Nuclear translocation of AMPK-α1 potentiates striatal neurodegeneration in Huntington's disease

Journal of Cell Biology

Volumn 194, Issue 2, 2011, Pages 209-227

  Ju, Tz Chuen ^a,b   Chen, Hui Mei ^b   Lin, Jiun Tsai ^b   Chang, Ching Pang ^b   Chang, Wei Cheng ^a   Kang, Jheng Jie ^a   Sun, Cheng Pu ^a   Tao, Mi Hua ^b   Tu, Pang Hsien ^b   Chang, Chen ^b   Dickson, Dennis W ^c   Chern, Yijuang ^a,b  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b INSTITUTE OF BIOMEDICAL SCIENCES   (Taiwan)

^c MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE MONOPHOSPHATE ACTIVATED PROTEIN KINASE ALPHA 1; HUNTINGTIN; PROTEIN BCL 2; PROTEIN KINASE; UNCLASSIFIED DRUG;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN ATROPHY; CELL DEATH; CELL ENERGY; CELL LOSS; CELL NUCLEUS; CELL PROTECTION; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; CYTOTOXICITY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME INACTIVATION; EVOKED RESPONSE; FEMALE; GENE TRANSLOCATION; HUMAN; HUMAN CELL; HUNTINGTON CHOREA; MALE; MOUSE; NERVE CELL; NERVE DEGENERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; STRIATE CORTEX; TRANSGENIC MOUSE;

ACTIVE TRANSPORT, CELL NUCLEUS; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL NUCLEUS; CELLS, CULTURED; HUMANS; HUNTINGTON DISEASE; MICE; MICE, TRANSGENIC; MUTATION; NEOSTRIATUM; NERVE DEGENERATION; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS C-BCL-2;

MUS; MUS MUSCULUS;

EID: 79961116788     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201105010     Document Type: Article

References (67)

