CaMKII activity is reduced in skeletal muscle during sepsis

Journal of Cellular Biochemistry

Volumn 114, Issue 6, 2013, Pages 1294-1305

  Aversa, Zaira ^a,b   Alamdari, Nima ^a   Castillero, Estibaliz ^a   Muscaritoli, Maurizio ^b   Fanelli, Filippo Rossi ^b   Hasselgren, Per Olof ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

Author keywords

Atrogin 1; Camkii; GSK 3 ; MuRF1; Muscle Wasting; Sepsis

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II BETA; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II DELTA; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II GAMMA; GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN SERINE THREONINE KINASE; RECOMBINANT TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CECAL LIGATION AND PUNCTURE; CELL CULTURE; CONTROLLED STUDY; ENZYME ACTIVITY; LIGATION; MALE; MUSCLE ATROPHY; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; PUNCTURE; RAT; SEPSIS; SKELETAL MUSCLE;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL LINE; GENE EXPRESSION; GLYCOGEN SYNTHASE KINASE 3; MALE; MUSCLE FIBERS, FAST-TWITCH; MUSCLE, SKELETAL; PERITONITIS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; SEPSIS; SERUM RESPONSE FACTOR;

RATTUS;

EID: 84876212670     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24469     Document Type: Article

References (63)

