Regulation of the mTOR signaling network in hibernating thirteen-lined ground squirrels

Journal of Experimental Biology

Volumn 215, Issue 10, 2012, Pages 1720-1727

  Wu, Cheng Wei ^a   Storey, Kenneth B ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

4EBP; Akt; Ictidomys tridecemlineatus; Torpor arousal cycle; Translational control

Indexed keywords

INITIATION FACTOR; MTOR PROTEIN, HUMAN; PROTEIN KINASE B; TARGET OF RAPAMYCIN KINASE;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; ENVIRONMENT; HIBERNATION; METABOLISM; PHOSPHORYLATION; PROTEIN SYNTHESIS; SCIURIDAE; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TEMPERATURE;

ANIMALS; ENVIRONMENT; EUKARYOTIC INITIATION FACTORS; HIBERNATION; MODELS, BIOLOGICAL; MUSCLE, SKELETAL; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; PROTO-ONCOGENE PROTEINS C-AKT; SCIURIDAE; SIGNAL TRANSDUCTION; TEMPERATURE; TOR SERINE-THREONINE KINASES;

MAMMALIA; SPERMOPHILUS TRIDECEMLINEATUS;

EID: 84861125607     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.066225     Document Type: Article

References (57)

1. Abnous, K., Dieni, C. A. and Storey, K. B. (2008). Regulation of Akt during hibernation in Richardson's ground squirrels. Biochim. Biophys. Acta 1780, 185-193. (Pubitemid 351162895)
2. Brauch, K. M., Dhruv, N. D., Hanse, E. A. and Andrews, M. T. (2005). Digital transcriptome analysis indicates adaptive mechanisms in the heart of a hibernating mammal. Physiol. Genom. 23, 227-234. (Pubitemid 44437981)
3. Brooks, N. E., Myburgh, K. H. and Storey, K. B. (2011). Myostatin levels in skeletal muscle of hibernating ground squirrels. J. Exp. Biol. 214, 2522-2527.
4. Cai, D., McCarron, R. M., Yu, E. Z., Li, Y. and Hallenbeck, J. M. (2004). Akt phosphorylation and kinase activity are down-regulated during hibernation in the 13-lined ground squirrel. Brain Res. 1014, 14-21. (Pubitemid 38798448)
5. Carey, H. V., Andrews, M. T. and Martin, S. L. (2003). Mammalian hibernation: Cellular and molecular responses to depressed metabolism and low temperature. Physiol. Rev. 83, 1153-1181. (Pubitemid 37222270)
6. Carrera, A. C. (2004). TOR signaling in mammals. J. Cell Sci. 117, 4615-4616. (Pubitemid 39433427)
7. Connolly, E., Braunstein, S., Formenti, S. and Schneider, R. J. (2006). Hypoxia inhibits protein synthesis through a 4E-BP1 and elongation factor 2 kinase pathway controlled by mTOR and uncoupled in breast cancer cells. Mol. Cell. Biol. 26, 3955-3965. (Pubitemid 43726410)
8. Eddy, S. F., Morin, P., Jr and Storey, K. B. (2005). Cloning and expression of PPARgamma and PGC-1alpha from the hibernating ground squirrel, Spermophilus tridecemlineatus. Mol. Cell. Biochem. 269, 175-182. (Pubitemid 40287815)
9. Fahlman, A., Storey, J. M. and Storey, K. B. (2000). Gene up-regulation in heart during mammalian hibernation. Cryobiology 40, 332-342. (Pubitemid 30666408)
10. Foster, K. G. and Fingar, D. C. (2010). Mammalian target of rapamycin (mTOR): Conducting the cellular signaling symphony. J. Biol. Chem. 285, 14071-14077.
11. Frerichs, K. U., Smith, C. B., Brenner, M., DeGracia, D. J., Krause, G. S., Marrone, L., Dever, T. E. and Hallenbeck, J. M. (1998). Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc. Natl. Acad. Sci. USA 95, 14511-14516. (Pubitemid 28549398)
12. Hay, N. and Sonenberg, N. (2004). Upstream and downstream of mTOR. Genes Dev. 18, 1926-1945. (Pubitemid 39071573)
13. Hittel, D. and Storey, K. B. (2001). Differential expression of adipose-and heart-type fatty acid binding proteins in hibernating ground squirrels. Biochim. Biophys. Acta 1522, 238-243. (Pubitemid 34075550)
14. Huang, J. and Manning, B. D. (2008). The TSC1-TSC2 complex: A molecular switchboard controlling cell growth. Biochem. J. 412, 179-190. (Pubitemid 351758225)
15. Inoki, K., Li, Y., Zhu, T., Wu, J. and Guan, K. L. (2002). TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat. Cell. Biol. 4, 648-657. (Pubitemid 34993700)
