Mouse amp-activated protein kinase γ3 subunit R225Q mutation affecting mouse growth performance when fed a high-energy diet

Journal of Animal Science

Volumn 88, Issue 4, 2010, Pages 1332-1340

  Zhao, J X ^a   Yan, X ^a   Tong, J F ^a   Means, W J ^a   McCormick, R J ^a   Zhu, M J ^a   Du, M ^a  

^a UNIVERSITY OF WYOMING   (United States)

Author keywords

Amp activated protein kinase; Energy; Fat accumulation; Growth performance; Muscle; Rendement napole gene

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ISOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MYOSIN; PRKAG3 PROTEIN, MOUSE; PROTEIN KINASE B;

ANIMAL; ANIMAL DISEASE; ARTICLE; CHEMISTRY; DIET; EATING; ENERGY METABOLISM; ENZYMOLOGY; FEMALE; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; IMMUNOBLOTTING; MALE; METABOLISM; MOUSE; MUTATION; PHYSIOLOGY; SKELETAL MUSCLE; TRANSGENIC MOUSE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DIET; EATING; ENERGY METABOLISM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; GENOTYPE; IMMUNOBLOTTING; MALE; MICE; MICE, TRANSGENIC; MUSCLE, SKELETAL; MUTATION; MYOSINS; PROTEIN ISOFORMS; PROTO-ONCOGENE PROTEINS C-AKT;

ANIMALIA; MUS; MUS MUSCULUS; SUIDAE;

EID: 77949756861     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2009-2376     Document Type: Article

References (44)

