Genetic circuitry of Survival motor neuron, the gene underlying spinal muscular atrophy

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 26, 2013, Pages

  Sen, Anindya ^a   Dimlich, Douglas N ^a   Guruharsha, K G ^a   Kankel, Mark W ^a   Hori, Kazuya ^a   Yokokura, Takakazu ^a,e   Brachat, Sophie ^b,c   Richardson, Delwood ^b   Loureiro, Joseph ^b   Sivasankaran, Rajeev ^b   Curtis, Daniel ^b   Davidow, Lance S ^a   Rubin, Lee L ^a   Hart, Anne C ^d   Van Vactor, David ^a   Artavanis Tsakonas, Spyros ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

^c NOVARTIS PHARMA AG   (Switzerland)

^d BROWN UNIVERSITY   (United States)

^e OKINAWA INSTITUTE OF SCIENCE AND TECHNOLOGY GRADUATE UNIVERSITY   (Japan)

Author keywords

ALS; Disease model; Neurodegeneration; Neuromuscular junction; Proteomics

Indexed keywords

SURVIVAL MOTOR NEURON PROTEIN;

ARTICLE; BIOINFORMATICS; CHEMICAL INTERACTION; CONTROLLED STUDY; DROSOPHILA; GENE IDENTIFICATION; GENE INTERACTION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SPINAL MUSCULAR ATROPHY;

ALS; DISEASE MODEL; NEURODEGENERATION; NEUROMUSCULAR JUNCTION; PROTEOMICS;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DROSOPHILA PROTEINS; GENE REGULATORY NETWORKS; GENES, INSECT; HUMANS; KNOWLEDGE BASES; NEUROMUSCULAR JUNCTION; PHENOTYPE; RNA INTERFERENCE; RNA-BINDING PROTEINS; SPECIES SPECIFICITY; SPINAL MUSCULAR ATROPHIES OF CHILDHOOD;

EID: 84879524441     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1301738110     Document Type: Article

References (65)

