Mitochondrial dynamic abnormalities in amyotrophic lateral sclerosis

Translational Neurodegeneration

Volumn 4, Issue 1, 2015, Pages

  Jiang, Zhen ^a   Wang, Wenzhang ^a   Perry, George ^b   Zhu, Xiongwei ^a   Wang, Xinglong ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b University of San Antonio   (United States)

Author keywords

ALS; Mitochondrial biogenesis and mitophagy; Mitochondrial dynamics; Mitochondrial dysfunction; Mitochondrial fission and fusion; Mitochondrial trafficking

Indexed keywords

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; BIOGENESIS; CELL FISSION; CELL FUNCTION; CELL FUSION; CELL MIGRATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; DISORDERS OF MITOCHONDRIAL FUNCTIONS; HUMAN; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; NONHUMAN; PRIORITY JOURNAL;

EID: 84938063858     PISSN: None     EISSN: 20479158     Source Type: Journal    
DOI: 10.1186/s40035-015-0037-x     Document Type: Article

References (88)

1. Gordon PH. Amyotrophic Lateral Sclerosis: An update for 2013 Clinical Features, Pathophysiology, Management and Therapeutic Trials. Aging and Dis. 2013;4(5):295-310.
2. Leigh PN. Chapter 13 Amyotrophic lateral sclerosis. Handb Clin Neurol. 2007;82:249-78.
3. Su B, Wang X, Zheng L, Perry G, Smith MA, Zhu X. Abnormal mitochondrial dynamics and neurodegenerative diseases. Biochim Biophys Acta. 2010;1802(1):135-42.
4. Tan W, Pasinelli P, Trotti D. Role of mitochondria in mutant SOD1 linked amyotrophic lateral sclerosis. Biochim Biophys Acta. 2014;1842(8):1295-301.
5. Benard G, Bellance N, James D, Parrone P, Fernandez H, Letellier T, et al. Mitochondrial bioenergetics and structural network organization. J Cell Sci. 2007;120(Pt 5):838-48.
6. Delettre C, Lenaers G, Griffoin JM, Gigarel N, Lorenzo C, Belenguer P, et al. Nuclear gene OPA1, encoding a mitochondrial dynamin-related protein, is mutated in dominant optic atrophy. Nat Genet. 2000;26(2):207-10.
7. Sheng ZH. Mitochondrial trafficking and anchoring in neurons: New insight and implications. J Cell Biol. 2014;204(7):1087-98.
8. Kawamata H, Manfredi G. Import, Maturation, and Function of SOD1 and Its Copper Chaperone CCS in the Mitochondrial Intermembrane Space. Antioxid Redox Sign. 2010;13(9):1375-84.
9. Mattiazzi M, D'Aurelio M, Gajewski CD, Martushova K, Kiaei M, Beal MF, et al. Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J Biol Chem. 2002;277(33):29626-33.
10. Liu J, Lillo C, Jonsson PA, Vande Velde C, Ward CM, Miller TM, et al. Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron. 2004;43(1):5-17.
11. Bergemalm D, Jonsson PA, Graffmo KS, Andersen PM, Brannstrom T, Rehnmark A, et al. Overloading of stable and exclusion of unstable human superoxide dismutase-1 variants in mitochondria of murine amyotrophic lateral sclerosis models. J Neurosci. 2006;26(16):4147-54.
12. Deng HX, Shi Y, Furukawa Y, Zhai H, Fu RG, Liu ED, et al. Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria. P Natl Acad Sci USA. 2006;103(18):7142-7.
13. Israelson A, Arbel N, Da Cruz S, Ilieva H, Yamanaka K, Shoshan-Barmatz V, et al. Misfolded mutant SOD1 directly inhibits VDAC1 conductance in a mouse model of inherited ALS. Neuron. 2010;67(4):575-87.
14. Wiedemann FR, Manfredi G, Mawrin C, Beal MF, Schon EA. Mitochondrial DNA and respiratory chain function in spinal cords of ALS patients. J Neurochem. 2002;80(4):616-25.
