Acute daily psychological stress causes increased atrophic gene expression and myostatin-dependent muscle atrophy

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 3, 2010, Pages

  Allen, David L ^a   McCall, Gary E ^a   Loh, Amanda S ^a   Madden, Molly C ^a   Mehan, Ryan S ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Atrogenes; Fast twitch; Restraint stress; Soleus; Tibialis anterior

Indexed keywords

ATROGIN 1; MESSENGER RNA; MYOSTATIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITORY SUBUNIT P85ALPHA; UNCLASSIFIED DRUG; CORTICOSTERONE;

ANIMAL TISSUE; ARTICLE; BODY SIZE; CONTROLLED STUDY; GENE EXPRESSION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMMOBILIZATION STRESS; LEAN BODY WEIGHT; MALE; MENTAL STRESS; MOUSE; MUSCLE ATROPHY; NONHUMAN; PRIORITY JOURNAL; SOLEUS MUSCLE; THYMUS; TIBIALIS ANTERIOR MUSCLE; WILD TYPE; ANATOMY AND HISTOLOGY; ANIMAL; BLOOD; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; ORGAN SIZE; PHYSIOLOGY; SKELETAL MUSCLE; SPLEEN; WEIGHT REDUCTION;

ANIMALS; CORTICOSTERONE; GENE EXPRESSION REGULATION; MICE; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MYOSTATIN; ORGAN SIZE; RNA, MESSENGER; SPLEEN; STRESS, PSYCHOLOGICAL; THYMUS GLAND; WEIGHT LOSS;

EID: 77956681980     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00296.2010     Document Type: Article

References (54)

