Minor splicing pathway is not minor any more: Implications for the pathogenesis of motor neuron diseases

Neuropathology

Volumn 34, Issue 1, 2014, Pages 99-107

  Onodera, Osamu ^a   Ishihara, Tomohiko ^a   Shiga, Atsushi ^a   Ariizumi, Yuko ^a   Yokoseki, Akio ^a   Nishizawa, Masatoyo ^a  

^a NIIGATA UNIVERSITY   (Japan)

Author keywords

Amyotrophic lateral sclerosis; Gemini of coiled bodies; RNA splicing; Spliceosomes; U12 small nuclear RNA

Indexed keywords

SMALL NUCLEAR RNA;

AMYOTROPHIC LATERAL SCLEROSIS; ARTICLE; CELL DEATH; CENTRAL NERVOUS SYSTEM; CONSENSUS SEQUENCE; DONOR SITE; HUMAN; MOLECULAR PATHOLOGY; MOTOR NEURON DISEASE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RNA METABOLISM; SPINAL MUSCULAR ATROPHY; SPLICEOSOME; TDP 43 PROTEINOPATHY;

AMYOTROPHIC LATERAL SCLEROSIS; GEMINI OF COILED BODIES; RNA SPLICING; SPLICEOSOMES; U12 SMALL NUCLEAR RNA;

AMYOTROPHIC LATERAL SCLEROSIS; CELL NUCLEUS; DNA-BINDING PROTEINS; GEMINI OF COILED BODIES; HUMANS; MOTOR NEURON DISEASE; RNA; RNA SPLICING;

EID: 84892804110     PISSN: 09196544     EISSN: 14401789     Source Type: Journal    
DOI: 10.1111/neup.12070     Document Type: Article

References (72)

