Characterization of the AMP-activated protein kinase pathway in chickens

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 143, Issue 1, 2006, Pages 92-106

  Proszkowiec Weglarz, Monika ^a   Richards, Mark P ^a   Ramachandran, Ramesh ^b   McMurtry, John P ^a  

^a AGRICULTURAL RESEARCH SERVICE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

AMPK; Chicken; Energy balance; Gene expression; Hypothalamus; LKB1; MO25; Phosphorylation; Protein kinase; STRAD

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ISOENZYME; PROTEIN KINASE LKB1;

ABDOMEN; ANIMAL TISSUE; ARTICLE; BODY FAT; BRAIN; CHICKEN; CONTROLLED STUDY; DIET RESTRICTION; DUODENUM; ENERGY BALANCE; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; FOOD INTAKE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEART; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; KIDNEY; LIVER; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PANCREAS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REFEEDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE HOMOLOGY; SKELETAL MUSCLE; SPLEEN;

ANIMALIA; GALLUS GALLUS; MAMMALIA;

EID: 29344438854     PISSN: 10964959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cbpb.2005.10.009     Document Type: Article

References (80)

1. J. Adams, Z.-P. Chen, B.J.W. Van Denderen, C.J. Morton, M.W. Parker, L.A. Witters, D. Stapleton, and B.E. Kemp Intrasteric control of AMPK via the γ1 subunit AMP allosteric regulatory site Protein Sci. 13 2004 155 165
2. U. Andersson, K. Filipsson, C.R. Abbott, A. Woods, K. Smith, S.R. Bloom, D. Carling, and C.J. Small AMP-activated protein kinase plays a role in the control of food intake J. Biol. Chem. 279 2004 12005 12008
3. A.F. Bass, J. Boudeau, G.P. Sapkota, L. Smit, R. Medema, N.A. Morrice, D.R. Alessi, and H.C. Clevers Activation of the tumor suppressor kinase LKB1 by the STE20-like pseudokinase STRAD EMBO J. 22 2003 3062 3072
4. A. Bateman The structure of a domain common to archaebacteria and the homocystinuria disease protein Trends Biochem. Sci. 22 1997 12 13
5. E. Blair, C. Redwood, H. Ashrafian, M. Oliveira, J. Broxholme, B. Kerr, A. Salmon, I. Ostman-Smith, and H. Watkins Mutations in the γ2 subunit of AMP-activated protein kinase cause familial hyperthrophic cardiomyopathy: evidence for the central role of energy compromise in disease pathogenesis Hum. Mol. Genet. 10 2001 1215 1220
6. J. Boudeau, A.F. Bass, M. Deak, N.A. Morrice, A. Kieloch, M. Schutkowski, A.R. Prescott, H.C. Clevers, and D.R. Alessi MO25 α/β interact with STRAD α/β enhancing their ability to bind, activate and localize LKB1 in the cytoplasm EMBO J. 22 2003 5102 5114
7. C. Broberger, and T. Hökfelt Hypothalamic and vagal neuropeptide circuitries regulating food intake Physiol. Behav. 74 2001 669 682
8. M. Bronner, R. Hertz, and J. Bar-Tana Kinase-independent transcriptional co-activation of peroxisome proliferator-activated receptor α by AMP-activated protein kinase Biochem. J. 384 2004 295 305
9. D. Carling The AMP-activated protein kinase cascade-a unifying system for energy control Trends Biochem. Sci. 29 2004 18 24
10. D. Carling AMP-activated protein kinase: balancing the scales Biochimie 87 2005 87 91
11. D. Carling, and D.G. Hardie The substrate and sequence specificity of the AMP-activated protein kinase. Phosphorylation of glycogen synthase and phosphorylase kinase Biochim. Biophys. Acta 1012 1989 81 86
12. Z.-P. Chen, K.I. Mitchelhill, B.J. Michell, D. Stapleton, I. Rodriguez-Crespo, L.A. Witters, D.A. Power, P.R. Ortiz de Montellano, and B.E. Kemp AMP-activated protein kinase phosphorylation of endothelial NO synthase FEBS Lett. 443 1999 285 289
