AMPK agonist AICAR improves cognition and motor coordination in young and aged mice

Learning and Memory

Volumn 21, Issue 2, 2014, Pages 119-126

  Kobilo, Tali ^a   Guerrieri, Davide ^a   Zhang, Yongqing ^a   Collica, Sarah C ^a   Becker, Kevin G ^a   Van Praag, Henriette ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CENTRAL NERVOUS SYSTEM AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; HIPPOCAMPUS; MAZE LEARNING; MEMORY; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SKELETAL; PSYCHOMOTOR PERFORMANCE; RIBONUCLEOSIDES; SPACE PERCEPTION; TIME FACTORS;

EID: 84894286799     PISSN: 10720502     EISSN: 15495485     Source Type: Journal    
DOI: 10.1101/lm.033332.113     Document Type: Article

References (67)

1. Avraham H, Park SY, Schinkmann K, Avraham S. 2000. RAFTK/Pyk2-mediated cellular signaling. Cell Signal 12: 123-133.
2. Baumgartner RN, Rhyne RL, Troup C, Wayne S, Garry PJ. 1992. Appendicular skeletal muscle areas assessed by magnetic resonance imaging in older persons. J Gerontol 47: M67-M72.
3. Black JE, Isaacs KR, Anderson BJ, Alcantara AA, Greenough WT. 1990. Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats. Proc Natl Acad Sci 87: 5568-5572.
4. Bratic I, Trifunovic A. 2010. Mitochondrial energy metabolism and ageing. Biochim Biophys Acta 1797: 961-967.
5. Bueno Júnior CR, Pantaleão LC, Voltarelli VA, Bozi LH, Brum PC, Zatz M. 2012. Combined effect of AMPK/PPAR agonists and exercise training in mdx mice functional performance. PLoS One 7: e45699.
6. Cabeza-Arvelaiz Y, Fleming SM, Richter F, Masliah E, Chesselet MF, Schiestl RH. 2011. Analysis of striatal transcriptome in mice overexpressing human wild-type a-synuclein supports synaptic dysfunction and suggests mechanisms of neuroprotection for striatal neurons. Mol Neurodegener 6: 83.
7. Cheadle C, Vawter MP, Freed WJ, Becker KG. 2003. Analysis of microarray data using Z score transformation. J Mol Diagn 5: 73-81.
8. Chen Scarabelli C, McCauley RB, Yuan Z, Di Rezze J, Patel D, Putt J, Raddino R, Allebban Z, Abboud J, Scarabelli GM, et al. 2008. Oral administration of amino acidic supplements improves protein and energy profiles in skeletal muscle of aged rats: Elongation of functional performance and acceleration of mitochondrial recovery in adenosine triphosphate after exhaustive exertion. Am J Cardiol 101: 42E-48E.
9. Cheng A, Wan R, Yang JL, Kamimura N, Son TG, Ouyang X, Luo Y, Okun E, Mattson MP. 2012. Involvement of PGC-1a in the formation and maintenance of neuronal dendritic spines. Nat Comm 3: 1250.
10. Corsetti G, Pasini E, D'Antona G, Nisoli E, Flati V, Assanelli D, Dioguardi FS, Bianchi R. 2008. Morphometric changes induced by amino acid supplementation in skeletal and cardiac muscles of old mice. Am J Cardiol 101: 26E-34E.
11. Dagon Y, Avraham Y, Berry EM. 2006. AMPK activation regulates apoptosis, adipogenesis, and lipolysis by eIF2a in adipocytes. Biochem Biophys Res Commun 340: 43-47.
12. Dash PK, Orsi SA, Moore AN. 2006. Spatial memory formation and memory-enhancing effect of glucose involves activation of the tuberous sclerosis complex-Mammalian targetof rapamycin pathway. J Neurosci 26: 8048-8056.
13. De S, Zhang Y, Garner JR, Wang SA, Becker KG. 2010. Disease and phenotype gene set analysis of disease-based gene expression in mouse and human. Physiol Genomics 42A: 162-167.
14. Deng B, Glanzman D, Tidball JG. 2009. Nitric oxide generated by muscle corrects defects in hippocampal neurogenesis and neural differentiation caused by muscular dystrophy. J Physiol 587(Pt 8): 1769-1778.
15. Donkor J, Sariahmetoglu M, Dewald J, Brindley DN, Reue K. 2007. Three mammalian lipins act as phosphatidate phosphatases with distinct tissue expression patterns. J Biol Chem 282: 3450-3457.
16. Edgar R, Domrachev M, Lash AE. 2002. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
17. Erickson CA, Barnes CA. 2003. The neurobiology of memory changes in normal aging. Exp Gerontol 38: 61-69.
18. Figueiredo PA, Mota MP, Appell HJ, Duarte JA. 2008. The role of mitochondria in aging of skeletal muscle. Biogerontology 9: 67-84.
19. Fryer LG, Hajduch E, Rencurel F, Salt IP, Hundal HS, Hardie DG, Carling D. 2000. Activation of glucose transport by AMP-activated protein kinase via stimulation of nitric oxide synthase. Diabetes 49: 1978-1985.
