Linear motifs: Lost in (pre)translation

Trends in Biochemical Sciences

Volumn 37, Issue 8, 2012, Pages 333-341

  Weatheritt, Robert J ^a   Gibson, Toby J ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

Author keywords

Alternative promoter usage; Alternative splicing; Intrinsically disordered proteins; Linear motifs; Modular protein architecture; Protein domains; Signal transduction

Indexed keywords

BCL2 RELATED PROTEIN A1; CYCLIC AMP DEPENDENT PROTEIN KINASE; PEPTIDYLPROLYL ISOMERASE PIN1; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL X; PROTEIN KINASE C DELTA; PROTEIN MCL 1; PROTEIN TYROSINE KINASE A; PROTEOME; SYNAPSIN;

ALTERNATIVE RNA SPLICING; APOPTOSIS; BINDING AFFINITY; CELLULAR DISTRIBUTION; COMPLEX FORMATION; EXON; FOCAL ADHESION; NONHUMAN; PDZ DOMAIN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DEGRADATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REVIEW; RNA EDITING; SHORT LINEAR MOTIF; SIGNAL TRANSDUCTION;

ALTERNATIVE SPLICING; AMINO ACID MOTIFS; ANIMALS; APOPTOSIS; EXONS; HUMANS; MICRORNAS; PROMOTER REGIONS, GENETIC; PROTEIN BIOSYNTHESIS; PROTEIN INTERACTION MAPPING; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RNA EDITING; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84864311086     PISSN: 09680004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tibs.2012.05.001     Document Type: Review

References (98)