1. Anderson, K.A., T.J. Ribar, F. Lin, P.K. Noeldner, M.F. Green, M.J. Muehlbauer, L.A. Witters, B.E. Kemp, and A.R. Means. 2008. Hypothalamic CaMKK2 contributes to the regulation of energy balance. Cell Metab. 7:377-388.
2. Buckley, N.J., R. Johnson, C. Zuccato, A. Bithell, and E. Cattaneo. 2010. The role of REST in transcriptional and epigenetic dysregulation in Huntington's disease. Neurobiol. Dis. 39:28-39.
3. Cai, Y., G.A. Martens, S.A. Hinke, H. Heimberg, D. Pipeleers, and M. Van de Casteele. 2007. Increased oxygen radical formation and mitochondrial dysfunction mediate beta cell apoptosis under conditions of AMPactivated protein kinase stimulation. Free Radic. Biol. Med. 42:64-78.
4. Cattaneo, E., and L. Conti. 1998. Generation and characterization of embryonic striatal conditionally immortalized ST14A cells. J. Neurosci. Res. 53:223-234.
5. Chai, Y., S.L. Koppenhafer, S.J. Shoesmith, M.K. Perez, and H.L. Paulson. 1999. Evidence for proteasome involvement in polyglutamine disease: localization to nuclear inclusions in SCA3/MJD and suppression of polyglutamine aggregation in vitro. Hum. Mol. Genet. 8:673-682.
6. Chaturvedi, R.K., P. Adhihetty, S. Shukla, T. Hennessy, N. Calingasan, L. Yang, A. Starkov, M. Kiaei, M. Cannella, J. Sassone, et al. 2009. Impaired PGC-1alpha function in muscle in Huntington's disease. Hum. Mol. Genet. 18:3048-3065.
7. Chen, C.C., C.P. Sun, H.I. Ma, C.C. Fang, P.Y. Wu, X. Xiao, and M.H. Tao. 2009. Comparative study of anti-hepatitis B virus RNA interference by double-stranded adeno-associated virus serotypes 7, 8, and 9. Mol. Ther. 17:352-359.
8. Chen, Y., K. Zhou, R. Wang, Y. Liu, Y.D. Kwak, T. Ma, R.C. Thompson, Y. Zhao, L. Smith, L. Gasparini, et al. 2009. Antidiabetic drug metformin (GlucophageR) increases biogenesis of Alzheimer's amyloid peptides via up-regulating BACE1 transcription. Proc. Natl. Acad. Sci. USA. 106:3907-3912.
9. Chern, Y., H.L. Lai, J.C. Fong, and Y. Liang. 1993. Multiple mechanisms for desensitization of A2a adenosine receptor-mediated cAMP elevation in rat pheochromocytoma PC12 cells. Mol. Pharmacol. 44:950-958.
10. Chiang, M.C., Y.C. Lee, C.L. Huang, and Y. Chern. 2005. cAMP-response elementbinding protein contributes to suppression of the A2A adenosine receptor promoter by mutant Huntingtin with expanded polyglutamine residues. J. Biol. Chem. 280:14331-14340.
11. Chiang, M.C., H.M. Chen, Y.H. Lee, H.H. Chang, Y.C. Wu, B.W. Soong, C.M. Chen, Y.R. Wu, C.S. Liu, D.M. Niu, et al. 2007. Dysregulation of C/EBPalpha by mutant Huntingtin causes the urea cycle deficiency in Huntington's disease. Hum. Mol. Genet. 16:483-498.
12. Chou, S.Y., Y.C. Lee, H.M. Chen, M.C. Chiang, H.L. Lai, H.H. Chang, Y.C. Wu, C.N. Sun, C.L. Chien, Y.S. Lin, et al. 2005. CGS21680 attenuates symptoms of Huntington's disease in a transgenic mouse model. J. Neurochem. 93:310-320.
13. Chou, S.Y., J.Y. Weng, H.L. Lai, F. Liao, S.H. Sun, P.H. Tu, D.W. Dickson, and Y. Chern. 2008. Expanded-polyglutamine huntingtin protein suppresses the secretion and production of a chemokine (CCL5/RANTES) by astrocytes. J. Neurosci. 28:3277-3290.
14. Cong, F., and H. Varmus. 2004. Nuclear-cytoplasmic shuttling of Axin regulates subcellular localization of beta-catenin. Proc. Natl. Acad. Sci. USA. 101:2882-2887.
15. Cui, L., H. Jeong, F. Borovecki, C.N. Parkhurst, N. Tanese, and D. Krainc. 2006. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell. 127:59-69.
16. Escribano, C., C. Delgado-Martín, and J.L. Rodríguez-Fernández. 2009. CCR7-dependent stimulation of survival in dendritic cells involves inhibition of GSK3beta. J. Immunol. 183:6282-6295.
17. Estrada Sánchez, A.M., J. Mejía-Toiber, and L. Massieu. 2008. Excitotoxic neuronal death and the pathogenesis of Huntington's disease. Arch. Med. Res. 39:265-276.
