Regions essential for the interaction between Bcl-2 and SMN, the spinal muscular atrophy disease gene product

Cell Death and Differentiation

Volumn 7, Issue 4, 2000, Pages 374-383

  Sato, K ^a,b   Eguchi, Y ^a   Kodama, T S ^a   Tsujimoto, Y ^a,c  

^a JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; Bcl 2; SMN; Spinal muscular atrophy

Indexed keywords

GENE PRODUCT; PROTEIN BCL 2;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DELETION MUTANT; EXON; IMMUNOPRECIPITATION; MOLECULAR INTERACTION; MOTONEURON; NONHUMAN; PRIORITY JOURNAL; SPINAL MUSCULAR ATROPHY;

ANIMALIA;

EID: 0034035329     PISSN: 13509047     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.cdd.4400660     Document Type: Article

References (80)

1. Pearn J (1980) Classification of spinal muscular atrophies. Lancet 1: 919-922.
2. Dubowitz V (1995) The spinal muscular atrophies. In Dubowitz V (ed) Muscle Disorders in Childhood, 2nd ed. London, UK: W.B. Saunders. p.540
3. Lefebvre S, Burglen L, Reboullet S, Clermont O, Burlet P, Viollet L, Benichou B, Cruaud C, Millasseau P, Zeviani M, Paslier DL, Frezal J, Cohen D, Weissenbach J, Munnich A and Melki J (1995) Identification and characterization of a spinal muscular atrophy-determining gene. Cell 80: 155-165
4. Roy N, Mahadevan MS, McLean M, Shutler G, Yaraghi Z, Farahani R, Baird S, Besner-Johnston A, Lefebvre C, Kang X, Salih M, Aubry H, Tamai K, Guan X, Ioannou P, Crawford TO, Jong PJD, Surh L, Ikeda J-E, Korneluk RG and MacKenzie A (1995) The gene for neuronal apoptosis inhibitory protein is partially deleted in individuals with spinal muscular atrophy. Cell 80: 167-178
5. Carter TA, Bonnemann CG, Wang CH, Obici S, Parano E, De Fatima Bonaldo M, Ross BM, Penchaszadeh GK, Mackenzie A, Soares MB, Kunkel LM and Gilliam TC (1997) A multicopy transcription-repair gene, BTF2p44, maps to the SMA region and demonstrates SMA associated deletions. Hum. Mol Genet. 6: 229-236
6. Burglen L, Seroz T, Miniou P, Lefebvre S, Burlet P, Munnich A, Pequignot EV, Egly JM and Melki J (1997) The gene encoding p44, a subunit of the transcription factor TFIIH, is involved in large-scale deletions associated with Werdnig-Hoffmann disease. Am. J. Hum. Genet. 60: 72-79
7. Scharf JM, Endrizzi MG, Wetter A, Huang S, Thompson TG, Zerres K, Dietrich WF, Wirth B and Kunkel LM (1998) Identification of a candidate modifying gene for spinal muscular atrophy by comparative genomics. Nat. Genet. 20: 83-86
8. Lefebvre S, Burglen L, Frezal J, Munnich A and Melki J (1998) The role of the SMN gene in proximal spinal muscular atrophy. Hum. Mol. Genet. 7: 1531-1536
9. Cobben JM, van der Steege G, Grootscholten P, de Visser M, Scheffer H and Buys CH (1995) Deletions of the survival motor neuron gene in unaffected siblings of patients with spinal muscular atrophy. Am. J. Hum. Genet. 57: 805-808
10. Hahnen E, Forkert R, Marke C, Rudnik-Schoneborn S, Schonling J, Zerres K and Wirth B (1995) Molecular analysis of candidate genes on chromosome 5q13 in autosomal recessive spinal muscular atrophy: evidence of homozygous deletions of the SMN gene in unaffected individuals. Hum. Mol. Genet. 4: 1927-1933
11. Rodrigues NR, Owen N, Talbot K, Ignatius J, Dubowitz V and Davies KE (1995) Deletions in the survival motor neuron gene on 5q13 in autosomal recessive spinal muscular atrophy. Hum. Mol. Genet. 4: 631-634
