Mitochondrial abnormalities and low grade inflammation are present in the skeletal muscle of a minority of patients with amyotrophic lateral sclerosis; An observational myopathology study

Acta Neuropathologica Communications

Volumn 2, Issue 1, 2014, Pages

  Al Sarraj, Safa ^a   King, Andrew ^a   Cleveland, Matt ^b   Pradat, Pierre François ^c   Corse, Andrea ^d   Rothstein, Jeffrey D ^d   Leigh, Peter Nigel ^e   Abila, Bams ^b   Bates, Stewart ^b   Wurthner, Jens ^f   Meininger, Vincent ^c  

^a KING S COLLEGE HOSPITAL   (United Kingdom)

^b GLAXOSMITHKLINE   (United Kingdom)

^c SORBONNE UNIVERSITÉ   (France)

^d JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e BRIGHTON AND SUSSEX MEDICAL SCHOOL   (United Kingdom)

^f NOVARTIS PHARMA AG   (Switzerland)

Author keywords

Amyotrophic lateral Sclerosis; Inflammation; Mitochondria; Pathology and Muscle

Indexed keywords

CYTOCHROME C OXIDASE; DNA BINDING PROTEIN; P62 PROTEIN, HUMAN; RNA BINDING PROTEIN; TDP-43 PROTEIN, HUMAN;

ADULT; AMYOTROPHIC LATERAL SCLEROSIS; BIOPSY; BLOOD; COHORT ANALYSIS; FEMALE; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; MALE; METABOLISM; MIDDLE AGED; MITOCHONDRION; NECROSIS; PATHOLOGY; SKELETAL MUSCLE;

ADULT; AMYOTROPHIC LATERAL SCLEROSIS; BIOPSY; COHORT STUDIES; DNA-BINDING PROTEINS; ELECTRON TRANSPORT COMPLEX IV; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MIDDLE AGED; MITOCHONDRIA; MUSCLE, SKELETAL; NECROSIS; RNA-BINDING PROTEINS;

EID: 84964696520     PISSN: None     EISSN: 20515960     Source Type: Journal    
DOI: 10.1186/s40478-014-0165-z     Document Type: Review

References (57)

