α-Catalytic subunits of 5′ AMP-activated protein kinase display fiber-specific expression and are upregulated by chronic low-frequency stimulation in rat muscle

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 293, Issue 3, 2007, Pages

  Putman, Charles T ^a   Martins, Karen J B ^a   Gallo, Maria E ^a   Lopaschuk, Gary D ^a   Pearcey, Jean A ^a   MacLean, Ian M ^a   Saranchuk, Ryan J ^a   Pette, Dirk ^b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF KONSTANZ   (Germany)

Author keywords

Fast twitch muscle; Myosin heavy chain; Slow twitch muscle

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MYOSIN HEAVY CHAIN;

ARTICLE; CONTROLLED STUDY; ELECTROSTIMULATION; FAST MUSCLE; GASTROCNEMIUS MUSCLE; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MALE; MUSCLE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SKELETAL MUSCLE; SOLEUS MUSCLE; TIBIALIS ANTERIOR MUSCLE; UPREGULATION;

ANIMALS; BLOTTING, WESTERN; CATALYSIS; CELL NUCLEUS; ELECTRIC STIMULATION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; IMMUNOHISTOCHEMISTRY; ISOENZYMES; MALE; MULTIENZYME COMPLEXES; MUSCLE FIBERS; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; MYOSIN HEAVY CHAINS; PROTEIN-SERINE-THREONINE KINASES; RATS; RATS, SPRAGUE-DAWLEY; UP-REGULATION;

EID: 34548459307     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00609.2006     Document Type: Article

References (74)

