Retrotransposition and mutation events yield Rap1 GTPases with differential signalling capacity

BMC Evolutionary Biology

Volumn 10, Issue 1, 2010, Pages

  Zemojtel, Tomasz ^a,b   Duchniewicz, Marlena ^d   Zhang, Zhongchun ^e   Paluch, Taisa ^e   Luz, Hannes ^a   Penzkofer, Tobias ^b,c   Scheele, Jürgen S ^d   Zwartkruis, Fried J T ^e  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d UNIVERSITY OF FREIBURG   (Germany)

^e UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; ENZYME ACTIVITY; GENETIC ANALYSIS; HUMAN EVOLUTION; MUTATION; PROTEIN; RNA;

MURINAE;

RAP1 PROTEIN;

ANIMAL; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOUSE; RETROPOSON; REVERSE TRANSCRIPTION;

ANIMALS; HUMANS; MICE; MODELS, MOLECULAR; RAP1 GTP-BINDING PROTEINS; RETROELEMENTS; REVERSE TRANSCRIPTION;

EID: 77649335136     PISSN: None     EISSN: 14712148     Source Type: Journal    
DOI: 10.1186/1471-2148-10-55     Document Type: Article

References (53)

1. Adaptive evolution of a duplicated pancreatic ribonuclease gene in a leaf-eating monkey. J Zhang YP Zhang HF Rosenberg, Nat Genet 2002 30 411 5 10.1038/ng852 11925567
2. Human LINE retrotransposons generate processed pseudogenes. C Esnault J Maestre T Heidmann, Nat Genet 2000 24 363 7 10.1038/74184 10742098
3. L1Base: from functional annotation to prediction of active LINE-1 elements. T Penzkofer T Dandekar T Zemojtel, Nucleic Acids Res 2005 33 498 500 10.1093/nar/gki044 15608246
4. A retrocopy of a gene can functionally displace the source gene in evolution. AN Krasnov MM Kurshakova VE Ramensky PV Mardanov EN Nabirochkina SG Georgieva, Nucleic Acids Res 2005 33 6654 61 10.1093/nar/gki969 16314324
5. Birth and adaptive evolution of a hominoid gene that supports high neurotransmitter flux. F Burki H Kaessmann, Nat Genet 2004 36 1061 3 10.1038/ng1431 15378063
6. The origin of new genes: glimpses from the young and old. M Long E Betran K Thornton W Wang, Nat Rev Genet 2003 4 865 75 10.1038/nrg1204 14634634
7. Retroposons - seeds of evolution. J Brosius, Science 1991 251 753 10.1126/science.1990437 1990437
8. On "genomenclature": a comprehensive (and respectful) taxonomy for pseudogenes and other "junk DNA". J Brosius SJ Gould, Proc Natl Acad Sci USA 1992 89 10706 10 10.1073/pnas.89.22.10706 1279691
9. Emergence of young human genes after a burst of retroposition in primates. AC Marques I Dupanloup N Vinckenbosch A Reymond H Kaessmann, PLoS Biol 2005 3 357 10.1371/journal.pbio.0030357 16201836
10. Evolutionary fate of retroposed gene copies in the human genome. N Vinckenbosch I Dupanloup H Kaessmann, Proc Natl Acad Sci USA 2006 103 3220 5 10.1073/pnas.0511307103 16492757
11. Extensive gene traffic on the mammalian X chromosome. JJ Emerson H Kaessmann E Betran M Long, Science 2004 303 537 40 10.1126/science.1090042 14739461
12. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. JR McCarrey K Thomas, Nature 1987 326 501 5 10.1038/326501a0 3453121
13. Extracellular signal-regulated activation of Rap1 fails to interfere in Ras effector signalling. FJ Zwartkruis RM Wolthuis NM Nabben B Franke JL Bos, Embo J 1998 17 5905 12 10.1093/emboj/17.20.5905 9774335
14. GEFs and GAPs: critical elements in the control of small G proteins. JL Bos H Rehmann A Wittinghofer, Cell 2007 129 865 77 10.1016/j.cell.2007.05.018 17540168
15. Vascular endothelial cadherin-mediated cell-cell adhesion regulated by a small GTPase, Rap1. S Fukuhra A Sakurai A Yamagishi K Sako N Mochizuki, J Biochem Mol Biol 2006 39 132 9 16584626
16. Biology of the Rap proteins, members of the ras superfamily of GTP-binding proteins. GM Bokoch, Biochem J 1993 289 Pt 1 17 24 8424755
