Alkaline stress-induced autophagy is mediated by mTORC1 inactivation

Journal of Cellular Biochemistry

Volumn 112, Issue 9, 2011, Pages 2566-2573

  Suk, Jinkyu ^a   Kwak, Sang Su ^a   Lee, Jae Ho ^a   Choi, Ji Hye ^a   Lee, Sang Hee ^a   Lee, Dong Hwan ^b   Byun, Boohyeong ^c   Lee, Geon Hyoung ^d   Joe, Cheol O ^a  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Soonchunhyang University   (South Korea)

^c Daegu Haany University   (South Korea)

^d Kunsan National University   (South Korea)

Author keywords

Alkaline stress; Autophagy; LC3; mTOR; pH

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; PROTEIN KINASE B;

ALKALINE STRESS; ANIMAL CELL; ARTICLE; AUTOLYSOSOME; AUTOPHAGOSOME; AUTOPHAGY; CELL SIZE; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME INACTIVATION; HELA CELL; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STRESS;

ALKALOSIS; AUTOPHAGY; CELL SIZE; DOWN-REGULATION; ENZYME ACTIVATION; HEK293 CELLS; HELA CELLS; HUMANS; LYSOSOMES; MICROTUBULE-ASSOCIATED PROTEINS; MONOMERIC GTP-BINDING PROTEINS; MUTATION, MISSENSE; NEUROPEPTIDES; PHAGOSOMES; PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

MAMMALIA;

EID: 84860410788     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.23181     Document Type: Article

References (47)