1. Adams J, Chen ZP, Van Denderen BJ, Morton CJ, Parker MW, Witters LA, Stapleton D, Kemp BE. Intrasteric control of AMPK via the gamma1 subunit AMP allosteric regulatory site. Protein Sci 13: 155-165, 2004.
2. Ai H, Ihlemann J, Hellsten Y, Lauritzen HP, Hardie DG, Galbo H, Ploug T. Effect of fiber type and nutritional state on AICAR- and contraction-stimulated glucose transport in rat muscle. Am J Physiol Endocrinol Metab 282: E1291-E1300, 2002.
3. Bamford JA, Lopaschuk GD, MacLean IM, Reinhart ML, Dixon WT, Putman CT. Effects of chronic AICAR administration on metabolic and contractile phenotype in rat skeletal muscle. Can J Physiol Pharmacol 81: 1072-1082, 2003.
4. Bamford JA, Putman CT, Mushahwar VK. Intraspinal microstimulation preferentially recruits fatigue-resistant muscle fibres and generates gradual force in rat. J Physiol 569: 873-884, 2005.
5. Barazzoni R. Skeletal muscle mitochondrial protein metabolism and function in ageing and type 2 diabetes. Curr Opin Clin Nutr Metab Care 7: 97-102, 2004.
6. Barnes BR, Marklund S, Steiler TL, Walter M, Hjalm G, Amarger V, Mahlapuu M, Leng Y, Johansson C, Galuska D, Lindgren K, Abrink M, Stapleton D, Zierath JR, Andersson L. The AMPK-gamma 3 isoform has a key role for carbohydrate and lipid metabolism in glycolytic skeletal muscle. J Biol Chem 279: 38441-38447, 2004.
7. Bass A, Brdiczka D, Eyer P, Hofer S, Pette D. Metabolic differentiation of distinct muscle types at the level of enzymatic organization. Eur J Biochem 10: 198-206, 1969.
8. Brooke MH, Kaiser KK. Three "myosin adenosine triphosphatase" systems: the nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 18: 670-672, 1970.
9. Buhl ES, Jessen N, Pold R, Ledet T, Flyvbjerg A, Pedersen SB, Pedersen O, Schmitz O, Lund S. Long-term AICAR administration reduces metabolic disturbances and lowers blood pressure in rats displaying features of the insulin resistance syndrome. Diabetes 51: 2199-2206, 2002.
10. Buhl ES, Jessen N, Schmitz O, Pedersen SB, Pedersen O, Holman GD, Lund S. Chronic treatment with 5-aminoimidazole-4-carboxamide-1-beta-D-ribofuranoside increases insulin-stimulated glucose uptake and GLUT4 translocation in rat skeletal muscles in a fiber type-specific manner. Diabetes 50: 12-17, 2001.
11. Carling D. The AMP-activated protein kinase cascade - a unifying system for energy control. Trends Biochem Sci 29: 18-24, 2004.
12. Cheung PC, Salt IP, Davies SP, Hardie DG, Carling D. Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. Biochem J 346: 659-669, 2000.
13. Corton JM, Gillespie JG, Hawley SA, Hardie DG. 5-Aminoimidazole-4-carboxamide ribonucleoside: a specific method for activating AMP-activated protein kinase in intact cells? Eur J Biochem 229: 558-565, 1995.
14. Durante PE, Mustard KJ, Park SH, Winder WW, Hardie DG. Effects of endurance training on activity and expression of AMP-activated protein kinase isoforms in rat muscles. Am J Physiol Endocrinol Metab 283: E178-E186, 2002.
15. Erim Z, De Luca CJ, Mineo K, Aoki T. Rank-ordered regulation of motor units. Muscle Nerve 19: 563-573, 1996.
16. Frosig C, Jorgensen SB, Hardie DG, Richter EA, Wojtaszewski JF. 5′-AMP-activated protein kinase activity and protein expression are regulated by endurance training in human skeletal muscle. Am J Physiol Endocrinol Metab 286: E411-E417, 2004.
17. Gallo M, Gordon T, Syrotuik D, Shu Y, Tyreman N, Maclean I, Kenwell Z, Putman CT. Effects of long-term creatine feeding and running on isometric functional measures and myosin heavy chain content of rat skeletal muscles. Pflügers Arch 452: 744-755, 2006.
18. Green HJ, Reichmann H, Pette D. Fiber type specific transformations in the enzyme activity pattern of rat vastus lateralis muscle by prolonged endurance training. Pflügers Arch 399: 216-222, 1983.
19. Hämäläinen N, Pette D. The histochemical profiles of fast fiber types IIB, IID, and IIA in skeletal muscles of mouse, rat, and rabbit. J Histochem Cytochem 41: 733-743, 1993.
20. Hämäläinen N, Pette D. Patterns of myosin isoforms in mammalian skeletal muscle fibres. Microsc Res Tech 30: 381-389, 1995.
21. Hämäläinen N, Pette D. Slow-to-fast transitions in myosin expression of rat soleus muscle by phasic high-frequency stimulation. FEBS Lett 399: 220-222, 1996.
22. Hansen G, Martinuk KJB, Bell GJ, MacLean IM, Martin T, Putman CT. Effects of spaceflight on myosin heavy chain content, fibre morphology and succinate dehydrogenase activity in rat diaphragm muscle. Pflügers Arch 448: 239-247, 2004.
23. Hardie DG. Minireview: the AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144: 5179-5183, 2003.
24. Hardie DG. AMP-activated protein kinase: a key system mediating metabolic responses to exercise. Med Sci Sports Exerc 36: 28-34, 2004.
25. Hardie DG, Carling D. The AMP-activated protein kinase - fuel gauge of the mammalian cell? Eur J Biochem 246: 259-273, 1997.
