Hypoxia causes autophagic stress and derangement of metabolic adaptation in a cell model of amyotrophic lateral sclerosis

Journal of Neurochemistry

Volumn 129, Issue 3, 2014, Pages 413-425

  Cimini, Sara ^a   Rizzardini, Milena ^a   Biella, Gloria ^a   Cantoni, Lavinia ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

3 methyladenine; amyotrophic lateral sclerosis; autophagy; Cu Zn superoxide dismutase; hypoxia; mitoch ondria

Indexed keywords

3-METHYLADENINE; AMYOTROPHIC LATERAL SCLEROSIS; AUTOPHAGY; CU, ZN SUPEROXIDE DISMUTASE; HYPOXIA; MITOCH-ONDRIA;

ADAPTATION, PHYSIOLOGICAL; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AUTOPHAGY; BLOTTING, WESTERN; CELL HYPOXIA; DISEASE MODELS, ANIMAL; HUMANS; MICE; MOTOR NEURONS; MUTATION; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE; TRANSFECTION;

EID: 84899415973     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12642     Document Type: Article

References (70)

1. Aggarwal S. P., Zinman L., Simpson E., et al,. (2010) Safety and efficacy of lithium in combination with riluzole for treatment of amyotrophic lateral sclerosis: a randomised, double-blind, placebo-controlled trial. Lancet Neurol. 9, 481-488.
2. Barber S. C., and, Shaw P. J., (2010) Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Free Radic. Biol. Med. 48, 629-641.
3. Beghi E., Chiò A., Couratier P., et al,. and Eurals Consortium (2011) The epidemiology and treatment of ALS: focus on the heterogeneity of the disease and critical appraisal of therapeutic trials. Amyotroph. Lateral Scler. 12, 1-10.
4. Billington R. A., Travelli C., Ercolano E., Galli U., Roman C. B., Grolla A. A., Canonico P. L., Condorelli F., and, Genazzani A. A., (2008) Characterization of NAD uptake in mammalian cells. J. Biol. Chem. 283, 6367-6374.
5. Boya P., González-Polo R. A., Casares N., et al,. (2005) Inhibition of macroautophagy triggers apoptosis. Mol. Cell. Biol. 25, 1025-1040.
6. Büchner M., Li H., Huber R., Timmler M., Sehrsam I., Kasischke K., Völkel H., Ludolph A. C., and, Riepe M. W., (1999) Impaired tolerance to repetitive hypoxia in hippocampal slices of Cu, Zn superoxide dismutase transgenic mice. Neurosci. Lett. 276, 131-134.
7. Canu N., Tufi R., Serafino A. L., Amadoro G., Ciotti M. T., and, Calissano P., (2005) Role of the autophagic-lysosomal system on low potassium-induced apoptosis in cultured cerebellar granule cells. J. Neurochem. 92, 1228-1242.
8. Castino R., Bellio N., Follo C., Murphy D., and, Isidoro C., (2010) Inhibition of PI3k class III-dependent autophagy prevents apoptosis and necrosis by oxidative stress in dopaminergic neuroblastoma cells. Toxicol. Sci. 117, 152-162.
9. Chen S., Zhang X., Song L., and, Le W., (2012) Autophagy dysregulation in amyotrophic lateral sclerosis. Brain Pathol. 22, 110-116.
10. Chu C. T., (2008) Eaten alive: autophagy and neuronal cell death after hypoxia-ischemia. Am. J. Pathol. 172, 284-287.
11. D'Alessandro G., Calcagno E., Tartari S., Rizzardini M., Invernizzi R. W., and, Cantoni L., (2011) Glutamate and glutathione interplay in a motor neuronal model of amyotrophic lateral sclerosis reveals altered energy metabolism. Neurobiol. Dis. 43, 346-355.
12. Dobrowolski R., and, De Robertis E. M., (2011) Endocytic control of growth factor signalling: multivesicular bodies as signalling organelles. Nat. Rev. Mol. Cell Biol. 13, 53-60.
13. Duffy L. M., Chapman A. L., Shaw P. J., and, Grierson A. J., (2011) The role of mitochondria in the pathogenesis of amyotrophic lateral sclerosis. Neuropathol. Appl. Neurobiol. 37, 336-352.
14. Durán R. V., Oppliger W., Robitaille A. M., Heiserich L., Skendaj R., Gottlieb E., and, Hall M. N., (2012) Glutaminolysis activates Rag-mTORC1 signaling. Mol. Cell 47, 349-358.