20. Granger R, Wiebe SP, Taketani M, Lynch G. 1996. Distinct memory circuits composing the hippocampal region. Hippocampus 6: 567-578.
21. Hardie DG. 2011a. Energy sensing bythe AMP-activated protein kinase and its effects on muscle metabolism. Proc Nutr Soc 70: 92-99.
22. Hardie DG. 2011b. Sensing of energy and nutrients by AMP-activated protein kinase. Am J Clin Nutr 93: 891S-896S.
23. Hardie DG, Ross FA, Hawley SA. 2012. AMPK: A nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13: 251-262.
24. Harris RA, Bowker-Kinley MM, Wu P, Jeng J, Popov KM. 1997. Dihydrolipoamide dehydrogenase-binding protein of the human pyruvate dehydrogenase complex. DNA-derived amino acid sequence, expression, and reconstitution of the pyruvate dehydrogenase complex. J Biol Chem 272: 19746-19751.
25. Hillman CH, Erickson KI, Kramer AF. 2008. Be smart, exercise your heart: Exercise effects on brain and cognition. Nat Rev Neurosci 9: 58-65.
26. Kobilo T, van Praag H. 2012. Muscle fatigue and cognition: What is the link? Front Physiol 3: 14.
27. Kobilo T, Yuan C, van Praag H. 2011. Endurance factors improve hippocampal neurogenesis and spatial memory in mice. Learn Mem 18: 103-107.
28. Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB. 2010. Sarcopenia: Etiology, clinical consequences, intervention, and assessment. Osteoporos Int 21: 543-559.
29. Ljubicic V, Hood DA. 2009. Diminished contraction-induced intracellular signaling towards mitochondrial biogenesis in aged skeletal muscle. Aging Cell 8: 394-404.
30. Mansouri A, Muller FL, Liu Y, Ng R, Faulkner J, Hamilton M, Richardson A, Huang TT, Epstein CJ, Van Remmen H. 2006. Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging. Mech Ageing Dev 127: 298-306.
31. Marangos PJ, Loftus T, Wiesner J, Lowe T, Rossi E, Browne CE, Gruber HE. 1990. Adenosinergic modulation of homocysteine-induced seizures in mice. Epilepsia 31: 239-246.
32. März P, Probst A, Lang S, Schwager M, Rose-John S, Otten U, Ozbek S. 2004. Ataxin-10, the spinocerebellar ataxia type 10 neurodegenerative disorder protein, is essential for survival of cerebellar neurons. J Biol Chem 279: 35542-35550.
33. Mattson MP. 2012. Energy intake and exercise as determinants of brain health and vulnerability to injury and disease. Cell Metab 16: 706-722.
34. Mattson MP, Magnus T. 2006. Ageing and neuronal vulnerability. Nat Rev Neurosci 7: 278-294.
35. McDermott C, Cardoso MC, Yu YT, Andres V, Leifer D, Krainc D, Lipton SA, Nadal-Ginard B. 1993. hMEF2C gene encodes skeletal muscle-and brain-specific transcription factors. J Mol Cell Biol 13: 2564-2577.
36. Mironova YA, Giger RJ. 2013. Where no synapses go: Gatekeepers of circuit remodeling and synaptic strength. Trends Neurosci 36: 363-373.
37. Miura S, Kai Y, Kamei Y, Bruce CR, Kubota N, Febbraio MA, Kadowaki T, Ezaki O. 2009. a2-AMPK activity is not essential for an increase in fatty acid oxidation during low-intensity exercise. Am J Physiol Endocrinol Metab 296: E47-E55.
38. Morris RG, Garrud P, Rawlins JN, O'Keefe J. 1982. Place navigation impaired in rats with hippocampal lesions. Nature 24: 681-683.
39. Nagata A, Suzuki Y, Igarashi M, Eguchi N, Toh H, Urade Y, Hayaishi O.1991. Human brain prostaglandin D synthase has been evolutionarily differentiated from lipophilic-ligand carrier proteins. Proc Natl Acad Sci 88: 4020-4024.
40. Nakamura T, Komiya M, Sone K, Hirose E, Gotoh N, Morii H, Ohta Y, Mori N. 2002. Grit, a GTPase-activating protein for the Rho family, regulates neurite extension through association with the TrkA receptor and N-Shc and CrkL/Crk adapter molecules. Mol Cell Biol 22: 8721-8734.
41. Nakamura K, Nakano S, Miyoshi T, Yamanouchi K, Matsuwaki T, Nishihara M. 2012. Age-related resistance of skeletal muscle-derived progenitor cells to SPARC may explain a shift from myogenesis to adipogenesis. Aging 4: 40-48.
42. Narkar VA, Downes M, Yu RT, Embler E, Wang YX, Banayo E, Mihaylova MM, Nelson MC, Zou Y, Juguilon H, et al. 2008. AMPK and PPARd agonists are exercise mimetics. Cell 134: 405-415.