1. Davuluri R.V., et al. The functional consequences of alternative promoter use in mammalian genomes. Trends Genet. 2008, 24:167-177.
2. Wang E.T., et al. Alternative isoform regulation in human tissue transcriptomes. Nature 2008, 456:470-476.
3. Li J.B., et al. Genome-wide identification of human RNA editing sites by parallel DNA capturing and sequencing. Science 2009, 324:1210-1213.
4. Kim T.H., et al. A high-resolution map of active promoters in the human genome. Nature 2005, 436:876-880.
5. Graveley B.R. Alternative splicing: increasing diversity in the proteomic world. Trends Genet. 2001, 17:100-107.
6. Stamm S., et al. Function of alternative splicing. Gene 2005, 344:1-20.
7. Romero P.R., et al. Alternative splicing in concert with protein intrinsic disorder enables increased functional diversity in multicellular organisms. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:8390-8395.
8. Fuxreiter M., et al. Local structural disorder imparts plasticity on linear motifs. Bioinformatics 2007, 23:950-956.
9. Weatheritt R.J., et al. The identification of short linear motif-mediated interfaces within the human interactome. Bioinformatics 2012, 28:976-982.
10. Dinkel H., et al. ELM - the database of eukaryotic linear motifs. Nucleic Acids Res. 2012, 40:D242-D251.
11. Davey N.E., et al. Attributes of short linear motifs. Mol. Biosyst. 2012, 8:268-281.
12. Diella F., et al. Understanding eukaryotic linear motifs and their role in cell signaling and regulation. Front Biosci. 2008, 13:6580-6603.
13. Tompa P. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett. 2005, 579:3346-3354.
14. Chen F.C., et al. Alternatively and constitutively spliced exons are subject to different evolutionary forces. Mol. Biol. Evol. 2006, 23:675-682.
15. Weatheritt R.J., et al. Linear motifs confer functional diversity onto splice variants. Nucleic Acids Res. 2012, 10.1093/nar/gks442.
16. Bignone P.A., et al. Phosphorylation of a threonine unique to the short C-terminal isoform of betaII-spectrin links regulation of alpha-beta spectrin interaction to neuritogenesis. J. Biol. Chem. 2007, 282:888-896.
17. Diegelmann S., et al. The conserved protein kinase-A target motif in synapsin of Drosophila is effectively modified by pre-mRNA editing. BMC Neurosci. 2006, 7:76.
18. Martin K.C., Ephrussi A. mRNA localization: gene expression in the spatial dimension. Cell 2009, 136:719-730.
19. Small I., et al. Two birds with one stone: genes that encode products targeted to two or more compartments. Plant Mol. Biol. 1998, 38:265-277.
20. Otterlei M., et al. Nuclear and mitochondrial splice forms of human uracil-DNA glycosylase contain a complex nuclear localisation signal and a strong classical mitochondrial localisation signal, respectively. Nucleic Acids Res. 1998, 26:4611-4617.
21. Caradonna S., Muller-Weeks S. The nature of enzymes involved in uracil-DNA repair: isoform characteristics of proteins responsible for nuclear and mitochondrial genomic integrity. Curr. Protein Pept. Sci. 2001, 2:335-347.
22. Tinkelenberg B.A., et al. Identification of sequence determinants of human nuclear dUTPase isoform localization. Exp. Cell Res. 2003, 287:39-46.
23. Joubert L., et al. New sorting nexin (SNX27) and NHERF specifically interact with the 5-HT4a receptor splice variant: roles in receptor targeting. J. Cell Sci. 2004, 117:5367-5379.
24. Coupar I.M., et al. Human 5-HT(4) and 5-HT(7) receptor splice variants: are they important?. Curr. Neuropharmacol. 2007, 5:224-231.
25. Eden E., et al. Proteome half-life dynamics in living human cells. Science 2011, 331:764-768.
26. Peters J.M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 2006, 7:644-656.
27. Kieffer I., et al. Differential mitotic degradation of the CDC25B phosphatase variants. Oncogene 2007, 26:7847-7858.
28. Marcel V., Hainaut P. p53 isoforms - a conspiracy to kidnap p53 tumor suppressor activity?. Cell Mol. Life Sci. 2009, 66:391-406.
29. Bodmer D., et al. Isoform-specific dephosphorylation of dynamin1 by calcineurin couples neurotrophin receptor endocytosis to axonal growth. Neuron 2011, 70:1085-1099.
30. Van Roey K., et al. Motif switches: decision-making in cell regulation. Curr. Opin. Struct. Biol. 2012, 10.1016/j.sbi.2012.03.004.
31. Muraoka-Cook R.S., et al. ErbB4 splice variants Cyt1 and Cyt2 differ by 16 amino acids and exert opposing effects on the mammary epithelium in vivo. Mol. Cell Biol. 2009, 29:4935-4948.
32. Sundvall M., et al. Isoform-specific monoubiquitination, endocytosis, and degradation of alternatively spliced ErbB4 isoforms. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:4162-4167.
33. Sundvall M., et al. Cell death or survival promoted by alternative isoforms of ErbB4. Mol. Biol. Cell 2010, 21:4275-4286.
34. Fan Y.X., et al. EGFR kinase possesses a broad specificity for ErbB phosphorylation sites, and ligand increases catalytic-centre activity without affecting substrate binding affinity. Biochem. J. 2005, 392:417-423.