15. Borthwick GM, Johnson MA, Ince PG, Shaw PJ, Turnbull DM. Mitochondrial enzyme activity in amyotrophic lateral sclerosis: implications for the role of mitochondria in neuronal cell death. Ann Neurol. 1999;46(5):787-90.
16. Genova ML, Pich MM, Bernacchia A, Bianchi C, Biondi A, Bovina C, et al. The mitochondrial production of reactive oxygen species in relation to aging and pathology. Ann N Y Acad Sci. 2004;1011:86-100.
17. Adam-Vizi V. Production of reactive oxygen species in brain mitochondria: contribution by electron transport chain and non-electron transport chain sources. Antioxid Redox Signal. 2005;7(9-10):1140-9.
18. Pitkanen S, Robinson BH. Mitochondrial complex I deficiency leads to increased production of superoxide radicals and induction of superoxide dismutase. J Clin Invest. 1996;98(2):345-51.
19. Rizzardini M, Mangolini A, Lupi M, Ubezio P, Bendotti C, Cantoni L. 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. 2005;232(1-2):95-103.
20. Shaw PJ, Ince PG, Falkous G, Mantle D. Oxidative damage to protein in sporadic motor neuron disease spinal cord. Ann Neurol. 1995;38(4):691-5.
21. Ikawa M, Okazawa H, Tsujikawa T, Matsunaga A, Yamamura O, Mori T, et al. Increased oxidative stress is related to disease severity in the ALS motor cortex: A PET study. Neurology. 2015;84(20):2033-9.
22. Kihira T, Okamoto K, Yoshida S, Kondo T, Iwai K, Wada S, et al. Environmental characteristics and oxidative stress of inhabitants and patients with amyotrophic lateral sclerosis in a high-incidence area on the Kii Peninsula, Japan. Int Med. 2013;52(13):1479-86.
23. Siklos L, Engelhardt J, Harati Y, Smith RG, Joo F, Appel SH. Ultrastructural evidence for altered calcium in motor nerve terminals in amyotropic lateral sclerosis. Ann Neurol. 1996;39(2):203-16.
24. Damiano M, Starkov AA, Petri S, Kipiani K, Kiaei M, Mattiazzi M, et al. Neural mitochondrial Ca2+ capacity impairment precedes the onset of motor symptoms in G93A Cu/Zn-superoxide dismutase mutant mice. J Neurochem. 2006;96(5):1349-61.
25. Kim HJ, Magrane J, Starkov AA, Manfredi G. The mitochondrial calcium regulator cyclophilin D is an essential component of oestrogen-mediated neuroprotection in amyotrophic lateral sclerosis. Brain: a J Neurol. 2012;135(Pt 9):2865-74.
26. Parone PA, Da Cruz S, Han JS, McAlonis-Downes M, Vetto AP, Lee SK, et al. Enhancing mitochondrial calcium buffering capacity reduces aggregation of misfolded SOD1 and motor neuron cell death without extending survival in mouse models of inherited amyotrophic lateral sclerosis. J Neurosci. 2013;33(11):4657-71.
27. Tradewell ML, Durham HD. Calpastatin reduces toxicity of SOD1G93A in a culture model of amyotrophic lateral sclerosis. Neuroreport. 2010;21(15):976-9.
28. Hirano A, Donnenfeld H, Sasaki S, Nakano I. Fine structural observations of neurofilamentous changes in amyotrophic lateral sclerosis. J Neuropathol Exp Neurol. 1984;43(5):461-70.
29. Vande Velde C, McDonald KK, Boukhedimi Y, McAlonis-Downes M, Lobsiger CS, Bel Hadj S, et al. Misfolded SOD1 associated with motor neuron mitochondria alters mitochondrial shape and distribution prior to clinical onset. PLoS One. 2011;6(7), e22031.
30. Song W, Song Y, Kincaid B, Bossy B, Bossy-Wetzel E. Mutant SOD1G93A triggers mitochondrial fragmentation in spinal cord motor neurons: neuroprotection by SIRT3 and PGC-1alpha. Neurobiol Dis. 2013;51:72-81.
31. Vinsant S, Mansfield C, Jimenez-Moreno R, Del Gaizo MV, Yoshikawa M, Hampton TG, et al. Characterization of early pathogenesis in the SOD1(G93A) mouse model of ALS: part II, results and discussion. Brain and Behavior. 2013;3(4):431-57.