16. Kelly, J. M. and McBride, B. W. (1990). The sodium pump and other mechanisms of thermogenesis in selected tissues. Proc. Nutr. Soc. 49, 185-202.
17. Kim, D. H., Sarbassov, D. D., Ali, S. M., Latek, R. R., Guntur, K. V., Erdjument-Bromage, H., Tempst, P. and Sabatini, D. M. (2003). GbL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol. Cell 11, 895-904. (Pubitemid 36566312)
18. Kim, E., Goraksha-Hicks, P., Li, L., Neufeld, T. P. and Guan, K. L. (2008). Regulation of TORC1 by Rag GTPases in nutrient response. Nat. Cell Biol. 10, 935-945.
19. Kovacina, K. S., Park, G. Y., Bae, S. S., Guzzetta, A. W., Schaefer, E., Birnbaum, M. J. and Roth, R. A. (2003). Identification of a proline-rich Akt substrate as a 14-3-3 binding partner. J. Biol. Chem. 278, 10189-10194. (Pubitemid 36800278)
20. Lee, K., Park, J. Y., Yoo, W., Gwag, T., Lee, J. W., Byun, M. W. and Choi, I. (2008). Overcoming muscle atrophy in a hibernating mammal despite prolonged disuse in dormancy: Proteomic and molecular assessment. J. Cell. Biochem. 104, 642-656. (Pubitemid 351671651)
21. Lee, K., So, H., Gwag, T., Ju, H., Lee, J. W., Yamashita, M. and Choi, I. (2010). Molecular mechanism underlying muscle mass retention in hibernating bats: Role of periodic arousal. J. Cell. Physiol. 222, 313-319.
22. Ma, X. M. and Blenis, J. (2009). Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 10, 307-318.
23. MacDonald, J. A. and Storey, K. B. (1999). Regulation of ground squirrel Na+ K+-ATPase activity by reversible phosphorylation during hibernation. Biochem. Biophys. Res. Commun. 254, 424-429. (Pubitemid 29290416)
24. Mamady, H. and Storey, K. B. (2006). Up-regulation of the endoplasmic reticulum molecular chaperone GRP78 during hibernation in thirteen-lined ground squirrels. Mol. Cell. Biochem. 292, 89-98. (Pubitemid 44697403)
25. Mathews, M. B., Sonenberg, N. and Hershey, J. W. B. (2000). Origins and principles of translational control. In Translational Control of Gene Expression (ed. M.B. Mathews), pp. 1-31. New York: Cold Spring Harbor Laboratory Press.
26. Meyuhas, O., Avni, D. and Shama, S. (1996). Translational control of ribosomal protein mRNAs in eukaryotes. In Translational Control (ed. J. W. B. Hershey, M. B. Mathews and N. Sonenberg), pp. 363-388. New York: Cold Spring Harbor Laboratory Press.
27. McArthur, M. D. and Milsom, W. K. (1991). Changes in ventilation and respiratory sensitivity associated with hibernation in Columbian (Spermophilus columbianus) and golden-mantled (Spermophilus lateralis) ground squirrels. Physiol. Zool. 64, 940-959.
28. McManus, E. J. and Alessi, D. R. (2002).TSC1-TSC2: A complex tale of PKBmediated S6K regulation. Nat. Cell Biol. 4, 214-216.
29. McMullen, D. C. and Hallenbeck, J. (2010). Regulation of Akt during torpor in the hibernating ground squirrel, Ictidomys tridecemlineatus. J. Comp. Physiol. B 180, 927-934.
30. Morin, P., Jr and Storey, K. B. (2006). Evidence for a reduced transcriptional state during hibernation in ground squirrels. Cryobiology 53, 310-318. (Pubitemid 46026754)
31. Morin, P., Jr, Ni, Z., McMullen, D. C. and Storey, K. B. (2008). Expression of Nrf2 and its downstream gene targets in hibernating 13-lined ground squirrels, Spermophilus tridecemlineatus. Mol. Cell. Biochem. 312, 121-129.
32. Nielsen, P. J., Thomas, G. and Maller, J. L. (1982). Increased phosphorylation of ribosomal protein S6 during meiotic maturation of Xenopus oocytes. Proc. Natl. Acad. Sci. USA 79, 2937-2941. (Pubitemid 12032346)
33. Nowell, M. M., Choi, H. and Rourke, B. C. (2011). Muscle plasticity in hibernating ground squirrels (Spermophilus lateralis) is induced by seasonal, but not lowtemperature, mechanisms. J. Comp. Physiol. B 181, 147-164.
34. Pende, M., Um, S. H., Mieulet, V., Sticker, M., Goss, V. L., Mestan, J., Mueller, M., Fumagalli, S., Kozma, S. C. and Thomas, G. (2004). S6K1-/-/S6K2-/-mice exhibit perinatal lethality and rapamycin-sensitive 5-terminal oligopyrimidine mRNA translation and reveal a mitogen-activated protein kinase-dependent S6 kinase pathway. Mol. Cell. Biol. 24, 3112-3124. (Pubitemid 38452057)
