Transcriptome profiling following neuronal and glial expression of ALS-linked SOD1 in drosophila

G3: Genes, Genomes, Genetics

Volumn 3, Issue 4, 2013, Pages 695-708

  Kumimoto, Emily L ^a   Fore, Taylor R ^a   Zhang, Bing ^a,b  

^a UNIVERSITY OF OKLAHOMA   (United States)

^b UNIVERSITY OF MISSOURI   (United States)

Author keywords

ALS; Drosophila; Glia; Motoneuron; SOD1

Indexed keywords

HYDROGEN PEROXIDE; TRANSCRIPTOME;

ADULT; ALLELE; AMYOTROPHIC LATERAL SCLEROSIS; AMYOTROPHIC LATERAL SCLEROSIS LINKED SOD1 GENE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DROSOPHILA; G85R GENE; GENE; GENE EXPRESSION; GLIA; LIFESPAN; LIPID PEROXIDATION; MALE; MICROARRAY ANALYSIS; MOTONEURON; MOTOR PERFORMANCE; MUTANT; NONHUMAN; OXIDATIVE STRESS; SYNAPTIC TRANSMISSION; WILD TYPE;

DROSOPHILA MELANOGASTER;

EID: 84883247818     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.113.005850     Document Type: Article

References (127)

1. Afifi, A. K., F. P. Aleu, J. Goodgold, and B. Mackay, 1966 Ultrastructure of atrophic muscle in amyotrophic lateral sclerosis. Neurology 16: 475-481.
2. Alexianu, M. E., M. Kozovska, and S. H. Appel, 2001 Immune reactivity in a mouse model of familial ALS correlates with disease progression. Neurology 57: 1282-1289.
3. Barrett, T., D. B. Troup, S. E. Wilhite, P. Ledoux, C. Evangelista et al., 2011 NCBI GEO: archive for functional genomics data sets-10 years on. Nucleic Acids Res. 39: D1005-D1010.
4. Bier, E., L. Y. Jan, and Y. N. Jan, 1990 rhomboid, a gene required for dorsoventral axis establishment and peripheral nervous system development in Drosophila melanogaster. Genes Dev. 4: 190-203.
5. Boillee, S., C. Vande Velde, and D. W. Cleveland, 2006a ALS: a disease of motor neurons and their nonneuronal neighbors. Neuron 52: 39-59.
6. Boillee, S., K. Yamanaka, C. S. Lobsiger, N. G. Copeland, N. A. Jenkins et al., 2006b Onset and progression in inherited ALS determined by motor neurons and microglia. Science 312: 1389-1392.
7. Brand, A. H., and N. Perrimon, 1993 Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
8. Brockington, A., P. R. Heath, H. Holden, P. Kasher, F. L. Bender et al., 2010 Downregulation of genes with a function in axon outgrowth and synapse formation in motor neurones of the VEGFdelta/delta mouse model of amyotrophic lateral sclerosis. BMC Genomics 11: 203.
9. Brooks, K. J., M. D. Hill, P. D. Hockings, and D. G. Reid, 2004 MRI detects early hindlimb muscle atrophy in Gly93Ala superoxide dismutase-1 (G93A SOD1) transgenic mice, an animal model of familial amyotrophic lateral sclerosis. NMR Biomed. 17: 28-32.
10. Bruijn, L. I., M. W. Becher, M. K. Lee, K. L. Anderson, N. A. Jenkins et al., 1997 ALS-linked SOD1 mutant G85R mediates damage to astrocytes and promotes rapidly progressive disease with SOD1-containing inclusions. Neuron 18: 327-338.
11. Bruijn, L. I., T. M. Miller, and D. W. Cleveland, 2004 Unraveling the mechanisms involved in motor neuron degeneration in ALS. Annu. Rev. Neurosci. 27: 723-749.
12. Calabrese, V., C. Cornelius, S. Cuzzocrea, I. Iavicoli, E. Rizzarelli et al., 2011 Hormesis, cellular stress response and vitagenes as critical determinants in aging and longevity. Mol. Aspects Med. 32: 279-304.
13. Carri, M. T., A. Ferri, M. Cozzolino, L. Calabrese, and G. Rotilio, 2003 Neurodegeneration in amyotrophic lateral sclerosis: the role of oxidative stress and altered homeostasis of metals. Brain Res. Bull. 61: 365-374.
14. Chen, H., Y. Guo, M. Hu, W. Duan, G. Chang et al., 2010 Differential expression and alternative splicing of genes in lumbar spinal cord of an amyotrophic lateral sclerosis mouse model. Brain Res. 1340: 52-69.