12. Chang JG, Jong YJ, Huang JM, Wang WS, Yang TY, Chang CP, Chen YJ and Lin SP (1995) Molecular basis of spinal muscular atrophy in Chinese. Am. J. Hum. Genet. 57: 1503-1505
13. Bussaglia E, Clermont O, Tizzano E, Lefebvre S, Burglen L, Cruaud C, Urtizberea JA, Colomer J, Munnich A, Baiget M and Melki J (1995) A frame-shift deletion in the survival motor neuron gene in Spanish spinal muscular atrophy patients. Nat. Genet. 11: 335-337
14. Velasco E, Valero C, Valero A, Moreno F and Hernandez-Chico C (1996) Molecular analysis of the SMN and NAIP genes in Spanish spinal muscular atrophy (SMA) families and correlation between number of copies of cBCD541 and SMA phenotype. Hum. Mol. Genet. 5: 257-263
15. Rodrigues NR, Owen N, Talbot K, Patel S, Muntoni F, Ignatius J, Dubowitz V and Davies KE (1996) Gene deletions in spinal muscular atrophy. J. Med. Genet. 33: 93-96
16. Brahe C, Clermont O, Zappata S, Tiziano F, Melki J and Neri G (1996) Frameshift mutation in the survival motor neuron gene in a severe case of SMA type I. Hum. Mol. Genet. 5: 1971-1976
17. Parsons DW, McAndrew PE, Monani UR, Mendell JR, Burghes AH and Prior TW (1996) An 11 base pair duplication in exon 6 of the SMN gene produces a type I spinal muscular atrophy (SMA) phenotype: further evidence for SMN as the primary SMA-determining gene. Hum. Mol. Genet. 5: 1727-1732
18. Talbot K, Ponting CP, Theodosiou AM, Rodrigues NR, Surtees R, Mountford R and Davies KE (1997) Missense mutation clustering in the survival motor neuron gene: a role for a conserved tyrosine and glycine rich region of the protein in RNA metabolism? Hum. Mol. Genet. 6: 497-500
19. Hahnen E, Schonling J, Rudnik-Schoneborn S, Raschke H, Zerres K and Wirth B (1997) Missense mutations in exon 6 of the survival motor neuron gene in patients with spinal muscular atrophy (SMA). Hum. Mol. Genet. 6: 821-825
20. Simard LR, Rochette C, Semionov A, Morgan K and Vanasse M (1997) SMN(T) and NAIP mutations in Canadian families with spinal muscular atrophy (SMA): genotype/phenotype correlations with disease severity. Am. J. Med. Genet. 72: 51-58
21. Zerres K, Wirth B and Rudnik-Schoneborn S (1997) Spinal muscular atrophy clinical and genetic correlations. Neuromuscul. Disord. 7: 202-207
22. Parsons DW, McAndrew PE, Allinson PS, Parker Jr WD, Burghes AH and Prior TW (1998) Diagnosis of spinal muscular atrophy in an SMN non-deletion patient using a quantitative PCR screen and mutation analysis. J. Med. Genet. 35: 674-676
23. Lefebvre S, Burlet P, Liu Q, Bertrandy S, Clermont O, Munnich A, Dreyfuss G and Melki J (1997) Correlation between severity and SMN protein level in spinal muscular atrophy. Nat. Genet. 16: 265-269
24. Gavrilov DK, Shi X, Das K, Gilliam TC and Wang CH (1998) Differential SMN2 expression associated with SMA severity. Nat. Genet. 20: 230-231
25. van der Steege G, Grootscholten PM, Cobben JM, Zappata S, Scheffer H, den Dunnen JT, van Ommen GJ, Brahe C and Buys CH (1996) Apparent gene conversions involving the SMN gene in the region of the spinal muscular atrophy locus on chromosome 5. Am. J. Hum. Genet. 59: 834-838