1. Abraham ST, Shaw C,. 2006. Increased expression of δCaMKII isoforms in skeletal muscle regeneration: Implications in dystrophic muscle disease. J Cell Biochem 97: 621-632.
2. Alamdari N, Smith IJ, Aversa Z, Hasselgren PO,. 2010. Sepsis and glucocorticoids upregulate p300 and downregulate HDAC6 expression and activity in skeletal muscle. Am J Physiol Regul Integr Comp Physiol 299: R509-R520.
3. Alamdari N, Aversa Z, Castillero E, Gurav A, Petkova V, Tizio S, Hasselgren PO,. 2012. Resveratrol prevents dexamethasone-induced expression of the muscle atrophy-related ubiquitin ligases atrogin-1 and MuRF1 in cultured myotubes through a SIRT1-dependent mechanism. Biochem Biophys Res Commun 417: 528-533.
4. Aversa Z, Alamdari N, Hasselgren PO,. 2011. Molecules modulating gene transcription during muscle wasting in cancer, sepsis and other critical illness. Crit Rev Clin Lab Sci 48: 71-86.
5. Bayer KU, Schulman H,. 2001. Regulation of signal transduction by protein targeting: The case for CaMKII. Biochem Biophys Res Commun 289: 917-923.
6. Bayer KU, Lohler J, Harbers K,. 1996. An alternative, nonkinase product of the brain-specifically expressed Ca2+/calmodulin-dependent kinase IIα isoform gene in skeletal muscle. Mol Cell Biol 16: 29-36.
7. Bayer KU, Harbers K, Schulman H,. 1998. αKAP is an anchoring protein for a novel CaM kinase II isoform in skeletal muscle. EMBO J 17: 5598-5605.
8. Brozinik JT, Reynolds TH, Dean D, Cartee G, Cushman SW,. 1999. 1-[N,O-Bis-(5-isoquinolinesulphonyl)-N-methyl- L -tyrosyl]-4-phenylpiperazine (KN-62), an inhibitor of calcium-dependent calmodulin protein kinase II, inhibits both insulin- and hypoxia-stimulated glucose transport in skeletal muscle. Biochem J 339: 533-540.
9. Chin ER,. 2004. The role of calcium and calcium/calmodulin-dependent kinases in skeletal muscle plasticity and mitochondrial biogenesis. Proc Nutr Soc 63: 279-286.
10. Croissant JD, Kim JH, Eichele G, Goering L, Lough J, Prywes R, Schwartz RJ,. 1996. Avian serum response factor expression restricted primarily to muscle cell lineages is required for α-actin gene transcription. Dev Biol 177: 250-264.
11. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA,. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378: 785-789.
12. Dhar A, Castillo L,. 2011. Insulin resistance in critical illness. Curr Opin Pediatr 23: 269-274.
13. Doble BW, Woodgett JR,. 2003. GSK-3: Tricks of the trade for a multitasking kinase. J Cell Sci 116: 1175-1186.
14. Erondu NE, Kennedy MB,. 1985. Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain. J Neurosci 5: 3270-3277.
15. Evenson AR, Menconi MJ, Mitchell JC, Hasselgren PO,. 2004. Dexamethasone increases protein degradation in cultured myotubes through a calcium-calmodulin kinase II (CaMK-II) dependent mechanism. J Surg Res 121: 277-278 (abstr).
16. Evenson AR, Fareed MU, Menconi MJ, Mitchell JC, Hasselgren PO,. 2005. GSK-3β inhibitors reduce protein degradation in muscles from septic rats and in dexamethasone-treated myotubes. Int J Biochem Cell Biol 37: 2226-2238.
17. Fluck M, Booth FW, Waxham MN,. 2000a. Skeletal muscle CaMKII enriches in nuclei and phosphorylates myogenic factor SRF at multiple sites. Biochem Biophys Res Commun 270: 488-494.
18. Fluck M, Waxham MN, Hamilton MT, Booth FW,. 2000b. Skeletal muscle Ca2+-independent kinase activity increases during either hypertrophy or running. J Appl Physiol 88: 352-358.
19. Fredriksson K, Rooyackers O,. 2007. Mitochondrial function in sepsis: Respiratory versus leg muscle. Crit Care Med 35: S449-S453.
20. Gonnella P, Alamdari N, Tizio S, Aversa Z, Petkova V, Hasselgren PO,. 2011. C/EBPβ regulates dexamethasone-induced muscle cell atrophy and expression of atrogin-1 and MuRF1. J Cell Biochem 112: 1737-1748.
21. Hasselgren PO, James JH, Benson DW, Hall-Angeras M, Angeras U, Hiyama DT, Li S, Fischer JE,. 1989. Total and myofibrillar protein breakdown in different types of rat skeletal muscle: Effects of sepsis and regulation by insulin. Metabolism 38: 634-640.
22. Hasselgren PO, Alamdari N, Aversa Z, Gonnella P, Smith IJ, Tizio S,. 2010. Corticosteroids and muscle wasting-Role of transcription factors, nuclear cofactors, and hyperacetylation. Curr Opin Clin Nutr Metabol Care 13: 423-428.
