweine B, Taillandier D, Tilignac T. Ubiquitin-proteasome-dependent proteolysis in skeletal muscle. Reprod Nutr Dev 38: 153-165, 1998.
4. Bahr BA, Bendiske J. The neuropathogenic contributions of lysosomal dysfunction. J Neurochem 83: 481-489, 2002.
5. Bechet D, Tassa A, Taillandier D, Combaret L, Attaix D. Lysosomal proteolysis in skeletal muscle. Int J Biochem Cell Biol 37: 2098-2114, 2005.
6. Bjorkqvist M, Petersen A, Bacos K, Isaacs J, Norlen P, Gil J, Popovic N, Sundler F, Bates GP, Tabrizi SJ, Brundin P, Mulder H. Progressive alterations in the hypothalamic-pituitary-adrenal axis in the R6/2 transgenic mouse model of Huntington's disease. Hum Mol Genet 15: 1713-1721, 2006.
7. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294: 1704-1708, 2001.
8. Carter RJ, Lione LA, Humby T, Mangiarini L, Mahal A, Bates GP, Dunnett SB, Morton AJ. Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation. J Neurosci 19: 3248-3257, 1999.
9. Chaturvedi RK, Adhihetty P, Shukla S, Hennessy T, Calingasan N, Yang L, Starkov A, Kiaei M, Cannella M, Sassone J, Ciammola A, Squitieri F, Beal MF. Impaired PGC-1alpha function in muscle in Huntington's disease. Hum Mol Genet 18: 3048-3065, 2009.
10. Chaturvedi RK, Calingasan NY, Yang L, Hennessey T, Johri A, Beal MF. Impairment of PGC-1alpha expression, neuropathology and hepatic steatosis in a transgenic mouse model of Huntington's disease following chronic energy deprivation. Hum Mol Genet 19: 3190-3205, 2010.
11. Ciammola A, Sassone J, Alberti L, Meola G, Mancinelli E, Russo MA, Squitieri F, Silani V. Increased apoptosis, Huntingtin inclusions and altered differentiation in muscle cell cultures from Huntington's disease subjects. Cell Death Differ 13: 2068-2078, 2006.
12. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E, Glass DJ. The E3 ligase MuRF1 degrades myosin heavy chain protein in dexamethasonetreated skeletal muscle. Cell Metab 6: 376-385, 2007.
13. Cui L, Jeong H, Borovecki F, Parkhurst CN, Tanese N, Krainc D. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127: 59-69, 2006.
14. Ding WX, Yin XM. Sorting, recognition and activation of the misfolded protein degradation pathways through macroautophagy and the proteasome. Autophagy 4: 141-150, 2008.
15. Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, Price SR, Mitch WE. Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113: 115-123, 2004.
16. Duennwald ML, Lindquist S. Impaired ERAD and ER stress are early and specific events in polyglutamine. Genes Dev 22: 3308-3319, 2008.
17. Dupont-Versteegden EE. Apoptosis in skeletal muscle and its relevance to atrophy. World J Gastroenterol 12: 7463-7466, 2006.
18. Fain JN, Del Mar NA, Meade CA, Reiner A, Goldowitz D. Abnormalities in the functioning of adipocytes from R6/2 mice that are transgenic for the Huntington's disease mutation. Hum Mol Genet 10: 145-152, 2001.
19. Furuno K, Goodman MN, Goldberg AL. Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J Biol Chem 265: 8550-8557, 1990.
20. Glass D, Roubenoff R. Recent advances in the biology and therapy of muscle wasting. Ann NY Acad Sci 1211: 25-36, 2010.
21. Goodman AO, Murgatroyd PR, Medina-Gomez G, Wood NI, Finer N, Vidal-Puig AJ, Morton AJ, Barker RA. The metabolic profile of early Huntington's disease- a combined human and transgenic mouse study. Exp Neurol 210: 691-698, 2008.
22. Heng MY, Duong DK, Albin RL, Tallaksen-Greene SJ, Hunter JM, Lesort MJ, Osmand A, Paulson HL, Detloff PJ. Early autophagic response in a novel knock-in model of Huntington disease. Hum Mol Genet 19: 3702-3720, 2010.