43. Nelson JF, Felicio LS, Randall PK, Sims C, Finch CE. 1982. A longitudinal study of estrous cyclicity in aging C57BL/6J mice: I. Cycle frequency, length and vaginal cytology. Biol Reprod 27: 327-339.
44. Ornatsky OI, McDermott JC. 1996. MEF2 protein expression, DNA binding specificity and complex formation, and transcriptional activity in muscle and non-muscle cells. J Biol Chem 271: 24927-24933.
45. Pedersen PL, Amzel LM. 1993. ATP synthases. Structure, reaction center, mechanism, and regulation of one of nature's most unique machines. J Biol Chem 268: 9937-9940.
46. Pedersen BK, Febbraio MA. 2012. Muscles, exercise and obesity: Skeletal muscle as a secretory organ. Nat Rev Endocrinol 8: 4574-4565.
47. Pedersen BK, Steensberg A, Fischer C, Keller C, Keller P, Plomgaard P, Febbraio M, Saltin B. 2003. Searching for the exercise factor: Is IL-6 a candidate? J Muscle Res Cell Motil 24: 113-119.
48. Peterson CM, Johannsen DL, Ravussin E. 2012. Skeletal muscle mitochondria and aging: A review. J Aging Res 2012: 194821.
49. Pfaffl MW. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
50. Potter WB, O'Riordan KJ, Barnett D, Osting SM, Wagoner M, Burger C, Roopra A. 2010. Metabolic regulation of neuronal plasticity by the energy sensor AMPK. PLoS One 5: 8996.
51. Qiang W, Weiqiang K, Qing Z, Pengju Z, Yi L. 2007. Aging impairs insulin-stimulated glucose uptake in rat skeletal muscle via suppressing AMPKa. Exp Mol Med 39: 535-543.
52. Reznick RM, Zong H, Li J, Morino K, Moore IK, Yu HJ, Liu ZX, Dong J, Mustard KJ, Hawley SA, et al. 2007. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab 5: 151-156.
53. Sakuma K, Yamaguchi A. 2011. The recent understanding of the neurotrophin's role in skeletal muscle adaptation. J Biomed Biotechnol 2011: 201696.
54. Segatto O, Anastasi S, Alemà S. 2011. Regulation of epidermal growth factor receptor signalling by inducible feedback inhibitors. J Cell Sci 124(Pt 11): 1785-1793.
55. Sun X-y, Hayashi Y, Xu S, Kanou Y, Takagishi Y, Tang Y-p, Murata Y. 2011. Inactivation of the Rcan2 gene in mice ameliorates the age-and diet-induced obesity by causing a reduction in food intake. PLoS One 6: e14605.
56. Teng FY, Tang BL. 2008. Cell autonomous function of Nogo and reticulons: The emerging story at the endoplasmic reticulum. J Cell Physiol 216: 303-308.
57. Teng FY, Tang BL. 2013. Nogo/RTN4 isoforms and RTN3 expression protect SH-SY5Y cells against multiple death insults. Mol Cell Biochem 384: 7-19.
58. Terry AV Jr. 2009. Spatial navigation (water maze) tasks. In Methods of behavior analysis in neuroscience, 2nd ed. (ed. Buccafusco JJ), Chapter 13. CRC Press, Boca Raton, FL.
59. Thomson DM, Winder WW. 2009. AMP-activated protein kinase control of fat metabolism in skeletal muscle. Acta Physiol (Oxf) 196: 147-154.
60. van Praag H. 2008. Neurogenesis and exercise: Past and future directions. Neuromolecular Med 10: 128-140.
61. van Rooij E, Quiat D, Johnson BA, Sutherland LB, Qi X, Richardson JA, Kelm RJ Jr., Olson EN. 2009. A familyof microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev Cell 17: 662-673.
62. Walker JE. 1992. The NADH: Ubiquinone oxidoreductase (complex I) of respiratory chains. Q Rev Biophys 25: 253-324.
63. Wu QF, Yang L, Li S, Wang Q, Yuan XB, Gao X, Bao L, Zhang X. 2012. Fibroblast growth factor 13 is a microtubule-stabilizing protein regulating neuronal polarization and migration. Cell 149: 1549-1564.
64. Xu Y, Zhang HT, O'Donnell JM. 2011. Phosphodiesterases in the central nervous system: Implications in mood and cognitive disorders. Handb Exp Pharmacol 204: 447-485.
65. Zhang Y, De S, Garner JR, Smith K, Wang SA, Becker KG. 2010. Systematic analysis, comparison, and integration of disease based human genetic association data and mouse genetic phenotypic information. BMC Med Genomics 3: 1.
66. Zong H, Ren JM, Young LH, Pypaert M, Mu J, Birnbaum MJ, Shulman GI. 2002. AMP kinase is required for mitochondrial biogenesis in skeletal muscle in response to chronic energy deprivation. Proc Natl Acad Sci 99: 15983-15987.
67. Zwetsloot KA, Westerkamp LM, Holmes BF, Gavin TP. 2008. AMPK regulates basal skeletal muscle capillarization and VEGF expression, but is not necessary for the angiogenic response to exercise. J Physiol 586: 6021-6035.