1. Bai JH, Wang HJ, Zhou HM,. 1998. Alkaline-induced unfolding and salt-induced folding of pig heart lactate dehydrogenase under high pH conditions. Int J Biol Macromol 23: 127-133.
2. Balgi AD, Fonseca BD, Donohue E, Tsang TC, Lajoie P, Proud CG, Nabi IR, Roberge M,. 2009. Screen for chemical modulators of autophagy reveals novel therapeutic inhibitors of mTORC1 signaling. PLoS One 4: e7124.
3. Chan EY,. 2009. mTORC1 phosphorylates the ULK1-mAtg13-FIP200 autophagy regulatory complex. Sci Signal 2: pe51.
4. Eng CH, Yu K, Lucas J, White E, Abraham RT,. 2010. Ammonia derived from glutaminolysis is a diffusible regulator of autophagy. Sci Signal 3: ra31.
5. Eskelinen EL,. 2005. Maturation of autophagic vacuoles in Mammalian cells. Autophagy 1: 1-10.
6. Fimia GM, Stoykova A, Romagnoli A, Giunta L, Di Bartolomeo S, Nardacci R, Corazzari M, Fuoco C, Ucar A, Schwartz P, Gruss P, Piacentini M, Chowdhury K, Cecconi F,. 2007. Ambra1 regulates autophagy and development of the nervous system. Nature 447: 1121-1125. (Pubitemid 47014434)
7. Fingar DC, Blenis J,. 2004. Target of rapamycin (TOR): An integrator of nutrient and growth factor signals and coordinator of cell growth and cell cycle progression. Oncogene 23: 3151-3171. (Pubitemid 38638827)
8. Fingar DC, Salama S, Tsou C, Harlow E, Blenis J,. 2002. Mammalian cell size is controlled by mTOR and its downstream targets S6K1 and 4EBP1/eIF4E. Genes Dev 16: 1472-1487. (Pubitemid 34686329)
9. Freundt EC, Czapiga M, Lenardo MJ,. 2007. Photoconversion of Lysotracker Red to a green fluorescent molecule. Cell Res 17: 956-958. (Pubitemid 350126866)
10. Galla JH,. 2000. Metabolic alkalosis. J Am Soc Nephrol 11: 369-375. (Pubitemid 30064861)
11. Gillies RJ, Martinez-Zaguilan R, Martinez GM, Serrano R, Perona R,. 1990. Tumorigenic 3T3cells maintain an alkaline intracellular pH under physiological conditions. Proc Natl Acad Sci U S A 87: 7414-7418.
12. Gordon PB, Holen I, Fosse M, Rotnes JS, Seglen PO,. 1993. Dependence of hepatocytic autophagy on intracellularly sequestered calcium. J Biol Chem 268: 26107-26112. (Pubitemid 23361674)
13. Gulati P, Gaspers LD, Dann SG, Joaquin M, Nobukuni T, Natt F, Kozma SC, Thomas AP, Thomas G,. 2008. Amino acids activate mTOR complex 1 via Ca2+/CaM signaling to hVps34. Cell Metab 7: 456-465. (Pubitemid 351598024)
14. Han EK, Leverson JD, McGonigal T, Shah OJ, Woods KW, Hunter T, Giranda VL, Luo Y,. 2007. Akt inhibitor A-443654 induces rapid Akt Ser-473 phosphorylation independent of mTORC1 inhibition. Oncogene 26: 5655-5661. (Pubitemid 47267835)
15. Harrington LS, Findlay GM, Lamb RF,. 2005. Restraining PI3K: mTOR signalling goes back to the membrane. Trends Biochem Sci 30: 35-42. (Pubitemid 40093739)
16. Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N, Guan JL, Oshiro N, Mizushima N,. 2009. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 20: 1981-1991.
17. Hoyer-Hansen M, Bastholm L, Szyniarowski P, Campanella M, Szabadkai G, Farkas T, Bianchi K, Fehrenbacher N, Elling F, Rizzuto R, Mathiasen IS, Jaattela M,. 2007. Control of macroautophagy by calcium, calmodulin-dependent kinase kinase-beta, and Bcl-2. Mol Cell 25: 193-205. (Pubitemid 46109606)
18. Jacinto E, Loewith R, Schmidt A, Lin S, Ruegg MA, Hall A, Hall MN,. 2004. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol 6: 1122-1128. (Pubitemid 39468014)
19. Jiang H, Vogt PK,. 2008. Constitutively active Rheb induces oncogenic transformation. Oncogene 27: 5729-5740.
20. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, Kundu M, Kim DH,. 2009. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20: 1992-2003.
21. Jung CH, Ro SH, Cao J, Otto NM, Kim DH,. 2010. mTOR regulation of autophagy. FEBS Lett 584: 1287-1295.
22. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM,. 2002. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110: 163-175. (Pubitemid 34876545)
23. Klionsky DJ,. 2005. The molecular machinery of autophagy: Unanswered questions. J Cell Sci 118: 7-18. (Pubitemid 40277100)
24. Laplante M, Sabatini DM,. 2009. mTOR signaling at a glance. J Cell Sci 122: 3589-3594.