23. Heidenreich O, Neininger A, Schratt G, Zinck R, Cahill MA, Eagel K, Kotlyarov A, Kraft R, Kostka S, Gaestel M, Nordheim A,. 1999. MAPKAP kinase 2 phosphorylates serum response factor in vitro and in vivo. J Biol Chem 274: 14434-14443.
24. Hudmon A, Schulman H,. 2002. Structure-function of the multifunctional Ca2+/calmodulin-dependent protein kinase II. Biochem J 364: 593-611.
25. Illario M, Monaco S, Cavallo AL, Esposito I, Formisano P, D'Andrea L, Cipolletta E, Trimarco B, Fenzi G, Rossi G, Vitale M,. 2009. Calcium-calmodulin-dependent kinase II (CaMKII) mediates insulin-stimulated proliferation and glucose uptake. Cell Signal 21: 786-792.
26. Klaude M, Mori M, Tjader I, Gustafsson T, Wernerman J, Rooyackers O,. 2012. Protein metabolism and gene expression in skeletal muscle of critically ill patients with sepsis. Clin Sci 122: 133-142.
27. Kwiatowski AP, King MM,. 1989. Autophosphorylation of the type II calmodulin-dependent protein kinase is essential for formation of a proteolytic fragment with catalytic activity. Implications for long-term synaptic potentiation. Biochemistry 28: 5380-5385.
28. Ladner KJ, Caligiuri MA, Guttridge DC,. 2003. Tumor necrosis factor-regulated biphasic activation of NF-kB is required for cytokine-induced loss of skeletal muscle gene products. J Biol Chem 278: 2294-2303.
29. Lecker SH, Goldberg AL, Mitch WE,. 2006. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 17: 1807-1819.
30. Macpherson P, Kostrominova T, Tang H, Goldman D,. 2002. Protein kinase C and calcium/calmodulin-activated protein kinase II (CaMKII) suppresses nicotinic acetylcholine receptor gene expression in mammalian muscle. A specific role for CaMKII in activity-dependent gene expression. J Biol Chem 277: 15638-15646.
31. Means AR,. 2000. Regulatory cascades involving calmodulin-dependent protein kinases. Mol Endocrinol 14: 4-13.
32. Menconi M, Wei W, Yang H, Wray C, Hasselgren PO,. 2004. Treatment of cultured myotubes with the calcium ionophore A23187 increases proteasome activity via a CaMK-II-caspase-calpain-dependent mechanism. Surgery 136: 135-142.
33. Menconi M, Gonnella P, Petkova V, Lecker S, Hasselgren PO,. 2008. Dexamethasone and corticosterone induce similar, but not identical muscle wasting responses in cultured L6 and C2C12 myotubes. J Cell Biochem 105: 353-364.
34. Menconi MJ, Arany ZP, Alamdari N, Aversa Z, Gonnella P, O'Neal P, Smith I, Tizio S, Hasselgren PO,. 2010. Sepsis and glucocorticoids downregulate the expression of the nuclear cofactor PGC-1beta in skeletal muscle. Am J Physiol Endocrinol Metab 299: E533-E543.
35. Meyer T, Hanson PI, Stryer L, Schulman H,. 1992. Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science 256: 1199-1201.
36. Miller SG, Kennedy MB,. 1986. Regulation of brain type II Ca2+/calmodulin-dependent protein kinase by autophosporylation: A Ca2 + -triggered switch. Cell 44: 861-870.
37. O'Leary H, Sui X, Lin PJ, Volpe P, Bayer KU,. 2006. Nuclear targeting of the CaMKII anchoring protein αKAP is regulated by alternative splicing and protein kinases. Brain Res 1086: 17-26.
38. Park HK, Qatanani M, Briggs ER, Ahima RS, Lazar MA,. 2011. Inflammatory induction of human resistin causes insulin resistance in endotoxemic mice. Diabetes 60: 775-783.
39. Rivera VM, Miranti CK, Misra RP, Ginty DD, Chen RH, Blenis J, Greenberg ME,. 1993. A growth factor-induced kinase phosphorylates the serum response factor at a site that regulates its DNA-binding activity. Mol Cell Biol 13: 6260-6273.
40. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ,. 2001. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat Cell Biol 3: 1009-1013.
41. Rose AJ, Hargreaves M,. 2003. Exercise increases Ca2+-calmodulin- dependent protein kinase II activity in human skeletal muscle. J Physiol 553 (1): 303-309.
42. Rose AJ, Kiens B, Richter EA,. 2006. Ca2+-calmodulin-dependent protein kinase expression and signaling in skeletal muscle during exercise. J Physiol 574: 889-903.