1. Shaw PJ: Molecular and cellular pathology of neurodegeneration in motor neuron disease. J Neurol Neurosurg Psychiatry 2005, 76: 1046-1057. 10.1136/jnnp.2004.048652
2. Mitchell JD, Borasio GD: Amyotrophic lateral sclerosis. Lancet 2007, 369: 2031-2041. 10.1016/S0140-6736(07)60944-1
3. Pasinelli P, Brown RH: Molecular biology of amyotrophic lateral sclerosis; insight from genetics. Nat Rev Neuroscience 2006, 7: 710-723. 10.1038/nrn1971
4. Love S, Louis DN, Ellison DW. Disease of movement disorder and system degeneration; motor neurone disease. Greenfield's Neuropathology, eight Edition 2008: Chapter 22, 947-961.
5. Pasinelli P, Belford ME, Lennon N, Bacskai BJ, Hyman BT, Trotti D, Brown BH: Amyotrophic lateral sclerosis associated SOD1 binds and aggregate with Bcl2 in spinal cord mitochondria. Neuron 2004, 43: 19-30. 10.1016/j.neuron.2004.06.021
6. Al-Sarraj S, King A, Troackes C, Smith B, Maekawa S, Bodi I, Rogeli B, Al-Chalabi A, Hortobagyi T, Shaw CE: p62 positive, TDP43 negative neuronal cytoplasmic inclusion in the cerebellum and hippocampus define the pathology of C9orf72 FTLD-MND. Acta Neuropathol 2011, 122(6):691-702. 10.1007/s00401-011-0911-2
7. Sreedharan J, Blair IP, Tripathi VB, Hu X, Vance C, Rogelj B, Ackerley S, Durnall JC, Williams KL, Buratti E, Baralle F, De Belleroche J, Mitchell JD, Leigh PN, Al-Chalabi A, Miller CC, Nicholson G, Shaw CE: TDP43 mutations in familial and sporadic amyotrophic lateral sclerosis. Science 2008, 319(5870):1668-1672. 10.1126/science.1154584
8. Krasnianski A, Deschauer M, Neudecker S, Gellerich FN, Müller T, Schoser BG, Krasnianski M, Zierz S: Mitochondrial changes in skeletal muscle in amyotrophic lateral sclerosis and other neurogenic atrophies. Brain 2005, 128: 1870-1876. 10.1093/brain/awh540
9. Vance C, Rogelj B, Hortobagyi T, De Vos KJ, Nishimura AL, Sreedharan J, Hu X, Smith B, Ruddy D, Wright P, Ganesalingam J, Williams KL, Tripathi V, Al-Saraj S, Al-Chalabi A, Leigh PN, Blair IP, Nicholson G, de Belleroche J, Gallo JM, Miller CC, Shaw CE: Mutations in FUS, an RNA processing protein, cause familial amyotrophic lateral sclerosis type 6. Science 2009, 323(5918):1208-1211. 10.1126/science.1165942
10. Rosen DR, Teepu S, David P, Figlewicz DA, Peter S, Afif H, Deirdre D, Jun G, O'Regan JP, Han-Xiang D, Zohra R, Aldis K, Diane MK-Y, Annarueber C, Gaston SM, Ralph B, Tanzi RE, Halperin JJ, Brian H, Van den Bergh R, Wu-Yen H, Thomas B, Gang D, Mulder DW, Celestine S, Laing NG, Edwin S, Pericak-Vance MA, Jonathan H, Rouleau GA, Gusella JS, Robert Horvitz H, Brown Jr RH: Mutation in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362(6415):59-62. 10.1038/362059a0
11. Vielhaber S, Kunz D, Winkler K, Wiedemann FR, Kirches E, Feistner H, Heinze HJ, Elger CE, Schubert W, Kunz WS: Mitochondrial DNA abnormalities in skeletal muscle of patients with sporadic amyotrophic lateral sclerosis. Brain 2000, 123: 1339-1348. 10.1093/brain/123.7.1339
12. Hirano M, Angelini C, Montagna P, Hays AP, Tanji K, Mitsumoto H, Gordon PH, Naini AB, DiMauro S, Rowland LP: Amyotrophic lateral sclerosis with ragged red fibres. Arch Neurol 2008, 65(3):403-406. 10.1001/archneurol.2007.65
13. Magrane J, Hervias I, Henning MS, Damiaso M, Kawamata H, Manfredi G: Mutant SOD1 in neuronal mitochondria causes toxicity and mitochondrial dynamic abnormalities. Hummol Genet 2009, 18: 4552-4558.
14. Dal Canto MC, Gurney ME: Neuropathological changes in two lines of mice carrying a transgene for mutant human CWZN SOD and are over-expressing wild human SOD; a model of familial amyotrophic lateral sclerosis. Brain Res 1995, 676: 25-40. 10.1016/0006-8993(95)00063-V
15. Wiedermann FR, Winkler K, Kuznetsov AV, Von Bossanyi P, Dietzmann K, Kunz WS: Impairment of mitochondrial function in skeletal muscle of patients with amyotrophic lateral sclerosis. J Neurol Sci 1998, 146: 65-72. 10.1016/S0022-510X(98)00008-2
16. Comi GP, Bordoni A, Salani S, Franceschina L, Sciacco M, Prelle A, Fortunato F, Zeviani M, Napoli L, Bresolin N, Moggio M, Ausenda CD, Taanman JW, Scarlato G: Cytochrome c oxidase subunit 1 microdeletion in a patient with motor neuron disease. Ann Neurol 1998, 43(1):110-116. 10.1002/ana.410430119