15. Fornai F., Longone P., Cafaro L., et al,. (2008) Lithium delays progression of amyotrophic lateral sclerosis. Proc. Natl Acad. Sci. USA 105, 2052-2057.
16. Frezza C., Zheng L., Tennant D. A., Papkovsky D. B., Hedley B. A., Kalna G., Watson D. G., and, Gottlieb E., (2011) Metabolic profiling of hypoxic cells revealed a catabolic signature required for cell survival. PLoS ONE 6, e24411.
17. Geisler S., Holmström K. M., Skujat D., Fiesel F. C., Rothfuss O. C., Kahle P. J., and, Springer W., (2010) PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat. Cell Biol. 12, 119-131.
18. Guégan C., and, Przedborski S., (2003) Programmed cell death in amyotrophic lateral sclerosis. J. Clin. Invest. 111, 153-161.
19. Hetz C., Thielen P., Matus S., Nassif M., Court F., Kiffin R., Martinez G., Cuervo A. M., Brown R. H., and, Glimcher L. H., (2009) XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Genes Dev. 23, 2294-2306.
20. Higgins G. C., Devenish R. J., Beart P. M., and, Nagley P., (2011) Autophagic activity in cortical neurons under acute oxidative stress directly contributes to cell death. Cell. Mol. Life Sci. 68, 3725-3740.
21. Hui S. T., Andres A. M., Miller A. K., et al,. (2008) Txnip balances metabolic and growth signaling via PTEN disulfide reduction. Proc. Natl Acad. Sci. USA 105, 3921-3926.
22. Jung C. H., Ro S. H., Cao J., Otto N. M., and, Kim D. H., (2010) mTOR regulation of autophagy. FEBS Lett. 584, 1287-1295.
23. Kabuta T., Suzuki Y., and, Wada K., (2006) Degradation of amyotrophic lateral sclerosis-linked mutant Cu, Zn-superoxide dismutase proteins by macroautophagy and the proteasome. J. Biol. Chem. 281, 30524-30533.
24. Kang R., Zeh H. J., Lotze M. T., and, Tang D., (2011) The Beclin 1 network regulates autophagy and apoptosis. Cell Death Differ. 18, 571-580.
25. Kim H., Scimia M. C., Wilkinson D., Trelles R. D., Wood M. R., Bowtell D., Dillin A., Mercola M., and, Ronai Z. A., (2011) Fine-tuning of Drp1/Fis1 availability by AKAP121/Siah2 regulates mitochondrial adaptation to hypoxia. Mol. Cell 44, 532-544.
26. Kunchithapautham K., and, Rohrer B., (2007) Apoptosis and autophagy in photoreceptors exposed to oxidative stress. Autophagy 3, 433-441.
27. Lee J. A., (2009) Autophagy in neurodegeneration: two sides of the same coin. BMB Rep. 42, 324-330.
28. Lee J. A., and, Gao F. B., (2009) Inhibition of autophagy induction delays neuronal cell loss caused by dysfunctional ESCRT-III in frontotemporal dementia. J. Neurosci. 29, 8506-8511.
29. Lee I. H., Cao L., Mostoslavsky R., Lombard D. B., Liu J., Bruns N., Tsokos M., Alt F. W., and, Finkel T., (2008) A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc. Natl Acad. Sci. USA 105, 3374-3379.
30. Li L., Zhang X., and, Le W., (2010) Autophagy dysfunction in Alzheimer's disease. Neurodegener. Dis. 7, 265-271.
31. Lim J. H., Lee Y. M., Chun Y. S., Chen J., Kim J. E., and, Park J. W., (2010) Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha. Mol. Cell 38, 864-878.
32. Mali Y., and, Zisapel N., (2010) VEGF up-regulation by G93A superoxide dismutase and the role of malate-aspartate shuttle inhibition. Neurobiol. Dis. 37, 673-681.
33. Mali Y., and, Zisapels N., (2008) Gain of interaction of ALS-linked G93A superoxide dismutase with cytosolic malate dehydrogenase. Neurobiol. Dis. 32, 133-141.
34. McKenna M. C., Waagepetersen H. S., Schousboe A., and, Sonnewald U., (2006) Neuronal and astrocytic shuttle mechanisms for cytosolic-mitochondrial transfer of reducing equivalents: current evidence and pharmacological tools. Biochem. Pharmacol. 71, 399-407.
35. Mehrpour M., Esclatine A., Beau I., and, Codogno P., (2010) Overview of macroautophagy regulation in mammalian cells. Cell Res. 20, 748-762.