15. Chiu, A. Y., P. Zhai, M. C. Dal Canto, T. M. Peters, Y. W. Kwon et al., 1995 Age-dependent penetrance of disease in a transgenic mouse model of familial amyotrophic lateral sclerosis. Mol. Cell. Neurosci. 6: 349-362.
16. Chiu, I. M., H. Phatnani, M. Kuligowski, J. C. Tapia, M. A. Carrasco et al., 2009 Activation of innate and humoral immunity in the peripheral nervous system of ALS transgenic mice. Proc. Natl. Acad. Sci. U S A 106: 20960-20965.
17. Cox, L. E., L. Ferraiuolo, E. F. Goodall, P. R. Heath, A. Higginbottom et al., 2010 Mutations in CHMP2B in lower motor neuron predominant amyotrophic lateral sclerosis (ALS). PLoS ONE 5: e9872.
18. Craigon, D. J., N. James, J. Okyere, J. Higgins, J. Jotham et al., 2004 NASCArrays: a repository for microarray data generated by NASC's transcriptomics service. Nucleic Acids Res. 32: D575-D577.
19. Dal Canto, M. C., and M. E. Gurney, 1994 Development of central nervous system pathology in a murine transgenic model of human amyotrophic lateral sclerosis. Am. J. Pathol. 145: 1271-1279.
20. D'arrigo, A., D. Colavito, E. Pena-Altamira, M. Fabris, M. Dam et al., 2010 Transcriptional profiling in the lumbar spinal cord of a mouse model of amyotrophic lateral sclerosis: a role for wild-type superoxide dismutase 1 in sporadic disease? J. Mol. Neurosci. 41: 404-415.
21. Deng, H. X., Y. Shi, Y. Furukawa, H. Zhai, R. G. Fu et al., 2006 Conversion to the amyotrophic lateral sclerosis phenotype is associated with intermolecular linked insoluble aggregates of SOD1 in mitochondria. Proc. Natl. Acad. Sci. U S A 103: 7142-7147.
22. Dennis, G., B. T. Sherman, D. A. Hosack, J. Yang, W. Gao et al., 2003 DAVID: Database for annotation, visualization, and integrated discovery. Genome Biol. 4(5): P3.
23. Desai, C. J., J. G. Gindhart Jr, L. S. Goldstein, and K. Zinn, 1996 Receptor tyrosine phosphatases are required for motor axon guidance in the Drosophila embryo. Cell 84: 599-609.
24. Diaz-Arrastia, R., 2000 Homocysteine and neurologic disease. Arch. Neurol. 57: 1422-1427.
25. Elia, A. J., T. L. Parkes, K. Kirby, P. St George-Hyslop, G. L. Boulianne et al., 1999 Expression of human FALS SOD in motorneurons of Drosophila. Free Radic. Biol. Med. 26: 1332-1338.
26. Feany, M. B., and W. W. Bender, 2000 A Drosophila model of Parkinson's disease. Nature 404: 394-398.
27. Feng, Z., H. Liu, J. Lang, Y. Li, M. Shu et al., 2009 SK66-his, a novel glycinerich peptide derived from Drosophila with antibacterial activity. Biosci. Biotechnol. Biochem. 73: 769-771.
28. Ferraiuolo, L., A. Higginbottom, P. R. Heath, S. Barber, D. Greenald et al., 2011 Dysregulation of astrocyte-motoneuron cross-talk in mutant superoxide dismutase 1-related amyotrophic lateral sclerosis. Brain 134: 2627-2641.
29. Ferraiuolo, L., P. R. Heath, H. Holden, P. Kasher, J. Kirby et al., 2007 Microarray analysis of the cellular pathways involved in the adaptation to and progression of motor neuron injury in the SOD1 G93A mouse model of familial ALS. J. Neurosci. 27: 9201-9219.
30. Finelli, A., A. Kelkar, H. J. Song, H. Yang, and M. Konsolaki, 2004 A model for studying Alzheimer's Abeta42-induced toxicity in Drosophila melanogaster. Mol. Cell. Neurosci. 26: 365-375.
31. Fischer, L. R., D. G. Culver, P. Tennant, A. A. Davis, M. Wang et al., 2004 Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp. Neurol. 185: 232-240.
32. Frey, D., C. Schneider, L. Xu, J. Borg, W. Spooren et al., 2000 Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motoneuron diseases. J. Neurosci. 20: 2534-2542.