26. Hardie DG, Salt IP, Hawley SA, Davies SP. AMP-activated protein kinase: an ultrasensitive system for monitoring cellular energy charge. Biochem J 338: 717-722, 1999.
27. Harris AJ, Fitzsimons RB, McEwan JC. Neural control of the sequence of expression of myosin heavy chain isoforms in foetal mammalian muscles. Development 107: 751-769, 1989.
28. Hofmann S, Pette D. Low-frequency stimulation of rat fast-twitch muscle enhances the expression of hexokinase II and both the translocation and expression of glucose transporter 4 (GLUT-4). Eur J Biochem 219: 307-315, 1994.
29. Holmes BF, Kurth-Kraczek EJ, Winder WW. Chronic activation of 5′-AMP-activated protein kinase increases GLUT-4, hexokinase, and glycogen in muscle. J Appl Physiol 87: 1990-1995, 1999.
30. Hudson ER, Pan DA, James J, Lucocq JM, Hawley SA, Green KA, Baba O, Terashima T, Hardie DG. A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias. Curr Biol 13: 861-866, 2003.
31. Hurst D, Taylor EB, Cline TD, Greenwood LJ, Compton CL, Lamb JD, Winder WW. AMP-activated protein kinase kinase activity and phosphorylation of AMP-activated protein kinase in contracting muscle of sedentary and endurance-trained rats. Am J Physiol Endocrinol Metab 289: E710-E715, 2005.
32. Hutber CA, Hardie DG, Winder WW. Electrical stimulation inactivates muscle acetylCoA carboxylase and increases AMP-activated protein kinase. Am J Physiol Endocrinol Metab 272: E262-E266, 1997.
33. Jones TE, Baar K, Ojuka E, Chen M, Holloszy JO. Exercise induces an increase in muscle UCP3 as a component of the increase in mitochondrial biogenesis. Am J Physiol Endocrinol Metab 284: E96-E101, 2003.
34. Kefas BA, Cai Y, Kerckhofs K, Ling Z, Martens G, Heimberg H, Pipeleers D, Van de CM. Metformin-induced stimulation of AMP-activated protein kinase in beta-cells impairs their glucose responsiveness and can lead to apoptosis. Biochem Pharmacol 68: 409-416, 2004.
35. Langfort J, Viese M, Ploug T, Dela F. Time course of GLUT4 and AMPK protein expression in human skeletal muscle during one month of physical training. Scand J Med Sci Sports 13: 169-174, 2003.
36. Leverve XM, Guigas B, Detaille D, Batandier C, Koceir EA, Chauvin C, Fontaine E, Wiernsperger NF. Mitochondrial metabolism and type-2 diabetes: a specific target of metformin. Diabetes Metaby 29: 6S88-6S94, 2003.
37. Lowry OH, Rosebrough NJ, Farr AL, Randell RJ. Protein measurements with the folin phenol reagent. J Biol Chem 193: 265-275, 1951.
38. Mahlapuu M, Johansson C, Lindgren K, Hjalm G, Barnes BR, Krook A, Zierath JR, Andersson L, Marklund S. Expression profiling of the gamma-subunit isoforms of AMP-activated protein kinase suggests a major role for gamma3 in white skeletal muscle. Am J Physiol Endocrinol Metab 286: E194-E200, 2004.
39. Martins KJ, Gordon T, Pette D, Dixon WT, Foxcroft GR, MacLean IM, Putman CT. Effect of satellite cell ablation on low-frequency-stimulated fast-to-slow fibre-type transitions in rat skeletal muscle. J Physiol 572: 281-294, 2006.
40. McGee SL, Howlett KF, Starkie RL, Cameron-Smith D, Kemp BE, Hargreaves M. Exercise increases nuclear AMPK alpha2 in human skeletal muscle. Diabetes 52: 926-928, 2003.
41. Mitchelhill KI, Michell BJ, House CM, Stapleton D, Dyck J, Gamble J, Ullrich C, Witters LA, Kemp BE. Posttranslational modifications of the 5′-AMP-activated protein kinase beta1 subunit. J Biol Chem 272: 24475-24479, 1997.
42. Neufer PD, Dohm GL. Exercise induces a transient increase in transcription of the GLUT-4 gene in skeletal muscle. Am J Physiol Cell Physiol 265: C1597-C1603, 1993.
43. Nielsen JN, Mustard KJ, Graham DA, Yu H, MacDonald CS, Pilegaard H, Goodyear LJ, Hardie DG, Richter EA, Wojtaszewski JF. 5′-AMP-activated protein kinase activity and subunit expression in exercise-trained human skeletal muscle. J Appl Physiol 94: 631-641, 2003.
44. Nuhr M, Crevenna R, Gohlsch B, Bittner C, Pleiner J, Wiesinger G, Fialka-Moser V, Quittan M, Pette D. Functional and biochemical properties of chronically stimulated human skeletal muscle. Eur J Appl Physiol 89: 202-208, 2003.
45. Nuhr MJ, Pette D, Berger R, Quittan M, Crevenna R, Huelsman M, Wiesinger GF, Moser P, Fialka-Moser V, Pacher R. Beneficial effects of chronic low-frequency stimulation of thigh muscles in patients with advanced chronic heart failure. Eur Heart J 25: 136-143, 2004.
46. Patti ME, Butte AJ, Crunkhorn S, Cusi K, Berria R, Kashyap S, Miyazaki Y, Kohane I, Costello M, Saccone R, Landaker EJ, Goldfine AB, Mun E, Defronzo R, Finlayson J, Kahn CR, Mandarino LJ. Coordinated reduction of genes of oxidative metabolism in humans with insulin resistance and diabetes: Potential role of PGC1 and NRF1. Proc Natl Acad Sci USA 100: 8466-8471, 2003.
47. Pette D. Training effects on the contractile apparatus. Acta Physiol Scand 162: 367-376, 1998.
48. Pette D. Historical perspectives: plasticity of mammalian skeletal muscle. J Appl Physiol 90: 1119-1124, 2001.