35. Pestova, T. V. and Hellen, C. U. (2003). Translation elongation after assembly of ribosomes on the cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes Dev. 17, 181-186. (Pubitemid 36105891)
36. Pullen, N. and Thomas, G. (1997). The modular phosphorylation and activation of p70s6k. FEBS Lett. 410, 78-82.
37. Rolfe, D. F. and Brown, G. C. (1997). Cellular energy utilization and molecular origin of standard metabolic rate in mammals. Physiol. Rev. 77, 731-758. (Pubitemid 27328739)
38. Ruggero, D. and Sonenberg, N. (2005). The Akt of translational control. Oncogene 24, 7426-7434. (Pubitemid 41637982)
39. Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., Walsh, K., Schiaffino, S., Lecker, S. H. and Goldberg, A. L. (2004). Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117, 399-412. (Pubitemid 38534545)
40. Schmelzle, T. and Hall, M. N. (2000). TOR, a central controller of cell growth. Cell 103, 253-262.
41. Song, G., Ouyang, G. and Bao. S. (2005). The activation of Akt/PKB signaling pathway and cell survival. J. Cell. Mol. Med. 9, 59-71.
42. Stitt, T. N., Drujan, D., Clarke, B. A., Panaro, F., Timofeyva, Y., Kline, W. O., Gonzalez, M., Yancopoulos, G. D. and Glass, D. J. (2004). The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell 14, 395-403. (Pubitemid 38591410)
43. Storey, K. B. (2010). Out cold: Biochemical regulation of mammalian hibernation. Gerontology 56, 220-230.
44. Storey, K. B. and Storey, J. M. (2004). Mammalian hibernation: Biochemical adaptation and gene expression. In Functional Metabolism, Regulation and Adaptation (ed. K. B. Storey), pp. 443-471. Hoboken, NJ: Wiley-Liss.
45. Storey, K. B. and Storey, J. M. (2007). Tribute to P. L. Lutz: Putting life on ?pause'-molecular regulation of hypometabolism. J. Exp. Biol. 210, 1700-1714. (Pubitemid 46953573)
46. Storey, K. B. and Storey, J. M. (2010). Metabolic rate depression: The biochemistry of mammalian hibernation. Adv. Clin. Chem. 52, 77-108.
47. Tokunaga, C., Yoshino, K. and Yonezawa, K. (2004). mTOR integrates amino acidand energy-sensing pathways. Biochem. Biophys. Res. Commun. 313, 443-446. (Pubitemid 37543606)
48. van Breukelen, F., Sonenberg, N. and Martin, S. L. (2004). Seasonal and statedependent changes of eIF4E and 4E-BP1 during mammalian hibernation: Implications for the control of translation during torpor. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, 349-353.
49. Vander Haar, E., Lee, S. I., Bandhakavi, S., Griffin, T. J. and Kim, D. H. (2007). Insulin signalling to mTOR mediated by the Akt/PKB substrate PRAS40. Nat. Cell Biol. 9, 316-323. (Pubitemid 46344611)
50. Wang, L., Harris, T. E. and Lawrence, J. C., Jr (2008). Regulation of proline-rich Akt substrate of 40 kDa (PRAS40) function by mammalian target of rapamycin complex 1 (mTORC1)-mediated phosphorylation. J. Biol. Chem. 283, 15619-15627.
51. Wang, L. C. H. and Wolowyk, M. W. (1987). Topor in mammals and birds. Can. J. Zool. 66, 133-137.
52. Wang, X. and Proud, C. G. (2006). The mTOR pathway in the control of protein synthesis. Physiology 21, 362-369. (Pubitemid 44511764)
53. Wickler, S. J., Hoyt, D. F. and van Breukelen, F. (1991). Disuse atrophy in the hibernating golden-mantled ground squirrel, Spermophilus lateralis. Am. J. Physiol. 261, 1214-1217.
54. Yan, J., Barnes, B. M., Kohl, F. and Marr, T. G. (2008). Modulation of gene expression in hibernating arctic ground squirrels. Physiol. Genomics 32, 170-181. (Pubitemid 351186324)
55. Yang, Q. and Guan, K. L. (2007). Expanding mTOR signaling. Cell Res. 17, 666-681. (Pubitemid 47255937)
56. Zatzman, M. L. (1984). Renal and cardiovascular effects of hibernation and hypothermia. Cryobiology 21, 593-614. (Pubitemid 15221650)
57. Zhegunov, G. F., Mikulinsky, Y. E. and Kudokotseva, E. V. (1988). Hyperactivation of protein synthesis in tissues of hibernating animals on arousal. CryoLetters 9, 236-245.