13. P.C. Cheung, I.P. Salt, S.P. Davies, D.G. Hardie, and D. Carling Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding Biochem. J. 346 2000 659 669
14. J.M. Corton, J.G. Gillespie, S.A. Hawley, and D.G. Hardie 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur. J. Biochem. 229 1995 558 565
15. B.E. Crute, K. Seefeld, J. Gamble, B.E. Kemp, and L.A. Witters Functional domains of the α1 catalytic subunit of the AMP-activated protein kinase J. Biol. Chem. 273 1998 35347 35354
16. C. Culmsee, J. Monnig, B.E. Kemp, and M.P. Mattson AMP-activated protein kinase is highly expressed in neurons in the developing rat brain and promotes neuronal survival following glucose deprivation J. Mol. Neurosci. 17 2001 45 58
17. T. Daniel, and D. Carling Functional analysis of mutations in the γ2 subunit of AMP-activated protein kinase associated with cardiac hypertrophy and Wolff-Parkinson-White syndrome J. Biol. Chem. 277 2002 51017 51024
18. C FEBS Lett. 377 1995 421 425
19. D.M. Denbow Food intake regulation in birds J. Exp. Zool. 283 1999 333 338
20. J.R.B. Dyck, G. Gao, J. Widmer, D. Stapleton, C.S. Fernandez, B.E. Kemp, and L.A. Witters Regulation of 5′-AMP-activated protein kinase activity by the noncatalytic β and γ subunits J. Biol. Chem. 271 1996 17798 17803
21. J.K. Elmquist, C.F. Elias, and C.B. Saper From lesions to leptin: hypothalamic control of food intake and body weight Neuron 22 1999 221 232
22. G. Gao, C.S. Fernandez, D. Stapleton, A.S. Auster, J. Widmer, J.R.B. Dyck, B.E. Kemp, and L.A. Witters Non-catalytic β- and γ-subunit isoforms of the 5′-AMP-activated protein kinase J. Biol. Chem. 271 1996 8675 8681
23. J.G. Gillespie, and D.G. Hardie Phosphorylation and inactivation of HMG-CoA reductase at the AMP-activated protein kinase site in response to fructose treatment of isolated rat hepatocytes FEBS Lett. 306 1992 59 62
24. A.A. Gonzalez, R. Kumar, J.D. Mulligan, A.J. Davis, R. Weindruch, and K.W. Saupe Metabolic adaptations to fasting and chronic caloric restriction in heart, muscle, and liver do not include changes in AMPK activity Am. J. Physiol.: Endocrinol. Metab. 287 2004 E1032 E1037
25. S.A. Habinowski, and L.A. Witters The effects of AICAR on adipocyte differentiation of 3T3-L1 cells Biochem. Biophys. Res. Commun. 286 2001 852 856
26. D.G. Hardie The AMP-activated protein kinase pathway - new players upstream and downstream J. Cell Sci. 117 2004 5479 5487
27. D.G. Hardie AMP-activated protein kinase: a master switch in glucose and lipid metabolism Rev. Endocr. Metab. Disord. 5 2004 119 125
28. D.G. Hardie, D. Carling, and M. Carlson The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Ann. Rev. Biochem. 67 1998 821 855
29. 2+/calmodulin activates the calmodulin-dependent protein kinase I cascade, via three independent mechanisms J. Biol. Chem. 270 1995 27186 27191
30. S.A. Hawley, M. Davison, A. Woods, S.P. Davies, R.K. Beri, D. Carling, and D.G. Hardie Characterization of the AMP-activated protein kinase from rat liver and identification of threonine-172 as the major site at which it phosphorylates AMP-activated protein kinase J. Biol. Chem. 271 1996 27879 27887
31. S.A. Hawley, J. Boudeau, J.L. Reid, K.J. Mustard, L. Udd, T.P. Mäkelä, D.R. Alessi, and D.G. Hardie Complexes between the LKB1 tumor suppressor, STRADα/β and MO25α/β are upstream kinases in the AMP-activated protein kinase cascade J. Biol. 2 2003 28.1 28.16
32. R.L. Hazelwood, and F.W. Lorenz Effects of fasting and insulin on carbohydrate metabolism of the domestic fowl Am. J. Physiol. 197 1959 47 51