1. Arad, M., D. W. Benson, A. R. Perez-Atayde, W. J. McKenna, E. A. Sparks, R. J. Kanter, K. McGarry, J. G. Seidman, and C. E. Seidman. 2002. Constitutively active AMP kinase mutations cause glycogen storage disease mimicking hypertrophic cardiomyopathy. J. Clin. Invest. 109:357-362.
2. Barnes, B. R., S. Glund, Y. C. Long, G. Hjalm, L. Andersson, and J. R. Zierath. 2005. 5′-AMP-activated protein kinase regulates skeletal muscle glycogen content and ergogenics. FASEB J. 19:773-779.
3. Barnes, B. R., S. Marklund, T. L. Steiler, M. Walter, G. Hjalm, V. Amarger, M. Mahlapuu, Y. Leng, C. Johansson, D. Galuska, K. Lindgren, M. Abrink, D. Stapleton, J. R. Zierath, and L. Andersson. 2004. The 5′-AMP-activated protein kinase gamma3 isoform has a key role in carbohydrate and lipid metabolism in glycolytic skeletal muscle. J. Biol. Chem. 279:38441-38447.
4. Carr, C. C., J. B. Morgan, E. P. Berg, S. D. Carter, and F. K. Ray. 2006. Growth performance, carcass composition, quality, and enhancement treatment of fresh pork identified through deoxyribonucleic acid marker-assisted selection for the Rendement Napole gene. J. Anim. Sci. 84:910-917.
5. Cheung, P. C., I. P. Salt, S. P. Davies, D. G. Hardie, and D. Carling. 2000. Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. Biochem. J. 346:659-669.
6. Copenhafer, T. L., B. T. Richert, A. P. Schinckel, A. L. Grant, and D. E. Gerrard. 2006. Augmented postmortem glycolysis does not occur early postmortem in AMPK73-mutated porcine muscle of halothane positive pigs. Meat Sci. 73:590-599.
7. Costford, S. R., N. Kavaslar, N. Ahituv, S. N. Chaudhry, W. S. Schackwitz, R. Dent, L. A. Pennacchio, R. McPherson, and M. E. Harper. 2007. Gain-of-function R225W mutation in human AMPKgamma(3) causing increased glycogen and decreased triglyceride in skeletal muscle. PLoS ONE 2:E903.
8. Daniel, T., and D. Carling. 2002. Functional analysis of mutations in the gamma 2 subunit of AMP-activated protein kinase associated with cardiac hypertrophy and Wolff-Parkinson-White syndrome. J. Biol. Chem. 277:51017-51024.
9. Donovan, M. J., G. Paulino, and H. E. Raybould. 2009. Activation of hindbrain neurons in response to gastrointestinal lipid is attenuated by high fat, high energy diets in mice prone to dietinduced obesity. Brain Res. 1248:136-140.
10. Du, M., Q. W. Shen, K. R. Underwood, J. F. Tong, and M. J. Zhu. 2009. AMP-activated protein kinase in muscle growth, fat deposition, and meat quality. CRC Press, Boca Raton, FL.
11. Garcia-Roves, P. M., M. E. Osler, M. H. Holmstrom, and J. R. Zierath. 2008. Gain-of-function R225Q mutation in AMP-activated protein kinase gamma3 subunit increases mitochondrial biogenesis in glycolytic skeletal muscle. J. Biol. Chem. 283:35724-35734.
12. Gregory, P. C., M. McFadyen, and D. V. Rayner. 1989. Duodenal infusion of fat, cholecystokinin secretion and satiety in the pig. Physiol. Behav. 45:1021-1024.
13. Hamilton, D. N., M. Ellis, M. D. Hemann, F. K. McKeith, K. D. Miller, and K. W. Purser. 2002. The impact of longissimus glycolytic potential and short-term feeding of magnesium sulfate heptahydrate prior to slaughter on carcass characteristics and pork quality. J. Anim. Sci. 80:1586-1592.
14. Hamilton, D. N., M. Ellis, K. D. Miller, F. K. McKeith, and D. F. Parrett. 2000. The effect of the Halothane and Rendement Napole genes on carcass and meat quality characteristics of pigs. J. Anim. Sci. 78:2862-2867.
15. Hardie, D. G. 2004. AMP-activated protein kinase: A key system mediating metabolic responses to exercise. Med. Sci. Sports Exerc. 36:28-34.
16. Kim, J., R. S. Solis, E. B. Arias, and G. D. Cartee. 2004. Postcontraction insulin sensitivity: Relationship with contraction protocol, glycogen concentration, and 5′ AMP-activated protein kinase phosphorylation. J. Appl. Physiol. 96:575-583.
17. Le Roy, P., J. M. Elsen, J. C. Caritez, A. Talmant, H. Juin, P. Sellier, and G. Monin. 2000. Comparison between the three porcine RN genotypes for growth, carcass composition and meat quality traits. Genet. Sel. Evol. 32:165-186.
18. Lebret, B., P. Le Roy, G. Monin, L. Lefaucheur, J. C. Caritez, A. Talmant, J. M. Elsen, and P. Sellier. 1999. Influence of the three RN genotypes on chemical composition, enzyme activities, and myofiber characteristics of porcine skeletal muscle. J. Anim. Sci. 77:1482-1489.
19. Masuzaki, H., J. Paterson, H. Shinyama, N. M. Morton, J. J. Mullins, J. R. Seckl, and J. S. Flier. 2001. A transgenic model of visceral obesity and the metabolic syndrome. Science 294:2166-2170.
20. Milan, D., J. T. Jeon, C. Looft, V. Amarger, A. Robic, M. Thelander, C. Rogel-Gaillard, S. Paul, N. Iannuccelli, L. Rask, H. Ronne, K. Lundstrom, N. Reinsch, J. Gellin, E. Kalm, P. L. Roy, P. Chardon, and L. Andersson. 2000. A mutation in PRK- AG3 associated with excess glycogen content in pig skeletal muscle. Science 288:1248-1251.
21. Miller, K. D., M. Ellis, F. K. McKeith, B. S. Bidner, and D. J. Meisinger. 2000. Frequency of the Rendement Napole RN- allele in a population of American Hampshire pigs. J. Anim. Sci. 78:1811-1815.
22. Moeller, S. J., T. J. Baas, T. D. Leeds, R. S. Emnett, and K. M. Irvin. 2003. Rendement Napole gene effects and a comparison of glycolytic potential and DNA genotyping for classification of Rendement Napole status in Hampshire-sired pigs. J. Anim. Sci. 81:402-410.