17. Crugnola V, Lamperti C, Lucchini V, Ronchi D, Peverelli L, Prelle A, Sciacco M, Bordoni A, Fassone E, Fortunato F, Corti S, Silani V, Bresolin N, Di Mauro S, Comi GP, Moggio M: Mitochondrial respiratory chain dysfunction in muscle from patient with amyotrophic lateral sclerosis. Arch Neurol 2010, 67(7):849-854. 10.1001/archneurol.2010.128
18. Xu Z, Jung C, Higgins C, Levine J, Kong J: Mitochondrial degeneration in amyotrophic lateral sclerosis. J Bioenerg Biomembr 2004, 36(4):395-399. 10.1023/B:JOBB.0000041774.12654.e1
19. Altoniemi T, Jaronen Y, Keksa-Goldstein V, Koistinaho J: Mutant SOD1 from spinal cord of G93A rats is destabilised and binds to inner mitochondria membrane. Neurobiol Dis 2008, 32: 479-485. 10.1016/j.nbd.2008.08.010
20. Ferri A, Cozzolino M, Crosio C, Nencini M, Casciati A: Familial ALS - superoxide dismutases associated with mitochondrias and shift redox potential. Proc Natl Acad Sci U S A 2006, 103: 13860-13865. 10.1073/pnas.0605814103
21. 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. 10.1016/j.jns.2005.02.004
22. Duffy LM, Chapman AL, Shaw PJ, Grierson AJ: Review: the role of mitochondria in the pathogenesis of amyotrophic lateral sclerosis. Neuropathol Appl Neurobiol 2011, 37: 336-352. 10.1111/j.1365-2990.2011.01166.x
23. Echaniz-Laguna A, Zoll J, Ribera F, Tranchant C, Warter JM, Lonsdorfer J, Lampert E: Mitochondrial respiratory chain function in skeletal muscle of ALS patients. Ann Neurol 2002, 52(5):623-627. 10.1002/ana.10357
24. Echaniz-Laguna A, Zoll J, Ponsot E, N'guessan B, Tranchant C, Loeffler JP, Lampert E: Muscle mitochondrial function in amyotrophic lateral sclerosis is progressively altered as the disease develops: a temporal study in man. Exp Neurol 2006, 198: 25-30. 10.1016/j.expneurol.2005.07.020
25. Brierley EJ, Johnson MA, Lightowlers RN, James OF, Turnbull DM: Role of mitochondrial DNA in human ageing; implication of the central nervous system and muscle. Ann Neurol 1998, 43(2):217-223. 10.1002/ana.410430212
26. Brierley EJ, Johnson MA, James OF, Turnbull DM: Mitochondrial involvement in the ageing is fact and controversies. Mol Cell Biochem 1997, 174(102):325-328. 10.1023/A:1006847319162
27. Johnston W, Karpati G, Carpenter S, Arnold D, Shoubridge EA: Late-onset mitochondrial myopathy. Ann Neurol 1995, 37(1):16-23. 10.1002/ana.410370106
28. Magnus T, Beck M, Gless R, Puls I, Naumann M, Toyka KV: Disease progression in amyotrophic lateral sclerosis: predictors of survival. Muscle Nerve 2002, 25(5):709-714. 10.1002/mus.10090
29. Ro LS, Lai SL, Chen CM, Chen ST: Deleted 4977-bp mitochondrial DNA mutation is associated with sporadic amyotrophic lateral sclerosis: a hospital-based case-control study. Muscle Nerve 2003, 28: 737-743. 10.1002/mus.10504
30. Rubio-Gozalbo ME, Smeitink JA, Ruitenbeek W, Ter Laak H, Mullaart RA, Schuelke M, Mariman EC, Sengers RC, Gabreëls FJ: Spinal muscular atrophy-like picture, cardiomyopathy and cytochrome c oxidase deficiency. Neurology 1999, 52(2):383-386. 10.1212/WNL.52.2.383
31. Fetoni V, Brierm E, Carrara F, Mora M, Zeviani M: Monomelic amyotrophy associated with the 7472insC mutation in the mtDNA tRNA ser(UCN) gene. Neuromuscul Disord 2004, 14(11):723-726. 10.1016/j.nmd.2004.07.002
32. Finsterer J: Mitochondriopathy mimicking amyotrophic lateral sclerosis. Neurologist 2003, 9(1):45-48. 10.1097/01.nrl.0000038589.58012.a8
33. Finisterer J: Lactate stress testing in sporadic amyotrophic lateral sclerosis. Int J Neurosci 2005, 115: 583-591. 10.1080/00207450590522847
34. Karpati G: Structural and molecular basis of skeletal muscle diseases; effects of denervation on muscle. ISN Neuropathology Press Basal 2002, Chapter 13: 252-256.
35. Dupuis L, Oudart H, Rene F, de Aguilar JL G, Loeffler JP: Evidence for defective energy homeostasis in amyotrophic lateral sclerosis: enefit of a high-energy diet in a transgenic mouse model. Proc Natl Acad Sci U S A 2004, 101: 11159-11164. 10.1073/pnas.0402026101
36. Dupuis L, de Aguilar JL G, Oudart H, de Tapia M, Barbeito L, Loeffler JP: Mitochondria in amyotrophic lateral sclerosis: a trigger and a target. Neurodegener Dis 2004, 1: 245-254. 10.1159/000085063
