Endolysosomal Deficits Augment Mitochondria Pathology in Spinal Motor Neurons of Asymptomatic fALS Mice

Neuron

Volumn 87, Issue 2, 2015, Pages 355-370

  Xie, Yuxiang ^a   Zhou, Bing ^a   Lin, Mei Yao ^a   Wang, Shiwei ^a   Foust, Kevin D ^b   Sheng, Zu Hang ^a  

^a NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR SNAPIN; DYNEIN ADENOSINE TRIPHOSPHATASE; MOLECULAR MOTOR; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; NUCLEAR PROTEIN; SNAPIN PROTEIN, MOUSE; SOD1 G93A PROTEIN; TRIM27 PROTEIN, MOUSE; VESICULAR TRANSPORT PROTEIN;

AMYOTROPHIC LATERAL SCLEROSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASYMPTOMATIC DISEASE; AUTOPHAGY; BIOACCUMULATION; CELL METABOLISM; CELL SURVIVAL; CONTROLLED STUDY; DISEASE ASSOCIATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDOLYSOSOMAL DEFICIT; FEMALE; LYSOSOME STORAGE DISEASE; MALE; MOTONEURON; MOUSE; NERVE FIBER; NEUROIMAGING; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; RETROGRADE NERVE FIBER TRANSPORT; AGE; ANIMAL; CELL CULTURE; DISEASE COURSE; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC TRANSDUCTION; GENETICS; HUMAN; LYSOSOME; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; NERVE CELL; PATHOLOGY; SPINAL CORD; TIME; TRANSGENIC MOUSE; ULTRASTRUCTURE;

AGE FACTORS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; AUTOPHAGY; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HUMANS; LYSOSOMES; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE; MICE, TRANSGENIC; MITOCHONDRIA; NEURONS; NUCLEAR PROTEINS; SPINAL CORD; SUPEROXIDE DISMUTASE; TIME FACTORS; TRANSDUCTION, GENETIC; VESICULAR TRANSPORT PROTEINS;

EID: 84937425823     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2015.06.026     Document Type: Article

References (55)