33. A. Hemminki, D. Markie, I. Tomlinson, E. Avizienyte, S. Roth, A. Loukola, G. Bignell, W. Warren, M. Aminoff, P. Höglund, H. Järvinen, P. Kristo, K. Pelin, M. Ridanpää, R. Salovaara, T. Toro, W. Bodmer, S. Olschwang, A.S. Olsen, M.R. Stratton, A. de la Chapelle, and L.A. Aaltonen A serine/threonine kinase gene defective in Peutz-Jeghers syndrome Nature 391 1998 184 187
34. Y.H. Hong, U.S. Varanasi, W. Yang, and T. Leff AMP-activated protein kinase regulates HNF4α transcriptional activity by inhibiting dimer formation and decreasing protein stability J. Biol. Chem. 278 2003 27495 27501
35. E.R. Hudson, D.A. Pan, J. James, J.M. Lucocq, S.A. Hawley, K.A. Green, O. Baba, T. Terashima, and D.G. Hardie A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias Curr. Biol. 13 2003 861 866
36. 2+/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases J. Biol. Chem. 280 2005 29060 29066
37. D.E. Jenne, H. Reimann, J. Nezu, W. Friedel, S. Loff, R. Jeschke, O. Müller, W. Back, and M. Zimmer Puetz-Jeghers syndrome is caused by mutation in a novel serine threonine kinase Nat. Genet. 18 1998 38 43
38. R.G. Jones, D.R. Plas, S. Kubek, M. Buzzai, J. Mu, Y. Xu, M.J. Birnbaum, and C.B. Thompson AMP-activated protein kinase induces a p53-dependent metabolic checkpoint Mol. Cell 18 2005 283 293
39. V.K. Kaushik, M.E. Young, D.J. Dean, T.G. Kurowski, A.K. Saha, and N.B. Ruderman Regulation of fatty acid oxidation and glucose metabolism in rat soleus muscle: effects of AICAR Am. J. Physiol.: Endocrinol. Metab. 281 2001 E335 E340
40. B.E. Kemp Bateman domains and adenosine derivatives form a binding contract J. Clin. Invest. 113 2004 182 184
41. B.E. Kemp, D. Stapleton, D.J. Campbell, Z.-P. Chen, S. Murthy, M. Walter, A. Gupta, J.J. Adams, F. Katsis, B. van Denderen, I.G. Jennings, T. Iseli, B.J. Michell, and L.A. Witters AMP-activated protein kinase, super metabolic regulator Biochem. Soc. Trans. 31 Pt 1 2003 162 168
42. W.J. Kuenzel Neuroanatomical substrates involved in the control of food intake Poult. Sci. 68 1989 926 937
43. W.J. Kuenzel, and M. Masson A Stereotaxic Atlas of the Brain of the Chick (Gallus domesticus) 1988 The Johns Hopkins University Press Baltimore, MD and London, MD
44. W.J. Kuenzel, M.M. Beck, and R. Teruyama Neural sites and pathways regulating food intake in birds: a comparative analysis to mammalian system J. Exp. Zool. 283 1999 348 364
45. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
46. D.R. Langslow, E.J. Butler, C.N. Hales, and A.W. Pearson The response of plasma insulin, glucose and non-esterified fatty acids to various hormones, nutrients and drugs in the domestic fowl J. Endocrinol. 46 1970 243 260
47. I. Leclerc, C. Lenzner, L. Gourdon, S. Vaulont, A. Kahn, and B. Viollet Hepatocyte nuclear factor-4α involved in type 1 maturity-onset diabetes of the young is a novel target of AMP-activated protein kinase Diabetes 50 2001 1515 1521
48. K. Lee, B. Li, X. Xi, Y. Suh, and R.J. Martin Role of neuronal energy status in the regulation of adenosine 5′-monophosphate-activated protein kinase, orexigenic neuropeptides expression, and feeding behavior Endocrinology 146 2005 3 10
49. J.M. Lizcano, O. Göransson, R. Toth, M. Deak, N.A. Morrice, J. Boudeau, S.A. Hawley, L. Udd, T.P. Mäkelä, D.G. Hardie, and D.R. Alessi LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1 EMBO J. 23 2004 833 843
50. J.J.F.P. Luiken, S.L.M. Coort, J. Willems, W.A. Coumans, A. Bonen, G.J. van der Vusse, and J.F.C. Glatz Contraction-induced fatty acid translocase/CD36 translocation in rat cardiac myocytes is mediated through AMP-activated protein kinase signaling Diabetes 52 2003 1627 1634