33. Gao, F. B., J. E. Brenman, L. Y. Jan, and Y. N. Jan, 1999 Genes regulating dendritic outgrowth, branching, and routing in Drosophila. Genes Dev. 13: 2549-2561.
34. Goldstein, A. Y., Y. N. Jan, and L. Luo, 2005 Function and regulation of Tumbleweed (RacGAP50C) in neuroblast proliferation and neuronal morphogenesis. Proc. Natl. Acad. Sci. U S A 102: 3834-3839.
35. Gong, Y. H., A. S. Parsadanian, A. Andreeva, W. D. Snider, and J. L. Elliott, 2000 Restricted expression of G86R Cu/Zn superoxide dismutase in astrocytes results in astrocytosis but does not cause motoneuron degeneration. J. Neurosci. 20: 660-665.
36. Gonzalez De Aguilar, J. L., C. Niederhauser-Wiederkehr, B. Halter, M. De Tapia, F. Di Scala et al., 2008 Gene profiling of skeletal muscle in an amyotrophic lateral sclerosis mouse model. Physiol. Genomics 32: 207-218.
37. Greene, J. C., A. J. Whitworth, I. Kuo, L. A. Andrews, M. B. Feany et al., 2003 Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc. Natl. Acad. Sci. U S A 100: 4078-4083.
38. Greeve, I., D. Kretzschmar, J. A. Tschape, A. Beyn, C. Brellinger et al., 2004 Age-dependent neurodegeneration and Alzheimer-amyloid plaque formation in transgenic Drosophila. J. Neurosci. 24: 3899-3906.
39. Gurney, M. E., H. Pu, A. Y. Chiu, M. C. Dal Canto, C. Y. Polchow et al., 1994 Motor neuron degeneration in mice that express a human Cu,Zn superoxide dismutase mutation. Science 264: 1772-1775.
40. Hall, E. D., J. A. Oostveen, and M. E. Gurney, 1998 Relationship of microglial and astrocytic activation to disease onset and progression in a transgenic model of familial ALS. Glia 23: 249-256.
41. Halter, D. A., J. Urban, C. Rickert, S. S. Ner, K. Ito et al., 1995 The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121: 317-332.
42. Hercus, M. J., V. Loeschcke, and S. I. Rattan, 2003 Lifespan extension of Drosophila melanogaster through hormesis by repeated mild heat stress. Biogerontology 4: 149-156.
43. Higgins, C. M. J., C. W. Jung, H. L. Ding, and Z. S. Xu, 2002 Mutant Cu, Zn superoxide dismutase that causes motoneuron degeneration is present in mitochondria in the CNS. J. Neurosci. 22(6): RC215.
44. Higgins, C. M. J., C. W. Jung, and Z. S. Xu, 2003 ALS-associated mutant SOD1G93A causes mitochondrial vacuolation by expansion of the intermembrane space and by involvement of SOD1 aggregation and peroxisomes. BMC Neurosci. 4: 16.
45. Hirano, A., H. Donnenfeld, S. Sasaki, and I. Nakano, 1984a Fine structural observations of neurofilamentous changes in amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 43: 461-470.
46. Hirano, A., I. Nakano, L. T. Kurland, D. W. Mulder, P. W. Holley et al., 1984b Fine structural study of neurofibrillary changes in a family with amyotrophic lateral sclerosis. J. Neuropathol. Exp. Neurol. 43: 471-480.
47. Huang, D. W., B. T. Sherman, and R. A. Lempicki, 2009 Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4: 44-57.
48. Iijima, K., H. P. Liu, A. S. Chiang, S. A. Hearn, M. Konsolaki et al., 2004 Dissecting the pathological effects of human Abeta40 and Abeta42 in Drosophila: a potential model for Alzheimer's disease. Proc. Natl. Acad. Sci. U S A 101: 6623-6628.
49. Irizarry, R. A., B. M. Bolstad, F. Collin, L. M. Cope, B. Hobbs et al., 2003 Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31: e15.
50. Islam, R., E. L. Kumimoto, H. Bao, and B. Zhang, 2012 ALS-linked SOD1 in glial cells enhances b-N-methylamino L-alanine (BMAA)-induced toxicity in Drosophila. F1000Research 1: 47.