1. Beal M.F. Mitochondria, free radicals, and neurodegeneration. Curr. Opin. Neurobiol. 1996, 6:661-666.
2. Bilsland L.G., Sahai E., Kelly G., Golding M., Greensmith L., Schiavo G. Deficits in axonal transport precede ALS symptoms invivo. Proc. Natl. Acad. Sci. USA 2010, 107:20523-20528.
3. Boland B., Kumar A., Lee S., Platt F.M., Wegiel J., Yu W.H., Nixon R.A. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J.Neurosci. 2008, 28:6926-6937.
4. Cai Q., Lu L., Tian J.-H., Zhu Y.-B., Qiao H., Sheng Z.-H. Snapin-regulated late endosomal transport is critical for efficient autophagy-lysosomal function in neurons. Neuron 2010, 68:73-86.
5. Castillo K., Nassif M., Valenzuela V., Rojas F., Matus S., Mercado G., Court F.A., van Zundert B., Hetz C. Trehalose delays the progression of amyotrophic lateral sclerosis by enhancing autophagy in motoneurons. Autophagy 2013, 9:1308-1320.
6. Chen H., Chan D.C. Mitochondrial dynamics--fusion, fission, movement, and mitophagy--in neurodegenerative diseases. Hum. Mol. Genet. 2009, 18(R2):R169-R176.
7. Cheng X.-T., Zhou B., Lin M.Y., Cai Q., Sheng Z.-H. Axonal autophagosomes recruit dynein for retrograde transport through fusion with late endosomes. J.Cell Biol. 2015, 209:377-386.
8. Chiò A., Borghero G., Calvo A., Capasso M., Caponnetto C., Corbo M., Giannini F., Logroscino G., Mandrioli J., Marcello N., et al. LITALS Study Group. Lithium carbonate in amyotrophic lateral sclerosis: lack of efficacy in a dose-finding trial. Neurology 2010, 75:619-625.
9. Cleveland D.W., Rothstein J.D. From Charcot to Lou Gehrig: deciphering selective motor neuron death in ALS. Nat. Rev. Neurosci. 2001, 2:806-819.
10. Cozzolino M., Ferri A., Valle C., Carrì M.T. Mitochondria and ALS: implications from novel genes and pathways. Mol. Cell. Neurosci. 2013, 55:44-49.
11. De Vos K.J., Chapman A.L., Tennant M.E., Manser C., Tudor E.L., Lau K.-F., Brownlees J., Ackerley S., Shaw P.J., McLoughlin D.M., et al. Familial amyotrophic lateral sclerosis-linked SOD1 mutants perturb fast axonal transport to reduce axonal mitochondria content. Hum. Mol. Genet. 2007, 16:2720-2728.
12. Dion P.A., Daoud H., Rouleau G.A. Genetics of motor neuron disorders: new insights into pathogenic mechanisms. Nat. Rev. Genet. 2009, 10:769-782.
13. Fischer L.R., Culver D.G., Tennant P., Davis A.A., Wang M., Castellano-Sanchez A., Khan J., Polak M.A., Glass J.D. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 2004, 185:232-240.
14. Fornai F., Longone P., Cafaro L., Kastsiuchenka O., Ferrucci M., Manca M.L., Lazzeri G., Spalloni A., Bellio N., Lenzi P., et al. Lithium delays progression of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA 2008, 105:2052-2057.
15. Foust K.D., Wang X., McGovern V.L., Braun L., Bevan A.K., Haidet A.M., Le T.T., Morales P.R., Rich M.M., Burghes A.H.M., Kaspar B.K. Rescue of the spinal muscular atrophy phenotype in a mouse model by early postnatal delivery of SMN. Nat. Biotechnol. 2010, 28:271-274.
16. Gal J., Ström A.-L., Kilty R., Zhang F., Zhu H. p62 accumulates and enhances aggregate formation in model systems of familial amyotrophic lateral sclerosis. J.Biol. Chem. 2007, 282:11068-11077.
17. Gill A., Kidd J., Vieira F., Thompson K., Perrin S. No benefit from chronic lithium dosing in a sibling-matched, gender balanced, investigator-blinded trial using a standard mouse model of familial ALS. PLoS ONE 2009, 4:e6489.
18. Gurney M.E., Pu H., Chiu A.Y., Dal Canto M.C., Polchow C.Y., Alexander D.D., Caliendo J., Hentati A., Kwon Y.W., Deng H.X., et al. Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 1994, 264:1772-1775.
19. Hafezparast M., Klocke R., Ruhrberg C., Marquardt A., Ahmad-Annuar A., Bowen S., Lalli G., Witherden A.S., Hummerich H., Nicholson S., et al. Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 2003, 300:808-812.
20. Hariri M., Millane G., Guimond M.P., Guay G., Dennis J.W., Nabi I.R. Biogenesis of multilamellar bodies via autophagy. Mol. Biol. Cell 2000, 11:255-268.
21. Harris H., Rubinsztein D.C. Control of autophagy as a therapy for neurodegenerative disease. Nat. Rev. Neurol. 2012, 8:108-117.
22. Ilieva H., Polymenidou M., Cleveland D.W. Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond. J.Cell Biol. 2009, 187:761-772.
23. Kang J.-S., Tian J.-H., Pan P.-Y., Zald P., Li C., Deng C., Sheng Z.-H. Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 2008, 132:137-148.
24. Kiselyov K., Jennigs J.J., Rbaibi Y., Chu C.T. Autophagy, mitochondria and cell death in lysosomal storage diseases. Autophagy 2007, 3:259-262.
25. Lambrechts D., Storkebaum E., Morimoto M., Del-Favero J., Desmet F., Marklund S.L., Wyns S., Thijs V., Andersson J., van Marion I., et al. VEGF is a modifier of amyotrophic lateral sclerosis in mice and humans and protects motoneurons against ischemic death. Nat. Genet. 2003, 34:383-394.
26. Lee S., Sato Y., Nixon R.A. Lysosomal proteolysis inhibition selectively disrupts axonal transport of degradative organelles and causes an Alzheimer's-like axonal dystrophy. J.Neurosci. 2011, 31:7817-7830.
27. Li L., Zhang X., Le W. Altered macroautophagy in the spinal cord of SOD1 mutant mice. Autophagy 2008, 4:290-293.
28. Ligon L.A., LaMonte B.H., Wallace K.E., Weber N., Kalb R.G., Holzbaur E.L.F. Mutant superoxide dismutase disrupts cytoplasmic dynein in motor neurons. Neuroreport 2005, 16:533-536.