32. Vinsant S, Mansfield C, Jimenez-Moreno R, Del Gaizo MV, Yoshikawa M, Hampton TG, et al. Characterization of early pathogenesis in the SOD1(G93A) mouse model of ALS: part I, background and methods. Brain and Behavior. 2013;3(4):335-50.
33. Magrane J, Cortez C, Gan WB, Manfredi G. Abnormal mitochondrial transport and morphology are common pathological denominators in SOD1 and TDP43 ALS mouse models. Hum Mol Genet. 2014;23(6):1413-24.
34. Xu YF, Gendron TF, Zhang YJ, Lin WL, D'Alton S, Sheng H, et al. Wild-type human TDP-43 expression causes TDP-43 phosphorylation, mitochondrial aggregation, motor deficits, and early mortality in transgenic mice. J Neurosci. 2010;30(32):10851-9.
35. Xu YF, Zhang YJ, Lin WL, Cao X, Stetler C, Dickson DW, et al. Expression of mutant TDP-43 induces neuronal dysfunction in transgenic mice. Mol Neurodegener. 2011;6:73.
36. Wang W, Li L, Lin WL, Dickson DW, Petrucelli L, Zhang T, et al. The ALS disease-associated mutant TDP-43 impairs mitochondrial dynamics and function in motor neurons. Hum Mol Genet. 2013;22(23):4706-19.
37. Chan DC. Mitochondria: dynamic organelles in disease, aging, and development. Cell. 2006;125(7):1241-52.
38. Bleazard W, McCaffery JM, King EJ, Bale S, Mozdy A, Tieu Q, et al. The dynamin-related GTPase Dnm1 regulates mitochondrial fission in yeast. Nat Cell Biol. 1999;1(5):298-304.
39. McBride HM, Neuspiel M, Wasiak S. Mitochondria: more than just a powerhouse. Current Biology : CB. 2006;16(14):R551-60.
40. Loson OC, Song Z, Chen H, Chan DC. Fis1, Mff, MiD49 and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol Biol Cell. 2013;24(5):659-67.
41. Detmer SA, Chan DC. Functions and dysfunctions of mitochondrial dynamics. Nat Rev Mol Cell Biol. 2007;8(11):870-9.
42. Liu W, Yamashita T, Tian F, Morimoto N, Ikeda Y, Deguchi K, et al. Mitochondrial fusion and fission proteins expression dynamically change in a murine model of amyotrophic lateral sclerosis. Curr Neurovasc Res. 2013;10(3):222-30.
43. Picard M, Shirihai OS, Gentil BJ, Burelle Y. Mitochondrial morphology transitions and functions: implications for retrograde signaling? Am J Physiol Regul Integr Comp Physiol. 2013;304(6):R393-406.
44. 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(2):433-46.
45. Liu W, Acin-Perez R, Geghman KD, Manfredi G, Lu B, Li C. Pink1 regulates the oxidative phosphorylation machinery via mitochondrial fission. Proc Natl Acad Sci U S A. 2011;108(31):12920-4.
46. Cogliati S, Frezza C, Soriano ME, Varanita T, Quintana-Cabrera R, Corrado M, et al. Mitochondrial cristae shape determines respiratory chain supercomplexes assembly and respiratory efficiency. Cell. 2013;155(1):160-71.
47. Sasaki S, Iwata M. Mitochondrial alterations in the spinal cord of patients with sporadic amyotrophic lateral sclerosis. J Neuropathol Exp Neurol. 2007;66(1):10-6.
48. De Vos KJ, Chapman AL, Tennant ME, Manser C, Tudor EL, Lau KF, et al. Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum Mol Genet. 2007;16(22):2720-8.
49. Sotelo-Silveira JR, Lepanto P, Elizondo V, Horjales S, Palacios F, Martinez-Palma L, et al. Axonal mitochondrial clusters containing mutant SOD1 in transgenic models of ALS. Antioxid Redox Signal. 2009;11(7):1535-45.
50. Igaz LM, Kwong LK, Lee EB, Chen-Plotkin A, Swanson E, Unger T, et al. Dysregulation of the ALS-associated gene TDP-43 leads to neuronal death and degeneration in mice. J Clin Invest. 2011;121(2):726-38.
