Apoptosis and myostatin mRNA are upregulated in the skeletal muscle of patients with chronic kidney disease

Kidney International

Volumn 79, Issue 7, 2011, Pages 773-782

  Verzola, Daniela ^a   Procopio, Vanessa ^a   Sofia, Antonella ^a   Villaggio, Barbara ^a   Tarroni, Alice ^a   Bonanni, Alice ^a   Mannucci, Irene ^a   De Cian, Franco ^b   Gianetta, Ezio ^b   Saffioti, Stefano ^a   Garibotto, Giacomo ^a,c  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c Division of Nephrology   (Italy)

Author keywords

Akt; apoptosis; chronic renal disease; myostatin; protein energy wasting

Indexed keywords

INTERLEUKIN 6; MESSENGER RNA; MYOSTATIN; PROTEIN C JUN; PROTEIN KINASE B; SINGLE STRANDED DNA; SOMATOMEDIN C; STRESS ACTIVATED PROTEIN KINASE;

ADULT; AGED; APOPTOSIS; ARTICLE; CHRONIC KIDNEY DISEASE; CLINICAL ARTICLE; CONTROLLED STUDY; DNA FRAGMENTATION; DOWN REGULATION; FEMALE; GENE EXPRESSION REGULATION; HUMAN; MALE; MUSCLE BIOPSY; NICK END LABELING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RECTUS ABDOMINIS MUSCLE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION;

EID: 79952697136     PISSN: 00852538     EISSN: 15231755     Source Type: Journal    
DOI: 10.1038/ki.2010.494     Document Type: Article

References (53)