51. M. Mahlapuu, C. Johansson, K. Lindgren, G. Hjälm, B.R. Barnes, A. Krook, J.R. Zierath, L. Andersson, and S. Marklund Expression profiling of the γ-subunit isoform of AMP-activated protein kinase suggests a major role for γ3 in white skeletal muscle Am. J. Physiol.: Endocrinol. Metab. 286 2004 E194 E200
52. G.F. Merrill, E.J. Kurth, D.G. Hardie, and W.W. Winder AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle Am. J. Physiol. 273 1997 E1107 E1112
53. S.-I. Mikami Immunocytochemistry of the avian hypothalamus and adenohypophysis Int. Rev. Cytol. 103 1986 189 248
54. D. Milan, J.-T. Jeon, C. Looft, V. Amarger, A. Robic, M. Thelander, C. Rogel-Gaillard, S. Paul, N. Iannuccelli, L. Rask, H. Ronne, K. Lundström, N. Reinsch, J. Gellin, E. Kalm, P. Le Roy, P. Chardon, and L. Andersson A mutation in PRKAG3 associated with excess glycogen content in pig skeletal muscle Science 288 2000 1248 1251
55. Y. Minokoshi, T. Alquier, N. Furukawa, Y.-B. Kim, A. Lee, B. Xue, J. Mu, F. Foufelle, P. Ferré, M.J. Birnbaum, B.J. Stuck, and B.B. Kahn AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus Nature 428 2004 569 574
56. K.I. Mitchelhill, D. Stapleton, G. Gao, C. House, B. Michell, F. Katsis, L.A. Witters, and B.E. Kemp Mammalian AMP-activated protein kinase shares structural and functional homology with the catalytic domain of yeast Snf1 protein kinase J. Biol. Chem. 269 1994 2361 2364
57. M.R. Munday, M.R. Milic, S. Takhar, M.J. Holness, and M.C. Sugden The short-term regulation of hepatic acetyl-CoA carboxylase during starvation and re-feeding in the rat Biochem. J. 280 1991 733 737
58. D. Phillips-Singh, Q. Li, S. Takeuchi, T. Okhubo, P.J. Sharp, and T. Boswell Fasting differentially regulates expression of agouti-related peptide, pro-opiomelanocortin, prepro-orexin, and vasoactive intestinal polypeptide mRNAs in the hypothalamus of Japanese quail Cell Tissue Res. 313 2003 217 225
59. R. Rafaeloff-Phail, L. Ding, L. Corner, W.-K. Yeh, D. McClure, H. Guo, K. Emerson, and H. Brooks Biochemical regulation of mammalian AMP-activated protein kinase activity by NAD and NADH J. Biol. Chem. 279 2004 52934 52939
60. M.P. Richards Genetic regulation of feed intake and energy balance in poultry Poult. Sci. 82 2003 907 916
61. M.P. Richards, and S.M. Poch Quantitative analysis of gene expression by reverse transcription polymerase chain reaction and capillary electrophoresis with laser-induced fluorescence detection Mol. Biotechnol. 21 2002 19 37
62. S. Rozen, and H.J. Skaletsky Primer3 on the WWW for general users and for biologist programmers S. Krawetz S. Misener Bioinformatics Methods and Protocols: Methods in Molecular Biology 2000 Humana Press Totowa, NJ 365 386
63. K. Sakamoto, A. McCarthy, D. Smith, K.A. Green, D.G. Hardie, A. Ashworth, and D.R. Alessi Deficiency of LKB1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction EMBO J. 24 2005 1810 1820
64. I. Salt, J.W. Celler, S.A. Hawley, A. Prescott, A. Woods, D. Carling, and D.G. Hardie AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the α2 isoform Biochem. J. 334 1998 177 187
65. J.W. Scott, S.A. Hawley, K.A. Green, M. Anis, G. Stewart, G.A. Scullion, D.G. Norman, and D.G. Hardie CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations J. Clin. Invest. 113 2004 274 284
66. N. Snapir, and B. Robinzon Role of the basomedial hypothalamus in regulation of adiposity, food intake, and reproductive traits in the domestic fowl Poult. Sci. 68 1989 948 957
67. D. Stapleton, G. Gao, B.J. Michell, J. Widmer, K. Mitchelhill, T. The, C.M. House, L.A. Witters, and B.E. Kemp Mammalian 5′-AMP-activated protein kinase non-catalytic subunits are homologues of proteins that interact with yeast Snf1 protein kinase J. Biol. Chem. 269 1994 29343 29346