1. Lefebvre S, et al. (1997) Correlation between severity and SMN protein level in spinal muscular atrophy. Nat Genet 16(3):265-269.
2. Workman E, Kolb SJ, Battle DJ (2012) Spliceosomal small nuclear ribonucleoprotein biogenesis defects and motor neuron selectivity in spinal muscular atrophy. Brain Res 1462:93-99.
3. Burghes AH, Beattie CE (2009) Spinal muscular atrophy: Why do low levels of survival motor neuron protein make motor neurons sick? Nat Rev Neurosci 10(8):597-609.
4. Lefebvre S, et al. (1995) Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80(1):155-165.
5. Lorson CL, Hahnen E, Androphy EJ, Wirth B (1999) A single nucleotide in the SMN gene regulates splicing and is responsible for spinal muscular atrophy. Proc Natl Acad Sci USA 96(11):6307-6311.
6. Monani UR, et al. (1999) A single nucleotide difference that alters splicing patterns distinguishes the SMA gene SMN1 from the copy gene SMN2. Hum Mol Genet 8(7): 1177-1183.
7. Feldkötter M, Schwarzer V, Wirth R, Wienker TF, Wirth B (2002) Quantitative analyses of SMN1 and SMN2 based on real-time lightCycler PCR: Fast and highly reliable carrier testing and prediction of severity of spinal muscular atrophy. Am J Hum Genet 70(2): 358-368.
8. Schrank B, et al. (1997) Inactivation of the survival motor neuron gene, a candidate gene for human spinal muscular atrophy, leads to massive cell death in early mouse embryos. Proc Natl Acad Sci USA 94(18):9920-9925.
9. Chan YB, et al. (2003) Neuromuscular defects in a Drosophila survival motor neuron gene mutant. Hum Mol Genet 12(12):1367-1376.
10. Miguel-Aliaga I, Chan YB, Davies KE, van den Heuvel M (2000) Disruption of SMN function by ectopic expression of the human SMN gene in Drosophila. FEBS Lett 486(2):99-102.
11. Rajendra TK, et al. (2007) A Drosophila melanogaster model of spinal muscular atrophy reveals a function for SMN in striated muscle. J Cell Biol 176(6):831-841.
12. Chang HC, et al. (2008) Modeling spinal muscular atrophy in Drosophila. PLoS ONE 3(9):e3209.
13. Guruharsha KG, et al. (2011) A protein complex network of Drosophila melanogaster. Cell 147(3):690-703.
14. Artavanis-Tsakonas S (2004) Accessing the Exelixis collection. Nat Genet 36(3):207.
15. Thibault ST, et al. (2004) A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat Genet 36(3):283-287.
16. Huang W, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4(1):44-57.
17. Huang W, Sherman BT, Lempicki RA (2009) Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37(1):1-13.
18. Sen A, et al. (2011) Modeling spinal muscular atrophy in Drosophila links Smn to FGF signaling. J Cell Biol 192(3):481-495.
19. Enright AJ, Van Dongen S, Ouzounis CA (2002) An efficient algorithm for large-scale detection of protein families. Nucleic Acids Res 30(7):1575-1584.
20. Ashburner M, et al.; The Gene Ontology Consortium (2000) Gene ontology: Tool for the unification of biology. Nat Genet 25(1):25-29.
21. Sharma A, et al. (2005) A role for complexes of survival of motor neurons (SMN) protein with gemins and profilin in neurite-like cytoplasmic extensions of cultured nerve cells. Exp Cell Res 309(1):185-197.
22. Leung KM, et al. (2006) Asymmetrical beta-actin mRNA translation in growth cones mediates attractive turning to netrin-1. Nat Neurosci 9(10):1247-1256.
23. Al-Ramahi I, et al. (2007) dAtaxin-2 mediates expanded Ataxin-1-induced neurodegeneration in a Drosophila model of SCA1. PLoS Genet 3(12):e234.
24. Piazzon N, et al. (2008) In vitro and in cellulo evidences for association of the survival of motor neuron complex with the fragile X mental retardation protein. J Biol Chem 283(9):5598-5610.
25. Oprea GE, et al. (2008) Plastin 3 is a protective modifier of autosomal recessive spinal muscular atrophy. Science 320(5875):524-527.
26. Dimitriadi M, et al. (2010) Conserved genes act as modifiers of invertebrate SMN loss of function defects. PLoS Genet 6(10):e1001172.
27. Rossoll W, et al. (2003) Smn, the spinal muscular atrophy-determining gene product, modulates axon growth and localization of beta-actin mRNA in growth cones of motoneurons. J Cell Biol 163(4):801-812.
28. Zhang HL, et al. (2003) Active transport of the survival motor neuron protein and the role of exon-7 in cytoplasmic localization. J Neurosci 23(16):6627-6637.
29. Bowerman M, Beauvais A, Anderson CL, Kothary R (2010) Rho-kinase inactivation prolongs survival of an intermediate SMA mouse model. Hum Mol Genet 19(8): 1468-1478.
30. Osterloh JM, et al. (2012) dSarm/Sarm1 is required for activation of an injury-induced axon death pathway. Science 337(6093):481-484.
31. Rossoll W, et al. (2002) Specific interaction of Smn, the spinal muscular atrophy determining gene product, with hnRNP-R and gry-rbp/hnRNP-Q: A role for Smn in RNA processing in motor axons? Hum Mol Genet 11(1):93-105.
32. Hofmann Y, Lorson CL, Stamm S, Androphy EJ, Wirth B (2000) Htra2-beta 1 stimulates an exonic splicing enhancer and can restore full-length SMN expression to survival motor neuron 2 (SMN2). Proc Natl Acad Sci USA 97(17):9618-9623.