25. Levine B, Kroemer G,. 2008. Autophagy in the pathogenesis of disease. Cell 132: 27-42.
26. Long X, Ortiz-Vega S, Lin Y, Avruch J,. 2005. Rheb binding to mammalian target of rapamycin (mTOR) is regulated by amino acid sufficiency. J Biol Chem 280: 23433-23436. (Pubitemid 40884818)
27. Madshus IH,. 1988. Regulation of intracellular pH in eukaryotic cells. Biochem J 250: 1-8.
28. Majima HJ, Oberley TD, Furukawa K, Mattson MP, Yen HC, Szweda LI, St Clair DK,. 1998. Prevention of mitochondrial injury by manganese superoxide dismutase reveals a primary mechanism for alkaline-induced cell death. J Biol Chem 273: 8217-8224. (Pubitemid 28168878)
29. Manning BD,. 2004. Balancing Akt with S6K: Implications for both metabolic diseases and tumorigenesis. J Cell Biol 167: 399-403. (Pubitemid 39489047)
30. Marcaggi P, Coles JA,. 2001. Ammonium in nervous tissue: Transport across cell membranes, fluxes from neurons to glial cells, and role in signalling. Prog Neurobiol 64: 157-183. (Pubitemid 32195411)
31. Mizushima N, Levine B, Cuervo AM, Klionsky DJ,. 2008. Autophagy fights disease through cellular self-digestion. Nature 451: 1069-1075. (Pubitemid 351317450)
32. Murachi T, Yamazaki M,. 1970. Changes in conformation and enzymatic activity of stem bromelain in alkaline media. Biochemistry 9: 1935-1938.
33. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, Lane H, Hofmann F, Hicklin DJ, Ludwig DL, Baselga J, Rosen N,. 2006. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 66: 1500-1508. (Pubitemid 43259931)
34. Pattingre S, Espert L, Biard-Piechaczyk M, Codogno P,. 2008. Regulation of macroautophagy by mTOR and Beclin 1 complexes. Biochimie 90: 313-323. (Pubitemid 351181247)
35. Regula CS, Pfeiffer JR, Berlin RD,. 1981. Microtubule assembly and disassembly at alkaline pH. J Cell Biol 89: 45-53. (Pubitemid 11066129)
36. Rose BD,. 1994. Clinical physiology of acid-base and electrolyte disorders. New York: McGraw-Hill, Health Professions Division. p x, 916 p.
37. Rose C, Kresse W, Kettenmann H,. 2005. Acute insult of ammonia leads to calcium-dependent glutamate release from cultured astrocytes, an effect of pH. J Biol Chem 280: 20937-20944. (Pubitemid 40805650)
38. Rubinsztein DC, Gestwicki JE, Murphy LO, Klionsky DJ,. 2007. Potential therapeutic applications of autophagy. Nat Rev Drug Discov 6: 304-312. (Pubitemid 46505881)
39. Sarbassov DD, Ali SM, Kim DH, Guertin DA, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM,. 2004. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr Biol 14: 1296-1302. (Pubitemid 38991819)
40. Sarbassov DD, Ali SM, Sabatini DM,. 2005. Growing roles for the mTOR pathway. Curr Opin Cell Biol 17: 596-603. (Pubitemid 41540408)
41. Sarkar S, Ravikumar B, Floto RA, Rubinsztein DC,. 2009. Rapamycin and mTOR-independent autophagy inducers ameliorate toxicity of polyglutamine- expanded huntingtin and related proteinopathies. Cell Death Differ 16: 46-56.
42. Shioi T, McMullen JR, Kang PM, Douglas PS, Obata T, Franke TF, Cantley LC, Izumo S,. 2002. Akt/protein kinase B promotes organ growth in transgenic mice. Mol Cell Biol 22: 2799-2809. (Pubitemid 34263000)
43. Vairo G, Cocks BG, Cragoe EJ Jr, Hamilton JA,. 1992. Selective suppression of growth factor-induced cell cycle gene expression by Na+/H+ antiport inhibitors. J Biol Chem 267: 19043-19046.
44. Wang L, Lawrence JC Jr, Sturgill TW, Harris TE,. 2009. Mammalian target of rapamycin complex 1 (mTORC1) activity is associated with phosphorylation of raptor by mTOR. J Biol Chem 284: 14693-14697.
45. Williams A, Sarkar S, Cuddon P, Ttofi EK, Saiki S, Siddiqi FH, Jahreiss L, Fleming A, Pask D, Goldsmith P, O'Kane CJ, Floto RA, Rubinsztein DC,. 2008. Novel targets for Huntington's disease in an mTOR-independent autophagy pathway. Nat Chem Biol 4: 295-305. (Pubitemid 351550888)
46. Wullschleger S, Loewith R, Hall MN,. 2006. TOR signaling in growth and metabolism. Cell 124: 471-484. (Pubitemid 43199434)
47. Xu L, Fidler IJ,. 2000. Acidic pH-induced elevation in interleukin 8 expression by human ovarian carcinoma cells. Cancer Res 60: 4610-4616. (Pubitemid 32103647)