Regulation of GLUT4 expression in denervated skeletal muscle

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 296, Issue 6, 2009, Pages

  Jensen, Ellis B ^a   Zheng, Donghai ^b   Russell, Robert A ^c   Bassel Duby, Rhonda ^d   Sanders Williams, R ^e   Olson, Ann Louise ^c   Lynis Dohm, G ^b  

^a VITERBO UNIVERSITY   (United States)

^b EAST CAROLINA UNIVERSITY   (United States)

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

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^e DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Denervation; Exercise; Glucose; GLUT4 enhancer factor; Myocyte enhancer factor 2

Indexed keywords

CHLORAMPHENICOL ACETYLTRANSFERASE; GLUCOSE TRANSPORTER 4; MYOCYTE ENHANCER FACTOR 2;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; MOUSE; MUSCLE DENERVATION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; REPORTER GENE; SKELETAL MUSCLE;

ANIMALS; BINDING SITES; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 4; CHLORAMPHENICOL O-ACETYLTRANSFERASE; DNA-BINDING PROTEINS; DOWN-REGULATION; GENES, REPORTER; GLUCOSE TRANSPORTER TYPE 4; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE DENERVATION; MUSCLE, SKELETAL; MYOGENIC REGULATORY FACTORS; PROMOTER REGIONS, GENETIC; RNA, MESSENGER; SCIATIC NERVE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 67049160439     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.90651.2008     Document Type: Article

References (49)