23. Hunt MJ, Morton AJ. Atypical diabetes associated with inclusion formation in the R6/2 mouse model of Huntington's disease is not improved by treatment with hypoglycaemic agents. Exp Brain Res Experimentelle Hirnforschung 166: 220-229, 2005.
24. Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115: 577-590, 2003.
25. Irrcher I, Ljubicic V, Kirwan AF, Hood DA. AMP-activated protein kinase-regulated activation of the PGC-1alpha promoter in skeletal muscle cells. PLoS One 3: e3614, 2008.
26. Iwata A, Christianson JC, Bucci M, Ellerby LM, Nukina N, Forno LS, Kopito RR. Increased susceptibility of cytoplasmic over nuclear polyglutamine aggregates to autophagic degradation. Proc Natl Acad Sci USA 102: 13135-13140, 2005.
27. Jager S, Handschin C, St-Pierre J, Spiegelman BM. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci USA 104: 12017-12022, 2007.
28. Jagoe RT, Goldberg AL. What do we really know about the ubiquitinproteasome pathway in muscle atrophy? Curr Opin Clin Nutr Metab Care 4: 183-190, 2001.
29. Jana NR, Zemskov EA, Wang G, Nukina N. Altered proteasomal function due to the expression of polyglutamine-expanded truncated Nterminal huntingtin induces apoptosis by caspase activation through mitochondrial cytochrome c release. Hum Mol Genet 10: 1049-1059, 2001.
30. Jenkins BG, Andreassen OA, Dedeoglu A, Leavitt B, Hayden M, Borchelt D, Ross CA, Ferrante RJ, Beal MF. Effects of CAG repeat length, HTT protein length and protein context on cerebral metabolism measured using magnetic resonance spectroscopy in transgenic mouse models of Huntington's disease. J Neurochem 95: 553-562, 2005.
31. Kiechle T, Dedeoglu A, Kubilus J, Kowall NW, Beal MF, Friedlander RM, Hersch SM, Ferrante RJ. Cytochrome C and caspase-9 expression in Huntington's disease. Neuromol Med 1: 183-195, 2002.
32. Krawiec BJ, Nystrom GJ, Frost RA, Jefferson LS, Lang CH. AMPactivated protein kinase agonists increase mRNA content of the musclespecific ubiquitin ligases MAFbx and MuRF1 in C2C12 cells. Am J Physiol Endocrinol Metab 292: E1555-E1567, 2007.
33. Lee CE, McArdle A, Griffiths RD. The role of hormones, cytokines and heat shock proteins during age-related muscle loss. Clin Nutr 26: 524-534, 2007.
34. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/ caspase-9 complex initiates an apoptotic protease cascade. Cell 91: 479-489, 1997.
35. Liang Y, She P, Wang X, Demarest K. The messenger RNA profiles in liver, hypothalamus, white adipose tissue, and skeletal muscle of female Zucker diabetic fatty rats after topiramate treatment. Metabolism 55: 1411-1419, 2006.
36. Lione LA, Carter RJ, Hunt MJ, Bates GP, Morton AJ, Dunnett SB. Selective discrimination learning impairments in mice expressing the human Huntington's disease mutation. J Neurosci 19: 10428-10437, 1999.
37. Luthi-Carter R, Hanson SA, Strand AD, Bergstrom DA, Chun W, Peters NL, Woods AM, Chan EY, Kooperberg C, Krainc D, Young AB, Tapscott SJ, Olson JM. Dysregulation of gene expression in the R6/2 model of polyglutamine disease: parallel changes in muscle and brain. Hum Mol Genet 11: 1911-1926, 2002.
38. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P, Burden SJ, Di Lisi R, Sandri C, Zhao J, Goldberg AL, Schiaffino S, Sandri M. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 6: 458-471, 2007.
39. Martinez-Vicente M, Talloczy Z, Wong E, Tang G, Koga H, Kaushik S, de Vries R, Arias E, Harris S, Sulzer D, Cuervo AM. Cargo recognition failure is responsible for inefficient autophagy in Huntington's disease. Nat Neurosci 13: 567-576, 2010.
40. Mihm MJ, Amann DM, Schanbacher BL, Altschuld RA, Bauer JA, Hoyt KR. Cardiac dysfunction in the R6/2 mouse model of Huntington's disease. Neurobiol Dis 25: 297-308, 2007.