1. Yoo KH, Kovesdy CP, Kalantar-Zadeh K. Why is protein-energy wasting associated with mortality in chronic kidney disease? Semin Nephrol 2009; 29: 3-14.
2. Kopple JD, Greene T, Chumlea WC et al. Relationship between nutritional status and the glomerular filtration rate: results from the MDRD study. Kidney Int 2000; 57: 1688-1703. (Pubitemid 30207928)
3. Lim VS, Kopple JD. Protein metabolism in patients with chronic renal failure: role of uraemia and dialysis. Kidney Int 2000; 58: 1-10. (Pubitemid 30429844)
4. Mitch WE. Malnutrition: a frequent misdiagnosis for hemodialysis patients. J Clin Invest 2002; 110: 437-439. (Pubitemid 34919696)
5. Stevinkel P, Heimburger O, Lindholm B. Wasting, but not malnutrition, predicts cardiovascular mortality in end-stage renal disease. Nephrol Dial Transpl 2004; 19: 2181-2183. (Pubitemid 39214108)
6. Mitch WE, Goldberg AL. Mechanisms of muscle wasting: the role of ubiquitin-proteasome system. N Engl J Med 1996; 335: 1897-1905. (Pubitemid 26419198)
7. Lecker SH, Goldberg AL, Mitch WE. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 2006; 17: 1807-1819. (Pubitemid 44036165)
8. Du J, Wang X, Meireles CL et al. Activation of caspase-3 is an initial step triggering muscle proteolysis in catabolic conditions. J Clin Invest 2004; 113: 115-123. (Pubitemid 38541638)
9. Bailey JL, Price SR, Zheng B et al. Chronic kidney disease causes defects in signaling through the insulin receptor substrate/phosphatidylinositol 3-kinase/Akt pathway: implications for muscle atrophy. J Am Soc Nephrol 2006; 17: 1388-1394. (Pubitemid 43673419)
10. Workeneh BT, Mitch WE. Review of muscle wasting associated with chronic kidney disease. Am J Clin Nutr 2010; 91: 1128S-1132S.
11. Dupont-Versteegden EE. Apoptosis in skeletal muscle and its relevance to atrophy. World J Gastroenterol 2006; 12: 7463-7466. (Pubitemid 46017743)
12. Gundersen K, Bruusgaard JC. Nuclear domains during muscle atrophy: nuclei lost or paradigm lost? J Physiol 2008; 586: 2675-2681. (Pubitemid 351766595)
13. Frost RA, Lang CH. Protein kinase B/Akt: a nexus of growth factor and cytokine signaling in determining muscle mass. J Appl Physiol 2007; 103: 378-387. (Pubitemid 47092315)
14. Yamaguchi H, Wang H-G. The protein kinase PKB/Akt regulates cell servival and apoptosis by inhibiting Bax conformational change. Oncogene 2001; 20: 7779-7786. (Pubitemid 33121951)
15. Lee SW, Dai G, Hu Z et al. Regulation of muscle protein degradation: coordinated control of apoptotic and ubiquitin-proteasome systems by phosphatidynositol-3-kinase. J Am Soc Nephrol 2004; 15: 1537-1545. (Pubitemid 38679678)
16. Zhang L, Wang XH, Wang H et al. Satellite cell dysfunction and impaired IGF-I signaling cause CKD-induced muscle atrophy. J Am Soc Nephrol 2010; 21: 419-427.
17. Glass DJ. Skeletal muscle hypertrophy and blocking atrophy signaling pathways. Int J Biochem Cell Biol 2005; 37: 1974-1984. (Pubitemid 41206815)
18. Sun DF, Chen Y, Rabkin R. Work-induced changes in skeletal muscle IGF-I and myostatin gene expression in uraemia. Kidney Int 2006; 70: 453-459. (Pubitemid 44141571)
19. Cheung WW, Rosengren S, Boyle DL et al. Modulation of melanocortin signaling ameliorates uremic cachexia. Kidney Int 2008; 74: 180-186. (Pubitemid 351915082)
20. Gonzalez-Cadavid NF, Taylor WE, Yarasheski K et al. Organization of the human myostatin gene and expression in healthy men and HIV-infected men with muscle wasting. Proc Natl Acad Sci USA 1998; 95: 14938-14949.
21. Reardon KA, Davis J, Kapsa RM et al. Myostatin, insulin-like growth factor-1, and leukemia inhibitory factor mRNAs are upregulated in chronic human disuse muscle atrophy. Muscle Nerve 2001; 24: 893-899. (Pubitemid 32549972)
22. Wang H, Casaburi R, Taylor WE et al. Skeletal muscle mRNA for IGF-IEa, IGF-II, and IGF-I receptor is decreased in sedentary chronic hemodialysis patients. Kidney Int 2005; 68: 352-361. (Pubitemid 43181395)
23. Frankfurt OS, Robb JA, Sugarbaker EV. Monoclonal Ab to single-stranded DNA is a specific and sensitive cellular marker of apoptosis. Exp Cell Res 1996; 226: 387-397. (Pubitemid 26260564)
24. Frankfurt OS. Repair protocols. Eukaryotic systems. Methods Mol Biol 1999; 113: 621-631.
25. Hawke TJ, Garry DJ. Myogenic satellite cells: physiology to molecular biology. J Appl Physiol 2001; 91: 534-551. (Pubitemid 32681081)
26. Garibotto G, Sofia A, Procopio V et al. Peripheral tissue release of interleukin-6 in patients with chronic kidney diseases: effects of end-stage renal disease and microinflammatory state. Kidney Int 2006; 70: 384-390. (Pubitemid 44086590)