37. Bradley J, Taanman JW, Kallis C, Orrel R: Increased sensitivity of myoblasts to oxidative stress in amyotrophic lateral sclerosis peripheral tissue. Exp Neurol 2009, 218: 92-97. 10.1016/j.expneurol.2009.04.007
38. Manfredi G, Xu Z: Mitochondrial function and its role in motor neuron degeneration in ALS. Mitochondrion 2005, 5: 77-87. 10.1016/j.mito.2005.01.002
39. Werydt P, Moler T: Neuro-inflammation in the pathogenesis of amyotrophic lateral sclerosis. Neuroreport 2005, 16(6):527-531. 10.1097/00001756-200504250-00001
40. Beal MF: Mitochondria take center stage in ageing and neurodegneneration. Ann Neurol 2005, 58: 49-505. 10.1002/ana.20624
41. Borthwick GM, Taylor RW, Walls TJ, Tonska K, Taylor GA, Shaw PJ, Ince PG, Turnbull DM: Motor neuron disease in a patient with a mitochondrial tRNA mutation. Ann Neurol 2006, 59: 570-574. 10.1002/ana.20758
42. Wiedermann 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):616-625. 10.1046/j.0022-3042.2001.00731.x
43. Sasaki S, Iwata M: Mitochondrial alterations in the spinal cord of patients with sporadic amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 2007, 66: 10-16. 10.1097/nen.0b013e31802c396b
44. Simpson EP, Yen AA, Appel SH: Oxidative stress: a common denominator in the pathogenesis of amyotrophic lateral sclerosis. Curr Opin Rheumatol 2003, 15(6):730-736. 10.1097/00002281-200311000-00008
45. Siciliano G, Pastorini E, Pasquali L, Manca ML, Iudice A, Murri L: Impaired oxidative metabolism in exercising muscle from ALS patients. J Neurol Sci 2009, 191: 61-65. 10.1016/S0022-510X(01)00620-7
46. Mattiazzi M, D'Aurelio N, Gajewski CD, Martushova K, Kiaei M, Beal MF, Manfredi G: Mutated human SOD1 causes dysfunction of oxidative phosphorylation in mitochondria of transgenic mice. J Biol Chem 2002, 33: 29626-29633. 10.1074/jbc.M203065200
47. Grehl T, Fishcer S, Muller K, Malin JP, Zang J: A Prospective Study to Evaluate the Impact of 31P-MRS to Determinate. 2007.
48. Dupuis L, de Aguilar Jl G, Echaniz-Laguna A, Eschbach J, Rene F, Oudart H, Halter B, Huze C, Schaeffer L, Bouillaud F, Loeffler JP: Muscle mitochondrial uncoupling dismantles neuromuscular junction and triggers distal degeneration of motor neurons. PLoS One 2009, 4: e5390. 10.1371/journal.pone.0005390
49. Moissek K, Strong MJ: Innate immunity in amyotrophic lateral sclerosis. Biochem Biophys Acta 2006, 1176(11-12):1083-1093.
50. Sargsyan SA, Monk PN, Shau PJ: Microglia as potential contributors to motor neurone injury in amyotrophic lateral sclerosis. Glia 2005, 51(4):241-253. 10.1002/glia.20210
51. Dewil M, Van Den Bosch L, Robberecht W: Microglia in amyotrophic lateral sclerosis. Acta Neurol Belg 2007, 107(3):63-70.
52. Yamanaka K, Chun SJ, Boillee S, Fujimori-Tonou N, Yamashita H, Gutmann DH, Takahashi R, Misawa H, Cleveland DW: Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat Neurosci 2008, 11(3):251-253. 10.1038/nn2047
53. Fischer LR, Gulver DG, Tennat P, Davis AA, Wang M, Castellano-Sanchez A, Khan J: Amyotrophic lateral sclerosis is a distal axonopathy; evidence in mice and man. Exp Neurol 2004, 85: 232-240. 10.1016/j.expneurol.2003.10.004
54. Jokic N, de Aguilar JL G, Dimou L, Lin S, Fergania A: The neurite outgrowth inhibitor NOGO-A promotes degeneration in amyotrophic lateral sclerosis model. EMBO Rep 2006, 11: 1162-1167. 10.1038/sj.embor.7400826
55. Pradat PF, Bruneteau G, Gozalez de Aguilar JL, Dupuisis L, Jokic N, Salachas F, Le Forestier N, Echaniz-Laguna A, Dubourg O, Hauw JJ, Tranchant C, Loeffler JP, Meininger V: Muscle NOGO-A expression is prognostic marker in lower motor neuron syndrome. Ann Neurol 2007, 62: 15-20. 10.1002/ana.21122
56. Mancuso M, Confori FL, Rocchi A, Tessitore A, Muglia M, Tedeschi G, Panza D, Monsurrò M, Sola P, Mandrioli J, Choub A, DelCorona A, Manca ML, Mazzei R, Sprovieri T, Filosto M, Salviati A, Valentino P, Bono F, Caracciolo M, Simone IL, La Bella V, Majorana G, Siciliano G, Murri L, Quattrone A: Could mitochondrial haplogroups paly a role in sporadic amyotrophic lateral sclerosis? Neurosci Lett 2004, 371: 158-162. 10.1016/j.neulet.2004.08.060
57. Dupuis L, Loeffler JP: Neuromuscular junction destruction during amyotrophic lateral sclerosis: insights from transgenic models. Curr Opin Pharmacol 2009, 9: 31-346. 10.1016/j.coph.2009.03.007