26. Hahnen E, Schonling J, Rudnik-Schoneborn S, Zerres K and Wirth B (1996) Hybrid survival motor neuron genes in patients with autosomal recessive spinal muscular atrophy: new insights into molecular mechanisms responsible for the disease. Am. J. Hum. Genet. 59: 1057-1065
27. Campbell L, Potter A, Ignatius J, Dubowitz V and Davies K (1997) Genomic variation and gene conversion in spinal muscular atrophy: implications for disease process and clinical phenotype. Am. J. Hum. Genet. 61: 40-50
28. Taylor JE, Thomas NH, Lewis CM, Abbs SJ, Rodrigues NR, Davies KE and Mathew CG (1998) Correlation of SMNt and SMNc gene copy number with age of onset and survival in spinal muscular atrophy. Eur. J. Hum. Genet. 6: 467-474
29. Talbot K, Rodrigues NR, Ignatius J, Muntoni F and Davies KE (1997) Gene conversion at the SMN locus in autosomal recessive spinal muscular atrophy does not predict a mild phenotype. Neuromuscul. Disord. 7: 198-201
30. McAndrew PE, Parsons DW, Simard LR, Rochette C, Ray PN, Mendell JR, Prior TW and Burghes AH (1997) Identification of proximal spinal muscular atrophy carriers and patients by analysis of SMNT and SMNC gene copy number. Am. J. Hum. Genet. 60: 1411-1422
31. Liu Q and Dreyfuss G (1996) A novel nuclear structure containing the survival of motor neurons proteins. EMBO J. 15: 3555-3565
32. Liu Q, Fischer U, Wang F and Dreyfuss G (1997) The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins. Cell 90: 1013-1021
33. Fischer U, Liu Q and Dreyfuss G (1997) The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis. Cell 90: 1023-1029
34. Pellizzoni L, Kataoka N, Charroux B and Dreyfuss G (1998) A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing. Cell 95: 615-624
35. Lorson CL and Androphy EJ (1998) The domain encoded by exon 2 of the survival motor neuron protein mediates nucleic acid binding. Hum. Mol. Genet. 7: 1269-1275
36. Bertrandy S, Burlet P, Clermont O, Huber C, Fondrat C, Thierry-Mieg D, Munnich A and Lefebvre S (1999) The RNA-binding properties of SMN: deletion analysis of the zebrafish orthologue defines domains conserved in evolution. Hum. Mol. Genet. 8: 775-782
37. Strasswimmer J, Lorson CL, Breiding DE, Chen JJ, Le T, Burghes AH and Androphy EJ (1999) Identification of survival motor neuron as a transcriptional activator-binding protein. Hum. Mol. Genet. 8: 1219-1226
38. Iwahashi H, Eguchi Y, Yasuhara N, Hanafusa T, Matsuzawa Y and Tsujimoto Y (1997) Synergistic anti-apoptotic activity between Bcl-2 and SMN implicated in spinal muscular atrophy. Nature 390: 413-417
39. Adams JM and Cory S (1998) The Bcl-2 protein family: arbiters of cell survival. Science 281: 1322-1326
40. Tsujimoto Y (1998) Role of Bcl-2 family proteins in apoptosis: apoptosomes or mitochondria? Genes Cells 3: 697-707
41. Muchmore SW, Sattler M, Liang H, Meadows RP, Harlan JE, Yoon HS, Nettesheim D, Chang BS, Thompson CB, Wong SL, Ng SL and Fesik SW (1996) X-ray and NMR structure of human Bcl-xL, an inhibitor of programmed cell death. Nature 381; 335-341
42. Fang G, Chang BS, Kim CN, Perkins C, Thompson CB and Bhalla KN (1998) "Loop" domain is necessary for taxol-induced mobility shift and phosphorylation of Bcl-2 as well as for inhibiting taxol-induced cytosolic accumulation of cytochrome c and apoptosis. Cancer Res. 58: 3202-3208
43. Srivastava RK, Mi QS, Hardwick JM and Longo DL (1999) Deletion of the loop region of Bcl-2 completely blocks paclitaxel-induced apoptosis. Proc. Natl. Acad. Sci. USA 96: 3775-3780
