Mitochondrial permeability transition pore induces mitochondria injury in Huntington disease

Molecular Neurodegeneration

Volumn 8, Issue 1, 2013, Pages

  Quintanilla, Rodrigo A ^a,b   Jin, Youngnam N ^a   Von Bernhardi, Rommy ^b   Johnson, Gail Vw ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^b PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

Author keywords

Huntingtin; Huntington's disease; Mitochondria dysfunction; Mitochondria permeability transition pore; Mitochondrial fragmentation; Oxidative stress; Striatal cells

Indexed keywords

CALCIUM; CYCLOSPORIN A; HUNTINGTIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; POLYGLUTAMINE; REACTIVE OXYGEN METABOLITE; TACROLIMUS; THAPSIGARGIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; CALCIUM TRANSPORT; CELL MUTANT; CELL VIABILITY; CONTROLLED STUDY; DEPOLARIZATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EMBRYO; EXON; HUNTINGTON CHOREA; MITOCHONDRION; NONHUMAN; PROTEIN EXPRESSION; RAT; WILD TYPE;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; HUMANS; HUNTINGTON DISEASE; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; NERVE TISSUE PROTEINS; NEURONS; RATS; REACTIVE OXYGEN SPECIES;

EID: 84889876549     PISSN: None     EISSN: 17501326     Source Type: Journal    
DOI: 10.1186/1750-1326-8-45     Document Type: Article

References (60)