43. Rose AJ, Alsted TJ, Kobbero JB, Richter EA,. 2007. Regulation and function of Ca2+-calmodulin-dependent protein kinase II of fast-twitch rat skeletal muscle. J Physiol 580 (3): 993-1005.
44. Sacchetto R, Bovo E, Damiani E,. 2005. The Ca2+-calmodulin dependent protein kinase II system of skeletal muscle sarcoplasmic reticulum. Basic Appl Myol 15: 5-17.
45. Schakman O, Gilson H, Thissen JP,. 2008. Mechanisms of glucocorticoid-induced myopathy. J Endocrinol 197: 1-10.
46. Singh P, Salih M, Tuana BS,. 2009. α-Kinase anchoring protein αKAP interacts with SERCA2A to spatially position Ca2+/calmodulin- dependent protein kinase II and modulate phospholamban phosphorylation. J Biol Chem 284: 28212-28221.
47. Singla SI, Hudmon A, Goldberg JM, Smith JL, Schulman H,. 2001. Molecular characterization of calmodulin trapping by calcium/calmodulin-dependent protein kinase II. J Biol Chem 276: 29353-29360.
48. Smith JAH, Kohn TA, Chetty AK, Ojuka EO,. 2008. CaMK activation during exercise is required for histone hyperacetylation and MEF2A binding at the MEF2 site on the Glut 4 gene. Am J Physiol Endocrinol Metab 295: E698-E704.
49. Soderling TR, Stull JT,. 2001. Structure and regulation of calcium/calmodulin-dependent protein kinases. Chem Rev 101: 2341-2351.
50. Song B, Lai B, Zheng Z, Zhang Y, Luo J, Wang C, Chen Y, Woodgett JR, Li M,. 2010. Inhibitory phosphorylation of GSK-3 by CaMKII couples depolarization to neuronal survival. J Biol Chem 285: 41122-41134.
51. Soulez M, Tuil D, Kahn A, Gilgenkrantz H,. 1996. The serum response factor (SRF) is needed for muscle-specific activation of CArG boxes. Biochem Biophys Res Commun 219: 418-422.
52. Stephens NA, Gallagher IJ, Rooyackers O, Skipworth RJ, Tan BH, Marstrand T, Ross JA, Guttridge DC, Lundell L, Fearon KC, Timmons JA,. 2010. Using transcriptomics to identify and validate novel biomarkers of human skeletal muscle cancer cachexia. Genome Med 2: 1-12.
53. Tiao G, Fagan JM, Samuels N, James JH, Hudson K, Lieberman M, Fischer JE, Hasselgren PO,. 1994. Sepsis stimulates nonlysosomal, energy-dependent proteolysis and increases ubiquitin mRNA levels in rat skeletal muscle. J Clin Invest 94: 2255-2264.
54. Tiao G, Fagan J, Roegner V, Lieberman M, Wang JJ, Fischer JE, Hasselgren PO,. 1996. Energy-ubiquitin-dependent muscle proteolysis during sepsis in rats is regulated by glucocorticoids. J Clin Invest 97: 339-348.
55. Tiao G, Lieberman MA, Fischer JE, Hasselgren PO,. 1997. Intracellular regulation of protein degradation during sepsis is different in fast- and slow-twitch muscle. Am J Physiol Regul Integr Comp Physiol 272: R849-R856.
56. Vanasco V, Cimolai MC, Evelson P, Alvarez S,. 2008. The oxidative stress and the mitochondrial dysfunction caused by endotoxin are prevented by alpha-lipoc acid. Free Radic Res 42: 815-823.
57. Vyas DR, Spangenburg EE, Abraha TW, Childs TE, Booth FW,. 2002. GSK-3β negatively regulates skeletal myotube hypertrophy. Am J Physiol Cell Physiol 283: C545-C551.
58. Wang X, Hu Z, Hu J, Du J, Mitch WE,. 2006. Insulin resistance accelerates muscle protein degradation: Activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling. Endocrinology 147: 4160-4168.
59. Witczak CA, Jessen N, Warro DM, Toyoda T, Fujii N, Anderson ME, Hirshman MF, Goodyear LJ,. 2010. CaMKII regulates contraction-induced, but not insulin-induced, glucose uptake in mouse skeletal muscle. Am J Physiol Endocrinol Metab 298: E1150-E1160.
60. Wray CJ, Mammen JMV, Hershko D, Hasselgren PO,. 2003. Sepsis upregulates the gene expression of multiple ubiquitin ligases in skeletal muscle. Int J Biochem Cell Biol 35: 698-705.
61. Wright DC, Fick CA, Olesen JB, Lim K, Barnes BR, Craig BW,. 2004. A role for calcium/calmodulin kinase in insulin stimulated glucose transport. Life Sci 74: 815-825.
62. Zamir O, Hasselgren PO, Higashiguchi T, Frederick JA, Fischer JE,. 1992a. Tumor necrosis factor (TNF) and interleukin-1 (IL-1) induce muscle proteolysis through different mechanisms. Mediat Inflam 1: 247-250.
63. Zamir O, Hasselgren PO, Kunkel SL, Frederick J, Higashiguchi T, Fischer JE,. 1992b. Evidence that tumor necrosis factor participates in the regulation of muscle proteolysis during sepsis. Arch Surg 127: 170-174.