Massive expansions of Dscam splicing diversity via staggered homologous recombination during arthropod evolution

RNA

Volumn 16, Issue 1, 2010, Pages 91-105

  Lee, Christopher ^a   Kim, Namshin ^a,c   Roy, Meenakshi ^a   Graveley, Brenton R ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^c Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Alternative splicing; Dscam; Evolution

Indexed keywords

DOWN SYNDROME CELL ADHESION MOLECULE PROTEIN; IMMUNOGLOBULIN; PROTEIN; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; DROSOPHILA PROTEIN; DSCAM PROTEIN, DROSOPHILA;

ARTHROPOD; ARTICLE; EXON; GENE CLUSTER; GENE STRUCTURE; GENETIC RECOMBINATION; GENETIC VARIABILITY; MOLECULAR EVOLUTION; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA SPLICING; SEQUENCE HOMOLOGY; ANIMAL; DNA MICROARRAY; DROSOPHILA MELANOGASTER; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENETICS; GENOME; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY;

ARTHROPODA; HEXAPODA;

ANIMALS; ARTHROPODS; BASE SEQUENCE; CELL ADHESION MOLECULES; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENE EXPRESSION PROFILING; GENETIC VARIATION; GENOME, INSECT; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHYLOGENY; RECOMBINATION, GENETIC; RNA SPLICING; SEQUENCE HOMOLOGY;

EID: 75649092310     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.1812710     Document Type: Article

References (49)