1. Kanning KC, Kaplan A, Henderson CE. Motor neuron diversity in development and disease. Annu Rev Neurosci 2010; 33: 409-440.
2. Clowney EJ, LeGros MA, Mosley CP etal. Nuclear aggregation of olfactory receptor genes governs their monogenic expression. Cell 2012; 151: 724-737.
3. Lafarga M, Casafont I, Bengoechea R, Tapia O, Berciano MT. Cajal's contribution to the knowledge of the neuronal cell nucleus. Chromosoma. Springer 2009; 118: 437-443.
4. Kwong LK, Neumann M, Sampathu DM, Lee VMY, Trojanowski JQ. TDP-43 proteinopathy: the neuropathology underlying major forms of sporadic and familial frontotemporal lobar degeneration and motor neuron disease. Acta Neuropathol 2007; 114 (1): 63-70.
5. Geser F, Lee VMY, Trojanowski JQ. Amyotrophic lateral sclerosis and frontotemporal lobar degeneration: a spectrum of TDP-43 proteinopathies. Neuropathology 2010; 30: 103-112.
6. Lagier-Tourenne C, Polymenidou M, Cleveland DW. TDP-43 and FUS/TLS: emerging roles in RNA processing and neurodegeneration. Hum Mol Genet 2010; 19 (R1): R46-R64.
7. Lattante S, Rouleau GA, Kabashi E. TARDBP and FUS mutations associated with amyotrophic lateral sclerosis: summary and update. Hum Mutat 2013; 34: 812-826.
8. Yokoseki A, Shiga A, Tan C-F etal. TDP-43 mutation in familial amyotrophic lateral sclerosis. Ann Neurol 2008; 63: 538-542.
9. Wang IF, Reddy NM, Shen CKJ. Higher order arrangement of the eukaryotic nuclear bodies. Proc Natl Acad Sci U S A 2002; 99: 13583-13588.
10. Casafont I, Bengoechea R, Tapia O, Berciano MT, Lafarga M. TDP-43 localizes in mRNA transcription and processing sites in mammalian neurons. J Struct Biol 2009; 167: 235-241.
11. Zhang ZC, Chook YM. Structural and energetic basis of ALS-causing mutations in the atypical proline-tyrosine nuclear localization signal of the Fused in Sarcoma protein (FUS). Proc Natl Acad Sci U S A 2012; 109: 12017-12021.
12. Tan C-F, Eguchi H, Tagawa A etal. TDP-43 immunoreactivity in neuronal inclusions in familial amyotrophic lateral sclerosis with or without SOD1 gene mutation. Acta Neuropathol 2007; 113: 535-542.
13. Mori F, Tanji K, Zhang H-X etal. Maturation process of TDP-43-positive neuronal cytoplasmic inclusions in amyotrophic lateral sclerosis with and without dementia. Acta Neuropathol 2008; 116: 193-203.
14. Lee EB, Lee VMY, Trojanowski JQ. Gains or losses: molecular mechanisms of TDP43-mediated neurodegeneration. Nat Rev Neurosci 2012; 13 (1): 38-50.
15. Onodera O, Sugai A, Konno T, Tada M, Koyama A, Nishizawa M. What is the key player in TDP-43 pathology in ALS: disappearance from the nucleus or inclusion formation in the cytoplasm? Neurol. Clin Neurosci 2013; 1 (1): 11-17.
16. Gendron TF, Petrucelli L. Rodent models of TDP-43 proteinopathy: investigating the mechanisms of TDP-43-mediated neurodegeneration. J Mol Neurosci 2011; 45: 486-499.
17. Buratti E, Baralle FE. TDP-43: gumming up neurons through protein-protein and protein-RNA interactions. Trends Biochem Sci 2012; 37: 237-247.
18. Polymenidou M, Lagier-Tourenne C, Hutt KR etal. Long pre-mRNA depletion and RNA missplicing contribute to neuronal vulnerability from loss of TDP-43. Nat Neurosci 2011; 14: 459-468.
19. Tollervey JR, Curk T, Rogelj B etal. Characterizing the RNA targets and position-dependent splicing regulation by TDP-43. Nat Neurosci 2011; 14: 452-458.
20. Jiang Y-M, Yamamoto M, Kobayashi Y etal. Gene expression profile of spinal motor neurons in sporadic amyotrophic lateral sclerosis. Ann Neurol 2005; 57: 236-251.
21. Rabin SJ, Kim JMH, Baughn M etal. Sporadic ALS has compartment-specific aberrant exon splicing and altered cell-matrix adhesion biology. Hum Mol Genet 2010; 19: 313-328.
22. Polymenidou M, Lagier-Tourenne C, Hutt KR, Bennett CF, Cleveland DW, Yeo GW. Misregulated RNA processing in amyotrophic lateral sclerosis. Brain Res 2012; 1462: 3-15.
