Neurobiology of Aging
Volume 29, Issue 1 , Pages 84-94 , January 2008

Loss of spastic paraplegia gene atlastin induces age-dependent death of dopaminergic neurons in Drosophila

  • Youngseok Lee

      Affiliations

    • Department of Biological Sciences, Korea Advanced Institute of Science & Technology, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea
    • GenExel-Sein Inc., KAIST, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea
    • These authors contributed equally to this work.
    • ,
  • Donggi Paik

      Affiliations

    • Department of Biological Sciences, Korea Advanced Institute of Science & Technology, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea
    • These authors contributed equally to this work.
    • ,
  • Sunhoe Bang

      Affiliations

    • Department of Biological Sciences, Korea Advanced Institute of Science & Technology, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea
    • ,
  • Jongkyun Kang

      Affiliations

    • Department of Biological Sciences, Korea Advanced Institute of Science & Technology, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea
    • ,
  • Bumkoo Chun

      Affiliations

    • Department of Biological Sciences, Korea Advanced Institute of Science & Technology, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea
    • ,
  • Seungbok Lee

      Affiliations

    • Department of Cell and Developmental Biology, Dental Research Institute, School of Dentistry, Seoul National University, Seoul 110-740, Republic of Korea
    • ,
  • Eunkyung Bae

      Affiliations

    • GenExel-Sein Inc., KAIST, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea
    • ,
  • Jongkyung Chung

      Affiliations

    • Department of Biological Sciences, Korea Advanced Institute of Science & Technology, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea
    • ,
  • Jaeseob Kim

      Affiliations

    • Department of Biological Sciences, Korea Advanced Institute of Science & Technology, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea
    • GenExel-Sein Inc., KAIST, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea
    • Corresponding Author InformationCorresponding author at: Department of Biological Sciences, Korea Advanced Institute of Science & Technology, 373-1 Guseong-Dong, Yuseong-Gu, Daejeon 305-701, Republic of Korea. Tel.: +82 42 869 2632.

Received 7 June 2006 ,Revised 28 August 2006 ,Accepted 6 September 2006.