1. 2+/calmodulin-dependent protein kinase IV-deficient mice. Am J Physiol Cell Physiol 287: C1311-C1319, 2004.
2. Block NE, Menick DR, Robinson KA, Buse MG. Effect of denervation on the expression of two glucose transporter isoforms in rat hindlimb muscle. J Clin Invest 88: 1546-1552, 1991.
3. Brozinick JT Jr, McCoid SC, Reynolds TH, Nardone NA, Hargrove DM, Stevenson RW, Cushman SW, Gibbs EM. GLUT4 overexpression in db/db mice dose-dependently ameliorates diabetes but is not a lifelong cure. Diabetes 50: 593-600, 2001. (Pubitemid 32195224)
4. Coderre L, Monfar MM, Chen KS, Heydrick SJ, Kurowski TG, Ruderman NB, Pilch PF. Alteration in the expression of GLUT-1 and GLUT-4 protein and messenger RNA levels in denervated rat muscles. Endocrinology 131: 1821-1825, 1992.
5. Eriksson J, Koranyi L, Bourey R, Schalin-Jantti C, Widen E, Mueckler M, Permutt AM, Groop LC. Insulin resistance in type 2 (non-insulin-dependent) diabetic patients and their relatives is not associated with a defect in the expression of the insulin-responsive glucose transporter (GLUT-4) gene in human skeletal muscle. Diabetologia 35: 143-147, 1992.
6. Ezaki O. Regulatory elements in the insulin-responsive glucose transporter (GLUT4) gene. Biochem Biophys Res Commun 241: 1-6, 1997. (Pubitemid 28033529)
7. Gibbs EM, Stock JL, McCoid SC, Stukenbrok HA, Pessin JE, Stevenson RW, Milici AJ, McNeish JD. Glycemic improvement in diabetic db/db mice by overexpression of the human insulin-regulatable glucose transporter (GLUT4). J Clin Invest 95: 1512-1518, 1995.
8. Grozinger CM, Schreiber SL. Regulation of histone deacetylase 4 and 5 and transcriptional activity by 14-3-3-dependent cellular localization. Proc Natl Acad Sci USA 97: 7835-7840, 2000. (Pubitemid 30460734)
9. Holmes BF, Lang DB, Birnbaum MJ, Mu J, Dohm GL. AMP kinase is not required for the GLUT4 response to exercise and denervation in skeletal muscle. Am J Physiol Endocrinol Metab 287: E739-E743, 2004. (Pubitemid 39237903)
10. Houmard JA, Egan PC, Neufer PD, Friedman JE, Wheeler WS, Israel RG, Dohm GL. Elevated skeletal muscle glucose transporter levels in exercise-trained middle-aged men. Am J Physiol Endocrinol Metab 261: E437-E443, 1991.
11. Houmard JA, Hickey MS, Tyndall GL, Gavigan KE, Dohm GL. Seven days of exercise increase GLUT-4 protein content in human skeletal muscle. J Appl Physiol 79: 1936-1938, 1995. (Pubitemid 26010562)
12. Houmard JA, Hortobagyi T, Neufer PD, Johns RA, Fraser DD, Israel RG, Dohm GL. Training cessation does not alter GLUT-4 protein levels in human skeletal muscle. J Appl Physiol 74: 776-781, 1993. (Pubitemid 23078174)
13. Houmard JA, Weidner MD, Dolan PL, Leggett-Frazier N, Gavigan KE, Hickey MS, Tyndall GL, Zheng D, Alshami A, Dohm GL. Skeletal muscle GLUT4 protein concentration and aging in humans. Diabetes 44: 555-560, 1995.
14. Hudmon A, Schulman H. Neuronal CA2+/calmodulin-dependent protein kinase II: the role of structure and autoregulation in cellular function. Annu Rev Biochem 71: 473-510, 2002. (Pubitemid 34800228)
15. Ikemoto S, Thompson KS, Takahashi M, Itakura H, Lane MD, Ezaki O. High fat diet-induced hyperglycemia: prevention by low level expression of a glucose transporter (GLUT4) minigene in transgenic mice. Proc Natl Acad Sci USA 92: 3096-3099, 1995.
16. Ishizuka T, Klepcyk P, Liu S, Panko L, Gibbs EM, Friedman JE. Effects of overexpression of human GLUT4 gene on maternal diabetes and fetal growth in spontaneous gestational diabetic C57BLKS/J Lepr(db/+) mice. Diabetes 48: 1061-1069, 1999. (Pubitemid 29226353)
17. Jones JP, Dohm GL. Regulation of glucose transporter GLUT-4 and hexokinase II gene transcription by insulin and epinephrine. Am J Physiol Endocrinol Metab 273: E682-E687, 1997. (Pubitemid 27475501)
18. Jones JP, Tapscott EB, Olson AL, Pessin JE, Dohm GL. Regulation of glucose transporters GLUT-4 and GLUT-1 gene transcription in denervated skeletal muscle. J Appl Physiol 84: 1661-1666, 1998. (Pubitemid 28225905)
19. Katz EB, Burcelin R, Tsao TS, Stenbit AE, Charron MJ. The metabolic consequences of altered glucose transporter expression in transgenic mice. J Mol Med 74: 639-652, 1996. (Pubitemid 26382250)
20. Koranyi LI, Bourey RE, Vuorinen-Markkola H, Koivisto VA, Mueckler M, Permutt MA, Yki-Jarvinen H. Level of skeletal muscle glucose transporter protein correlates with insulin-stimulated whole body glucose disposal in man. Diabetologia 34: 763-765, 1991.
21. Leturque A, Loizeau M, Vaulont S, Salminen M, Girard J. Improvement of insulin action in diabetic transgenic mice selectively overexpressing GLUT4 in skeletal muscle. Diabetes 45: 23-27, 1996. (Pubitemid 26010418)
22. Liu ML, Olson AL, Edgington NP, Moye-Rowley WS, Pessin JE. Myocyte enhancer factor 2 (MEF2) binding site is essential for C2C12 myotube-specific expression of the rat GLUT4/muscle-adipose facilitative glucose transporter gene. J Biol Chem 269: 28514-28521, 1994. (Pubitemid 24354600)
23. Liu ML, Olson AL, Moye-Rowley WS, Buse JB, Bell GI, Pessin JE. Expression and regulation of the human GLUT4/muscle-fat facilitative glucose transporter gene in transgenic mice. J Biol Chem 267: 11673-11676, 1992.
24. Liu Y, Randall WR, Schneider MF. Activity-dependent and -independent nuclear fluxes of HDAC4 mediated by different kinases in adult skeletal muscle. J Cell Biol 168: 887-897, 2005. (Pubitemid 40397003)