51. Jackson, G. R., I. Salecker, X. Dong, X. Yao, N. Arnheim et al., 1998 Polyglutamine-expanded human huntingtin transgenes induce degeneration of Drosophila photoreceptor neurons. Neuron 21: 633-642.
52. Jiang, Y. M., M. Yamamoto, Y. Kobayashi, T. Yoshihara, Y. Liang et al., 2005 Gene expression profile of spinal motor neurons in sporadic amyotrophic lateral sclerosis. Ann. Neurol. 57: 236-251.
53. Johnston, J. A., M. J. Dalton, M. E. Gurney, and R. R. Kopito, 2000 Formation of high molecular weight complexes of mutant Cu, Znsuperoxide dismutase in a mouse model for familial amyotrophic lateral sclerosis. Proc. Natl. Acad. Sci. U S A 97: 12571-12576.
54. Jones, W. M., and A. Bejsovec, 2005 RacGap50C negatively regulates wingless pathway activity during Drosophila embryonic development. Genetics 169: 2075-2086.
55. Jones, W. M., A. T. Chao, M. Zavortink, R. Saint, and A. Bejsovec, 2010 Cytokinesis proteins Tum and Pav have a nuclear role in Wnt regulation. J. Cell Sci. 123: 2179-2189.
56. Kanehisa, M., and S. Goto, 2000 KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28: 27-30.
57. Kanehisa, M., S. Goto, Y. Sato, M. Furumichi, and M. Tanabe, 2012 KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40: D109-D114.
58. Kennel, P. F., F. Finiels, F. Revah, and J. Mallet, 1996 Neuromuscular function impairment is not caused by motor neurone loss in FALS mice: an electromyographic study. Neuroreport 7: 1427-1431.
59. Kirby, J., E. Halligan, M. J. Baptista, S. Allen, P. R. Heath et al., 2005 Mutant SOD1 alters the motor neuronal transcriptome: implications for familial ALS. Brain 128: 1686-1706.
60. Kohen, R., and A. Nyska, 2002 Oxidation of biological systems: oxidative stress phenomena, antioxidants, redox reactions, and methods for their quantification. Toxicol. Pathol. 30: 620-650.
61. Kong, J. M., and Z. S. Xu, 1998 Massive mitochondrial degeneration in motor neurons triggers the onset of amyotrophic lateral sclerosis in mice expressing a mutant SOD1. J. Neurosci. 18: 3241-3250.
62. Kretzschmar, D., J. Tschape, A. Bettencourt Da Cruz, E. Asan, B. Poeck et al., 2005 Glial and neuronal expression of polyglutamine proteins induce behavioral changes and aggregate formation in Drosophila. Glia 49: 59- 72.
63. Kudo, L. C., L. Parfenova, N. Vi, K. Lau, J. Pomakian et al., 2010 Integrative gene-tissue microarray-based approach for identification of human disease biomarkers: application to amyotrophic lateral sclerosis. Hum. Mol. Genet. 19: 3233-3253.
64. Le Bourg, E., 2007 Hormetic effects on longevity of hydrogen peroxide in Drosophila melanogaster flies living on a poorly nutritious medium. Biogerontology 8: 327-344.
65. Le Bourg, E., and N. Minois, 1997 Increased longevity and resistance to heat shock in Drosophila melanogaster flies exposed to hypergravity. C. R. Acad. Sci. III 320: 215-221.
66. Le Bourg, E., P. Valenti, P. Lucchetta, and F. Payre, 2001 Effects of mild heat shocks at young age on aging and longevity in Drosophila melanogaster. Biogerontology 2: 155-164.
67. Lee, T., and L. Luo, 1999 Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451- 461.
68. Lee, W. C., M. Yoshihara, and J. T. Littleton, 2004 Cytoplasmic aggregates trap polyglutamine-containing proteins and block axonal transport in a Drosophila model of Huntington's disease. Proc. Natl. Acad. Sci. U S A 101: 3224-3229.
69. Lino, M. M., C. Schneider, and P. Caroni, 2002 Accumulation of SOD1 mutants in postnatal motoneurons does not cause motoneuron pathology or motoneuron disease. J. Neurosci. 22: 4825-4832.
70. Liu, J., C. Lillo, P. A. Jonsson, C. V. Velde, C. M. Ward et al., 2004 Toxicity of familial ALS-linked SOD1 mutants from selective recruitment to spinal mitochondria. Neuron 43: 5-17.