41. Mochel F, Charles P, Seguin F, Barritault J, Coussieu C, Perin L, Le Bouc Y, Gervais C, Carcelain G, Vassault A, Feingold J, Rabier D, Durr A. Early energy deficit in Huntington disease: identification of a plasma biomarker traceable during disease progression. PLoS ONE 2: e647, 2007.
42. Orth M, Cooper JM, Bates GP, Schapira AH. Inclusion formation in Huntington's disease R6/2 mouse muscle cultures. J Neurochem 87: 1-6, 2003.
43. Pandey UB, Nie Z, Batlevi Y, McCray BA, Ritson GP, Nedelsky NB, Schwartz SL, DiProspero NA, Knight MA, Schuldiner O, Padmanabhan R, Hild M, Berry DL, Garza D, Hubbert CC, Yao TP, Baehrecke EH, Taylor JP. HDAC6 rescues neurodegeneration and provides an essential link between autophagy and the UPS. Nature 447: 859-863, 2007.
44. Qin ZH, Wang Y, Kegel KB, Kazantsev A, Apostol BL, Thompson LM, Yoder J, Aronin N, DiFiglia M. Autophagy regulates the processing of amino terminal huntingtin fragments. Hum Mol Genet 12: 3231-3244, 2003.
45. Ribchester RR, Thomson D, Wood NI, Hinks T, Gillingwater TH, Wishart TM, Court FA, Morton AJ. Progressive abnormalities in skeletal muscle and neuromuscular junctions of transgenic mice expressing the Huntington's disease mutation. Eur J Neurosci 20: 3092-3114, 2004.
46. Saini A, Al-Shanti N, Stewart CE. Waste management-cytokines, growth factors and cachexia. Cytokine Growth Factor Rev 17: 475-486, 2006.
47. Sarkar S, Rubinsztein DC. Huntington's disease: degradation of mutant huntingtin by autophagy. FEBS J 275: 4263-4270, 2008.
48. Sassone J, Colciago C, Cislaghi G, Silani V, Ciammola A. Huntington's disease: the current state of research with peripheral tissues. Exp Neurol 219: 385-397, 2009.
49. Sawa A, Wiegand GW, Cooper J, Margolis RL, Sharp AH, Lawler JF Jr, Greenamyre JT, Snyder SH, Ross CA. Increased apoptosis of Huntington disease lymphoblasts associated with repeat length-dependent mitochondrial depolarization. Nat Med 5: 1194-1198, 1999.
50. Schmelzle T, Hall MN. TOR, a central controller of cell growth. Cell 103: 253-262, 2000.
51. She P, Reid TM, Bronson SK, Vary TC, Hajnal A, Lynch CJ, Hutson SM. Disruption of BCATm in mice leads to increased energy expenditure associated with the activation of a futile protein turnover cycle. Cell Metab 6: 181-194, 2007.
52. She P, Zhou Y, Zhang Z, Griffin K, Gowda K, Lynch CJ. Disruption of BCAA metabolism in mice impairs exercise metabolism and endurance. J Appl Physiol 108: 941-949, 2010.
53. Siu PM, Alway SE. Response and adaptation of skeletal muscle to denervation stress: the role of apoptosis in muscle loss. Front Biosci 14: 432-452, 2009.
54. Solomon V, Goldberg AL. Importance of the ATP-ubiquitin-proteasome pathway in the degradation of soluble and myofibrillar proteins in rabbit muscle extracts. J Biol Chem 271: 26690-26697, 1996.
55. Strand AD, Aragaki AK, Shaw D, Bird T, Holton J, Turner C, Tapscott SJ, Tabrizi SJ, Schapira AH, Kooperberg C, Olson JM. Gene expression in Huntington's disease skeletal muscle: a potential biomarker. Hum Mol Genet 14: 1863-1876, 2005.
56. Teles AV, Rosenstock TR, Okuno CS, Lopes GS, Bertoncini CR, Smaili SS. Increase in bax expression and apoptosis are associated in Huntington's disease progression. Neurosci Lett 438: 59-63, 2008.