35. Kojima C., et al. Regulation of Bin1 SH3 domain binding by phosphoinositides. EMBO J. 2004, 23:4413-4422.
36. Pineda-Lucena A., et al. A structure-based model of the c-Myc/Bin1 protein interaction shows alternative splicing of Bin1 and c-Myc phosphorylation are key binding determinants. J. Mol. Biol. 2005, 351:182-194.
37. Gibson T.J. Cell regulation: determined to signal discrete cooperation. Trends Biochem. Sci. 2009, 34:471-482.
38. Mantovani F., et al. Pin1 links the activities of c-Abl and p300 in regulating p73 function. Mol. Cell 2004, 14:625-636.
39. Strehler E.E., et al. Plasma membrane Ca2+ ATPases as dynamic regulators of cellular calcium handling. Ann. N.Y. Acad. Sci. 2007, 1099:226-236.
40. Strehler E.E., Zacharias D.A. Role of alternative splicing in generating isoform diversity among plasma membrane calcium pumps. Physiol. Rev. 2001, 81:21-50.
41. Caride A.J., et al. The plasma membrane Ca2+ pump isoform 4a differs from isoform 4b in the mechanism of calmodulin binding and activation kinetics: implications for Ca2+ signaling. J. Biol. Chem. 2007, 282:25640-25648.
42. Shoemaker B.A., et al. Speeding molecular recognition by using the folding funnel: the fly-casting mechanism. Proc. Natl. Acad. Sci. U.S.A. 2000, 97:8868-8873.
43. Choudhury R., et al. Differential clathrin binding and subcellular localization of OCRL1 splice isoforms. J. Biol. Chem. 2009, 284:9965-9973.
44. Anthis N.J., et al. Structural diversity in integrin/talin interactions. Structure 2010, 18:1654-1666.
45. Fornaro M., et al. Differential role of beta(1C) and beta(1A) integrin cytoplasmic variants in modulating focal adhesion kinase, protein kinase B/AKT, and Ras/Mitogen-activated protein kinase pathways. Mol. Biol. Cell 2000, 11:2235-2249.
46. Cerna J., et al. Dystrophin Dp71f associates with the beta1-integrin adhesion complex to modulate PC12 cell adhesion. J. Mol. Biol. 2006, 362:954-965.
47. Schaller M.D. Paxillin: a focal adhesion-associated adaptor protein. Oncogene 2001, 20:6459-6472.
48. Toutant M., et al. Alternative splicing controls the mechanisms of FAK autophosphorylation. Mol. Cell Biol. 2002, 22:7731-7743.
49. Legate K.R., Fassler R. Mechanisms that regulate adaptor binding to beta-integrin cytoplasmic tails. J. Cell Sci. 2009, 122:187-198.
50. Zent R., et al. Class- and splice variant-specific association of CD98 with integrin beta cytoplasmic domains. J. Biol. Chem. 2000, 275:5059-5064.
51. Zhang X.A., Hemler M.E. Interaction of the integrin beta1 cytoplasmic domain with ICAP-1 protein. J. Biol. Chem. 1999, 274:11-19.
52. Nieves B., et al. The NPIY motif in the integrin beta1 tail dictates the requirement for talin-1 in outside-in signaling. J. Cell Sci. 2010, 123:1216-1226.
53. Brown M.C., Turner C.E. Paxillin: adapting to change. Physiol. Rev. 2004, 84:1315-1339.
54. Tumbarello D.A., et al. Regulation of paxillin family members during epithelial-mesenchymal transformation: a putative role for paxillin delta. J. Cell Sci. 2005, 118:4849-4863.
55. Schwerk C., Schulze-Osthoff K. Regulation of apoptosis by alternative pre-mRNA splicing. Mol. Cell 2005, 19:1-13.
56. Puthalakath H., et al. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell 1999, 3:287-296.
57. Dehan E., et al. betaTrCP- and Rsk1/2-mediated degradation of BimEL inhibits apoptosis. Mol. Cell 2009, 33:109-116.
58. Jiang K., et al. Identification of a novel antiapoptotic human protein kinase C delta isoform, PKCdeltaVIII in NT2 cells. Biochemistry 2008, 47:787-797.
59. Vieyra D., et al. ING1 isoforms differentially affect apoptosis in a cell age-dependent manner. Cancer Res. 2002, 62:4445-4452.
60. Akgul C., et al. Alternative splicing of Bcl-2-related genes: functional consequences and potential therapeutic applications. Cell Mol. Life Sci. 2004, 61:2189-2199.
61. Rautureau G.J., et al. Intrinsically disordered proteins in bcl-2 regulated apoptosis. Int. J. Mol. Sci. 2010, 11:1808-1824.
62. Zha J., et al. Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science 2000, 290:1761-1765.
63. Linseman D.A., et al. Glycogen synthase kinase-3beta phosphorylates Bax and promotes its mitochondrial localization during neuronal apoptosis. J. Neurosci. 2004, 24:9993-10002.
64. Kutuk O., Letai A. Regulation of Bcl-2 family proteins by posttranslational modifications. Curr. Mol. Med. 2008, 8:102-118.
65. Hodi Z., et al. Alternatively spliced exon B of myosin Va is essential for binding the tail-associated light chain shared by dynein. Biochemistry 2006, 45:12582-12595.
66. Katyal S., Godbout R. Alternative splicing modulates Disabled-1 (Dab1) function in the developing chick retina. EMBO J. 2004, 23:1878-1888.
67. Gao Z., et al. The early isoform of disabled-1 functions independently of Reelin-mediated tyrosine phosphorylation in chick retina. Mol. Cell Biol. 2010, 30:4339-4353.