71. Livak, K. J., and T. D. Schmittgen, 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C[T]). Method. Methods 25: 402-408.
72. Lobsiger, C. S., S. Boillee, M. Mcalonis-Downes, A. M. Khan, M. L. Feltri et al., 2009 Schwann cells expressing dismutase active mutant SOD1 unexpectedly slow disease progression in ALS mice. Proc. Natl. Acad. Sci. U S A 106: 4465-4470.
73. Lohse, M., A. Nunes-Nesi, P. Kruger, A. Nagel, J. Hannemann et al., 2010 Robin: an intuitive wizard application for R-based expression microarray quality assessment and analysis. Plant Physiol. 153: 642-651.
74. Marcuzzo, S., I. Zucca, A. Mastropietro, N. K. De Rosbo, P. Cavalcante et al., 2011 Hind limb muscle atrophy precedes cerebral neuronal degeneration in G93A-SOD1 mouse model of amyotrophic lateral sclerosis: a longitudinal MRI study. Exp. Neurol. 231: 30-37.
75. Marley, R., and R. A. Baines, 2011 Increased persistent Na+ current contributes to seizure in the slamdance bang-sensitive Drosophila mutant. J. Neurophysiol. 106: 18-29.
76. Mcgeer, P. L., and E. G. Mcgeer, 2002 Inflammatory processes in amyotrophic lateral sclerosis. Muscle Nerve 26: 459-470.
77. Michel, C. I., R. Kraft, and L. L. Restifo, 2004 Defective neuronal development in the mushroom bodies of Drosophila fragile X mental retardation 1 mutants. J. Neurosci. 24: 5798-5809.
78. Miguel, L., T. Frebourg, D. Campion, and M. Lecourtois, 2011 Both cytoplasmic and nuclear accumulations of the protein are neurotoxic in Drosophila models of TDP-43 proteinopathies. Neurobiol. Dis. 41: 398-406.
79. Min, K. T., and S. Benzer, 1999 Preventing neurodegeneration in the Drosophila mutant bubblegum. Science 284: 1985-1988.
80. Mitchell, J. D., 2000 Amyotrophic lateral sclerosis: toxins and environment. Amyotroph. Lateral Scler. Other Motor Neuron Disord. 1: 235-250.
81. Mockett, R. J., S. N. Radyuk, J. J. Benes, W. C. Orr, and R. S. Sohal, 2003 Phenotypic effects of familial amyotrophic lateral sclerosis mutant Sod alleles in transgenic Drosophila. Proc. Natl. Acad. Sci. U S A 100: 301-306.
82. Morales, J., P. R. Hiesinger, A. J. Schroeder, K. Kume, P. Verstreken et al., 2002 Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron 34: 961-972.
83. Noordermeer, J. N., C. C. Kopczynski, R. D. Fetter, K. S. Bland, W. Y. Chen et al., 1998 Wrapper, a novel member of the Ig superfamily, is expressed by midline glia and is required for them to ensheath commissural axons in Drosophila. Neuron 21: 991-1001.
84. O'brien, K. P., M. Remm, and E. L. Sonnhammer, 2005 Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res. 33: D476-D480.
85. Pandey, U. B., and C. D. Nichols, 2011 Human disease models in Drosophila melanogaster and the role of the fly in therapeutic drug discovery. Pharmacol. Rev. 63: 411-436.
86. Papadimitriou, D., V. Le Verche, A. Jacquier, B. Ikiz, S. Przedborski et al., 2010 Inflammation in ALS and SMA: sorting out the good from the evil. Neurobiol. Dis. 37: 493-502.
87. Parkes, T. L., A. J. Elia, D. Dickinson, A. J. Hilliker, J. P. Phillips et al., 1998 Extension of Drosophila lifespan by overexpression of human SOD1 in motorneurons. Nat. Genet. 19: 171-174.
88. Pavlidis, P., and M. A. Tanouye, 1995 Seizures and failures in the giant fiber pathway of Drosophila bang-sensitive paralytic mutants. J. Neurosci. 15: 5810-5819.
89. Puttaparthi, K., C. Wojcik, B. Rajendran, G. N. Demartino, and J. L. Elliott, 2003 Aggregate formation in the spinal cord of mutant SOD1 transgenic mice is reversible and mediated by proteasomes. J. Neurochem. 87: 851-860.