1. Allen DL, Unterman TG. Regulation of myostatin expression and myoblast differentiation by FoxO and SMAD transcription factors. Am J Physiol Cell Physiol 292: C188-C199, 2007.
2. Allen DL, Cleary AS, Speaker KJ, Lindsay SF, Uyenishi J, Reed JM, Madden MC, Mehan RS. Myostatin, activin receptor IIb, and follistatin-like-3 gene expression are altered in adipose tissue and skeletal muscle of obese mice. Am J Physiol Endocrinol Metab 294: E918-E927, 2008.
3. Allen DL, Bandstra ER, Harrison BC, Thorng S, Stodieck LS, Kostenuik PJ, Morony S, Lacey DL, Hammond TG, Leinwand LL, Argraves WS, Bateman TA, Barth JL. Effects of spaceflight on murine skeletal muscle gene expression. J Appl Physiol 106: 582-595, 2009.
4. Björntorp P. Visceral fat accumulation: the missing link between psychosocial factors and cardiovascular disease? J Intern Med 230: 195-201, 1991.
5. Bose M, Oliván B, Laferrère B. Stress and obesity: the role of the hypothalamic-pituitary-adrenal axis in metabolic disease. Curr Opin Endocrinol Diabetes Obes 16: 340-346, 2009.
6. Branth S, Ronquist G, Stridsberg M, Hambraeus L, Kindgren E, Olsson R, Carlander D, Arnetz B. Development of abdominal fat and incipient metabolic syndrome in young healthy men exposed to long-term stress. Nutr Metab Cardiovasc Dis 17: 427-435, 2007. (Pubitemid 47069914)
7. Buynitsky T, Mostofsky DI. Restraint stress in biobehavioral research: Recent developments. Neurosci Biobehav Rev 33: 1089-1098, 2009.
8. Carlson CJ, Booth FW, Gordon SE. Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloading. Am J Physiol Regul Integr Comp Physiol 277: R601-R606, 1999.
9. Chauhan PS, Satti NK, Suri KA, Amina M, Bani S. Stimulatory effects of cuminum cyminum and flavonoid glycoside on cyclosporine-A and restraint stress induced immune-suppression in Swiss albino mice. Chem Biol Interact 185: 66-72, 2010.
10. Davern PJ, Chen D, Head GA, Chavez CA, Walther T, Mayorov DN. Role of angiotensin II Type 1A receptors in cardiovascular reactivity and neuronal activation after aversive stress in mice. Hypertension 54: 1262-1268, 2009.
11. de Haan M, van Herck H, Tolboom JB, Beynen AC, Remie R. Endocrine stress response in jugular-vein cannulated rats upon multiple exposure to either diethyl-ether, halothane/O2/N2O or sham anaesthesia. Lab Anim 36: 105-114, 2002. (Pubitemid 34311404)
12. Depke M, Fusch G, Domanska G, Geffers R, Völker U, Schuett C, Kiank C. Hypermetabolic syndrome as a consequence of repeated psychological stress in mice. Endocrinology 149: 2714-2723, 2008. (Pubitemid 351724510)
13. Engelbrecht AM, Smith C, Neethling I, Thomas M, Ellis B, Mattheyse M, Myburgh KH. Daily brief restraint stress alters signaling pathways and induces atrophy and apoptosis in rat skeletal muscle. Stress 13: 132-141, 2010.
14. Figueredo VM. The time has come for physicians to take notice: the impact of psychosocial stressors on the heart. Am J Med 122: 704-712, 2009.
15. Finestone HM, Alfeeli A, Fisher WA. Stress-induced physiologic changes as a basis for the biopsychosocial model of chronic musculoskeletal pain: a new theory? Clin J Pain 24: 767-775, 2008.
16. Gilson H, Schakman O, Combaret L, Lause P, Grobet L, Attaix D, Ketelslegers JM, Thissen JP. Myostatin gene deletion prevents glucocorticoid-induced muscle atrophy. Endocrinology 148: 452-460, 2007. (Pubitemid 46021477)
17. Giorgino F, Pedrini MT, Matera L, Smith RJ. Specific increase in p85alpha expression in response to dexamethasone is associated with inhibition of insulin-like growth factor-I stimulated phosphatidylinositol 3-kinase activity in cultured muscle cells. J Biol Chem 272: 7455-7463, 1997. (Pubitemid 27166458)
18. Godbout JP, Glaser R. Stress-induced immune dysregulation: implications for wound healing, infectious disease and cancer. J Neuroimmune Pharmacol 1: 421-427, 2006. (Pubitemid 44786675)
19. Grobet L, Martin LJ, Poncelet D, Pirottin D, Brouwers B, Riquet J, Schoeberlein A, Dunner S, Menissier F, Massabanda J, Fries R, Hanset R, Georges M. A deletion in the bovine myostatin gene causes the double-muscled phenotype in cattle. Nat Genet 17: 71-74, 1997.
20. Harris RB, Zhou J, Youngblood BD, Rybkin II, Smagin GN, Ryan DH. Effect of repeated stress on body weight and body composition of rats fed low- and high-fat diets. Am J Physiol Regul Integr Comp Physiol 275: R1928-R1938, 1998.
21. Jagoe RT, Lecker SH, Gomes M, Goldberg AL. Patterns of gene expression in atrophying skeletal muscles: response to food deprivation. FASEB J 16: 1697-1712, 2002. (Pubitemid 35345118)
22. Jeanplong F, Bass JJ, Smith HK, Kirk SP, Kambadur R, Sharma M, Oldham JM. Prolonged underfeeding of sheep increases myostatin and myogenic regulatory factor Myf-5 in skeletal muscle while IGF-I and myogenin are repressed. J Endocrinol 176: 425-437, 2003. (Pubitemid 36410425)
23. Ji M, Zhang Q, Ye J, Wang X, Yang W, Zhu D. Myostatin induces p300 degradation to silence cyclin D1 expression through the PI3K/PTEN/Akt pathway. Cell Signal 20: 1452-1458, 2008.
24. Jones BC, Sarrieau A, Reed CL, Azar MR, Mormède P. Contribution of sex and genetics to neuroendocrine adaptation to stress in mice. Psychoneuroendocrinology 23: 505-517, 1998. (Pubitemid 28459569)
25. Kivimäki M, Head J, Ferrie JE, Shipley MJ, Brunner E, Vahtera J, Marmot MG. Work stress, weight gain and weight loss: evidence for bidirectional effects of job strain on body mass index in the Whitehall II study. Int J Obes (Lond) 30: 982-987, 2006. (Pubitemid 43801200)
