Acute focal brain damage alters mitochondrial dynamics and autophagy in axotomized neurons

Cell Death and Disease

Volumn 5, Issue , 2014, Pages

  Cavallucci, V ^a   Bisicchia, E ^a   Cencioni, M T ^a   Ferri, A ^b   Latini, L ^a   Nobili, A ^a,c   Biamonte, F ^d   Nazio, F ^a   Fanelli, F ^c   Moreno, S ^e   Molinari, M ^a   Viscomi, M T ^a   D'Amelio, M ^a,c  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b CNR   (Italy)

^c UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^d CATHOLIC UNIVERSITY   (Italy)

^e ROMA TRE UNIVERSITY   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

CALCINEURIN; CYTOPLASM PROTEIN; DYNAMIN RELATED PROTEIN 1; MITOFUSIN 1; PARKIN; PHOSPHOTRANSFERASE; PTEN INDUCED PUTATIVE KINASE 1; RAPAMYCIN; UNCLASSIFIED DRUG; DNM1L PROTEIN, MOUSE; DYNAMIN;

ACUTE BRAIN DISEASE; ACUTE FOCAL BRAIN DAMAGE; ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BRAIN DAMAGE; BRAIN MITOCHONDRION; BRAIN NERVE CELL; CELL FUNCTION; CELL FUSION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME LOCALIZATION; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL FISSION; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOPHAGY; MOUSE; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN TRANSPORT; ACUTE DISEASE; ANIMAL; AXOTOMY; BIOLOGICAL MODEL; BRAIN INJURY; C57BL MOUSE; CEREBELLUM; DRUG EFFECTS; METABOLISM; MITOCHONDRION; NERVE CELL; NERVE DEGENERATION; PATHOLOGY; SURGERY; ULTRASTRUCTURE;

ACUTE DISEASE; ANIMALS; AUTOPHAGY; AXOTOMY; BRAIN INJURIES; CALCINEURIN; CEREBELLUM; DYNAMINS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE, INBRED C57BL; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL DYNAMICS; MODELS, BIOLOGICAL; NERVE DEGENERATION; NEURONS; SIROLIMUS;

EID: 84924984389     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.511     Document Type: Article

References (54)