25. McGee SL, Sparling D, Olson AL, Hargreaves M. Exercise increases MEF2- and GEF DNA-binding activity in human skeletal muscle. FASEB J 20: 348-349, 2006. (Pubitemid 46671167)
26. McGee SL, van Denderen BJ, Howlett KF, Mollica J, Schertzer JD, Kemp BE, Hargreaves M. AMP-activated protein kinase regulates GLUT4 transcription by phosphorylating histone deacetylase 5. Diabetes 57: 860-867, 2008.
27. McKinsey TA, Zhang CL, Lu J, Olson EN. Signal-dependent nuclear export of a histone deacetylase regulates muscle differentiation. Nature 408: 106-111, 2000.
28. Megeney LA, Michel RN, Boudreau CS, Fernando PK, Prasad M, Tan MH, Bonen A. Regulation of muscle glucose transport and GLUT-4 by nerve-derived factors and activity-related processes. Am J Physiol Regul Integr Comp Physiol 269: R1148-R1153, 1995. (Pubitemid 3006003)
29. Megeney LA, Neufer PD, Dohm GL, Tan MH, Blewett CA, Elder GC, Bonen A. Effects of muscle activity and fiber composition on glucose transport and GLUT-4. Am J Physiol Endocrinol Metab 264: E583-E593, 1993. (Pubitemid 23118171)
30. Muoio DM, Way JM, Tanner CJ, Winegar DA, Kliewer SA, Houmard JA, Kraus WE, Dohm GL. Peroxisome proliferator-activated receptor-alpha regulates fatty acid utilization in primary human skeletal muscle cells. Diabetes 51: 901-909, 2002. (Pubitemid 34438329)
31. Naya FJ, Wu C, Richardson JA, Overbeek P, Olson EN. Transcriptional activity of MEF2 during mouse embryogenesis monitored with a MEF2-dependent transgene. Development 126: 2045-2052, 1999. (Pubitemid 29271690)
32. Olson AL, Pessin JE. Transcriptional regulation of the human GLUT4 gene promoter in diabetic transgenic mice. J Biol Chem 270: 23491-23495, 1995.
33. Oshel KM, Knight JB, Cao KT, Thai MV, Olson AL. Identification of a 30-base pair regulatory element and novel DNA binding protein that regulates the human GLUT4 promoter in transgenic mice. J Biol Chem 275: 23666-23673, 2000. (Pubitemid 30624651)
34. Passier R, Zeng H, Frey N, Naya FJ, Nicol RL, McKinsey TA, Overbeek P, Richardson JA, Grant SR, Olson EN. CaM kinase signaling induces cardiac hypertrophy and activates the MEF2 transcription factor in vivo. J Clin Invest 105: 1395-1406, 2000. (Pubitemid 30322405)
35. Ren JM, Marshall BA, Mueckler MM, McCaleb M, Amatruda JM, Shulman GI. Overexpression of Glut4 protein in muscle increases basal and insulin-stimulated whole body glucose disposal in conscious mice. J Clin Invest 95: 429-432, 1995.
36. 2+-calmodulin- dependent protein kinase II activity in human skeletal muscle. J Physiol 553: 303-309, 2003.
37. 2+-calmodulin-dependent protein kinase expression and signalling in skeletal muscle during exercise. J Physiol 574: 889-903, 2006.
38. Santalucia T, Moreno H, Palacin M, Yacoub MH, Brand NJ, Zorzano A. A novel functional co-operation between MyoD, MEF2 and TRα1 is sufficient for the induction of GLUT4 gene transcription. J Mol Biol 314: 195-204, 2001. (Pubitemid 33105086)
39. Sigma-Aldrich. Calcium and Calmodulin-Dependent Protein Kinases Overview. St. Louis, MO: Sigma-Aldrich (Online).
40. Smith JA, Collins M, Grobler LA, Magee CJ, Ojuka EO. Exercise and CaMK activation both increase the binding of MEF2A to the GLUT4 promoter in skeletal muscle in vivo. Am J Physiol Endocrinol Metab 292: E413-E420, 2007. (Pubitemid 46220565)
41. Thai MV, Guruswamy S, Cao KT, Pessin JE, Olson AL. Myocyte enhancer factor 2 (MEF2)-binding site is required for GLUT4 gene expression in transgenic mice. Regulation of MEF2 DNA binding activity in insulin-deficient diabetes. J Biol Chem 273: 14285-14292, 1998. (Pubitemid 28319143)
42. Treadway JL, Hargrove DM, Nardone NA, McPherson RK, Russo JF, Milici AJ, Stukenbrok HA, Gibbs EM, Stevenson RW, Pessin JE. Enhanced peripheral glucose utilization in transgenic mice expressing the human GLUT4 gene. J Biol Chem 269: 29956-29961, 1994. (Pubitemid 24365165)
43. Tsao TS, Burcelin R, Katz EB, Huang L, Charron MJ. Enhanced insulin action due to targeted GLUT4 overexpression exclusively in muscle. Diabetes 45: 28-36, 1996. (Pubitemid 26010419)
44. Wang AH, Kruhlak MJ, Wu J, Bertos NR, Vezmar M, Posner BI, Bazett-Jones DP, Yang XJ. Regulation of histone deacetylase 4 by binding of 14-3-3 proteins. Mol Cell Biol 20: 6904-6912, 2000.
45. Winder WW, Taylor EB, Thomson DM. Role of AMP-activated protein kinase in the molecular adaptation to endurance exercise. Med Sci Sports Exerc 38: 1945-1949, 2006. (Pubitemid 44707799)
46. Wu H, Kanatous SB, Thurmond FA, Gallardo T, Isotani E, Bassel-Duby R, Williams RS. Regulation of mitochondrial biogenesis in skeletal muscle by CaMK. Science 296: 349-352, 2002. (Pubitemid 34303690)
47. Wu H, Naya FJ, McKinsey TA, Mercer B, Shelton JM, Chin ER, Simard AR, Michel RN, Bassel-Duby R, Olson EN, Williams RS. MEF2 responds to multiple calcium-regulated signals in the control of skeletal muscle fiber type. EMBO J 19: 1963-1973, 2000. (Pubitemid 30237572)
48. Wu H, Rothermel B, Kanatous S, Rosenberg P, Naya FJ, Shelton JM, Hutcheson KA, DiMaio JM, Olson EN, Bassel-Duby R, Williams RS. Activation of MEF2 by muscle activity is mediated through a calcineurin- dependent pathway. EMBO J 20: 6414-6423, 2001. (Pubitemid 33078714)
49. Zorzano A, Santalucia T, Palacin M, Guma A, Camps M. Searching for ways to upregulate GLUT4 glucose transporter expression in muscle. Gen Pharmacol 31: 705-713, 1998. (Pubitemid 28520046)