18. Florant, G.L., A.M. Fenn, J.E. Healy, G.K. Wilkerson, and R.J. Handa. 2010. To eat or not to eat: the effect of AICAR on food intake regulation in yellowbellied marmots (Marmota flaviventris). J. Exp. Biol. 213:2031-2037.
19. Fujii, N., T. Hayashi, M.F. Hirshman, J.T. Smith, S.A. Habinowski, L. Kaijser, J. Mu, O. Ljungqvist, M.J. Birnbaum, L.A. Witters, et al. 2000. Exercise induces isoform-specific increase in 5'AMP-activated protein kinase activity in human skeletal muscle. Biochem. Biophys. Res. Commun. 273:1150-1155.
20. Garcia-Gil, M., R. Pesi, S. Perna, S. Allegrini, M. Giannecchini, M. Camici, and M.G. Tozzi. 2003. 5'-aminoimidazole-4-carboxamide riboside induces apoptosis in human neuroblastoma cells. Neuroscience. 117:811-820.
21. Giampà, C., S. Middei, S. Patassini, A. Borreca, F. Marullo, D. Laurenti, G. Bernardi, M. Ammassari-Teule, and F.R. Fusco. 2009. Phosphodiesterase type IV inhibition prevents sequestration of CREB binding protein, protects striatal parvalbumin interneurons and rescues motor deficits in the R6/2 mouse model of Huntington's disease. Eur. J. Neurosci. 29:902-910.
22. Greer, E.L., P.R. Oskoui, M.R. Banko, J.M. Maniar, M.P. Gygi, S.P. Gygi, and A. Brunet. 2007. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J. Biol. Chem. 282: 30107-30119.
23. Hedbacker, K., and M. Carlson. 2006. Regulation of the nucleocytoplasmic distribution of Snf1-Gal83 protein kinase. Eukaryot. Cell. 5:1950-1956.
24. Horike, N., H. Sakoda, A. Kushiyama, H. Ono, M. Fujishiro, H. Kamata, K. Nishiyama, Y. Uchijima, Y. Kurihara, H. Kurihara, and T. Asano. 2008. AMP-activated protein kinase activation increases phosphorylation of glycogen synthase kinase 3beta and thereby reduces cAMP-responsive element transcriptional activity and phosphoenolpyruvate carboxykinase C gene expression in the liver. J. Biol. Chem. 283:33902-33910.
25. Hurlbert, M.S., W. Zhou, C. Wasmeier, F.G. Kaddis, J.C. Hutton, and C.R. Freed. 1999. Mice transgenic for an expanded CAG repeat in the Huntington's disease gene develop diabetes. Diabetes. 48:649-651.
26. Hurley, R.L., L.K. Barré, S.D. Wood, K.A. Anderson, B.E. Kemp, A.R. Means, and L.A. Witters. 2006. Regulation of AMP-activated protein kinase by multisite phosphorylation in response to agents that elevate cellular cAMP. J. Biol. Chem. 281:36662-36672.
27. Jäger, S., C. Handschin, J. St-Pierre, and B.M. Spiegelman. 2007. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. USA. 104:12017-12022.
28. Ju, T.C., S.D. Chen, C.C. Liu, and D.I. Yang. 2005. Protective effects of S-nitrosoglutathione against amyloid beta-peptide neurotoxicity. Free Radic. Biol. Med. 38:938-949.
29. Jung, J.E., J. Lee, J. Ha, S.S. Kim, Y.H. Cho, H.H. Baik, and I. Kang. 2004. 5-Aminoimidazole-4-carboxamide-ribonucleoside enhances oxidative stress-induced apoptosis through activation of nuclear factor-kappaB in mouse Neuro 2a neuroblastoma cells. Neurosci. Lett. 354:197-200.
30. Kefas, B.A., Y. Cai, Z. Ling, H. Heimberg, L. Hue, D. Pipeleers, and M. Van de Casteele. 2003. AMP-activated protein kinase can induce apoptosis of insulin-producing MIN6 cells through stimulation of c-Jun-N-terminal kinase. J. Mol. Endocrinol. 30:151-161.
31. Kodiha, M., J.G. Rassi, C.M. Brown, and U. Stochaj. 2007. Localization of AMP kinase is regulated by stress, cell density, and signaling through the MEK->ERK1/2 pathway. Am. J. Physiol. Cell Physiol. 293:C1427-C1436.
32. Landles, C., and G.P. Bates. 2004. Huntingtin and the molecular pathogenesis of Huntington's disease. Fourth in molecular medicine review series. EMBO Rep. 5:958-963.
33. Lee, M.J., C.P. Chang, Y.H. Lee, Y.C. Wu, H.W. Tseng, Y.Y. Tung, M.T. Wu, Y.H. Chen, L.T. Kuo, D. Stephenson, et al. 2009. Longitudinal evaluation of an N-ethyl-N-nitrosourea-created murine model with normal pressure hydrocephalus. PLoS ONE. 4:e7868.