1. Kroemer G, Dallaporta B, Resche-Rigon M. The mitochondrial death/life regulator in apoptosis and necrosis. Annu Rev Physiol 1998; 60: 619-642.
2. Hoppins S, Lackner L, Nunnari J. The machines that divide and fuse mitochondria. Annu Rev Biochem 2007; 76: 751-780.
3. Chen H, Chan DC. Physiological functions of mitochondrial fusion. Ann N YAcad Sci 2010; 1201: 21-25.
4. Chang CR, Blackstone C. Dynamic regulation of mitochondrial fission through modification of the dynamin-related protein Drp1. Ann N Y Acad Sci 2010; 1201: 34-39.
5. James DI, Parone PA, Mattenberger Y, Martinou JC. hFis1, a novel component of the mammalian mitochondrial fission machinery. J Biol Chem. 2003; 278: 36373-36379.
6. Smirnova E, Shurland DL, Ryazantsev SN, van der Bliek AM. A human dynamin-related protein controls the distribution of mitochondria. J Cell Biol 1998; 143: 351-358.
7. Cagalinec M, Safiulina D, Liiv M, Liiv J, Choubey V, Wareski P et al. Principles of the mitochondrial fusion and fission cycle in neurons. Cell Sci 2013; 126: 2187-2197.
8. Itoh K, Nakamura K, Iijima M, Sesaki H. Mitochondrial dynamics in neurodegeneration. Trends Cell Biol 2013; 23: 64-71.
9. Frank S, Gaume B, Bergmann-Leitner ES, Leitner WW, Robert EG, Catez F et al. The role of dynamin-related protein 1, a mediator of mitochondrial fission, in apoptosis. Dev Cell 2001; 1: 515-525.
10. Landes T, Martinou JC. Mitochondrial outer membrane permeabilization during apoptosis: the role of mitochondrial fission. Biochim Biophys Acta 2011; 1813: 540-545.
11. Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science 2000; 290: 1717-1721.
12. Wang K, Klionsky DJ. Mitochondria removal by autophagy. Autophagy 2011; 7: 297-300.
13. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S et al. Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 1998; 392: 605-608.
14. Matsuda N, Sato S, Shiba K, Okatsu K, Saisho K, Gautier CA et al. PINK1 stabilized by mitochondrial depolarization recruits Parkin to damaged mitochondria and activates latent Parkin for mitophagy. J Cell Biol 2010; 189: 211-221.
15. Narendra DP, Jin SM, Tanaka A, Suen DF, Gautier CA, Shen J et al. PINK1 is selectively stabilized on impaired mitochondria to activate Parkin. PLoS Biol 2010; 8: e1000298.
16. Vives-Bauza C, Zhou C, Huang Y, Cui M, de Vries RL, Kim J et al. PINK1-dependent recruitment of Parkin to mitochondria in mitophagy. Proc Natl Acad Sci USA 2010; 107: 378-383.
17. Valente EM, Abou-Sleiman PM, Caputo V, Muqit MM, Harvey K, Gispert S et al. Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science 2004; 304: 1158-1160.
18. Chan NC, Salazar AM, Pham AH, Sweredoski MJ, Kolawa NJ, Graham RL et al. Broad activation of the ubiquitin-proteasome system by Parkin is critical for mitophagy. Hum Mol Genet 2011; 20: 1726-1737.
19. Glauser L, Sonnay S, Stafa K, Moore DJ. Parkin promotes the ubiquitination and degradation of the mitochondrial fusion factor mitofusin 1. J Neurochem 2011; 118: 636-645.
20. Twig G, Elorza A, Molina AJ, Mohamed H, Wikstrom JD,Walzer G et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J 2008; 27: 433-446.
21. Viscomi MT, Florenzano F, Latini L, Molinari M. Remote cell death in the cerebellar system. Cerebellum 2009; 8: 184-191.
22. Viscomi MT, Molinari M. Remote neurodegeneration: multiple actors for one Play. Mol Neurobiol 2014; 50: 368-389.
23. Bramlett HM, Dietrich WD. Progressive damage after brain and spinal cord injury: pathomechanisms and treatment strategies. Prog Brain Res 2007; 161: 125-141.
24. Dihné M, Grommes C, Lutzenburg M, Witte OW, Block F. Different mechanisms of secondary neuronal damage in thalamic nuclei after focal cerebral ischemia in rats. Stroke 2002; 33: 3006-3011.
25. Zhang J, Zhang Y, Xing S, Liang Z, Zeng J. Secondary neurodegeneration in remote regions after focal cerebral infarction: a new target for stroke management? Stroke 2012; 43: 1700-1705.
26. Viscomi MT, D'Amelio M, Cavallucci V, Latini L, Bisicchia E, Nazio F et al. Stimulation of autophagy by rapamycin protects neurons from remote de generation after acute focal brain damage. Autophagy 2012; 8: 222-235.
27. Viscomi MT, Oddi S, Latini L, Pasquariello N, Florenzano F, Bernardi G et al. Selective CB2 receptor agonism protects central neurons from remote axotomy-induced apoptosis through the PI3K/Akt pathway. J Neurosci. 2009; 29: 4564-4570.