29. Maday S., Wallace K.E., Holzbaur E.L.F. Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J.Cell Biol. 2012, 196:407-417.
30. Magrané J., Manfredi G. Mitochondrial function, morphology, and axonal transport in amyotrophic lateral sclerosis. Antioxid. Redox Signal. 2009, 11:1615-1626.
31. Marinkovic P., Reuter M.S., Brill M.S., Godinho L., Kerschensteiner M., Misgeld T. Axonal transport deficits and degeneration can evolve independently in mouse models of amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. USA 2012, 109:4296-4301.
32. Mizushima N., Yamamoto A., Matsui M., Yoshimori T., Ohsumi Y. Invivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell 2004, 15:1101-1111.
33. Morimoto N., Nagai M., Ohta Y., Miyazaki K., Kurata T., Morimoto M., Murakami T., Takehisa Y., Ikeda Y., Kamiya T., Abe K. Increased autophagy in transgenic mice with a G93A mutant SOD1 gene. Brain Res. 2007, 1167:112-117.
34. Mórotz G.M., De Vos K.J., Vagnoni A., Ackerley S., Shaw C.E., Miller C.C.J. Amyotrophic lateral sclerosis-associated mutant VAPBP56S perturbs calcium homeostasis to disrupt axonal transport of mitochondria. Hum. Mol. Genet. 2012, 21:1979-1988.
35. Nixon R.A. The role of autophagy in neurodegenerative disease. Nat. Med. 2013, 19:983-997.
36. Osellame L.D., Duchen M.R. Quality control gone wrong: mitochondria, lysosomal storage disorders and neurodegeneration. Br. J. Pharmacol. 2014, 171:1958-1972.
37. Pan P.-Y., Tian J.-H., Sheng Z.-H. Snapin facilitates the synchronization of synaptic vesicle fusion. Neuron 2009, 61:412-424.
38. Perlson E., Jeong G.B., Ross J.L., Dixit R., Wallace K.E., Kalb R.G., Holzbaur E.L.F. A switch in retrograde signaling from survival to stress in rapid-onset neurodegeneration. J.Neurosci. 2009, 29:9903-9917.
39. Pizzasegola C., Caron I., Daleno C., Ronchi A., Minoia C., Carrì M.T., Bendotti C. Treatment with lithium carbonate does not improve disease progression in two different strains of SOD1 mutant mice. Amyotroph. Lateral Scler. 2009, 10:221-228.
40. Ravikumar B., Acevedo-Arozena A., Imarisio S., Berger Z., Vacher C., O'Kane C.J., Brown S.D.M., Rubinsztein D.C. Dynein mutations impair autophagic clearance of aggregate-prone proteins. Nat. Genet. 2005, 37:771-776.
41. Rosen D.R., Siddique T., Patterson D., Figlewicz D.A., Sapp P., Hentati A., Donaldson D., Goto J., O'Regan J.P., Deng H.X., et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 1993, 362:59-62.
42. Sarkar S., Floto R.A., Berger Z., Imarisio S., Cordenier A., Pasco M., Cook L.J., Rubinsztein D.C. Lithium induces autophagy by inhibiting inositol monophosphatase. J.Cell Biol. 2005, 170:1101-1111.
43. Sasaki S., Warita H., Murakami T., Shibata N., Komori T., Abe K., Kobayashi M., Iwata M. Ultrastructural study of aggregates in the spinal cord of transgenic mice with a G93A mutant SOD1 gene. Acta Neuropathol. 2005, 109:247-255.
44. Settembre C., Fraldi A., Jahreiss L., Spampanato C., Venturi C., Medina D., de Pablo R., Tacchetti C., Rubinsztein D.C., Ballabio A. A block of autophagy in lysosomal storage disorders. Hum. Mol. Genet. 2008, 17:119-129.
45. Shan X., Chiang P.-M., Price D.L., Wong P.C. Altered distributions of Gemini of coiled bodies and mitochondria in motor neurons of TDP-43 transgenic mice. Proc. Natl. Acad. Sci. USA 2010, 107:16325-16330.
46. Sheng Z.-H., Cai Q. Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat. Rev. Neurosci. 2012, 13:77-93.
47. Ström A.-L., Shi P., Zhang F., Gal J., Kilty R., Hayward L.J., Zhu H. Interaction of amyotrophic lateral sclerosis (ALS)-related mutant copper-zinc superoxide dismutase with the dynein-dynactin complex contributes to inclusion formation. J.Biol. Chem. 2008, 283:22795-22805.
48. Van Hoecke A., Schoonaert L., Lemmens R., Timmers M., Staats K.A., Laird A.S., Peeters E., Philips T., Goris A., Dubois B., et al. EPHA4 is a disease modifier of amyotrophic lateral sclerosis in animal models and in humans. Nat. Med. 2012, 18:1418-1422.
49. Williamson T.L., Cleveland D.W. Slowing of axonal transport is a very early event in the toxicity of ALS-linked SOD1 mutants to motor neurons. Nat. Neurosci. 1999, 2:50-56.
50. Wootz H., Weber E., Korhonen L., Lindholm D. Altered distribution and levels of cathepsinD and cystatins in amyotrophic lateral sclerosis transgenic mice: possible roles in motor neuron survival. Neuroscience 2006, 143:419-430.
51. Zhang F., Ström A.L., Fukada K., Lee S., Hayward L.J., Zhu H. Interaction between familial amyotrophic lateral sclerosis (ALS)-linked SOD1 mutants and the dynein complex. J.Biol. Chem. 2007, 282:16691-16699.
52. Zhang X., Li L., Chen S., Yang D., Wang Y., Zhang X., Wang Z., Le W. Rapamycin treatment augments motor neuron degeneration in SOD1(G93A) mouse model of amyotrophic lateral sclerosis. Autophagy 2011, 7:412-425.
53. Zhou B., Cai Q., Xie Y., Sheng Z.-H. Snapin recruits dynein to BDNF-TrkB signaling endosomes for retrograde axonal transport and is essential for dendrite growth of cortical neurons. Cell Rep. 2012, 2:42-51.
54. Zhu Y.B., Sheng Z.H. Increased axonal mitochondrial mobility does not slow amyotrophic lateral sclerosis (ALS)-like disease in mutant SOD1 mice. J.Biol. Chem. 2011, 286:23432-23440.
55. Zhu S., Stavrovskaya I.G., Drozda M., Kim B.Y.S., Ona V., Li M., Sarang S., Liu A.S., Hartley D.M., Wu D.C., et al. Minocycline inhibits cytochrome c release and delays progression of amyotrophic lateral sclerosis in mice. Nature 2002, 417:74-78.