90. Ravi, D., A. M. Wiles, S. Bhavani, J. Ruan, P. Leder et al., 2009 A network of conserved damage survival pathways revealed by a genomic RNAi screen. PLoS Genet. 5: e1000527.
91. Robinow, S., and K. White, 1991 Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 22: 443-461.
92. Rodrigues, M. C., D. G. Hernandez-Ontiveros, M. K. Louis, A. E. Willing, C. V. Borlongan et al., 2012 Neurovascular aspects of amyotrophic lateral sclerosis. Int. Rev. Neurobiol. 102: 91-106.
93. Rosen, D. R., 1993 Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 364: 362.
94. Rozen, S., and H. Skaletsky, 2000 Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132: 365-386.
95. Salzberg, A., D. D'evelyn, K. L. Schulze, J. K. Lee, D. Strumpf et al., 1994 Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development. Neuron 13: 269-287.
96. Satterfield, T. F., S. M. Jackson, and L. J. Pallanck, 2002 A Drosophila homolog of the polyglutamine disease gene SCA2 is a dosage-sensitive regulator of actin filament formation. Genetics 162: 1687-1702.
97. Schenck, A., B. Bardoni, C. Langmann, N. Harden, J. L. Mandel et al., 2003 CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38: 887-898.
98. Schindelin, J., I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair et al., 2012 Fiji: an open-source platform for biological-image analysis. Nat. Methods 9: 676-682.
99. Seegmiller, A. C., I. Dobrosotskaya, J. L. Goldstein, Y. K. Ho, M. S. Brown et al., 2002 The SREBP pathway in Drosophila: regulation by palmitate, not sterols. Dev. Cell 2: 229-238.
100. Sepp, K. J., and V. J. Auld, 2003 Reciprocal interactions between neurons and glia are required for Drosophila peripheral nervous system development. J. Neurosci. 23: 8221-8230.
101. Sherwood, N. T., Q. Sun, M. Xue, B. Zhang, and K. Zinn, 2004 Drosophila spastin regulates synaptic microtubule networks and is required for normal motor function. PLoS Biol. 2: e429.
102. Shibata, N., A. Hirano, M. Kobayashi, T. Siddique, H. X. Deng et al., 1996 Intense superoxide dismutase-1 immunoreactivity in intracytoplasmic hyaline inclusions of familial amyotrophic lateral sclerosis with posterior column involvement. J. Neuropathol. Exp. Neurol. 55: 481-490.
103. Smyth, G. K., 2004 Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3: Article3.
104. Somers, W. G., and R. Saint, 2003 A RhoGEF and Rho family GTPaseactivating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis. Dev. Cell 4: 29-39.
105. Tauber, J. M., P. A. Vanlandingham, and B. Zhang, 2011 Elevated levels of the vesicular monoamine transporter and a novel repetitive behavior in the Drosophila model of fragile X syndrome. PLoS ONE 6: e27100.
106. Thimgan, M. S., J. S. Berg, and A. E. Stuart, 2006 Comparative sequence analysis and tissue localization of members of the SLC6 family of transporters in adult Drosophila melanogaster. J. Exp. Biol. 209: 3383-3404.
107. Trotta, N., G. Orso, M. G. Rossetto, A. Daga, and K. Broadie, 2004 The hereditary spastic paraplegia gene, spastin, regulates microtubule stability to modulate synaptic structure and function. Curr. Biol. 14: 1135-1147.
108. Tweedie, S., M. Ashburner, K. Falls, P. Leyland, P. Mcquilton et al., 2009 FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res. 37: D555-D559.
109. Urban, S., J. R. Lee, and M. Freeman, 2001 Drosophila rhomboid-1 defines a family of putative intramembrane serine proteases. Cell 107: 173-182.
110. Vargas, M. R., M. Pehar, P. J. Diaz-Amarilla, J. S. Beckman, and L. Barbeito, 2008 Transcriptional profile of primary astrocytes expressing ALSlinked mutant SOD1. J. Neurosci. Res. 86: 3515-3525.