1. A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. The Huntington's Disease Collaborative Research Group, Cell 1993 72 971 983 10.1016/0092-8674(93)90585-E 8458085 (Pubitemid 23110238)
2. Loss of normal huntingtin function: new developments in Huntington's disease research. Cattaneo E, Rigamonti D, Goffredo D, Zuccato C, Squitieri F, Sipione S, Trends Neurosci 2001 24 182 188 10.1016/S0166-2236(00)01721-5 11182459 (Pubitemid 32166824)
3. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cui L, Jeong H, Borovecki F, Parkhurst CN, Tanese N, Krainc D, Cell 2006 127 59 69 10.1016/j.cell.2006.09.015 17018277 (Pubitemid 44466642)
4. Mechanism of neurodegenerative disease: role of the ubiquitin proteasome system. Petrucelli L, Dawson TM, Ann Med 2004 36 315 320 10.1080/ 07853890410031948 15224658 (Pubitemid 38789286)
5. The ubiquitin-proteasome system in Huntington's disease. Valera AG, Diaz-Hernandez M, Hernandez F, Ortega Z, Lucas JJ, Neuroscientist 2005 11 583 594 10.1177/1073858405280639 16282599 (Pubitemid 41611870)
6. Proteasome activator enhances survival of Huntington's disease neuronal model cells. Seo H, Sonntag KC, Kim W, Cattaneo E, Isacson O, PLoS ONE 2007 28 238
7. Early mitochondrial calcium defects in Huntington's disease are a direct effect of polyglutamines. Panov AV, Gutekunst CA, Leavitt BR, Hayden MR, Burke JR, Strittmatter WJ, Greenamyre JT, Nat Neurosci 2002 5 731 736 12089530 (Pubitemid 34827590)
8. Huntingtin and huntingtin-associated protein 1 influence neuronal calcium signaling mediated by inositol-(1,4,5) triphosphate receptor type 1. Tang TS, Tu H, Chan EY, Maximov A, Wang Z, Wellington CL, Hayden MR, Bezprozvanny I, Neuron 2003 39 227 239 10.1016/S0896-6273(03)00366-0 12873381 (Pubitemid 36897546)
9. Mitochondrial defect in Huntington's disease caudate nucleus. Gu M, Gash MT, Mann VM, Javoy-Agid F, Cooper JM, Schapira AH, Ann Neurol 1996 39 385 389 10.1002/ana.410390317 8602759 (Pubitemid 26100764)
10. Ca (2+)-dependent permeability transition and complex I activity in lymphoblast mitochondria from normal individuals and patients with Huntington's or Alzheimer's disease. Panov AV, Obertone T, Bennett-Desmelik J, Greenamyre JT, Ann N Y Acad Sci 1999 893 365 368 10.1111/j.1749-6632.1999.tb07856.x 10672268 (Pubitemid 30038106)
11. Striatal cells from mutant huntingtin knock-in mice are selectively vulnerable to mitochondrial complex II inhibitor-induced cell death through a non-apoptotic pathway. Ruan Q, Lesort M, MacDonald ME, Johnson GV, Hum Mol Genet 2004 13 669 681 10.1093/hmg/ddh082 14962977 (Pubitemid 38455955)
12. Mitochondrial function and parental sex effect in Huntington's disease. Mann VM, Cooper JM, Javoy-Agid F, Agid Y, Jenner P, Schapira AH, Lancet 1990 336 749 (Pubitemid 20309171)
13. Oxidative damage and metabolic dysfunction in Huntington's disease: selective vulnerability of the basal ganglia. Browne SE, Bowling AC, MacGarvey U, Baik MJ, Berger SC, Muqit MM, Bird ED, Beal MF, Ann Neurol 1997 41 646 653 10.1002/ana.410410514 9153527 (Pubitemid 27212659)
14. A YAC mouse model for Huntington's disease with full-length mutant huntingtin, cytoplasmic toxicity, and selective striatal neurodegeneration. Hodgson JG, Agopyan N, Gutekunst CA, Leavitt BR, LePiane F, Singaraja R, Smith DJ, Bissada N, McCutcheon K, Nasir J, Jamot L, Li XJ, Stevens ME, Rosemond E, Roder JC, Phillips AG, Rubin EM, Hersch SM, Hayden MR, Neuron 1999 23 181 192 10.1016/S0896-6273(00)80764-3 10402204 (Pubitemid 29262475)
15. Mitochondrial sensitivity and altered calcium handling underlie enhanced NMDA-induced apoptosis in YAC128 model of Huntington's disease. Fernandes HB, Baimbridge KG, Church J, Hayden MR, Raymond LA, J of Neurosci 2007 27 13614 13623 10.1523/JNEUROSCI.3455-07.2007 (Pubitemid 350278271)
16. Mitochondrial-dependent Ca2+ handling in Huntington's disease striatal cells: effect of histone deacetylase inhibitors. Oliveira JMA, Chen S, Almeida S, Riley R, Gonçalves J, Oliveira CR, Hayden MR, et al. J Neurosci 2006 26 11174 11186 10.1523/JNEUROSCI.3004-06.2006 17065457 (Pubitemid 44772205)
17. Mitochondrial respiration and ATP production are significantly impaired in striatal cells expressing mutant huntingtin. Milakovic T, Johnson GV, J Biol Chem 2005 280 30773 30782 10.1074/jbc.M504749200 15983033 (Pubitemid 41291807)
18. Mutant huntingtin expression induces mitochondrial calcium handling defects in clonal striatal cells: functional consequences. Milakovic T, Quintanilla RA, Johnson GV, J Biol Chem 2006 281 34785 34795 10.1074/jbc.M603845200 16973623 (Pubitemid 46036517)
19. Rosiglitazone treatment prevents mitochondrial dysfunction in mutant huntingtin-expressing cells: possible role of peroxisome proliferator-activated receptor-gamma (PPARgamma) in the pathogenesis of Huntington disease. Quintanilla RA, Jin YN, Fuenzalida K, Bronfman M, Johnson GVW, J Biol Chem 2008 283 25628 25637 10.1074/jbc.M804291200 18640979