17. Generation of specific antibodies against the rap1A, rap1B and rap2 small GTP-binding proteins. Analysis of rap and ras proteins in membranes from mammalian cells. FJ Klinz R Seifert I Schwaner H Gausepohl R Frank G Schultz, Eur J Biochem 1992 207 207 13 10.1111/j.1432-1033.1992.tb17039.x 1628649
18. Rap1b is required for normal platelet function and hemostasis in mice. M Chrzanowska-Wodnicka SS Smyth SM Schoenwaelder TH Fischer GC White, J Clin Invest 2005 115 680 7 15696195
19. Rap1A-deficient T and B cells show impaired integrin-mediated cell adhesion. M Duchniewicz T Zemojtel M Kolanczyk S Grossmann JS Scheele FJ Zwartkruis, Mol Cell Biol 2006 26 643 53 10.1128/MCB.26.2.643-653.2006 16382154
20. Inhibition of Rap1A binding to cytochrome b558 of NADPH oxidase by phosphorylation of Rap1A. GM Bokoch LA Quilliam BP Bohl AJ Jesaitis MT Quinn, Science 1991 254 1794 6 10.1126/science.1763330 1763330
21. Rap1a null mice have altered myeloid cell functions suggesting distinct roles for the closely related rap1a and 1b proteins. Y Li J Yan P De HC Chang A Yamauchi KW Christopherson NC Paranavitana X Peng C Kim V Munugulavadla R Kapur H Chen W Shou JC Stone MH Kaplan MC Dinauer DL Durden LA Quilliam, J Immunol 2007 179 8322 31 18056377
22. Defective angiogenesis, endothelial migration, proliferation, and MAPK signaling in Rap1b-deficient mice. M Chrzanowska-Wodnicka AE Kraus D Gale GC White J Vansluys, Blood 2008 111 2647 56 10.1182/blood-2007-08-109710 17993608
23. HRap1B-retro: a novel human processed rap1B gene blurs the picture? T Zemojtel T Penzkofer M Duchniewicz FJ Zwartkruis, Leukemia 2006 20 145 6 10.1038/sj.leu.2404040 16307016
24. Reply to 'hRap1B-retro: a novel human processed Rap1B gene blurs the picture?' by Zemojtel et al. E Gyan F Porteu M Fontenay, Leukemia 2006 20 146 147 10.1038/sj.leu.2404042 16307014
25. Targeting of human retrotransposon integration is directed by the specificity of the L1 endonuclease for regions of unusual DNA structure. GJ Cost JD Boeke, Biochemistry 1998 37 18081 93 10.1021/bi981858s 9922177
26. PAML: a program package for phylogenetic analysis by maximum likelihood. Z Yang, Comput Appl Biosci 1997 13 555 6 9367129
27. A codon-based model of nucleotide substitution for protein-coding DNA sequences. N Goldman Z Yang, Mol Biol Evol 1994 11 725 36 7968486
28. The evolutionary fate and consequences of duplicate genes. M Lynch JS Conery, Science 2000 290 1151 5 10.1126/science.290.5494.1151 11073452
29. ras oncogenes in human cancer: a review. JL Bos, Cancer Res 1989 49 4682 9 2547513
30. Mutational activation of N- and K-ras oncogenes in plasma cell dyscrasias. P Corradini M Ladetto C Voena A Palumbo G Inghirami DM Knowles M Boccadoro A Pileri, Blood 1993 81 2708 13 8490179
31. ras genes. M Barbacid, Annu Rev Biochem 1987 56 779 827 10.1146/annurev.bi.56.070187.004023 3304147
32. cAMP activates MAP kinase and Elk-1 through a B-Raf- and Rap1-dependent pathway. MR Vossler H Yao RD York MG Pan CS Rim PJ Stork, Cell 1997 89 73 82 10.1016/S0092-8674(00)80184-1 9094716
33. Ras/Rap effector specificity determined by charge reversal. N Nassar G Horn C Herrmann C Block R Janknecht A Wittinghofer, Nat Struct Biol 1996 3 723 9 10.1038/nsb0896-723 8756332
34. Rap-specific GTPase activating protein follows an alternative mechanism. T Brinkmann O Daumke U Herbrand D Kuhlmann P Stege MR Ahmadian A Wittinghofer, J Biol Chem 2002 277 12525 31 10.1074/jbc.M109176200 11812780