51. Janssens J, Wils H, Kleinberger G, Joris G, Cuijt I, Ceuterick-de Groote C, et al. Overexpression of ALS-associated p. M337V human TDP-43 in mice worsens disease features compared to wild-type human TDP-43 mice. Mol Neurobiol. 2013;48(1):22-35.
52. Guo X, Macleod GT, Wellington A, Hu F, Panchumarthi S, Schoenfield M, et al. The GTPase dMiro is required for axonal transport of mitochondria to Drosophila synapses. Neuron. 2005;47(3):379-93.
53. Kieran D, Hafezparast M, Bohnert S, Dick JR, Martin J, Schiavo G, et al. A mutation in dynein rescues axonal transport defects and extends the life span of ALS mice. J Cell Biol. 2005;169(4):561-7.
54. Frederick RL, Shaw JM. Moving mitochondria: establishing distribution of an essential organelle. Traffic. 2007;8(12):1668-75.
55. Sasaki S, Iwata M. Impairment of fast axonal transport in the proximal axons of anterior horn neurons in amyotrophic lateral sclerosis. Neurology. 1996;47(2):535-40.
56. Silverstein B, Feld S, Kozlowski LT. The availability of low-nicotine cigarettes as a cause of cigarette smoking among teenage females. J Health Soc Behav. 1980;21(4):383-8.
57. Schwarz TL. Mitochondrial trafficking in neurons. Cold Spring Harb Perspect Biol. 2013;5:6.
58. Zhang F, Wang W, Siedlak SL, Liu Y, Liu J, Jiang K, et al. Miro1 deficiency in amyotrophic lateral sclerosis. Front Aging Neurosci. 2015;7:100.
59. Ligon LA, LaMonte BH, Wallace KE, Weber N, Kalb RG, Holzbaur EL. Mutant superoxide dismutase disrupts cytoplasmic dynein in motor neurons. Neuroreport. 2005;16(6):533-6.
60. Wen HL, Lin YT, Ting CH, Lin-Chao S, Li H, Hsieh-Li HM. Stathmin, a microtubule-destabilizing protein, is dysregulated in spinal muscular atrophy. Hum Mol Genet. 2010;19(9):1766-78.
61. Lim KL, Ng XH, Grace LG, Yao TP. Mitochondrial dynamics and Parkinson's disease: focus on parkin. Antioxid Redox Signal. 2012;16(9):935-49.
62. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, et al. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98(1):115-24.
63. Wang J, Zhang Y, Tang L, Zhang N, Fan D. Protective effects of resveratrol through the up-regulation of SIRT1 expression in the mutant hSOD1-G93A-bearing motor neuron-like cell culture model of amyotrophic lateral sclerosis. Neurosci Lett. 2011;503(3):250-5.
64. Stribl C, Samara A, Trumbach D, Peis R, Neumann M, Fuchs H, et al. Mitochondrial dysfunction and decrease in body weight of a transgenic knock-in mouse model for TDP-43. J Biol Chem. 2014;289(15):10769-84.
65. Wong YC, Holzbaur EL. Optineurin is an autophagy receptor for damaged mitochondria in parkin-mediated mitophagy that is disrupted by an ALS-linked mutation. Proc Natl Acad Sci U S A. 2014;111(42):E4439-48.
66. Kimura Y, Fukushi J, Hori S, Matsuda N, Okatsu K, Kakiyama Y, et al. Different dynamic movements of wild-type and pathogenic VCPs and their cofactors to damaged mitochondria in a Parkin-mediated mitochondrial quality control system. Genes Cells. 2013;18(12):1131-43.
67. Gal J, Strom AL, Kwinter DM, Kilty R, Zhang J, Shi P, et al. Sequestosome 1/p62 links familial ALS mutant SOD1 to LC3 via an ubiquitin-independent mechanism. J Neurochem. 2009;111(4):1062-73.
68. Li L, Zhang X, Le W. Altered macroautophagy in the spinal cord of SOD1 mutant mice. Autophagy. 2008;4(3):290-3.
69. Zhang XJ, Li LA, Chen S, Yang DH, Wang Y, Zhang X, et al. Rapamycin treatment augments motor neuron degeneration in SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Autophagy. 2011;7(4):412-25.