57. Tsujimoto Y, Shimizu S. Another way to die: autophagic programmed cell death. Cell Death Differ 12, Suppl 2: 1528-1534, 2005.
58. Underwood BR, Broadhurst D, Dunn WB, Ellis DI, Michell AW, Vacher C, Mosedale DE, Kell DB, Barker RA, Grainger DJ, Rubinsztein DC. Huntington disease patients and transgenic mice have similar pro-catabolic serum metabolite profiles. Brain 129: 877-886, 2006.
59. van der Burg JM, Bacos K, Wood NI, Lindqvist A, Wierup N, Woodman B, Wamsteeker JI, Smith R, Deierborg T, Kuhar MJ, Bates GP, Mulder H, Erlanson-Albertsson C, Morton AJ, Brundin P, Petersen A, Bjorkqvist M. Increased metabolism in the R6/2 mouse model of Huntington's disease. Neurobiol Dis 29: 41-51, 2008.
60. Ventadour S, Attaix D. Mechanisms of skeletal muscle atrophy. Curr Opin Rheumatol 18: 631-635, 2006.
61. Vidal R, Caballero B, Couve A, Hetz C. Converging pathways in the occurrence of endoplasmic reticulum (ER) stress in Huntington's disease (Review). Curr Mol Med 11: 1-12, 2011
62. Vielma H, Mendez J, Druckenmiller M, Lukaski H. A practical and reliable method for determination of urinary 3-methylhistidine. J Biochem Biophys Methods 5: 75-82, 1981.
63. Vinciguerra M, Musaro A, Rosenthal N. Regulation of muscle atrophy in aging and disease. Adv Exp Med Biol 694: 211-233, 2010.
64. Wenz T, Rossi SG, Rotundo RL, Spiegelman BM, Moraes CT. Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proc Natl Acad Sci USA 106: 20405-20410, 2009.
65. Weydt P, Pineda VV, Torrence AE, Libby RT, Satterfield TF, Lazarowski ER, Gilbert ML, Morton GJ, Bammler TK, Strand AD, Cui L, Beyer RP, Easley CN, Smith AC, Krainc D, Luquet S, Sweet IR, Schwartz MW, La Spada AR. Thermoregulatory and metabolic defects in Huntington's disease transgenic mice implicate PGC-1alpha in Huntington's disease neurodegeneration. Cell Metab 4: 349-362, 2006.
66. Wing SS, Goldberg AL. Glucocorticoids activate the ATP-ubiquitindependent proteolytic system in skeletal muscle during fasting. Am J Physiol Endocrinol Metab 264: E668-E676, 1993.
67. Witt SH, Granzier H, Witt CC, Labeit S. MURF-1 and MURF-2 target a specific subset of myofibrillar proteins redundantly: towards understanding MURF-dependent muscle ubiquitination. J Mol Biol 350: 713-722, 2005.
68. Wohlgemuth SE, Seo AY, Marzetti E, Lees HA, Leeuwenburgh C. Skeletal muscle autophagy and apoptosis during aging: effects of calorie restriction and life-long exercise. Exp Gerontol 45: 138-148.
69. Wray CJ, Mammen JM, Hershko DD, Hasselgren PO. Sepsis upregulates the gene expression of multiple ubiquitin ligases in skeletal muscle. Int J Biochem Cell Biol 35: 698-705, 2003.
70. Yamamoto A, Cremona ML, Rothman JE. Autophagy-mediated clearance of huntingtin aggregates triggered by the insulin-signaling pathway. J Cell Biol 172: 719-731, 2006.
71. Yang D, Wang CE, Zhao B, Li W, Ouyang Z, Liu Z, Yang H, Fan P, O'Neill A, Gu W, Yi H, Li S, Lai L, Li XJ. Expression of Huntington's disease protein results in apoptotic neurons in the brains of cloned transgenic pigs. Hum Mol Genet 19: 3983-3994, 2010.
72. Young VR, Munro HN. Ntau-methylhistidine (3-methylhistidine) and muscle protein turnover: an overview. Fed Proc 37: 2291-2300, 1978.
73. Zong H, Ren JM, Young LH, Pypaert M, Mu J, Birnbaum MJ, Shulman GI. AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci USA 99: 15983-15987, 2002.