23. Nielsen, J. N., K. J. Mustard, D. A. Graham, H. Yu, C. S. MacDonald, H. Pilegaard, L. J. Goodyear, D. G. Hardie, E. A. Richter, and J. F. Wojtaszewski. 2003. 5′-AMP-activated protein kinase activity and subunit expression in exercise-trained human skeletal muscle. J. Appl. Physiol. 94:631-641.
24. Park, S., T. L. Scheffler, A. M. Gunawan, H. Shi, C. Zeng, K. M. Hannon, A. L. Grant, and D. E. Gerrard. 2009a. Chronic elevated calcium blocks AMPK-induced GLUT-4 expression in skeletal muscle. Am. J. Physiol. Cell Physiol. 296:C106-C115.
25. Park, S. K., A. M. Gunawan, T. L. Scheffler, A. L. Grant, and D. E. Gerrard. 2009b. Myosin heavy chain isoform content and energy metabolism can be uncoupled in pig skeletal muscle. J. Anim. Sci. 87:522-531.
26. Putman, C. T., K. J. Martins, M. E. Gallo, G. D. Lopaschuk, J. A. Pearcey, I. M. MacLean, R. J. Saranchuk, and D. Pette. 2007. Alpha-catalytic subunits of 5′AMP-activated protein kinase display fiber-specific expression and are upregulated by chronic low-frequency stimulation in rat muscle. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293:R1325-R1334.
27. Reading, A. J. 1966. Influence of room temperature on the growth of house mice. J. Mammal. 47:694-697.
28. Rogers, P., and G. P. Webb. 1980. Estimation of body fat in normal and obese mice. Br. J. Nutr. 43:83-86.
29. Rosenfeld, C. S., K. M. Grimm, K. A. Livingston, A. M. Brokman, W. E. Lamberson, and R. M. Roberts. 2003. Striking variation in the sex ratio of pups born to mice according to whether maternal diet is high in fat or carbohydrate. Proc. Natl. Acad. Sci. USA 100:4628-4632.
30. Sambandam, N., and G. D. Lopaschuk. 2003. AMP-activated protein kinase (AMPK) control of fatty acid and glucose metabolism in the ischemic heart. Prog. Lipid Res. 42:238-256.
31. Shen, Q. W., C. S. Jones, N. Kalchayanand, M. J. Zhu, and M. Du. 2005. Effect of dietary alpha-lipoic acid on growth, body composition, muscle pH, and AMP-activated protein kinase phosphorylation in mice. J. Anim. Sci. 83:2611-2617.
32. +/ calmodulin-dependent protein kinase kinase is involved in AMP-activated protein kinase activation by alpha-lipoic acid in C2C12 myotubes. Am. J. Physiol. Cell Physiol. 293:C1395-C1403.
33. Shi, H., J. M. Scheffler, J. M. Pleitner, C. Zeng, S. Park, K. M. Hannon, A. L. Grant, and D. E. Gerrard. 2008. Modulation of skeletal muscle fiber type by mitogen-activated protein kinase signaling. FASEB J. 22:2990-3000.
34. Shi, H., C. Zeng, A. Ricome, K. M. Hannon, A. L. Grant, and D. E. Gerrard. 2007. Extracellular signal-regulated kinase pathway is differentially involved in beta-agonist-induced hypertrophy in slow and fast muscles. Am. J. Physiol. Cell Physiol. 292:C1681-C1689.
35. Sidhu, J. S., Y. S. Rajawat, T. G. Rami, M. H. Gollob, Z. Wang, R. Yuan, A. J. Marian, F. J. DeMayo, D. Weilbacher, G. E. Taffet, J. K. Davies, D. Carling, D. S. Khoury, and R. Roberts. 2005. Transgenic mouse model of ventricular preexcitation and atrioventricular reentrant tachycardia induced by an AMP-activated protein kinase loss-of-function mutation responsible for Wolff-Parkinson-White syndrome. Circulation 111:21-29.
36. Tortoriello, D. V., J. E. McMinn, and S. C. Chua. 2007. Increased expression of hypothalamic leptin receptor and adiponectin accompany resistance to dietary-induced obesity and infertility in female C57BL/6J mice. Int. J. Obes. (Lond.) 31:395-402.
37. Underwood, K. R., J. Tong, M. J. Zhu, Q. W. Shen, W. J. Means, S. P. Ford, S. I. Paisley, B. W. Hess, and M. Du. 2007. Relationship between kinase phosphorylation, muscle fiber typing, and glycogen accumulation in Longissimus muscle of beef cattle with high and low intramuscular fat. J. Agric. Food Chem. 55:9698-9703.
38. Van Heek, M., D. S. Compton, C. F. France, R. P. Tedesco, A. B. Fawzi, M. P. Graziano, E. J. Sybertz, C. D. Strader, and H. R. Davis Jr. 1997. Diet-induced obese mice develop peripheral, but not central, resistance to leptin. J. Clin. Invest. 99:385-390.
39. Winder, W. W., B. F. Holmes, D. S. Rubink, E. B. Jensen, M. Chen, and J. O. Holloszy. 2000. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J. Appl. Physiol. 88:2219-2226.
40. Woods, S. C., and D. A. D'Alessio. 2008. Central control of body weight and appetite. J. Clin. Endocrinol. Metab. 93:S37-S50.
41. Yu, H., M. F. Hirshman, N. Fujii, J. M. Pomerleau, L. E. Peter, and L. J. Goodyear. 2006. Muscle-specific overexpression of wild type and R225Q mutant AMP-activated protein kinase gamma3-subunit differentially regulates glycogen accumulation. Am. J. Physiol. Endocrinol. Metab. 291:E557-E565.
42. Zhu, M. J., M. Du, B. W. Hess, W. J. Means, P. W. Nathanielsz, and S. P. Ford. 2007. Maternal nutrient restriction upregulates growth signaling pathways in the cotyledonary artery of cow placentomes. Placenta 28:361-368.
43. Zhu, M. J., M. Du, M. J. Nijland, P. W. Nathanielsz, B. W. Hess, G. E. Moss, and S. P. Ford. 2009. Down-regulation of growth signaling pathways linked to a reduced cotyledonary vascularity in placentomes of over-nourished, obese pregnant ewes. Placenta 30:405-410.
44. Zhu, M. J., B. Han, J. Tong, C. Ma, J. M. Kimzey, K. R. Underwood, Y. Xiao, B. W. Hess, S. P. Ford, P. W. Nathanielsz, and M. Du. 2008. AMP-activated protein kinase signalling pathways are down regulated and skeletal muscle development impaired in fetuses of obese, over-nourished sheep. J. Physiol. 586:2651-2664.