20. Mutant huntingtin directly increases susceptibility of mitochondria to the calcium-induced permeability transition and cytochrome c release. Choo YS, Johnson GV, MacDonald M, Detloff PJ, Lesort M, Hum Mol Genet 2004 13 1407 1420 10.1093/hmg/ddh162 15163634 (Pubitemid 39023049)
21. Mutant huntingtin aggregates impair mitochondrial movement and trafficking in cortical neurons. Chang DT, Rintoul GL, Pandipati S, Reynolds IJ, Neurobiol Dis 2006 22 388 400 10.1016/j.nbd.2005.12.007 16473015
22. Effects of overexpression of huntingtin proteins on mitochondrial integrity. Wang H, Lim PJ, Karbowski M, Monteiro MJ, Hum Mol Genet 2009 18 737 752 19039036
23. Mitochondrial loss, dysfunction and altered dynamics in Huntington's disease. Kim J, Moody JP, Edgerly CK, Bordiuk OL, Cormier K, Smith K, Beal MF, et al. Hum Mol Genet 2010 19 3919 3935 10.1093/hmg/ddq306 20660112
24. Impaired mitochondrial dynamics and Nrf2 signaling contribute to compromised responses to oxidative stress in striatal cells expressing full-length mutant huntingtin. Jin YN, Yu YV, Gundemir S, Jo C, Cui M, Tieu K, Johnson GVW, PLoS ONE 2013 8 57932 10.1371/journal.pone.0057932 23469253
25. Mitochondrial fission and cristae disruption increase the response of cell models of Huntington's disease to apoptotic stimuli. Costa V, Giacomello M, Hudec R, Lopreiato R, Ermak G, Lim D, Malorni W, Davies KJA, Carafoli E, Scorrano L, EMBO Mol Med 2010 2 490 503 10.1002/emmm.201000102 21069748
26. Abnormal mitochondrial dynamics, mitochondrial loss and mutant huntingtin oligomers in Huntington's disease: implications for selective neuronal damage. Shirendeb U, Reddy AP, Manczak M, Calkins MJ, Mao P, Tagle DA, Reddy PH, Hum Mol Gen 2011 20 1455 1488
27. Dominant phenotypes produced by the HD mutation in STHdh(Q111) striatal cells. Trettel F, Rigamonti D, Hilditch-Maguire P, Wheeler VC, Sharp AH, Persichetti F, Cattaneo E, MacDonald ME, Hum Mol Genet 2000 9 2799 2809 10.1093/hmg/9.19.2799 11092756
28. Role of mitochondrial dysfunction in the pathogenesis of Huntington's disease. Quintanilla RA, Johnson GVW, Brain Res Bull 2009 80 242 247 10.1016/j.brainresbull.2009.07.010 19622387
29. Relationships between superoxide levels and delayed calcium deregulation in cultured cerebellar granule cells exposed continuously to glutamate. Vesce S, Kirk L, Nicholls DG, J Neurochem 2004 90 683 693 10.1111/j.1471-4159.2004. 02516.x 15255947 (Pubitemid 38989400)
30. The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Rasola A, Bernardi P, Apoptosis 2007 12 815 833 10.1007/s10495-007-0723-y 17294078 (Pubitemid 46653292)
31. The mitochondrial permeability transition pore and its role in cell death. Crompton M, Biochem J 1999 341 233 249 10.1042/0264-6021:3410233 10393078 (Pubitemid 29373645)
32. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS, Am J Physiol Cell Physiol 2004 287 817 C833 10.1152/ajpcell.00139.2004 15355853 (Pubitemid 39238305)
33. p53 Opens the mitochondrial permeability transition pore to trigger necrosis. Vaseva AV, Marchenko ND, Ji K, Tsirka SE, Holzmann S, Moll UM, Cell 2012 149 1536 1548 10.1016/j.cell.2012.05.014 22726440
34. Dysregulation of mitochondrial calcium signaling and superoxide flashes cause mitochondrial genomic DNA damage in Huntington disease. Wang JQ, Chen Q, Wang X, Wang QC, Wang Y, Cheng HP, Guo C, et al. J Biol Chem 2013 288 3070 3084 10.1074/jbc.M112.407726 23250749
35. The permeability transition pore controls cardiac mitochondrial maturation and myocyte differentiation. Hom JR, Quintanilla RA, Hoffman DL, De Mesy Bentley K, Molkentin JD, Sheu SS, Porter GA Jr, Dev Cell 2011 21 469 478 10.1016/j.devcel.2011.08.008 21920313
36. Cyclosporin A, but not FK 506, protects mitochondria and neurons against hypoglycemic damage and implicates the mitochondrial permeability transition in cell death. Friberg H, Ferrand-Drake M, Bengtsson F, Halestrap AP, Wieloch T, J Neurosci 1998 18 5151 5159 9651198 (Pubitemid 28311932)
37. Effects of FK506 and cyclosporin A on calcium ionophore-induced mitochondrial depolarization and cytosolic calcium in astrocytes and neurons. Kahraman S, Bambrick LL, Fiskum G, J Neurosci Res 2011 89 1973 1978 10.1002/jnr.22709 21748780
38. Mitochondrial membrane potential and hydroethidine-monitored superoxide generation in cultured cerebellar granule cells. Budd SL, Castilho RF, Nicholls DG, FEBS Lett 1997 415 21 24 10.1016/S0014-5793(97)01088-0 9326361 (Pubitemid 27402041)
39. Mitochondrial formation of reactive oxygen species. Turrens JF, J Physiol Lond 2003 15 335 344 (Pubitemid 37321833)