111. Vijayvergiya, C., M. F. Beal, J. Buck, and G. Manfredi, 2005 Mutant superoxide dismutase 1 forms aggregates in the brain mitochondrial matrix of amyotrophic lateral sclerosis mice. J. Neurosci. 25: 2463-2470.
112. Warrick, J. M., H. L. Paulson, G. L. Gray-Board, Q. T. Bui, K. H. Fischbeck et al., 1998 Expanded polyglutamine protein forms nuclear inclusions and causes neural degeneration in Drosophila. Cell 93: 939-949.
113. Watanabe, M., M. Dykes-Hoberg, V. C. Culotta, D. L. Price, P. C. Wong et al., 2001 Histological evidence of protein aggregation in mutant SOD1 transgenic mice and in amyotrophic lateral sclerosis neural tissues. Neurobiol. Dis. 8: 933-941.
114. Watson, M. R., R. D. Lagow, K. Xu, B. Zhang, and N. M. Bonini, 2008 A Drosophila model for amyotrophic lateral sclerosis reveals motor neuron damage by human SOD1. J. Biol. Chem. 283: 24972-24981.
115. Wheeler, S. R., S. Banerjee, K. Blauth, S. L. Rogers, M. A. Bhat et al., 2009 Neurexin IV and Wrapper interactions mediate Drosophila midline glial migration and axonal ensheathment. Development 136: 1147-1157.
116. Wong, P. C., C. A. Pardo, D. R. Borchelt, M. K. Lee, N. G. Copeland et al., 1995 An adverse property of a familial ALS-linked SOD1 mutation causes motor neuron disease characterized by vacuolar degeneration of mitochondria. Neuron 14: 1105-1116.
117. Xiong, W. C., H. Okano, N. H. Patel, J. A. Blendy, and C. Montell, 1994 repo encodes a glial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 8: 981-994.
118. Xu, K., B. A. Bogert, W. Li, K. Su, A. Lee et al., 2004 The fragile X-related gene affects the crawling behavior of Drosophila larvae by regulating the mRNA level of the DEG/ENaC protein pickpocket1. Curr. Biol. 14: 1025- 1034.
119. Yang, W., and S. Hekimi, 2010 A mitochondrial superoxide signal triggers increased longevity in Caenorhabditis elegans. PLoS Biol. 8: e1000556.
120. Yang, Y., I. Nishimura, Y. Imai, R. Takahashi, and B. Lu, 2003 Parkin suppresses dopaminergic neuron-selective neurotoxicity induced by Pael- R in Drosophila. Neuron 37: 911-924.
121. Yang, Y., S. Gehrke, Y. Imai, Z. Huang, Y. Ouyang et al., 2006 Mitochondrial pathology and muscle and dopaminergic neuron degeneration caused by inactivation of Drosophila Pink1 is rescued by Parkin. Proc. Natl. Acad. Sci. U S A 103: 10793-10798.
122. Yeh, E., K. Gustafson, and G. L. Boulianne, 1995 Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila. Proc. Natl. Acad. Sci. U S A 92: 7036-7040.
123. Yoshihara, T., S. Ishigaki, M. Yamamoto, Y. Liang, J. Niwa et al., 2002 Differential expression of inflammation- and apoptosis-related genes in spinal cords of a mutant SOD1 transgenic mouse model of familial amyotrophic lateral sclerosis. J. Neurochem. 80: 158-167.
124. Zhang, H., J. Tan, E. Reynolds, D. Kuebler, S. Faulhaber et al., 2002 The Drosophila slamdance gene: a mutation in an aminopeptidase can cause seizure, paralysis and neuronal failure. Genetics 162: 1283-1299.
125. Zhang, X., S. Chen, L. Li, Q. Wang, and W. Le, 2010 Decreased level of 5-methyltetrahydrofolate: a potential biomarker for pre-symptomatic amyotrophic lateral sclerosis. J. Neurol. Sci. 293: 102-105.
126. Zhang, Y. Q., A. M. Bailey, H. J. Matthies, R. B. Renden, M. A. Smith et al., 2001 Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107: 591-603.
127. Zoccolella, S., I. L. Simone, P. Lamberti, V. Samarelli, R. Tortelli et al., 2008 Elevated plasma homocysteine levels in patients with amyotrophic lateral sclerosis. Neurology 70: 222-225.