23. Tollervey JR, Wang Z, Hortobágyi T etal. Analysis of alternative splicing associated with aging and neurodegeneration in the human brain. Genome Res 2011; 21: 1572-1582.
24. Shiga A, Ishihara T, Miyashita A etal. Alteration of POLDIP3 splicing associated with loss of function of TDP-43 in tissues affected with ALS. PLoS ONE 2012; 7 (8): e43120.
25. Lagier-Tourenne C, Polymenidou M, Hutt KR etal. Divergent roles of ALS-linked proteins FUS/TLS and TDP-43 intersect in processing long pre-mRNAs. Nat Neurosci 2012; 15: 1488-1497.
26. Kawahara Y, Mieda-Sato A. TDP-43 promotes microRNA biogenesis as a component of the Drosha and Dicer complexes. Proc Natl Acad Sci U S A 2012; 109: 3347-3352.
27. Mao YS, Zhang B, Spector DL. Biogenesis and function of nuclear bodies. Trends Genet 2011; 27: 295-306.
28. Caudron-Herger M, Rippe K. Nuclear architecture by RNA. Curr Opin Genet Dev 2012; 22: 179-187.
29. Dundr M. Nuclear bodies: multifunctional companions of the genome. Curr Opin Cell Biol 2012; 24: 415-422.
30. Nizami Z, Deryusheva S, Gall JG. The Cajal body and histone locus body. Cold Spring Harb Perspect Biol 2010; 2 (7): a000653.
31. Morris GE. The Cajal body. Biochim Biophys Acta 2008; 1783: 2108-2115.
32. Strzelecka M, Trowitzsch S, Weber G, LUhrmann R, Oates AC, Neugebauer KM. Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis. Nat Struct Mol Biol 2010; 17: 403-409.
33. Machyna M, Heyn P, Neugebauer KM. Cajal bodies: where form meets function. Wiley Interdiscip Rev RNA 2013; 4 (1): 17-34.
34. Ishihara T, Ariizumi Y, Shiga A etal. Decreased number of Gemini of coiled bodies and U12 snRNA level in amyotrophic lateral sclerosis. Hum Mol Genet 2013. doi: 10.1093/hmg/ddt262
35. Shan X, Chiang P-M, Price DL, Wong PC. Altered distributions of Gemini of coiled bodies and mitochondria in motor neurons of TDP-43 transgenic mice. Proc Natl Acad Sci U S A 2010; 107: 16325-16330.
36. Lefebvre S, Burlet P, Liu Q etal. Correlation between severity and SMN protein level in spinal muscular atrophy. Nat Genet 1997; 16: 265-269.
37. Tsuiji H, Iguchi Y, Furuya A etal. Spliceosome integrity is defective in the motor neuron diseases ALS and SMA. EMBO Mol Med 2013; 5: 221-234.
38. Avendaño-Vázquez SE, Dhir A, Bembich S, Buratti E, Proudfoot N, Baralle FE. Autoregulation of TDP-43 mRNA levels involves interplay between transcription, splicing, and alternative polyA site selection. Genes Dev 2012; 26: 1679-1684.
39. Pena E, Berciano MT, Fernandez R, Ojeda JL, Lafarga M. Neuronal body size correlates with the number of nucleoli and Cajal bodies, and with the organization of the splicing machinery in rat trigeminal ganglion neurons. J Comp Neurol 2001; 430: 250-263.
40. Berciano MT, Novell M, Villagra NT etal. Cajal body number and nucleolar size correlate with the cell body mass in human sensory ganglia neurons. J Struct Biol 2007; 158: 410-420.
41. Oyanagi K, Ikuta F, Horikawa Y. Evidence for sequential degeneration of the neurons in the intermediate zone of the spinal cord in amyotrophic lateral sclerosis: a topographic and quantitative investigation. Acta Neuropathol 1989; 77: 343-349.
42. Frey MR, Matera AG. RNA-mediated interaction of Cajal bodies and U2 snRNA genes. J Cell Biol 2001; 154: 499-509.
43. Jordan BA, Fernholz BD, Khatri L, Ziff EB. Activity-dependent AIDA-1 nuclear signaling regulates nucleolar numbers and protein synthesis in neurons. Nat Neurosci 2007; 10: 427-435.
44. Dundr M, Misteli T. Biogenesis of nuclear bodies. Cold Spring Harb Perspect Biol 2010; 2 (12): a000711.
45. Shevtsov SP, Dundr M. Nucleation of nuclear bodies by RNA. Nat Cell Biol 2011; 13: 167-173.
46. Bose JK, Wang IF, Hung L, Tarn W-Y, Shen CKJ. TDP-43 overexpression enhances exon 7 inclusion during the survival of motor neuron pre-mRNA splicing. J Biol Chem 2008; 283: 28852-28859.
47. Burghes AHM, Beattie CE. Spinal muscular atrophy: why do low levels of survival motor neuron protein make motor neurons sick? Nat Rev Neurosci 2009; 10: 597-609.