34. Liu, F.C., G.C. Wu, S.T. Hsieh, H.L. Lai, H.F. Wang, T.W. Wang, and Y. Chern. 1998. Expression of type VI adenylyl cyclase in the central nervous system: implication for a potential regulator of multiple signals in different neurotransmitter systems. FEBS Lett. 436:92-98.
35. Long, Y.C., and J.R. Zierath. 2006. AMP-activated protein kinase signaling in metabolic regulation. J. Clin. Invest. 116:1776-1783.
36. Lopez-Lopez, C., M.O. Dietrich, F. Metzger, H. Loetscher, and I. Torres-Aleman. 2007. Disturbed cross talk between insulin-like growth factor I and AMPactivated protein kinase as a possible cause of vascular dysfunction in the amyloid precursor protein/presenilin 2 mouse model of Alzheimer's disease. J. Neurosci. 27:824-831.
37. Ma, T.C., J.L. Buescher, B. Oatis, J.A. Funk, A.J. Nash, R.L. Carrier, and K.R. Hoyt. 2007. Metformin therapy in a transgenic mouse model of Huntington's disease. Neurosci. Lett. 411:98-103.
38. Mangiarini, L., K. Sathasivam, M. Seller, B. Cozens, A. Harper, C. Hetherington, M. Lawton, Y. Trottier, H. Lehrach, S.W. Davies, and G.P. Bates. 1996. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell. 87:493-506.
39. Martin, J.B., and J.F. Gusella. 1986. Huntington's disease. Pathogenesis and management. N. Engl. J. Med. 315:1267-1276.
40. McCullough, L.D., Z. Zeng, H. Li, L.E. Landree, J. McFadden, and G.V. Ronnett. 2005. Pharmacological inhibition of AMP-activated protein kinase provides neuroprotection in stroke. J. Biol. Chem. 280:20493-20502. doi:10.1074/jbc.M409985200.
41. Meisse, D., M. Van de Casteele, C. Beauloye, I. Hainault, B.A. Kefas, M.H. Rider, F. Foufelle, and L. Hue. 2002. Sustained activation of AMP-activated protein kinase induces c-Jun N-terminal kinase activation and apoptosis in liver cells. FEBS Lett. 526:38-42.
42. Musi, N., N. Fujii, M.F. Hirshman, I. Ekberg, S. Fröberg, O. Ljungqvist, A. Thorell, and L.J. Goodyear. 2001. AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise. Diabetes. 50:921-927.
43. Nicoletti, I., G. Migliorati, M.C. Pagliacci, F. Grignani, and C. Riccardi. 1991. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods. 139:271-279.
44. Okoshi, R., T. Ozaki, H. Yamamoto, K. Ando, N. Koida, S. Ono, T. Koda, T. Kamijo, A. Nakagawara, and H. Kizaki. 2008. Activation of AMPactivated protein kinase induces p53-dependent apoptotic cell death in response to energetic stress. J. Biol. Chem. 283:3979-3987.
45. Pan, T., M. Cai, L. Tang, L.Q. Zhou, B.J. Li, T. Zhu, H.Z. Li, S.Y. Li, X. Xiao, and Z.S. Chen. 2008. A novel approach of prophylaxis to HBV recurrence after liver transplantation. Virology. 382:1-9.
46. Parker, D., K. Ferreri, T. Nakajima, V.J. LaMorte, R. Evans, S.C. Koerber, C. Hoeger, and M.R. Montminy. 1996. Phosphorylation of CREB at Ser-133 induces complex formation with CREB-binding protein via a direct mechanism. Mol. Cell. Biol. 16:694-703.
47. Pratley, R.E., A.D. Salbe, E. Ravussin, and J.N. Caviness. 2000. Higher sedentary energy expenditure in patients with Huntington's disease. Ann. Neurol. 47:64-70.
48. Raney, M.A., and L.P. Turcotte. 2008. Evidence for the involvement of CaMKII and AMPK in Ca2+-dependent signaling pathways regulating FA uptake and oxidation in contracting rodent muscle. J. Appl. Physiol. 104:1366-1373.
49. Riol-Blanco, L., C. Delgado-Martín, N. Sánchez-Sánchez, L.M. Alonso-C, M.D. Gutiérrez-López, G.M. Del Hoyo, J. Navarro, F. Sánchez-Madrid, C. Cabañas, P. Sánchez-Mateos, and J.L. Rodríguez-Fernández. 2009. Immunological synapse formation inhibits, via NF-kappaB and FOXO1, the apoptosis of dendritic cells. Nat. Immunol. 10:753-760.
50. Salt, I., J.W. Celler, S.A. Hawley, A. Prescott, A. Woods, D. Carling, and D.G. Hardie. 1998. AMP-activated protein kinase: greater AMP dependence, and preferential nuclear localization, of complexes containing the alpha2 isoform. Biochem. J. 334:177-187.