References 

  1. Abel A, Fonknechten N, Hofer A, Durr A, Cruadu C, Voit T, et al. Early onset autosomal dominant spastic paraplegia caused by novel mutations in SPG3A. Neurogenetics. 2004;5:239–243
  2. Benzer S. From the gene to behavior. JAMA. 1971;218:1015–1022
  3. Casari G, De Fusco M, Ciarmatori S, Zeviani M, Mora M, Fernandez P, et al. Spastic paraplegia and OXPHOS impairment caused by mutations in paraplegin, a nuclear-encoded mitochondrial metalloprotease. Cell. 1998;93:973–983
  4. Dalpozzo F, Rossetto MG, Boaretto F, Sartori E, Mostacciuolo ML, Daga A, et al. Infancy onset hereditary spastic paraplegia associated with a novel atlastin mutation. Neurology. 2003;61:580–581
  5. D’Amico A, Tessa A, Sabino A, Bertini E, Santorelli FM, Servidei S. Incomplete penetrance in an SPG3A-linked family with a new mutation in the atlastin gene. Neurology. 2004;62:2138–2139
  6. Friggi-Grelin F, Iche M, Birman S. Targeted gene expression in Drosophila dopaminergic cells using regulatory sequences from tyrosine hydroxylase. Genesis. 2003;35:175–184
  7. Ganetzky B, Wu CF. Indirect suppression involving behavioral mutants with altered nerve excitability in Drosophila melanogaster. Genetics. 1982;100:597–614
  8. Harding AE. Hereditary spastic paraplegias. Semin Neurol. 1993;13:333–336
  9. Hazan J, Fonknechten N, Mavel D, Paternotte C, Samson D, Artiguenave F, et al. Spastin, a new AAA protein, is altered in the most frequent form of autosomal dominant spastic paraplegia. Nat Genet. 1999;23:296–303
  10. Jones SM, Howell KE, Henley JR, Cao H, McNiven MA. Role of dynamin in the formation of transport vesicles from the trans-Golgi network. Science. 1998;279:573–577
  11. Jouet M, Rsoenthal A, Armstrong G, MacFarlane J, Stenson R, Paterson J, et al. X-linked hydrocephalus result from mutations I the L1 gene. Nat Genet. 1994;7:402–407
  12. Klebe S, Deuschl G, Stolze H. Methylphenidate fails to improve gait and muscle tone in patients with sporadic and hereditary spastic paraplegia. Mov Disord. 2006;21:1468–1471
  13. Lang AE, Lozano AM. Parkinson's disease. Second of two parts. New Engl J Med. 1998;339:1044–1053
  14. Lee Y, Lee Y, Lee J, Bang S, Hyun S, Kang J, et al. Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster. Nat Genet. 2005;37(3):305–310
  15. Li H, Chaney S, Roberts IJ, Forte M, Hirsh J. Ectopic G-protein expression in dopamine and serotonin neurons blocks cocaine sensitization in Drosophila melanogaster. Curr Biol. 2000;10:211–214
  16. Micheli F, Cersosimo MG, Ramirez CZ. Hereditary spastic paraplegia associated with dopa-responsive Parkinsonism. Mov Disord. 2006;21(5):716–717
  17. Namekawa M, Ribai P, Nelson I, Forlani S, Fellmann F, Goizet C, et al. SPG3A is the most frequent cause of hereditary spastic paraplegia with onset before age 10 years. Neurology. 2006;66:112–114
  18. Nicoziani P, Vilhardt F, Llorente A, Hilout L, Courtoy PJ, Sandvig K, et al. Role for dynamin in late endosome dynamics and trafficking of the cation-independent mannose 6-phosphate receptor. Mol Biol Cell. 2000;11:481–495
  19. Ochoa GC, Slepnev VI, Neff L, Ringstad N, Takei K, Daniell L, et al. A functional link between dynamin and the actin cytoskeleton at podosomes. J Cell Biol. 2000;150:377–389
  20. Pendleton RG, Parvez F, Sayed M, Hillman R. Effects of pharmacological agents upon a transgenic model of Parkinson's disease in Drosophila melanogaster. J Pharmacol Exp Ther. 2002;300:91–96
  21. Pitts KR, Yoon Y, Krueger EW, McNiven MA. The dynamin-like protein DLP1 is essential for normal distribution and morphology of the endoplasmic reticulum and mitochondria in mammalian cells. Mol Biol Cell. 1999;10:4403–4417
  22. Reid E. Science in motion: common molecular pathological themes emerge in the hereditary spastic paraplegias. J Med Genet. 2003;40:81–86
  23. Reid E, Kloos M, Ahley-Koch A, Hughes L, Bevan S, Svenson IK, et al. A kinesin heavy chain (KIF5A) mutation in hereditary spastic paraplegia (SPG10). Am J Hum Genet. 2002;71:1189–1194
  24. Roll-Mecak A, Vale RD. The Drosophila homologue of the hereditary spastic paraplegia protein, spastin, severs and disassembles microtubules. Curr Biol. 2005;15:650–655
  25. Sanderson CM, Connell JW, Edwards TL, Bright NA, Duley S, Thompson A, et al. Spastin and atlastin, two proteins mutated in autosomal-dominant hereditary spastic paraplegia, are binding partners. Hum Mol Genet. 2006;15(2):307–318
  26. Sauter SM, Engel W, Neumann LM, Kunze J, Neesen J. Novel mutations in the Atlastin gene (SPG3A) in families with autosomal dominant hereditary spastic paraplegia and evidence for late onset forms of HSP linked to the SPG3A locus. Hum Mutat. 2004;23:98
  27. Scarano V, Mancini P, Criscuolo C, De Michele G, Rinaldi C, Tucci T, et al. The R495W mutation in SPG3A causes spastic paraplegia associated with axonal neuropathy. J Neurol. 2005;252(8):901–903
  28. Sherwood NT, Sun Q, Xue M, Zhang B, Zinn K. Drosophila spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS. 2004;2:2094–2111
  29. Suagier-Veber P, Munnich A, Bonneau D, Rozet JM, LeMerer M, Gil R, et al. X-linked spastic paraplegia and Pelizaeus-Merzbacher disease are allelic disorders at the proteolipid protein locus. Nat Genet. 1994;6:257–262
  30. Tessa A, Casali C, Damiano M, Bruno C, Fortini D, Patrono C, et al. SPG3A: an additional family carrying a new atlastin mutation. Neurology. 2002;59:2002–2005
  31. Trotta N, Orso G, Rossetto MG, Daga A, Broadie K. The hereditary spastic paraplegia gene, spastin, regulates microtubule stability to modulate synaptic structure and function. Curr Biol. 2004;14:1135–1147
  32. Wilkinson PA, Hart PE, Patel H, Warner TT, Crosby AH. SPG3A mutation screening in English families with early onset autosomal dominant hereditary spastic paraplegia. J Neurol Sci. 2003;216:43–45
  33. Yasuyama K, Kitamoto T, Salvaterra PM. Immunocytochemical study of choline acetyltransferase in Drosophila melanogaster: an analysis of cis-regulatory regions controlling expression in the brain of cDNA-transformed flies. J Comp Neurol. 1995;361(1):25–37
  34. Zhao X, Alvarado D, Rainier S, Lemons R, Hedera P, Weber CH, et al. Mutations in a newly identified GTPase gene cause autosomal dominant hereditary spastic paraplegia. Nat Genet. 2001;29:326–331
  35. Zhu P-P, Patterson A, Lavoie B, Stadler J, Shoeb M, Paterl R, et al. Cellular localization, oligomerization, and membrane association of the hereditary spastic paraplegia 3A (SPG3A) protein atlastin. J Biol Chem. 2003;278:49063–49071
  36. Zhu P-P, Soderblom C, Tao-Cheng J-H, Stadler J, Blackstone C. SPG3A protein atlastin-1 is enriched in growth cones and promotes axon elongation during neuronal development. Hum Mol Genet. 2006;15:1343–1353

PII: S0197-4580(06)00335-6

doi: 10.1016/j.neurobiolaging.2006.09.004

Neurobiology of Aging
Volume 29, Issue 1 , Pages 84-94 , January 2008

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