26. Kohno H, Ohkubo Y. Comparative glucoregulatory responses of mice to restraint and footshock stress stimuli. Biol Pharm Bull 21: 113-116, 1998. (Pubitemid 28120138)
27. Lang CH, Silvis C, Nystrom G, Frost RA. Regulation of myostatin by glucocorticoids after thermal injury. FASEB J 15: 1807-1809, 2001.
28. Laugero KD, Moberg GP. Energetic response to repeated restraint stress in rapidly growing mice. Am J Physiol Endocrinol Metab 279: E33-E43, 2000.
29. Laugero KD, Moberg GP. Effects of acute behavioral stress and LPS-induced cytokine release on growth and energetics in mice. Physiol Behav 68: 415-422, 2000.
30. Lee DL, Webb RC, Brands MW. Sympathetic and angiotensin-dependent hypertension during cage-switch stress in mice. Am J Physiol Regul Integr Comp Physiol 287: R1394-R1398, 2004.
31. Lee DL, Leite R, Fleming C, Pollock JS, Webb RC, Brands MW. Hypertensive response to acute stress is attenuated in interleukin-6 knockout mice. Hypertension 44: 259-263, 2004. (Pubitemid 39167220)
32. Ma K, Mallidis C, Artaza J, Taylor W, Gonzalez-Cadavid N, Bhasin S. Characterization of 5′-regulatory region of human myostatin gene: regulation by dexamethasone in vitro. Am J Physiol Endocrinol Metab 281: E1128-E1136, 2001.
33. Ma K, Mallidis C, Bhasin S, Mahabadi V, Artaza J, Gonzalez-Cadavid N, Arias J, Salehian B. Glucocorticoid-induced skeletal muscle atrophy is associated with upregulation of myostatin gene expression. Am J Physiol Endocrinol Metab 285: E363-E371, 2003.
34. Martrette JM, Hartmann N, Westphal A, Favot L. Effect of glucocorticoid receptor ligands on myosin heavy chains expression in rat skeletal muscles during controllable stress. J Muscle Res Cell Motil 25: 297-302, 2004. (Pubitemid 40941088)
35. McFarlane C, Plummer E, Thomas M, Hennebry A, Ashby M, Ling N, Smith H, Sharma M, Kambadur R. Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaB-independent, FoxO1-dependent mechanism. J Cell Physiol 209: 501-514, 2006. (Pubitemid 44484641)
36. McPherron AC, Lee SJ. Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94: 12457-12461, 1997.
37. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387: 83-90, 1997.
38. Menconi M, Gonnella P, Petkova V, Lecker S, Hasselgren PO. Dexamethasone and corticosterone induce similar, but not identical, muscle wasting responses in cultured L6 and C2C12 myotubes. J Cell Biochem 105: 353-364, 2008.
39. Morissette MR, Cook SA, Buranasombati C, Rosenberg MA, Rosenzweig A. Myostatin inhibits IGF-I-induced myotube hypertrophy through Akt. Am J Physiol Cell Physiol 297: C1124-C1132, 2009.
40. Nishimura M, Mikura M, Hirasaka K, Okumura Y, Nikawa T, Kawano Y, Nakayama M, Ikeda M. Effects of dimethyl sulphoxide and dexamethasone on mRNA expression of myogenesis- and muscle proteolytic system-related genes in mouse myoblastic C2C12 cells. J Biochem 144: 717-724, 2008.
41. Ploutz-Snyder LL, Tesch PA, Hather BM, Dudley GA. Vulnerability to dysfunction and muscle injury after unloading. Arch Phys Med Rehabil 77: 773-777, 1996.
42. Riley DA, Thompson JL, Krippendorf BB, Slocum GR. Review of spaceflight and hindlimb suspension unloading induced sarcomere damage and repair. Basic Appl Myol 5: 139-145, 1995.
43. Schuelke M, Wagner KR, Stolz LE, Hubner C, Riebel T, Komen W, Braun T, Tobin JF, Lee SJ. Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med 350: 2682-2688, 2004. (Pubitemid 38788003)
44. Surwit RS, Schneider MS, Feinglos MN. Stress and diabetes mellitus. Diabetes Care 15: 1413-1422, 1992.
45. Surwit RS, Schneider MS. Role of stress in the etiology and treatment of diabetes mellitus. Psychosom Med 55: 380-393, 1993. (Pubitemid 23216233)
46. Swiergiel AH, Leskov IL, Dunn AJ. Effects of chronic and acute stressors and CRF on depression-like behavior in mice. Behav Brain Res 186: 32-40, 2008.
47. Tamashiro KL, Hegeman MA, Sakai RR. Chronic social stress in a changing dietary environment. Physiol Behav 89: 536-542, 2006. (Pubitemid 44634571)
48. Tamashiro KL, Hegeman MA, Nguyen MM, Melhorn SJ, Ma LY, Woods SC, Sakai RR. Dynamic body weight and body composition changes in response to subordination stress. Physiol Behav 91: 440-448, 2007. (Pubitemid 47016539)
49. Thaker PH, Lutgendorf SK, Sood AK. The neuroendocrine impact of chronic stress on cancer. Cell Cycle 6: 430-433, 2007. (Pubitemid 46393445)
50. Torres SJ, Nowson CA. Relationship between stress, eating behavior, and obesity. Nutrition 23: 887-894, 2007.
51. Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ. Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol 296: C1258-C1270, 2009.
52. Waddell DS, Baehr LM, van den Brandt J, Johnsen SA, Reichardt HM, Furlow JD, Bodine SC. The glucocorticoid receptor and FOXO1 synergistically activate the skeletal muscle atrophy-associated MuRF1 gene. Am J Physiol Endocrinol Metab 295: E785-E797, 2008.
53. Watanabe T, Hashimoto M, Okuyama S, Inagami T, Nakamura S. Effects of targeted disruption of the mouse angiotensin II type 2 receptor gene on stress-induced hyperthermia. J Physiol 515: 881-885, 1999. (Pubitemid 29140120)
54. Wernstedt I, Edgley A, Berndtsson A, Fäldt J, Bergström G, Wallenius V, Jansson JO. Reduced stress- and cold-induced increase in energy expenditure in interleukin-6-deficient mice. Am J Physiol Regul Integr Comp Physiol 291: R551-R557, 2006. (Pubitemid 44352336)