51. Shaw, M.M., W.K. Gurr, R.J. McCrimmon, D.F. Schorderet, and R.S. Sherwin. 2007. 5'AMP-activated protein kinase alpha deficiency enhances stressinduced apoptosis in BHK and PC12 cells. J. Cell. Mol. Med. 11:286-298.
52. Stapleton, D., K.I. Mitchelhill, G. Gao, J. Widmer, B.J. Michell, T. Teh, C.M. House, C.S. Fernandez, T. Cox, L.A. Witters, and B.E. Kemp. 1996. Mammalian AMP-activated protein kinase subfamily. J. Biol. Chem. 271:611-614.
53. Stein, S.C., A. Woods, N.A. Jones, M.D. Davison, and D. Carling. 2000. The regulation of AMP-activated protein kinase by phosphorylation. Biochem. J. 345:437-443.
54. Swulius, M.T., and M.N. Waxham. 2008. Ca(2+)/calmodulin-dependent protein kinases. Cell. Mol. Life Sci. 65:2637-2657.
55. Tang, T.S., E. Slow, V. Lupu, I.G. Stavrovskaya, M. Sugimori, R. Llinás, B.S. Kristal, M.R. Hayden, and I. Bezprozvanny. 2005. Disturbed Ca2+ signaling and apoptosis of medium spiny neurons in Huntington's disease. Proc. Natl. Acad. Sci. USA. 102:2602-2607.
56. The Huntington's Disease Collaborative Research Group. 1993. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell. 72:971-983.
57. Tsuboi, T., G. da Silva Xavier, I. Leclerc, and G.A. Rutter. 2003. 5'-AMP-activated protein kinase controls insulin-containing secretory vesicle dynamics. J. Biol. Chem. 278:52042-52051.
58. Turnley, A.M., D. Stapleton, R.J. Mann, L.A. Witters, B.E. Kemp, and P.F. Bartlett. 1999. Cellular distribution and developmental expression of AMP-activated protein kinase isoforms in mouse central nervous system. J. Neurochem. 72:1707-1716.
59. Valenza, M., J.B. Carroll, V. Leoni, L.N. Bertram, I. Björkhem, R.R. Singaraja, S. Di Donato, D. Lutjohann, M.R. Hayden, and E. Cattaneo. 2007. Cholesterol biosynthesis pathway is disturbed in YAC128 mice and is modulated by huntingtin mutation. Hum. Mol. Genet. 16:2187-2198.
60. Warden, S.M., C. Richardson, J. O'Donnell Jr., D. Stapleton, B.E. Kemp, and L.A. Witters. 2001. Post-translational modifications of the beta-1 subunit of AMP-activated protein kinase affect enzyme activity and cellular localization. Biochem. J. 354:275-283.
61. Weekes, J., K.L. Ball, F.B. Caudwell, and D.G. Hardie. 1993. Specificity determinants for the AMP-activated protein kinase and its plant homologue analysed using synthetic peptides. FEBS Lett. 334:335-339.
62. Wojtaszewski, J.F., J.B. Birk, C. Frøsig, M. Holten, H. Pilegaard, and F. Dela. 2005. 5'AMP activated protein kinase expression in human skeletal muscle: effects of strength training and type 2 diabetes. J. Physiol. 564:563-573.
63. Woods, A., I. Salt, J. Scott, D.G. Hardie, and D. Carling. 1996. The alpha1 and alpha2 isoforms of the AMP-activated protein kinase have similar activities in rat liver but exhibit differences in substrate specificity in vitro. FEBS Lett. 397:347-351.
64. Xiao, X., J. Li, and R.J. Samulski. 1998. Production of high-titer recombinant adeno-associated virus vectors in the absence of helper adenovirus. J. Virol. 72:2224-2232.
65. Yang, W., Y.H. Hong, X.Q. Shen, C. Frankowski, H.S. Camp, and T. Leff. 2001. Regulation of transcription by AMP-activated protein kinase: phosphorylation of p300 blocks its interaction with nuclear receptors. J. Biol. Chem. 276:38341-38344.
66. Zang, Y., L.F. Yu, T. Pang, L.P. Fang, X. Feng, T.Q. Wen, F.J. Nan, L.Y. Feng, and J. Li. 2008. AICAR induces astroglial differentiation of neural stem cells via activating the JAK/STAT3 pathway independently of AMP-activated protein kinase. J. Biol. Chem. 283:6201-6208.
67. Zhang, Y., V.O. Ona, M. Li, M. Drozda, M. Dubois-Dauphin, S. Przedborski, R.J. Ferrante, and R.M. Friedlander. 2003. Sequential activation of individual caspases, and of alterations in Bcl-2 proapoptotic signals in a mouse model of Huntington's disease. J. Neurochem. 87:1184-1192.