VPS35 Deficiency or Mutation Causes Dopaminergic Neuronal Loss by Impairing Mitochondrial Fusion and Function

Cell Reports

Volumn 12, Issue 10, 2015, Pages 1631-1643

  Tang, Fu Lei ^a,b   Liu, Wei ^a,c   Hu, Jin Xia ^d   Erion, Joanna Ruth ^a   Ye, Jian ^c   Mei, Lin ^a   Xiong, Wen Cheng ^a,b  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c THIRD MILITARY MEDICAL UNIVERSITY   (China)

^d XUZHOU MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; MITOFUSIN 2; UBIQUITIN PROTEIN LIGASE E3; MITOCHONDRIAL PROTEIN; MUL1 PROTEIN, MOUSE; UBIQUITIN PROTEIN LIGASE; VESICULAR TRANSPORT PROTEIN; VPS35 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOACCUMULATION; CELL FUNCTION; CELL FUSION; CELL LOSS; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOWN REGULATION; GENE DELETION; GENE EXPRESSION; GENE MUTATION; IN VIVO STUDY; MOUSE; NERVE CELL CULTURE; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN STABILITY; UBIQUITINATION; VACUOLAR PROTEIN SORTING 35 GENE; ANIMAL; C57BL MOUSE; CELL CULTURE; GENETICS; KNOCKOUT MOUSE; METABOLISM; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PATHOLOGY; PHYSIOLOGY; PROTEIN TRANSPORT;

ALPHA-SYNUCLEIN; ANIMALS; CELLS, CULTURED; DOPAMINERGIC NEURONS; MEMBRANE POTENTIAL, MITOCHONDRIAL; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; PARKINSON DISEASE; PROTEIN TRANSPORT; UBIQUITIN-PROTEIN LIGASES; VESICULAR TRANSPORT PROTEINS;

EID: 84941177479     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.08.001     Document Type: Article

References (43)