33. Gangwani L, Mikrut M, Theroux S, Sharma M, Davis RJ (2001) Spinal muscular atrophy disrupts the interaction of ZPR1 with the SMN protein. Nat Cell Biol 3(4):376-383.
34. Ahmad S, Wang Y, Shaik GM, Burghes AH, Gangwani L (2012) The zinc finger protein ZPR1 is a potential modifier of spinal muscular atrophy. Hum Mol Genet 21(12): 2745-2758.
35. Claus P, Bruns AF, Grothe C (2004) Fibroblast growth factor-2(23) binds directly to the survival of motoneuron protein and is associated with small nuclear RNAs. Biochem J 384(Pt 3):559-565.
36. Makhortova NR, et al. (2011) A screen for regulators of survival of motor neuron protein levels. Nat Chem Biol 7(8):544-552.
37. Hensel N, et al. (2012) Analysis of the fibroblast growth factor system reveals alterations in a mouse model of spinal muscular atrophy. PLoS ONE 7(2):e31202.
38. Kwon JE, Kim EK, Choi EJ (2011) Stabilization of the survival motor neuron protein by ASK1. FEBS Lett 585(9):1287-1292.
39. Yanagawa S, Lee JS, Ishimoto A (1998) Identification and characterization of a novel line of Drosophila Schneider S2 cells that respond to wingless signaling. J Biol Chem 273(48):32353-32359.
40. Yu C, et al. (2011) Development of expression-ready constructs for generation of proteomic libraries. Methods Mol Biol 723:257-272.
41. Kariya S, et al. (2012) Mutant superoxide dismutase 1 (SOD1), a cause of amyotrophic lateral sclerosis, disrupts the recruitment of SMN, the spinal muscular atrophy protein to nuclear Cajal bodies. Hum Mol Genet 21(15):3421-3434.
42. Gu W, Pan F, Zhang H, Bassell GJ, Singer RH (2002) A predominantly nuclear protein affecting cytoplasmic localization of beta-actin mRNA in fibroblasts and neurons. J Cell Biol 156(1):41-51.
43. Glinka M, et al. (2010) The heterogeneous nuclear ribonucleoprotein-R is necessary for axonal beta-actin mRNA translocation in spinal motor neurons. Hum Mol Genet 19(10):1951-1966.
44. Fallini C, et al. (2011) The survival of motor neuron (SMN) protein interacts with the mRNA-binding protein HuD and regulates localization of poly(A) mRNA in primary motor neuron axons. J Neurosci 31(10):3914-3925.
45. Menon KP, et al. (2004) The translational repressor Pumilio regulates presynaptic morphology and controls postsynaptic accumulation of translation factor eIF-4E. Neuron 44(4):663-676.
46. Aberle H, et al. (2002) wishful thinking encodes a BMP type II receptor that regulates synaptic growth in Drosophila. Neuron 33(4):545-558.
47. McCabe BD, et al. (2003) The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction. Neuron 39(2): 241-254.
48. Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O (2009) Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol 11(9):1143-1149.
49. Lee YS, et al. (2009) Silencing by small RNAs is linked to endosomal trafficking. Nat Cell Biol 11(9):1150-1156.
50. Wu F, Yao PJ (2009) Clathrin-mediated endocytosis and Alzheimer's disease: An update. Ageing Res Rev 8(3):147-149.
51. Trushina E, et al. (2006) Mutant huntingtin inhibits clathrin-independent endocytosis and causes accumulation of cholesterol in vitro and in vivo. Hum Mol Genet 15(24): 3578-3591.
52. Kong L, et al. (2009) Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J Neurosci 29(3):842-851.
53. Gauthier J, et al. (2011) Truncating mutations in NRXN2 and NRXN1 in autism spectrum disorders and schizophrenia. Hum Genet 130(4):563-573.
54. Rujescu D, et al.; GROUP Investigators (2009) Disruption of the neurexin 1 gene is associated with schizophrenia. Hum Mol Genet 18(5):988-996.
55. Koenig M, et al. (1987) Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50(3):509-517.
56. Monaco AP, et al. (1986) Isolation of candidate cDNAs for portions of the Duchenne muscular dystrophy gene. Nature 323(6089):646-650.
57. Rosen DR, et al. (1993) Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362(6415):59-62.
58. Lesnick TG, et al. (2008) Beyond Parkinson disease: Amyotrophic lateral sclerosis and the axon guidance pathway. PLoS ONE 3(1):e1449.
59. Altschul SF, et al. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25(17):3389-3402.
60. Chen F, Mackey AJ, Vermunt JK, Roos DS (2007) Assessing performance of orthology detection strategies applied to eukaryotic genomes. PLoS ONE 2(4):e383.
61. Ostlund G, et al. (2010) InParanoid 7: New algorithms and tools for eukaryotic orthology analysis. Nucleic Acids Res 38(Database issue):D196-D203.
62. Chen F, Mackey AJ, Stoeckert CJ, Jr., Roos DS (2006) OrthoMCL-DB: Querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 34(Database issue):D363-D368.
63. Sayers EW, et al. (2012) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 40(Database issue):D13-D25.
64. Li L, Stoeckert CJ, Jr., Roos DS (2003) OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Res 13(9):2178-2189.
65. Shannon P, et al. (2003) Cytoscape: A software environment for integrated models of biomolecular interaction networks. Genome Res 13(11):2498-2504.