44. Yin XM, Oltvai ZN and Korsmeyer SJ (1994) BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature 369: 321-323
45. Takayama S, Sato T, Krajewski S, Kochel K, Irie S, Millan JA and Reed JC (1995) Cloning and functional analysis of BAG-1 : a novel Bcl-2-binding protein with anti-cell death activity. Cell 80: 279-284
46. Wang HG, Rapp UR and Reed JC (1996) Bcl-2 targets the protein kinase Raf-1 to mitochondria. Cell 87: 629-638
47. Datta SR, Dudek H, Tao X, Masters S, Fu H, Gotoh Y and Greenberg ME (1997) Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91: 231-241
48. del Peso L, Gonzalez-Garcia M, Page C, Herrera R and Nunez G (1997) Interleukin-3-induced phosphorylation of BAD through the protein kinase Akt. Science 278: 687-689
49. Harada H, Becknell B, Wilm M, Mann M, Huang LJ, Taylor SS, Scott JD and Korsmeyer SJ (1999) Phosphorylation and inactivation of BAD by mitochondria-anchored protein kinase. Mol. Cell 3: 3: 413-422
50. Ito T, Deng X, Carr B and May WS (1997) Bcl-2 phosphorylation required for anti-apoptosis function. J. Biol. Chem. 272: 11671-11673
51. Reed JC (1997) Cytochrome c: can't live with it-can't live without it. Cell 91: 559-562
52. Green DR and Reed JC (1998) Mitochondria and apoptosis. Science 281: 1309-1312
53. Zamzami N, Brenner C, Marzo I, Susin SA and Kroemer G (1998) Subcellular and submitochondrial mode of action of Bcl-2-like oncoproteins. Oncogene 16: 2265-2282
54. Shimizu S, Narita M and Tsujimoto Y (1999) Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC. Nature 399: 483-487
55. Spector MS, Desnoyers S, Hoeppner DJ and Hengartner MO (1997) Interaction between the C, elegans cell-death regulators CED-9 and CED-4. Nature 385: 653-656
56. Chinnaiyan AM, O'Rourke K, Lane BR and Dixit VM (1997) Interaction of CED-4 with CED-3 and CED-9: a molecular framework for cell death. Science 275: 1122-1126
57. Wu D, Wallen HD and Nunez G (1997) Interaction and regulation of subcellular localization of CED-4 by CED-9. Science 275: 1126-1129
58. Pan G, O'Rourke K and Dixit VM (1998) Caspase-9, Bcl-XL, and Apaf-1 form a ternary complex. J. Biol. Chem. 273: 5841-5845
59. Hu Y, Benedict MA, Wu D, Inohara N and Nunez G (1998) Bcl-XL interacts with Apaf-1 and inhibits Apaf-1-dependent caspase-9 activation. Proc. Natl. Acad. Sci. USA 95: 4386-4391
60. Merry DE, Veis DJ, Hickey WF and Korsmeyer SJ (1994) bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS. Development 120: 301-331
61. Yachnis AT, Giovanini MA, Erskin TA, Reier PJ and Anderson DK (1998) Developmental patterns of BCL-2 and BCL-X polypeptide expression in the human spinal cord. Exp. Neurol. 150: 82-97
62. Nguyen M, Millar DG, Yong VW, Korsmeyer SJ and Shore GC (1993) Targeting of Bcl-2 to the mitochondrial outer membrane by a COOH-terminal signal anchor sequence J. Biol. Chem. 268: 25265-25268
63. Aritomi M, Kunishima N, Inohara N, Ishibashi Y, Ohta S and Morikawa K (1997) Crystal structure of rat Bcl-xL. Implications for the function of the Bcl-2 protein family. J. Biol. Chem. 272: 27886-27892
64. Borner C, Martinou I, Mattmann C, Irmler M, Schaerer E, Martinou JC and Tschopp J (1994) The protein bcl-2 alpha does not require membrane attachment, but two conserved domains to suppress apoptosis. J. Cell Biol. 126: 1059-1068