35. Dynamic properties of the Ras switch I region and its importance for binding to effectors. M Spoerner C Herrmann IR Vetter HR Kalbitzer A Wittinghofer, Proc Natl Acad Sci USA 2001 98 4944 9 10.1073/pnas.081441398 11320243
36. Structural requirements for the interaction of p21ras with GAP, exchange factors, and its biological effector target. P Polakis F McCormick, J Biol Chem 1993 268 9157 60 8486615
37. Identification of the guanine nucleotide dissociation stimulator for Ral as a putative effector molecule of R-ras, H-ras, K-ras, and Rap. M Spaargaren JR Bischoff, Proc Natl Acad Sci USA 1994 91 12609 13 10.1073/pnas.91.26.12609 7809086
38. Linking Rap to cell adhesion. JL Bos, Curr Opin Cell Biol 2005 17 123 8 10.1016/j.ceb.2005.02.009 15780587
39. Rap1 promotes cell spreading by localizing Rac guanine nucleotide exchange factors. WT Arthur LA Quilliam JA Cooper, J Cell Biol 2004 167 111 22 10.1083/jcb.200404068 15479739
40. Retrocopy contributions to the evolution of the human genome. R Baertsch M Diekhans WJ Kent D Haussler J Brosius, BMC Genomics 2008 9 466 10.1186/1471-2164-9-466 18842134
41. Adult tissue-specific expression of a Dppa3-derived retrogene represents a postnatal transcript of pluripotent cell origin. SJ Elliman I Wu DM Kemp, J Biol Chem 2006 281 16 9 10.1074/jbc.C500415200 16291741
42. An X-to-autosome retrogene is required for spermatogenesis in mice. J Bradley A Baltus H Skaletsky M Royce-Tolland K Dewar DC Page, Nat Genet 2004 36 872 6 10.1038/ng1390 15258580
43. Genetic analysis of the Kirsten-ras-revertant 1 gene: potentiation of its tumor suppressor activity by specific point mutations. H Kitayama T Matsuzaki Y Ikawa M Noda, Proc Natl Acad Sci USA 1990 87 4284 8 10.1073/pnas.87.11.4284 2112251
44. RIAM, an Ena/VASP and Profilin ligand, interacts with Rap1-GTP and mediates Rap1-induced adhesion. EM Lafuente AA van Puijenbroek M Krause CV Carman GJ Freeman A Berezovskaya E Constantine TA Springer FB Gertler VA Boussiotis, Dev Cell 2004 7 585 95 10.1016/j.devcel.2004.07.021 15469846
45. Specificity in Ras and Rap signaling. JH Raaijmakers JL Bos, J Biol Chem 2009 284 10995 9 10.1074/jbc.R800061200 19091745
46. Role of ERas in promoting tumour-like properties in mouse embryonic stem cells. K Takahashi K Mitsui S Yamanaka, Nature 2003 423 541 5 10.1038/nature01646 12774123
47. Human ERas gene has an upstream premature polyadenylation signal that results in a truncated, noncoding transcript. T Kameda JA Thomson, Stem Cells 2005 23 1535 40 10.1634/stemcells.2005-0054 16081664
48. cDNA sequence of a new ras-related gene (rap2b) isolated from human platelets with sequence homology to rap2. FX Farrell CA Ohmstede BR Reep EG Lapetina, Nucleic Acids Res 1990 18 4281 10.1093/nar/18.14.4281 2115998
49. Model selection and model averaging in phylogenetics: advantages of akaike information criterion and bayesian approaches over likelihood ratio tests. D Posada TR Buckley, Syst Biol 2004 53 793 808 10.1080/10635150490522304 15545256
50. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. S Guindon O Gascuel, Syst Biol 2003 52 696 704 10.1080/10635150390235520 14530136
51. CONSEL: for assessing the confidence of phylogenetic tree selection. H Shimodaira M Hasegawa, Bioinformatics 2001 17 1246 7 10.1093/bioinformatics/17. 12.1246 11751242
52. EGFR signaling to p120-catenin through phosphorylation at Y228. DJ Mariner MA Davis AB Reynolds, J Cell Sci 2004 117 1339 50 10.1242/jcs.01001 14996911
53. GTPase-activating protein SH2-SH3 domains induce gene expression in a Ras-dependent fashion. RH Medema WL de Laat GA Martin F McCormick JL Bos, Mol Cell Biol 1992 12 3425 30 1321335