36. Menzies F. M., Cookson M. R., Taylor R. W., Turnbull D. M., Chrzanowska-Lightowlers Z. M., Dong L., Figlewicz D. A., and, Shaw P. J., (2002) Mitochondrial dysfunction in a cell culture model of familial amyotrophic lateral sclerosis. Brain 125, 1522-1533.
37. Metallo C. M., Gameiro P. A., Bell E. L., et al,. (2011) Reductive glutamine metabolism by IDH1 mediates lipogenesis under hypoxia. Nature 481, 380-384.
38. Miller R. G., Moore D. H., Forshew D. A., et al,., WALS Study Group. (2011) Phase II screening trial of lithium carbonate in amyotrophic lateral sclerosis: examining a more efficient trial design. Neurology 77, 973-979.
39. Montaser M., Lalmanach G., and, Mach L., (2002) CA-074, but not its methyl ester CA-074Me, is a selective inhibitor of cathepsin B within living cells. Biol. Chem. 383, 1305-1308.
40. Moreau C., Gosset P., Kluza J., Brunaud-Danel V., Lassalle P., Marchetti P., Defebvre L., Destée A., and, Devos D., (2011) Deregulation of the hypoxia inducible factor-1α pathway in monocytes from sporadic amyotrophic lateral sclerosis patients. Neuroscience 172, 110-117.
41. Nassif M., and, Hetz C., (2011) Targeting autophagy in ALS: a complex mission. Autophagy 7, 450-453.
42. Pan Y., Mansfield K. D., Bertozzi C. C., Rudenko V., Chan D. A., Giaccia A. J., and, Simon M. C., (2007) Multiple factors affecting cellular redox status and energy metabolism modulate hypoxia-inducible factor prolyl hydroxylase activity in vivo and in vitro. Mol. Cell. Biol. 27, 912-925.
43. Pivtoraiko V. N., Stone S. L., Roth K. A., and, Shacka J. J., (2009) Oxidative stress and autophagy in the regulation of lysosome-dependent neuron death. Antioxid. Redox Signal. 11, 481-496.
44. Raimondi A., Mangolini A., Rizzardini M., Tartari S., Massari S., Bendotti C., Francolini M., Borgese N., Cantoni L., and, Pietrini G., (2006) Cell culture models to investigate the selective vulnerability of motoneuronal mitochondria to familial ALS-linked G93ASOD1. Eur. J. Neurosci. 24, 387-399.
45. Reddi A. R., and, Culotta V. C., (2013) SOD1 integrates signals from oxygen and glucose to repress respiration. Cell 152, 224-235.
46. Richardson K., Allen S. P., Mortiboys H., Grierson A. J., Wharton S. B., Ince P. G., Shaw P. J., and, Heath P. R., (2013) The effect of SOD1 mutation on cellular bioenergetic profile and viability in response to oxidative stress and influence of mutation-type. PLoS ONE 8, e68256.
47. Rizzardini M., Mangolini A., Lupi M., Ubezio P., Bendotti C., and, Cantoni L., (2005) Low levels of ALS-linked Cu/Zn superoxide dismutase increase the production of reactive oxygen species and cause mitochondrial damage and death in motor neuron-like cells. J. Neurol. Sci. 232, 95-103.
48. Rizzardini M., Lupi M., Mangolini A., Babetto E., Ubezio P., and, Cantoni L., (2006) Neurodegeneration induced by complex I inhibition in a cellular model of familial amyotrophic lateral sclerosis. Brain Res. Bull. 69, 465-474.
49. Robberecht W., and, Philips T., (2013) The changing scene of amyotrophic lateral sclerosis. Nat. Rev. Neurosci. 14, 248-264.
50. Rubinsztein D. C., Cuervo A. M., Ravikumar B., Sarkar S., Korolchuk V., Kaushik S., and, Klionsky D. J., (2009) In search of an " autophagomometer". Autophagy 5, 585-589.
51. Semenza G. L., (2011) Hypoxia-inducible factor 1: regulator of mitochondrial metabolism and mediator of ischemic preconditioning. Biochim. Biophys. Acta 1813, 1263-1268.
52. Tan W., Naniche N., Bogush A., Pedrini S., Trotti D., and, Pasinelli P., (2013) Small peptides against the mutant SOD1/Bcl-2 toxic mitochondrial complex restore mitochondrial function and cell viability in mutant SOD1-mediated ALS. J. Neurosci. 33, 11588-11598.
53. Tankersley C. G., Haenggeli C., and, Rothstein J. D., (2007) Respiratory impairment in a mouse model of amyotrophic lateral sclerosis. J. Appl. Physiol. 102, 926-932.