65. Hanada M, Aime-Sempe C, Sato T and Reed JC (1995) Structure-function analysis of Bcl-2 protein. Identification of conserved domains important for homodimerization with Bcl-2 and heterodimerization with Bax. J. Biol. Chem. 270: 11962-11969
66. Hunter JJ and Parslow TG (1996) A peptide sequence from Bax that converts Bcl-2 into an activator of apoptosis. J. Biol. Chem. 271: 8521-8524
67. Lee LC, Hunter JJ, Mujeeb A, Turck C and Parslow TG (1996) Evidence for alphahelical conformation of an essential N-terminal region in the human Bcl2 protein. J. Biol. Chem. 271: 23284-23288
68. Huang DC, Adams JM and Cory S (1998) The conserved N-terminal BH4 domain of Bcl-2 homologues is essential for inhibition of apoptosis and interaction with CED-4. EMBO J. 17: 1029-1039
69. Shimizu S, Kinishi K, Kodama T and Tsujimoto Y (2000) BH4 of anti-apoptotic Bcl-2 family members closes VDAC, and inhibits apoptotic mitochondrial changes and cell death. Proc. Natl. Acad. Sci. USA In press
70. Mohaghegh P, Rodrigues NR, Owen N, Ponting CP, Le TT, Burghes AH and Davies KE (1999) Analysis of mutations in the tudor domain of the survival motor neuron protein SMN. Eur. J. Hum. Genet. 7: 519-525
71. Lorson CL, Strasswimmer J, Yao JM, Baleja JD, Hahnen E, Wirth B, Le T, Burghes AH and Androphy EJ (1998) SMN oligomerization defect correlates with spinal muscular atrophy severity. Nat. Genet. 19: 63-66
72. Parsons DW, McAndrew PE, Iannaccone ST, Mendell JR, Burghes AH and Prior TW (1998) Intragenic telSMN mutations: frequency, distribution, evidence of a founder effect, and modification of the spinal muscular atropohy phenotype by cenSMN copy number. Am. J. Hum. Genet. 63: 1712-1723
73. Wirth B, Herz M, Wetter A, Moskau S, Hahnen E, Rudnik-Schoneborri W, Wienker T and Zerres K (1999) Quantitative analysis of survival motor neuron copies: identification of subtle SMN1 mutations in patients with spinal muscular atrophy, genotype-phenotype correlation, and implications for genetic counseling. Am. J. Hum. Genet. 64: 1340-1356
74. Biros I and Forrest S (1999) Spinal muscular atrophy: untangling the knot? J. Med. Genet. 36: 1-8
75. Kolodziej PA and Young RA (1991) Epitope tagging and protein surveillance. Meth. Enzymol. 194: 508-519
76. Niwa H, Yamamura K and Miyazaki J (1991) Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108: 193-199
77. Iwahashi H, Hanafusa T, Eguchi Y, Nakajima H, Miyagawa J, Itoh N, Tomita K, Namba M, Kuwajima M, Noguchi T, Tsujimoto Y and Matsuzawa Y (1996) Cytokine-induced apoptotic cell death in a mouse pancreatic beta-cell line: inhibition by Bcl-2. Diabetologia 39: 530-536
78. Peitsch MC and Guex N (1997) Large-scale comparative protein modeling. In: Wilkins MR, Williams KL, Appel RO and Hochstrasser DF (eds) Proteome research: new frontiers in functional genomics. Springer. pp. 177-186
79. L-Bak peptide complex: recognition between regulators of apoptosis. Science 275: 983-986
80. van Gunsteren WF (1993) Molecular dynamics and stochastic dynamics simulation: A primer. In: van Gunsteren WF, Weiner PK, and Wilkinson AJ (eds). Computer Simulation of Biomolecular Systems, Theoretical and Experimental Applications, Vol. 2, The Netherlands: Escom Science Publishers, Leiden, pp. 3-36