49. Pette D, Staron RS. Mammalian skeletal muscle fiber-type transitions. Int Rev Cytol 170: 143-223, 1997.
50. Pette D, Staron RS. Myosin isoforms, muscle fiber types, and transitions. Microsc Res Tech 50: 500-509, 2000.
51. Pette D, Vrbová G. What does chronic electrical stimulation teach us about muscle plasticity? Muscle Nerve 22: 666-677, 1999.
52. Pold R, Jensen LS, Jessen N, Buhl ES, Schmitz O, Flyvbjerg A, Fujii N, Goodyear LJ, Gotfredsen CF, Brand CL, Lund S. Long-term AICAR administration and exercise prevents diabetes in ZDF rats. Diabetes 54: 928-934, 2005.
53. Ponticos M, Lu QL, Morgan JE, Hardie DG, Partridge TA, Carling D. Dual regulation of the AMP-activated protein kinase provides a novel mechanism for the control of creatine kinase in skeletal muscle. EMBO J 17: 1688-1699, 1998.
54. Putman CT, Dixon WT, Pearcey J, MacLean IM, Jendral MJ, Kiricsi M, Murdoch GK, Pette D. Chronic low-frequency stimulation upregulates uncoupling protein-3 in transforming rat fast-twitch skeletal muscle. Am J Physiol Regul Integr Comp Physiol 287: R1419-R1426, 2004.
55. Putman CT, Dixon WT, Pearcey JA, MacLean IM, Jendral MJ, Kiricsi M, Murdoch GK, Pette D. Chronic low-frequency stimulation upregulates uncoupling protein-3 in transforming rat fast-twitch skeletal muscle. Am J Physiol Regul Integr Comp Physiol 287: R1419-R1426, 2004.
56. Putman CT, Düsterhöft S, Pette D. Changes in satellite cell content and myosin isoforms in low-frequency-stimulated fast muscle of hypothyroid rat. J Appl Physiol 86: 40-51, 1999.
57. Putman CT, Düsterhöft S, Pette D. Satellite cell proliferation in low-frequency stimulated fast muscle of hypothyroid rat. Am J Physiol Cell Physiol 279: C682-C690, 2000.
58. Putman CT, Kiricsi M, Pearcey J, MacLean IM, Bamford JA, Murdoch GK, Dixon WT, Pette D. AMPK activation increases UCP-3 expression and mitochondrial enzyme activities in rat muscle without fibre type transitions. J Physiol 551.1: 169-178, 2003.
59. Putman CT, Xu X, Gillies E, MacLean IM, Bell GJ. Effects of strength, endurance and combined training on myosin heavy chain content and fibre type distribution in humans. Eur J Appl Physiol 92: 376-384, 2004.
60. Reichmann H, Hoppeler H, Mathieu-Costello O, von Bergen F, Pette D. Biochemical and ultrastructural changes of skeletal muscle mitochondria after chronic electrical stimulation in rabbits. Pflügers Arch 404: 1-9, 1985.
61. Salt IP, Celler JW, Hawley SA, Prescott A, Woods A, Carling D, Hardie DG. AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the alpha2 isoform. Biochem J 334: 177-187, 1998.
62. Scarpulla RC. Nuclear activators and coactivators in mammalian mitochondrial biogenesis. Biochim Biophys Acta 1576: 1-14, 2002.
63. Schiaffino S, Gorza L, Sartore S, Saggin L, Ausoni S, Vianello M, Gundersen K, Lomo T. Three myosin heavy chain isoforms in type 2 skeletal muscle fibres. J Muscle Res Cell Motil 10: 197-205, 1989.
64. Schrauwen P, Hardie DG, Roorda B, Clapham JC, Abuin A, Thomason-Hughes M, Green K, Frederik PM, Hesselink MK. Improved glucose homeostasis in mice overexpressing human UCP3: a role for AMP-kinase? Int J Obes Relat Metab Disord 28: 824-828, 2004.
65. Schrauwen P, Hesselink MK. Oxidative capacity, lipotoxicity, and mitochondrial damage in type 2 diabetes. Diabetes 53: 1412-1417, 2004.
66. Staron RS. Human skeletal muscle fiber types: delineation, development, and distribution. Can J Appl Physiol 22: 307-327, 1997.
67. Tsuboyama-Kasaoka N, Tsunoda N, Maruyama K, Takahashi M, Kim H, Ikemoto S, Ezaki O. Up-regulation of uncoupling protein 3 (UCP3) mRNA by exercise training and down-regulation of UCP3 by denervation in skeletal muscles. Biochem Biophys Res Commun 247: 498-503, 1998.
68. Vavvas D, Apazidis A, Saha AK, Gamble J, Patel A, Kemp BE, Witters LA, Ruderman NB. Contraction-induced changes in acetyl-CoA carboxylase and 5′-AMP-activated kinase in skeletal muscle. J Biol Chem 272: 13255-13261, 1997.
69. Winder WW, Hardie DG. Inactivation of acetylCoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am J Physiol Endocrinol Metab 270: E299-E304, 1996.
70. Winder WW, Hardie DG. AMP-activated protein kinase, a metabolic master switch: possible roles in type 2 diabetes. Am J Physiol Endocrinol Metab 277: E1-E10, 1999.
71. Winder WW, Holmes BF, Rubink DS, Jensen EB, Chen M, Holloszy JO. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J Appl Physiol 88: 2219-2226, 2000.
72. Wojtaszewski JF, Jorgensen SB, Hellsten Y, Hardie DG, Richter EA. Glycogen-dependent effects of 5-aminoimidazole-4-carboxamide (AICA)-riboside on AMP-activated protein kinase and glycogen synthase activities in rat skeletal muscle. Diabetes 51: 284-292, 2002.
73. Zahradka P, Larson DE, Sells BH. RNA polymerase II-directed gene transcription by rat skeletal muscle nuclear extracts. Exp Cell Res 185: 8-20, 1989.
74. 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.