68. D. Stapleton, K.I. Mitchelhill, G. Gao, J. Widmer, B.J. Michell, T. The, C.M. House, C.S. Fernandez, T. Cox, L.A. Witters, and B.E. Kemp Mammalian AMP-activated protein kinase subfamily J. Biol. Chem. 271 1996 611 614
69. D. Stapleton, E. Woollatt, K.I. Mitchelhill, J.K. Nicholl, C.S. Fernandez, B.J. Michell, L.A. Witters, D.A. Power, G.R. Sutherland, and B.E. Kemp AMP-activated protein kinase isoenzyme family: subunit structure and chromosomal location FEBS Lett. 409 1997 452 456
70. C. Thornton, M.A. Snowden, and D. Carling Identification of a novel AMP-activated protein kinase β subunit isoform that is highly expressed in skeletal muscle J. Biol. Chem. 273 1998 12443 12450
71. A.M. Turnley, D. Stapleton, R.J. Mann, L.A. Witters, B.E. Kemp, and P.F. Bartlett Cellular distribution and developmental expression of AMP-activated protein kinase isoforms in mouse central nervous system J. Neurochem. 72 1999 1707 1716
72. A.J.M. Verhoeven, A. Woods, C.H. Brennan, S.A. Hawley, D.G. Hardie, J. Scott, R.J. Beri, and D. Carling The AMP-activated protein kinase gene is highly expressed in rat skeletal muscle. Alternative splicing and tissue distribution of the mRNA Eur. J. Biochem. 228 1995 236 243
73. J.W. Wallis, J. Aerts, M.A.M. Groenen, R.P.M.A. Crooijmans, D. Layman, T.A. Graves, D.E. Scheer, C. Kremitzki, M.J. Fedele, N.K. Mudd, M. Cardenas, J. Higginbotham, J. Carter, R. McGrane, T. Gaige, K. Mead, J. Walker, D. Albracht, J. Davito, S.-P. Yang, S. Leong, A. Chinwalla, M. Sekhon, K. Wylie, J. Dodgson, M.N. Romanov, H. Cheng, P.J. de Jong, K. Osoegawa, M. Nefedov, H. Zhang, J.D. McPherson, M. Krzywinski, J. Schein, L. Hillier, E.R. Mardis, R.K. Wilson, and W.C. Warren A physical map of the chicken genome Nature 432 2004 761 764
74. X. Wang, J.R. Day, and R. Vasilatos-Younken The distribution of neuropeptide Y gene expression in the chicken brain Mol. Cell. Endocrinol. 147 2001 129 136
75. L.A. Witters, G. Gao, B.E. Kemp, and B. Quistorff Hepatic 5′-AMP-activated protein kinase: zonal distribution and relationship to acetyl-CoA carboxylase activity in varying nutritional states Arch. Biochem. Biophys. 308 1994 413 419
76. J.F.P. Wojtaszewski, S.B. Jørgensen, Y. Hellsten, D.G. Hardie, and E.A. Richter 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 2002 284 292
77. J.F.P. Wojtaszewski, C. MacDonald, J.N. Nielsen, Y. Hellsten, D.G. Hardie, B.E. Kemp, B. Kiens, and E.A. Richter Regulation of 5′AMP- activated protein kinase activity and substrate utilization in exercising human skeletal muscle Am. J. Physiol.: Endocrinol. Metab. 284 2003 E813 E822
78. A. Woods, D. Azzout-Marniche, M. Foretz, S.C. Stein, P. Lemarchand, P. Ferré, F. Foufelle, and D. Carling Characterization of the role of AMP-activated protein kinase in the regulation of glucose-activated gene expression using constitutively active and dominant negative forms of the kinase Mol. Cell. Biol. 20 2000 6704 6711
79. T. Yamauchi, J. Kamon, Y. Minokoshi, Y. Ito, H. Waki, S. Uchida, S. Yamashita, M. Noda, S. Kita, K. Ueki, K. Eto, Y. Akanuma, P. Froguel, F. Foufelle, P. Ferre, D. Carling, S. Kimura, R. Nagai, B.B. Kahn, and T. Kadowaki Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase Nat. Med. 8 2002 1288 1295
80. G. Zhou, R. Myers, Y. Li, Y. Chen, X. Shen, J. Fenyk-Melody, M. Wu, J. Ventre, T. Doebber, N. Fujii, N. Musi, M.F. Hirsman, L.J. Goodyear, and D.E. Moller Role of AMP-activated protein kinase in mechanism of metformin action J. Clin. Invest. 108 2001 1167 1174