68. Kindler S., et al. RNA transport and local control of translation. Annu. Rev. Cell Dev. Biol. 2005, 21:223-245.
69. Raju C.S., et al. In neurons, activity-dependent association of dendritically transported mRNA transcripts with the transacting factor CBF-A is mediated by A2RE/RTS elements. Mol. Biol. Cell 2011, 22:1864-1877.
70. An J.J., et al. Distinct role of long 3' UTR BDNF mRNA in spine morphology and synaptic plasticity in hippocampal neurons. Cell 2008, 134:175-187.
71. Pietrzykowski A.Z., et al. Posttranscriptional regulation of BK channel splice variant stability by miR-9 underlies neuroadaptation to alcohol. Neuron 2008, 59:274-287.
72. Tress M.L., et al. The implications of alternative splicing in the ENCODE protein complement. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:5495-5500.
73. Hattori D., et al. Dscam-mediated cell recognition regulates neural circuit formation. Annu. Rev. Cell Dev. Biol. 2008, 24:597-620.
74. Wojtowicz W.M., et al. Alternative splicing of Drosophila Dscam generates axon guidance receptors that exhibit isoform-specific homophilic binding. Cell 2004, 118:619-633.
75. Wang G.S., Cooper T.A. Splicing in disease: disruption of the splicing code and the decoding machinery. Nat. Rev. Genet. 2007, 8:749-761.
76. Touzot F., et al. Function of Apollo (SNM1B) at telomere highlighted by a splice variant identified in a patient with Hoyeraal-Hreidarsson syndrome. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:10097-10102.
77. Chen Y., et al. A shared docking motif in TRF1 and TRF2 used for differential recruitment of telomeric proteins. Science 2008, 319:1092-1096.
78. Kim E., et al. Insights into the connection between cancer and alternative splicing. Trends Genet. 2008, 24:7-10.
79. Grosso A.R., et al. The emerging role of splicing factors in cancer. EMBO Rep. 2008, 9:1087-1093.
80. Schmit T.L., Ahmad N. Regulation of mitosis via mitotic kinases: new opportunities for cancer management. Mol. Cancer Ther. 2007, 6:1920-1931.
81. Guardavaccaro D., et al. Control of chromosome stability by the beta-TrCP-REST-Mad2 axis. Nature 2008, 452:365-369.
82. Zhong J.L., et al. Distinct functions of natural ADAM-15 cytoplasmic domain variants in human mammary carcinoma. Mol. Cancer Res. 2008, 6:383-394.
83. Kleino I., et al. Alternative splicing of ADAM15 regulates its interactions with cellular SH3 proteins. J. Cell Biochem. 2009, 108:877-885.
84. Maretzky T., et al. Src stimulates fibroblast growth factor receptor-2 shedding by an ADAM15 splice variant linked to breast cancer. Cancer Res. 2009, 69:4573-4576.
85. Zammarchi F., et al. Antitumorigenic potential of STAT3 alternative splicing modulation. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:17779-17784.
86. Moulton H.M., et al. Peptide-morpholino conjugate: a promising therapeutic for Duchenne muscular dystrophy. Ann. N.Y. Acad. Sci. 2009, 1175:55-60.
87. Bauman J.A., et al. Anti-tumor activity of splice-switching oligonucleotides. Nucleic Acids Res. 2010, 38:8348-8356.
88. Cirak S., et al. Exon skipping and dystrophin restoration in patients with Duchenne muscular dystrophy after systemic phosphorodiamidate morpholino oligomer treatment: an open-label, phase 2, dose-escalation study. Lancet 2011, 378:595-605.
89. Fukata Y., et al. Epilepsy-related ligand/receptor complex LGI1 and ADAM22 regulate synaptic transmission. Science 2006, 313:1792-1795.
90. Mubiru J.N., et al. Alternative spliced variants of the alpha-methylacyl-CoA racemase gene and their expression in prostate cancer. Gene 2004, 327:89-98.
91. Balzac F., et al. Expression and functional analysis of a cytoplasmic domain variant of the beta 1 integrin subunit. J. Cell Biol. 1993, 121:171-178.
92. Ramjaun A.R., McPherson P.S. Multiple amphiphysin II splice variants display differential clathrin binding: identification of two distinct clathrin-binding sites. J. Neurochem. 1998, 70:2369-2376.
93. Damdimopoulos A.E., et al. An alternative splicing variant of the selenoprotein thioredoxin reductase is a modulator of estrogen signaling. J. Biol. Chem. 2004, 279:38721-38729.
94. DeMarco S.J., et al. Plasma membrane Ca2+ ATPase isoform 2b interacts preferentially with Na+/H+ exchanger regulatory factor 2 in apical plasma membranes. J. Biol. Chem. 2002, 277:10506-10511.
95. Fiol D.F., et al. A novel tilapia prolactin receptor is functionally distinct from its paralog. J. Exp. Biol. 2009, 212:2007-2015.
96. Russwurm C., et al. Dual acylation of PDE2A splice variant 3: targeting to synaptic membranes. J. Biol. Chem. 2009, 284:25782-25790.
97. Chan S.W., et al. Hippo pathway-independent restriction of TAZ and YAP by angiomotin. J. Biol. Chem. 2011, 286:7018-7026.
98. Kanehisa M., et al. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 2012, 40:D109-D114.