28. Viscomi MT, D'Amelio M. The 'Janus-faced role' of autophagy in neuronal sickness: focus on neurodegeneration. Mol Neurobiol 2012; 46: 513-521.
29. Lemasters JJ, Qian T, He L, Kim JS, Elmore SP, Cascio WE et al. Role of mitochondrial inner membrane permeabilization in necrotic cell death, apoptosis, and autophagy. Antioxid Redox Signal 2002; 4: 769-781.
30. Green DR, Kroemer G. The pathophysiology of mitochondrial cell death. Science 2004; 305: 626-629.
31. Pickrell AM, Fukui H, Wang X, Pinto M, Moraes CT. The striatum is highly susceptible to mitochondrial oxidative phosphorylation dysfunctions. J Neurosci 2011; 31: 9895-9904.
32. Narendra D, Tanaka A, Suen DF, Youle RJ. Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 2008; 183: 795-803.
33. Cereghetti GM, Stangherlin A, Martins de Brito O, Chang CR, Blackstone C, Bernardi P et al. Dephosphorylation by calcineurin regulates translocation of Drp1 to mitochondria. Proc Natl Acad Sci USA 2008; 105: 15803-15808.
34. Chan B, Greenan G, McKeon F, Ellenberger T. Identification of a peptide fragment of DSCR1 that competitively inhibits calcineurin activity in vitro and in vivo. Proc Natl Acad Sci USA 2005; 102: 13075-13080.
35. Fuentes JJ, Genescà L, Kingsbury TJ, Cunningham KW, Pérez-Riba M, Estivill X et al. DSCR1, overexpressed in Down syndrome, is an inhibitor of calcineurin-mediated signaling pathways. Hum Mol Genet 2000; 9: 1681-1690.
36. Sobrado M, Ramirez BG, Neria F, Lizasoain I, Arbones ML, Minami T et al. Regulator of calcineurin 1 (Rcan1) has a protective role in brain ischemia/reperfusion injury. J Neuroinflammation 2012; 9: 48-60.
37. Liu H, Wang P, Song W, Sun X. Degradation of regulator of calcineurin 1 (RCAN1) is mediated by both chaperone-mediated autophagy and ubiquitin proteasome pathways. FASEB J 2009; 23: 3383-3392.
38. Mizushima N, Kuma A. Autophagosomes in GFP-LC3 Transgenic Mice. Methods Mol Biol 2008; 445: 119-124.
39. Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8: 445-544.
40. Gomes LC, Scorrano L. Mitochondrial morphology in mitophagy and macroautophagy. Biochim. Biophys Acta 2013; 1833: 205-212.
41. Lee JM, Zipfel GJ, Choi DW. The changing landscape of ischaemic brain injury mechanisms. Nature 1999; 399: A7-A14.
42. Nicotera P, Orrenius S. The role of calcium in apoptosis. Cell Calcium 1998; 23: 173-801.
43. Zhivotovsky B, Orrenius S. Calcium and cell death mechanisms: a perspective from the cell death community. Cell Calcium 2011; 50: 211-221.
44. Brustovetsky N, Brustovetsky T, Jemmerson R, Dubinsky JM. Calcium-induced cytochrome c release from CNS mitochondria is associated with the permeability transition and rupture of the outer membrane. J Neurochem 2002; 80: 207-218.
45. Calì T, Ottolini D, Brini M. Mitochondrial Ca(2+) and neurodegeneration. Cell Calcium 2012; 52: 73-85.
46. Chaturvedi RK, Flint Beal M. Mitochondrial diseases of the brain. Free Radic Biol Med 2013; 63: 1-29.
47. Hartley D, Cooper GM. Role of mTOR in the degradation of IRS-1: regulation of PP2A activity. Cell Biochem 2002; 85: 304-314.
48. D'Amelio M, Sheng M, Cecconi F. Caspase-3 in the central nervous system: beyond apoptosis. Trends Neurosci 2012; 35: 700-709.
49. Zhang X, Yan H, Yuan Y, Gao J, Shen Z, Cheng Y et al. Cerebral ischemia-reperfusioninduced autophagy protects against neuronal injury by mitochondrial clearance. Autophagy 2013; 9: 1321-1333.
50. Hamacher-Brady A, Brady NR, Gottlieb RA. Enhancing macroautophagy protects against ischemia/reperfusion injury in cardiac myocytes. J Biol Chem 2006; 281: 29776-29787.
51. Frezza C, Cipolat S, Scorrano L. Organelle isolation: functional mitochondria from mouse liver, muscle and cultured fibroblasts. Nat Protoc 2007; 2: 287-295.
52. Qin ZH,Wang Y, Kikly KK, Sapp E, Kegel KB, Aronin N et al. Pro-caspase-8 is predominantly localized in mitochondria and released into cytoplasm upon apoptotic stimulation. J Biol Chem 2001; 276: 8079-8086.
53. D'Amelio M, Cavallucci V, Middei S, Marchetti C, Pacioni S, Ferri A et al. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nat Neurosci 2011; 14: 69-76.
54. Ferri A, Gabbianelli R, Casciati A, Paolucci E, Rotilio G, Carrì MT. Calcineurin activity is regulated both by redox compounds and by mutant familial amyotrophic lateral sclerosissuperoxide dismutase. J Neurochem 2000; 75: 606-613.