48. Piao Y, Hashimoto T, Takahama S etal. Survival motor neuron (SMN) protein in the spinal anterior horn cells of patients with sporadic amyotrophic lateral sclerosis. Brain Res 2011; 4 (1372): 152-159.
49. Yamazaki T, Chen S, Yu Y etal. FUS-SMN protein interactions link the motor neuron diseases ALS and SMA. Cell Rep 2012; 2: 799-806.
50. Freibaum BD, Chitta RK, High AA, Taylor JP. Global analysis of TDP-43 interacting proteins reveals strong association with RNA splicing and translation machinery. J Proteome Res 2010; 9: 1104-1120.
51. Dundr M, Hebert MD, Karpova TS etal. In vivo kinetics of Cajal body components. J Cell Biol 2004; 164: 831-842.
52. Coady TH, Lorson CL. SMN in spinal muscular atrophy and snRNP biogenesis. Wiley Interdiscip Rev RNA 2011; 2: 546-564.
53. Neuenkirchen N, Chari A, Fischer U. Deciphering the assembly pathway of Sm-class U snRNPs. FEBS Lett 2008; 582: 1997-2003.
54. Zhang Z, Lotti F, Dittmar K etal. SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell 2008; 133: 585-600.
55. Gabanella F, Butchbach MER, Saieva L, Carissimi C, Burghes AHM, Pellizzoni L. Ribonucleoprotein assembly defects correlate with spinal muscular atrophy severity and preferentially affect a subset of spliceosomal snRNPs. PLoS ONE 2007; 2 (9): e921.
56. Turunen JJ, Niemela EH, Verma B, Frilander MJ. The significant other: splicing by the minor spliceosome. Wiley Interdiscip Rev RNA 2013; 4: 61-76.
57. Lander ES, Linton LM, Birren B etal. Initial sequencing and analysis of the human genome. Nature 2001; 409 (6822): 860-921.
58. Patel AA, McCarthy M, Steitz JA. The splicing of U12-type introns can be a rate-limiting step in gene expression. EMBO J 2002; 21: 3804-3815.
59. Padgett RA. New connections between splicing and human disease. Trends Genet 2012; 28: 147-154.
60. Pierce MJ, Morse RP. The neurologic findings in Taybi-Linder syndrome (MOPD I/III): case report and review of the literature. Am J Med Genet 2012; 158A: 606-610.
61. Edery P, Marcaillou C, Sahbatou M etal. Association of TALS developmental disorder with defect in minor splicing component U4atac snRNA. Science 2011; 332 (6026): 240-243.
62. He H, Liyanarachchi S, Akagi K etal. Mutations in U4atac snRNA, a component of the minor spliceosome, in the developmental disorder MOPD I. Science 2011; 332 (6026): 238-240.
63. Abdel-Salam GMH, Abdel-Hamid MS, Issa M, Magdy A, El-Kotoury A, Amr K. Expanding the phenotypic and mutational spectrum in microcephalic osteodysplastic primordial dwarfism type I. Am J Med Genet 2012; 158A: 1455-1461.
64. Jia Y, Mu JC, Ackerman SL. Mutation of a U2 snRNA gene causes global disruption of alternative splicing and neurodegeneration. Cell 2012; 148 (1-2): 296-308.
65. O'Reilly D, Dienstbier M, Cowley SA etal. Differentially expressed, variant U1 snRNAs regulate gene expression in human cells. Genome Res 2013; 23: 281-291.
66. Lotti F, Imlach WL, Saieva L etal. An SMN-dependent U12 splicing event essential for motor circuit function. Cell 2012; 151: 440-454.
67. Roselli F, Caroni P. A circuit mechanism for neurodegeneration. Cell 2012; 151: 250-252.
68. Imlach WL, Beck ES, Choi BJ, Lotti F, Pellizzoni L, McCabe BD. SMN is required for sensory-motor circuit function in Drosophila. Cell 2012; 151: 427-439.
69. Worman HJ, Fong LG, Muchir A, Young SG. Laminopathies and the long strange trip from basic cell biology to therapy. J Clin Invest 2009; 119: 1825-1836.
70. Dechat T, Pfleghaar K, Sengupta K etal. Nuclear lamins: major factors in the structural organization and function of the nucleus and chromatin. Genes Dev 2008; 22: 832-853.
71. Zuela N, Bar DZ, Gruenbaum Y. Lamins in development, tissue maintenance and stress. EMBO Rep 2012; 13: 1070-1078.
72. Jung H-J, Lee JM, Yang SH, Young SG, Fong LG. Nuclear lamins in the brain - new insights into function and regulation. Mol Neurobiol 2013; 47 (1): 290-301.