54. Taylor C. T., (2008) Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem. J. 409, 19-26.
55. Walls K. C., Ghosh A. P., Ballestas M. E., Klocke B. J., and, Roth K. A., (2009) bcl-2/Adenovirus E1B 19-kd interacting protein 3 (BNIP3) regulates hypoxia-induced neural precursor cell death. J. Neuropathol. Exp. Neurol. 68, 1326-1338.
56. Walls K. C., Ghosh A. P., Franklin A. V., Klocke B. J., Ballestas M., Shacka J. J., Zhang J., and, Roth K. A., (2010) Lysosome dysfunction triggers Atg7-dependent neural apoptosis. J. Biol. Chem. 285, 10497-10507.
57. Wen X., Wu J., Wang F., Liu B., Huang C., and, Wei Y., (2013) Deconvoluting the role of reactive oxygen species and autophagy in human diseases. Free Radic. Biol. Med. 65, 402-410.
58. Wise D. R., Ward P. S., Shay J. E., Cross J. R., Gruber J. J., Sachdeva U. M., Platt J. M., DeMatteo R. G., Simon M. C., and, Thompson C. B., (2011) Hypoxia promotes isocitrate dehydrogenase dependent carboxylation of α-ketoglutarate to citrate to support cell growth and viability. Proc. Natl Acad. Sci. USA 108, 19611-19616.
59. Wu Y. T., Tan H. L., Shui G., Bauvy C., Huang Q., Wenk M. R., Ong C. N., Codogno P., and, Shen H. M., (2010) Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J. Biol. Chem. 285, 10850-10861.
60. Xu R., Wu C., Zhang X., Zhang Q., Yang Y., Yi J., Yang R., and, Tao Y., (2011) Linking hypoxic and oxidative insults to cell death mechanisms in models of ALS. Brain Res. 1372, 133-144.
61. Xue L., Fletcher G. C., and, Tolkovsky A. M., (1999) Autophagy is activated by apoptotic signalling in sympathetic neurons: an alternative mechanism of death execution. Mol. Cell. Neurosci. 14, 180-198.
62. Yoshida S., Hong S., Suzuki T., Nada S., Mannan A. M., Wang J., Okada M., Guan K. L., and, Inoki K., (2011) Redox regulates mammalian target of rapamycin complex 1 (mTORC1) activity by modulating the TSC1/TSC2-Rheb GTPase pathway. J. Biol. Chem. 286, 32651-32660.
63. Yoshimori T., Yamamoto A., Moriyama Y., Futai M., and, Tashiro Y., (1991) Bafilomycin A1, a specific inhibitor of vacuolar-type H(+)-ATPase, inhibits acidification and protein degradation in lysosomes of cultured cells. J. Biol. Chem. 266, 17707-17712.
64. Zhang X., and, Le W., (2010) Pathological role of hypoxia in Alzheimer's disease. Exp. Neurol. 223, 299-303.
65. Zhang H., Gao P., Fukuda R., Kumar G., Krishnamachary B., Zeller K. I., Dang C. V., and, Semenza G. L., (2007) HIF-1 inhibits mitochondrial biogenesis and cellular respiration in VHL-deficient renal cell carcinoma by repression of C-MYC activity. Cancer Cell 11, 407-420.
66. Zhang H., Bosch-Marce M., Shimoda L. A., Tan Y. S., Baek J. H., Wesley J. B., Gonzalez F. J., and, Semenza G. L., (2008) Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J. Biol. Chem. 283, 10892-10903.
67. Zhang X. D., Wang Y., Wu J. C., Lin F., Han R., Han F., Fukunaga K., and, Qin Z. H., (2009) Down-regulation of Bcl-2 enhances autophagy activation and cell death induced by mitochondrial dysfunction in rat striatum. J. Neurosci. Res. 87, 3600-3610.
68. Zhang X., Li L., Chen S., Yang D., Wang Y., Zhang X., Wang Z., and, Le W., (2011a) Rapamycin treatment augments motor neuron degeneration in SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Autophagy 7, 412-425.
69. Zhang Z., Yan J., Chang Y., ShiDu Yan. S., and, Shi H., (2011b) Hypoxia inducible factor-1 as a target for neurodegenerative diseases. Curr. Med. Chem. 18, 4335-4343.
70. Zhang K., Shi P., An T., Wang Q., Wang J., Li Z., Duan W., Li C., and, Guo Y., (2013) Food restriction-induced autophagy modulates degradation of mutant SOD1 in an amyotrophic lateral sclerosis mouse model. Brain Res. 1519, 112-119.