40. Oxidative stress is involved in the permeabilization of the inner membrane of brain mitochondria exposed to hypoxia/reoxygenation and low micromolar Ca§ssup§2+§esup§ Schild L, Reiser G, FEBS J 2005 272 3593 3601 10.1111/j.1742-4658.2005.04781.x 16008559 (Pubitemid 41021172)
41. Three distinct mechanisms generate oxygen free radicals in neurons and contribute to cell death during anoxia and reoxygenation. Abramov AY, Scorziello A, Duchen MR, J Neurosci 2007 27 1129 1138 10.1523/JNEUROSCI.4468-06.2007 17267568 (Pubitemid 46203321)
42. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Kalyanaraman B, Darley-Usmar V, Davies KJA, Dennery PA, Forman HJ, Grisham MB, Mann GE, et al. Free Radic Biol Med 2012 52 1 6 10.1016/j.freeradbiomed.2011.09.030 22027063
43. Properties of the permeability transition pore in mitochondria devoid of Cyclophilin D. Basso E, Fante L, Fowlkes J, Petronilli V, Forte MA, Bernardi P, J Biol Chem 2005 280 18558 18561 10.1074/jbc.C500089200 15792954 (Pubitemid 41379552)
44. Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Petronilli V, Miotto G, Canton M, Brini M, Colonna R, Bernardi P, Di Lisa F, Biophys J 1999 76 725 734 10.1016/S0006- 3495(99)77239-5 9929477 (Pubitemid 29264555)
45. Could successful (mitochondrial) networking help prevent Huntington's disease? EMBO Mol. Oliveira JM, Lightowlers RN, Med 2010 2 487 489
46. Mitochondrial dynamics and division in budding yeast. Shaw JM, Nunnari J, Trends Cell Biol 2002 12 178 184 10.1016/S0962-8924(01)02246-2 11978537 (Pubitemid 34442240)
47. Staying in aerobic shape: how the structural integrity of mitochondria and mitochondrial DNA is maintained. Scott SV, Cassidy-Stone A, Meeusen SL, Nunnari J, Curr Opin Cell Biol 2003 15 482 488 10.1016/S0955-0674(03)00070-X 12892790 (Pubitemid 36928052)
48. Impairing the mitochondrial fission and fusion balance: a new mechanism of neurodegeneration. Knott AB, Bossy-Wetzel E, Ann NY Acad Sci 2008 1147 283 292 10.1196/annals.1427.030 19076450
49. Normal huntingtin function: an alternative approach to Huntington's disease. Cattaneo E, Zuccato C, Tartari M, Nat Rev Neurosci 2005 6 919 930 16288298 (Pubitemid 41753086)
50. The apoptosome: signalling platform of cell death. Riedl SJ, Salvesen GS, Nat Rev Mol Cell Biol 2007 8 405 413 17377525 (Pubitemid 46643237)
51. Mitochondrial calcium uptake capacity as a therapeutic target in the R6/2 mouse model of Huntington's disease. Perry GM, Tallaksen-Greene S, Kumar A, Heng MY, Kneynsberg A, van Groen T, Detloff PT, Albin RL, Lesort M, Hum Mol Genet 2010 19 3354 3371 10.1093/hmg/ddq247 20558522
52. Increased susceptibility of striatal mitochondria to calcium-induced permeability transition. Brustovetsky N, Brustovetsky T, Purl KJ, Capano M, Crompton M, Dubinsky JM, J Neurosci 2003 23 4858 4867 12832508 (Pubitemid 36793212)
53. Cyclophilin D inactivation protects axons in experimental autoimmune encephalomyelitis, an animal model of multiple sclerosis. Forte M, Gold BG, Marracci G, Chaudhary P, Basso E, Johnsen D, Yu X, Fowlkes J, Bernardi P, Bourdette D, Proc Natl Acad Sci USA 2007 104 7558 7563 10.1073/pnas.0702228104 17463082 (Pubitemid 47185945)
54. Systematic behavioral evaluation of Huntington's disease transgenic and knock-in mouse models. Menalled L, El-Khodor BF, Patry M, Suarez-Fariñas M, Orenstein SJ, Zahasky B, Leahy C, Wheeler V, Yang XW, MacDonald M, et al. Neurobiol Dis 2009 35 319 336 10.1016/j.nbd.2009.05.007 19464370
55. Paradoxical delay in the onset of disease caused by super-long CAG repeat expansions in R6/2 mice. Morton AJ, Glynn D, Leavens W, Zheng Z, Faull RLM, Skepper JN, Wight JM, Neurobiol Dis 2009 33 331 341 10.1016/j.nbd.2008.11.015 19130884
56. Metabolic state determines sensitivity to cellular stress in Huntington disease: normalization by activation of PPARγ Jin YN, Hwang WY, Jo C, Johnson GVW, PLoS ONE 2012 7 30406 10.1371/journal.pone.0030406 22276192
57. Truncated tau and Aβ cooperatively impair mitochondria in primary neurons. Quintanilla RA, Dolan PJ, Jin YN, Johnson GVW, Neurobiol Aging 2012 33 25 e35
58. Type 2 transglutaminase differentially modulates striatal cell death in the presence of wild type or mutant huntingtin. Ruan Q, Quintanilla RA, Johnson GV, J Neurochem 2007 102 25 36 10.1111/j.1471-4159.2007.04491.x 17403029 (Pubitemid 46906262)
59. Neurotoxic calcium transfer from endoplasmic reticulum to mitochondria is regulated by cyclin-dependent kinase 5-dependent phosphorylation of Tau. Darios F, Muriel MP, Khondiker ME, Brice A, Ruberg M, J Neurosci 2005 25 4159 4168 10.1523/JNEUROSCI.0060-05.2005 15843619 (Pubitemid 40563392)
60. [Ca§ssup§2+§esup§]§ssub§i§esub§ signaling between mitochondria and endoplasmic reticulum in neurons is regulated by microtubules. Mironov SL, Ivannikov MV, Johansson M, J Biol Chem 2005 280 715 721 15516333 (Pubitemid 40165039)