27. Braga M, Sinha Hikim AP, Datta S et al. Involvement of oxidative stress and caspase 2-mediated intrinsic pathway signaling in age-related increase in muscle cell apoptosis in mice. Apoptosis 2008; 13: 822-883.
28. Sinha-Hikim I, Braga M, Shen R et al. Involvement of c-Jun NH2 -terminal kinase and nitric oxide-mediated mitochondria-dependent intrinsic pathway signaling in cardiotoxin-induced muscle cell death: role of testosterone. Apoptosis 2007; 12: 1965-1978. (Pubitemid 47498228)
29. McClung JM, Kavazis AN, Whidden MA et al. Antioxidant administration attenuates mechanical ventilation-induced rat diaphragm muscle atrophy independent of protein kinase B (PKB/Akt) signalling. J Physiol 2007; 585: 203-215. (Pubitemid 350131113)
30. Jejurikar SS, Henkelman EA, Cederna PS. Aging increases the susceptibility of skeletal muscle derived satellite cells to apoptosis. Exp Gerontol 2006; 41: 828-836. (Pubitemid 44557021)
31. Dupont-Versteegden EE. Apoptosis in muscle atrophy: relevance to sarcopenia. Exp Gerontol 2005; 40: 473-481. (Pubitemid 40884500)
32. Sandri M. Apoptotic signaling in skeletal muscle fibers during atrophy. Curr Opin Clin Nutr Metab Care 2002; 5: 249-253. (Pubitemid 40684669)
33. Tews DS. Muscle fiber apoptosis in neuromuscular diseases. Muscle Nerve 2005; 32: 443-458. (Pubitemid 41395978)
34. Hall ZW, Ralston E. Nuclear domains in muscle cells. Cell 1989; 59: 771-772. (Pubitemid 20022367)
35. Gundersen K, Sanes JR, Merlie JP. Neural regulation of muscle acetylcholine receptor epsilon- and alpha-subunit gene promoters in transgenic mice. J Cell Biol 1993; 123: 1535-1544. (Pubitemid 24012030)
36. Li LY, Luo X, Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 2001; 412: 95-99. (Pubitemid 32851517)
37. Bassel-Duby R, Olson EN. Signaling pathways in skeletal muscle remodeling. Annu Rev Biochem 2006; 75: 19-37. (Pubitemid 44118024)
38. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 1997; 387: 83-90. (Pubitemid 27202654)
39. Glass DJ. Signaling pathways perturbing muscle mass. Curr Opin Clin Nutr Metab Care 2010; 13: 225-229.
40. Lightfoot A, McArdle A, Griffiths RD. Muscle in defense. Crit Care Med 2009; 37(10 Suppl): S384-S390.
41. Shah VO, Dominic EA, Moseley P et al. Hemodialysis modulates gene expression profile in skeletal muscle. Am J Kidney Dis 2006; 48: 616-628. (Pubitemid 44425373)
42. Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 2009; 88: 1379-1406.
43. Varma V, Yao-Borengasser A, Rasouli N et al. Muscle inflammatory response and insulin resistance: synergistic interaction between macrophages and fatty acids leads to impaired insulin action. Am J Physiol Endocrinol Metab 2009; 296: E1300-E1310.
44. Sabio G, Kennedy NJ, Cavanagh-Kyros J et al. Role of muscle c-Jun NH2-terminal kinase 1 in obesity-induced insulin resistance. Mol Cell Biol 2010; 30: 106-115.
45. Hilder TL, Tou JC, Grindeland RE et al. Phosphorylation of insulin receptor substrate-1 serine 307 correlates with JNK activity in atrophic skeletal muscle. FEBS Lett 2003; 553: 63-67. (Pubitemid 37206325)
46. Huang Z, Chen D, Zhang K et al. Regulation of myostatin signaling by c-Jun N-terminal kinase in C2C12 cells. Cell Signal 2007; 19: 2286-2295. (Pubitemid 47361684)
47. Alen DL, Linderman JK, Roy RR et al. Apoptosis: a mechanism contributing to remodeling of skeletal muscle in response to hindlimb unweighting. Am J Physiol 1997; 273: C579-C587.
48. Kopple JD, Cohen AH, Wang H et al. Effect of exercise on mRNA levels for growth factors in skeletal muscle of hemodialysis patients. J Ren Nutr 2006; 16: 312-324. (Pubitemid 44548401)
49. Podhorska-Okolow M, Sandri M, Zampieri S et al. Apoptosis of myofibres and satellite cells: exercise-induced damage in skeletal muscle of the mouse. Neuropathol Appl Neurobiol 1998; 24: 518-531. (Pubitemid 29002283)
50. Siu PM, Pistilli EE, Butler DC et al. Aging influences cellular and molecular responses of apoptosis to skeletal muscle unloading. Am J Physiol Cell Physiol 2005; 288: C338-C349. (Pubitemid 40105345)
51. Dupont-Versteegden EE, Strotman BA, Gurley CM et al. Nuclear translocation of EndoG at the initiation of disuse muscle atrophy and apoptosis is specific to myonuclei. Am J Physiol Regul Integr Comp Physiol 2006; 291: R1730-R1740. (Pubitemid 44904141)
52. Verzola D, Gandolfo MT, Ferrario F et al. Apoptosis in the kidneys of patients with type II diabetic nephropathy. Kidney Int 2007; 72: 1262-1272. (Pubitemid 350059668)
53. Verzola D, Bertolotto MB, Villaggio B et al. Taurine prevents apoptosis induced by high ambient glucose in human tubule renal cells. J Investig Med 2002; 50: 443-451. (Pubitemid 35278685)