70. Zhang X, Chen S, Song L, Tang Y, Shen Y, Jia L, et al. MTOR-independent, autophagic enhancer trehalose prolongs motor neuron survival and ameliorates the autophagic flux defect in a mouse model of amyotrophic lateral sclerosis. Autophagy. 2014;10(4):588-602.
71. Hailey DW, Rambold AS, Satpute-Krishnan P, Mitra K, Sougrat R, Kim PK, et al. Mitochondria supply membranes for autophagosome biogenesis during starvation. Cell. 2010;141(4):656-67.
72. Zhao T, Huang X, Han L, Wang X, Cheng H, Zhao Y, et al. Central role of mitofusin 2 in autophagosome-lysosome fusion in cardiomyocytes. J Biol Chem. 2012;287(28):23615-25.
73. Bensimon G, Lacomblez L, Meininger V. A controlled trial of riluzole in amyotrophic lateral sclerosis. ALS/Riluzole Study Group. N Engl J Med. 1994;330(9):585-91.
74. Lacomblez L, Bensimon G, Leigh PN, Guillet P, Meininger V. Dose-ranging study of riluzole in amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis/Riluzole Study Group II. Lancet. 1996;347(9013):1425-31.
75. Cozzolino M, Carri MT. Mitochondrial dysfunction in ALS. Prog Neurobiol. 2012;97(2):54-66.
76. Matthews RT, Yang L, Browne S, Baik M, Beal MF. Coenzyme Q10 administration increases brain mitochondrial concentrations and exerts neuroprotective effects. Proc Natl Acad Sci U S A. 1998;95(15):8892-7.
77. Bordet T, Buisson B, Michaud M, Drouot C, Galea P, Delaage P, et al. Identification and characterization of cholest-4-en-3-one, oxime (TRO19622), a novel drug candidate for amyotrophic lateral sclerosis. J Pharmacol Exp Ther. 2007;322(2):709-20.
78. Martin LJ. Olesoxime, a cholesterol-like neuroprotectant for the potential treatment of amyotrophic lateral sclerosis. IDrugs: The Invest Drugs J. 2010;13(8):568-80.
79. Wang H, Guan Y, Wang X, Smith K, Cormier K, Zhu S, et al. Nortriptyline delays disease onset in models of chronic neurodegeneration. Eur J Neurosci. 2007;26(3):633-41.
80. Keep M, Elmer E, Fong KS, Csiszar K. Intrathecal cyclosporin prolongs survival of late-stage ALS mice. Brain Res. 2001;894(2):327-31.
81. Price NL, Gomes AP, Ling AJ, Duarte FV, Martin-Montalvo A, North BJ, et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab. 2012;15(5):675-90.
82. Da Cruz S, Parone PA, Lopes VS, Lillo C, McAlonis-Downes M, Lee SK, et al. Elevated PGC-1alpha activity sustains mitochondrial biogenesis and muscle function without extending survival in a mouse model of inherited ALS. Cell Metab. 2012;15(5):778-86.
83. Li Z, Okamoto K, Hayashi Y, Sheng M. The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses. Cell. 2004;119(6):873-87.
84. Misko A, Jiang S, Wegorzewska I, Milbrandt J, Baloh RH. Mitofusin 2 is necessary for transport of axonal mitochondria and interacts with the Miro/Milton complex. J Neurosci. 2010;30(12):4232-40.
85. Wang X, Su B, Lee HG, Li X, Perry G, Smith MA, et al. Impaired balance of mitochondrial fission and fusion in Alzheimer's disease. J Neurosci. 2009;29(28):9090-103.
86. Nguyen TT, Oh SS, Weaver D, Lewandowska A, Maxfield D, Schuler MH, et al. Loss of Miro1-directed mitochondrial movement results in a novel murine model for neuron disease. Proc Natl Acad Sci U S A. 2014;111(35):E3631-40.
87. Shi P, Gal J, Kwinter DM, Liu X, Zhu H. Mitochondrial dysfunction in amyotrophic lateral sclerosis. Biochim Biophys Acta. 2010;1802(1):45-51.
88. Archer SL. Mitochondrial dynamics--mitochondrial fission and fusion in human diseases. N Engl J Med. 2013;369(23):2236-51.