1. Alekseyenko AV, Kim N, Lee CJ. 2007. Global analysis of exon creation versus loss and the role of alternative splicing in 17 vertebrate genomes. RNA 13: 661-670. (Pubitemid 46641524)
2. Anastassiou D, Liu H, Varadan V. 2006. Variable window binding for mutually exclusive alternative splicing. Genome Biol 7: R2. doi: 10.1186/gb-2006-7-1-r2.
3. Black DL. 2000. Protein diversity from alternative splicing: A challenge for bioinformatics and post-genome biology. Cell 103: 367-370.
4. Brett D, Hanke J, Lehmann G, Haase S, Delbruck S, Krueger S, Reich J, Bork P. 2000. EST comparison indicates 38% of human mRNAs contain possible alternative splice forms. FEBS Lett 474: 83-86. (Pubitemid 30320837)
5. Brites D, McTaggart S, Morris K, Anderson J, Thomas K, Colson I, Fabbro T, Little TJ, Ebert D, Du Pasquier L. 2008. The Dscam homolog of the crustacean Daphnia is diversified by alternative splicing like in insects. Mol Biol Evol 25: 1429-1439. (Pubitemid 351882017)
6. Chen BE, Kondo M, Garnier A, Watson FL, Puettmann-Holgado R, Lamar DR, Schmucker D. 2006. The molecular diversity of Dscam is functionally required for neuronal wiring specificity in Drosophila. Cell 125: 607-620.
7. Crayton ME 3rd, Powell BC, Vision TJ, Giddings MC. 2006. Tracking the evolution of alternatively spliced exons within the Dscam family. BMC Evol Biol 6: 16.
8. Dong Y, Taylor HE, Dimopoulos G. 2006. AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biol 4: e229. doi: 10.1371/journal.pbio.0040229.
9. Felsenstein J. 1989. PHYLIP: Phylogeny inference package (version 3.2). Cladistics 5: 164-166.
10. Gansner ER, North SC. 1999. An open graph visualization system and its applications. Softw Pract Exper 30: 1203-1233.
11. Graveley BR. 2001. Alternative splicing: Increasing diversity in the proteomic world. Trends Genet 17: 100-107. (Pubitemid 32140790)
12. Graveley BR. 2005. Mutually exclusive splicing of the insect Dscam pre-mRNA directed by competing intronic RNA secondary structures. Cell 123: 65-73.
13. Graveley BR, Kaur A, Gunning D, Zipursky SL, Rowen L, Clemens JC. 2004. The organization and evolution of the dipteran and hymenopteran Down syndrome cell adhesion molecule (Dscam) genes. RNA 10: 1499-1506. (Pubitemid 39288184)
14. Hattori D, Demir E, Kim HW, Viragh E, Zipursky SL, Dickson BJ. 2007. Dscam diversity is essential for neuronal wiring and self-recognition. Nature 449: 223-227. (Pubitemid 47402366)
15. Hughes ME, Bortnick R, Tsubouchi A, Baumer P, Kondo M, Uemura T, Schmucker D. 2007. Homophilic Dscam interactions control complex dendrite morphogenesis. Neuron 54: 417-427. (Pubitemid 46659811)
16. Hummel T, Vasconcelos ML, Clemens JC, Fishilevich Y, Vosshall LB, Zipursky SL. 2003. Axonal targeting of olfactory receptor neurons in Drosophila is controlled by Dscam. Neuron 37: 221-231. (Pubitemid 36143818)
17. Kan Z, Rouchka EC, Gish WR, States DJ. 2001. Gene structure prediction and alternative splicing analysis using genomically aligned ESTs. Genome Res 11: 889-900. (Pubitemid 32447871)
18. Kim N, Lee C. 2007. Three-dimensional phylogeny explorer: Distinguishing paralogs, lateral transfer, and violation of 'molecular clock' assumption with 3D visualization. BMC Bioinformatics 8: 213.
19. Kondrashov FA, Koonin EV. 2001. Origin of alternative splicing by tandem exon duplication. Hum Mol Genet 10: 2661-2669.
20. Kreahling JM, Graveley BR. 2005. The iStem, a long-range RNA secondary structure element required for efficient exon inclusion in the Drosophila Dscam pre-mRNA. Mol Cell Biol 25: 10251-10260.
21. Kurtz J, Armitage SA. 2006. Alternative adaptive immunity in invertebrates. Trends Immunol 27: 493-496.
22. Lee C, Irizarry K. 2001. The GeneMine system for genome/proteome annotation and collaborative data mining. IBM Syst J 40: 592-603. (Pubitemid 32611104)
23. Letunic I, Copley RR, Bork P. 2002. Common exon duplication in animals and its role in alternative splicing. Hum Mol Genet 11: 1561-1567. (Pubitemid 34679256)
24. Lev-Maor G, Sorek R, Shomron N, Ast G. 2003. The birth of an alternatively spliced exon: 3′ Splice-site selection in Alu exons. Science 300: 1288-1291. (Pubitemid 36618239)
25. Maddison WP. 1997. Gene trees in species trees. Syst Biol 46: 523-536.
26. Matthews BJ, Kim ME, Flanagan JJ, Hattori D, Clemens JC, Zipursky SL, Grueber WB. 2007. Dendrite self-avoidance is controlled by Dscam. Cell 129: 593-604.
27. Meijers R, Puettmann-Holgado R, Skiniotis G, Liu JH, Walz T, Wang JH, Schmucker D. 2007. Structural basis of Dscam isoform specificity. Nature 449: 487-491. (Pubitemid 47509544)
28. Mironov AA, Fickett JW, Gelfand MS. 1999. Frequent alternative splicing of human genes. Genome Res 9: 1288-1293. (Pubitemid 30042512)
29. Modrek B, Resch A, Grasso C, Lee C. 2001. Genome-wide analysis of alternative splicing using human expressed sequence data. Nucleic Acids Res 29: 2850-2859. (Pubitemid 32685050)
30. Neves G, Zucker J, Daly M, Chess A. 2004. Stochastic yet biased expression of multiple Dscam splice variants by individual cells. Nat Genet 36: 240-246. (Pubitemid 38282748)
31. Olson S, Blanchette M, Park J, Savva Y, Yeo GW, Yeakley JM, Rio DC, Graveley BR. 2007. A regulator of Dscam mutually exclusive splicing fidelity. Nat Struct Mol Biol 14: 1134-1140. (Pubitemid 350223337)
32. Pan Q, Shai O, Lee LJ, Frey J, Blencowe BJ. 2008. Deep surveying of alternative splicing complexity in the human transcriptome by high-throughput sequencing. Nat Genet 40: 1413-1415.
33. Park JW, Graveley BR. 2007. Complex alternative splicing. Adv Exp Med Biol 623: 50-63.
34. Retief JD. 1999. Phylogenetic analysis using PHYLIP. In Bioinformatics methods and protocols (ed. SAKS Misener), Vol.132, pp. 243-258. Humana Press, New York.
35. Rice P, Longden I, Bleasby A. 2000. EMBOSS: The European Molecular Biology Open Software Suite. Trends Genet 16: 276-277.
36. Saitou N, Nei M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
37. Sawaya MR, Wojtowicz WM, Andre I, Qian B, Wu W, Baker D, Eisenberg D, Zipursky SL. 2008. A double S shape provides the structural basis for the extraordinary binding specificity of Dscam isoforms. Cell 134: 1007-1018.
38. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J, Muda M, Dixon JE, Zipursky SL. 2000. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 101: 671-684.
39. Soba P, Zhu S, Emoto K, Younger S, Yang SJ, Yu HH, Lee T, Jan LY, Jan YN. 2007. Drosophila sensory neurons require Dscam for dendritic self-avoidance and proper dendritic field organization. Neuron 54: 403-416. (Pubitemid 46659807)
40. Sorek R, Lev-Maor G, Reznik M, Dagan T, Belinky F, Graur D, Ast G. 2004. Minimal conditions for exonization of intronic sequences: 5′ splice site formation in alu exons. Mol Cell 14: 221-231. (Pubitemid 38515649)
41. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
42. Wang J, Zugates CT, Liang IH, Lee CH, Lee T. 2002. Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 33: 559-571. (Pubitemid 34188432)
43. Wang J, Ma X, Yang JS, Zheng X, Zugates CT, Lee CH, Lee T. 2004. Transmembrane/juxtamembrane domain-dependent Dscam distribution and function during mushroom body neuronal morphogenesis. Neuron 43: 663-672. (Pubitemid 39179726)
44. Wang ET, Sandberg R, Luo SJ, Khrebtukova I, Zhang L, Mayr C, Kingsmore SF, Schroth GP, Burge CB. 2008. Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476. (Pubitemid 352759009)
45. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, Kondo M, Rebel VI, Schmucker D. 2005. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 309: 1874-1878. (Pubitemid 41325101)
46. Wernersson R, Pedersen AG. 2003. RevTrans: Multiple alignment of coding DNA from aligned amino acid sequences. Nucleic Acids Res 31: 3537-3539. (Pubitemid 37442193)
47. Wojtowicz WM, Wu W, Andre I, Qian B, Baker D, Zipursky SL. 2007. A vast repertoire of Dscam binding specificities arises from modular interactions of variable Ig domains. Cell 130: 1134-1145. (Pubitemid 47410273)
48. Zhan XL, Clemens JC, Neves G, Hattori D, Flanagan JJ, Hummel T, Vasconcelos ML, Chess A, Zipursky SL. 2004. Analysis of Dscam diversity in regulating axon guidance in Drosophila mushroom bodies. Neuron 43: 673-686. (Pubitemid 39179727)
49. Zipursky SL, Wojtowicz WM, Hattori D. 2006. Got diversity? Wiring the fly brain with Dscam. Trends Biochem Sci 31: 581-588. (Pubitemid 44436940)