1. Braschi E., Zunino R., McBride H.M. MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission. EMBO Rep. 2009, 10:748-754.
2. Braschi E., Goyon V., Zunino R., Mohanty A., Xu L., McBride H.M. Vps35 mediates vesicle transport between the mitochondria and peroxisomes. Curr. Biol. 2010, 20:1310-1315.
3. Chan D.C. Dissecting mitochondrial fusion. Dev. Cell 2006, 11:592-594.
4. Chan D.C. Mitochondrial fusion and fission in mammals. Annu. Rev. Cell Dev. Biol. 2006, 22:79-99.
5. Chen L.B. Mitochondrial membrane potential in living cells. Annu. Rev. Cell Biol. 1988, 4:155-181.
6. Chen H., Detmer S.A., Ewald A.J., Griffin E.E., Fraser S.E., Chan D.C. Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J. Cell Biol. 2003, 160:189-200.
7. Eaton S. Retromer retrieves wntless. Dev. Cell 2008, 14:4-6.
8. Gasser T. Update on the genetics of Parkinson's disease. Mov. Disord. 2007, 22(Suppl 17):S343-S350.
9. Haelterman N.A., Yoon W.H., Sandoval H., Jaiswal M., Shulman J.M., Bellen H.J. A mitocentric view of Parkinson's disease. Annu. Rev. Neurosci. 2014, 37:137-159.
10. Itoh K., Nakamura K., Iijima M., Sesaki H. Mitochondrial dynamics in neurodegeneration. Trends Cell Biol. 2013, 23:64-71.
11. Karbowski M., Youle R.J. Dynamics of mitochondrial morphology in healthy cells and during apoptosis. Cell Death Differ. 2003, 10:870-880.
12. Knott A.B., Perkins G., Schwarzenbacher R., Bossy-Wetzel E. Mitochondrial fragmentation in neurodegeneration. Nat. Rev. Neurosci. 2008, 9:505-518.
13. Lee Y., Dawson V.L., Dawson T.M. Animal models of Parkinson's disease: vertebrate genetics. Cold Spring Harb. Perspect. Med. 2012, 2:a009324.
14. Lee S., Sterky F.H., Mourier A., Terzioglu M., Cullheim S., Olson L., Larsson N.G. Mitofusin 2 is necessary for striatal axonal projections of midbrain dopamine neurons. Hum. Mol. Genet. 2012, 21:4827-4835.
15. Lin X., Parisiadou L., Sgobio C., Liu G., Yu J., Sun L., Shim H., Gu X.L., Luo J., Long C.X., et al. Conditional expression of Parkinson's disease-related mutant α-synuclein in the midbrain dopaminergic neurons causes progressive neurodegeneration and degradation of transcription factor nuclear receptor related 1. J. Neurosci. 2012, 32:9248-9264.
16. Lokireddy S., Wijesoma I.W., Teng S., Bonala S., Gluckman P.D., McFarlane C., Sharma M., Kambadur R. The ubiquitin ligase Mul1 induces mitophagy in skeletal muscle in response to muscle-wasting stimuli. Cell Metab. 2012, 16:613-624.
17. Losón O.C., Song Z., Chen H., Chan D.C. Fis1, Mff, MiD49, and MiD51 mediate Drp1 recruitment in mitochondrial fission. Mol. Biol. Cell 2013, 24:659-667.
18. MacLeod D.A., Rhinn H., Kuwahara T., Zolin A., Di Paolo G., McCabe B.D., Marder K.S., Honig L.S., Clark L.N., Small S.A., Abeliovich A. RAB7L1 interacts with LRRK2 to modify intraneuronal protein sorting and Parkinson's disease risk. Neuron 2013, 77:425-439.
19. Martin I., Dawson V.L., Dawson T.M. Recent advances in the genetics of Parkinson's disease. Annu. Rev. Genomics Hum. Genet. 2011, 12:301-325.
20. Muhammad A., Flores I., Zhang H., Yu R., Staniszewski A., Planel E., Herman M., Ho L., Kreber R., Honig L.S., et al. Retromer deficiency observed in Alzheimer's disease causes hippocampal dysfunction, neurodegeneration, and Abeta accumulation. Proc. Natl. Acad. Sci. USA 2008, 105:7327-7332.
21. Nielsen M.S., Gustafsen C., Madsen P., Nyengaard J.R., Hermey G., Bakke O., Mari M., Schu P., Pohlmann R., Dennes A., Petersen C.M. Sorting by the cytoplasmic domain of the amyloid precursor protein binding receptor SorLA. Mol. Cell. Biol. 2007, 27:6842-6851.
22. Okamoto K., Shaw J.M. Mitochondrial morphology and dynamics in yeast and multicellular eukaryotes. Annu. Rev. Genet. 2005, 39:503-536.
23. Pham A.H., Meng S., Chu Q.N., Chan D.C. Loss of Mfn2 results in progressive, retrograde degeneration of dopaminergic neurons in the nigrostriatal circuit. Hum. Mol. Genet. 2012, 21:4817-4826.
24. Pickrell A.M., Youle R.J. The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson's disease. Neuron 2015, 85:257-273.
25. Savitt J.M., Dawson V.L., Dawson T.M. Diagnosis and treatment of Parkinson disease: molecules to medicine. J. Clin. Invest. 2006, 116:1744-1754.
26. Seaman M.N. Cargo-selective endosomal sorting for retrieval to the Golgi requires retromer. J. Cell Biol. 2004, 165:111-122.
27. Seaman M.N. The retromer complex - endosomal protein recycling and beyond. J. Cell Sci. 2012, 125:4693-4702.
28. Small S.A., Petsko G.A. Retromer in Alzheimer disease, Parkinson disease and other neurological disorders. Nat. Rev. Neurosci. 2015, 16:126-132.
29. Small S.A., Kent K., Pierce A., Leung C., Kang M.S., Okada H., Honig L., Vonsattel J.P., Kim T.W. Model-guided microarray implicates the retromer complex in Alzheimer's disease. Ann. Neurol. 2005, 58:909-919.
30. Tabuchi M., Yanatori I., Kawai Y., Kishi F. Retromer-mediated direct sorting is required for proper endosomal recycling of the mammalian iron transporter DMT1. J. Cell Sci. 2010, 123:756-766.
31. Tanaka A., Cleland M.M., Xu S., Narendra D.P., Suen D.F., Karbowski M., Youle R.J. Proteasome and p97 mediate mitophagy and degradation of mitofusins induced by Parkin. J. Cell Biol. 2010, 191:1367-1380.
32. Tang F.L., Erion J.R., Tian Y., Liu W., Yin D.M., Ye J., Tang B., Mei L., Xiong W.C. VPS35 in dopamine neurons is required for endosome-to-Golgi retrieval of Lamp2a, a receptor of chaperone-mediated autophagy that is critical for α-synuclein degradation and prevention of pathogenesis of Parkinson's disease. J. Neurosci. 2015, 35:10613-10628.
33. Vilariño-Güell C., Wider C., Ross O.A., Dachsel J.C., Kachergus J.M., Lincoln S.J., Soto-Ortolaza A.I., Cobb S.A., Wilhoite G.J., Bacon J.A., et al. VPS35 mutations in Parkinson disease. Am. J. Hum. Genet. 2011, 89:162-167.
34. von Coelln R., Thomas B., Andrabi S.A., Lim K.L., Savitt J.M., Saffary R., Stirling W., Bruno K., Hess E.J., Lee M.K., et al. Inclusion body formation and neurodegeneration are parkin independent in a mouse model of alpha-synucleinopathy. J. Neurosci. 2006, 26:3685-3696.
35. Wang C.L., Tang F.L., Peng Y., Shen C.Y., Mei L., Xiong W.C. VPS35 regulates developing mouse hippocampal neuronal morphogenesis by promoting retrograde trafficking of BACE1. Biol. Open 2012, 1:1248-1257.
36. Wen L., Tang F.L., Hong Y., Luo S.W., Wang C.L., He W., Shen C., Jung J.U., Xiong F., Lee D.H., et al. VPS35 haploinsufficiency increases Alzheimer's disease neuropathology. J. Cell Biol. 2011, 195:765-779.
37. Westermann B. Mitochondrial fusion and fission in cell life and death. Nat. Rev. Mol. Cell Biol. 2010, 11:872-884.
38. Westermann B. Bioenergetic role of mitochondrial fusion and fission. Biochim. Biophys. Acta 2012, 1817:1833-1838.
39. Yin D.M., Chen Y.J., Lu Y.S., Bean J.C., Sathyamurthy A., Shen C., Liu X., Lin T.W., Smith C.A., Xiong W.C., Mei L. Reversal of behavioral deficits and synaptic dysfunction in mice overexpressing neuregulin 1. Neuron 2013, 78:644-657.
40. Zhu X.J., Wang C.Z., Dai P.G., Xie Y., Song N.N., Liu Y., Du Q.S., Mei L., Ding Y.Q., Xiong W.C. Myosin X regulates netrin receptors and functions in axonal path-finding. Nat. Cell Biol. 2007, 9:184-192.
41. Zhuang X., Masson J., Gingrich J.A., Rayport S., Hen R. Targeted gene expression in dopamine and serotonin neurons of the mouse brain. J. Neurosci. Methods 2005, 143:27-32.
42. Zimprich A., Benet-Pagès A., Struhal W., Graf E., Eck S.H., Offman M.N., Haubenberger D., Spielberger S., Schulte E.C., Lichtner P., et al. A mutation in VPS35, encoding a subunit of the retromer complex, causes late-onset Parkinson disease. Am. J. Hum. Genet. 2011, 89:168-175.
43. Züchner S., Mersiyanova I.V., Muglia M., Bissar-Tadmouri N., Rochelle J., Dadali E.L., Zappia M., Nelis E., Patitucci A., Senderek J., et al. Mutations in the mitochondrial GTPase mitofusin 2 cause Charcot-Marie-Tooth neuropathy type 2A. Nat. Genet. 2004, 36:449-451.