An Sp185/333 gene cluster from the purple sea urchin and putative microsatellite-mediated gene diversification

BMC Genomics

Volumn 11, Issue 1, 2010, Pages

  Miller, Chase A ^a,c   Buckley, Katherine M ^b,d   Easley, Rebecca L ^b,e   Smith, L Courtney ^b  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b GEORGE WASHINGTON UNIVERSITY   (United States)

^c BOSTON COLLEGE   (United States)

^d Sunnybrook Health Sciences Centre   (Canada)

^e TECHLAB INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; CONTROLLED STUDY; DNA FLANKING REGION; GENE; GENE CLUSTER; GENE CONVERSION; GENE DUPLICATION; GENE ISOLATION; GENE SEQUENCE; GENETIC LINKAGE; GENETIC ORGANIZATION; GENETIC VARIABILITY; GENOMIC INSTABILITY; MICROSATELLITE MARKER; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; SEA URCHIN; SEQUENCE HOMOLOGY; SP185 333 GENE; ANIMAL; DNA SEQUENCE; GENETICS; GENOME; MOLECULAR GENETICS; REPRODUCIBILITY; SEGMENTAL DUPLICATION; SEQUENCE ALIGNMENT; STRONGYLOCENTROTUS; TRANSPOSON;

ANIMALIA; ECHINOIDEA; STRONGYLOCENTROTUS PURPURATUS;

MICROSATELLITE DNA; SPACER DNA;

ANIMALS; BASE SEQUENCE; CHROMOSOMES, ARTIFICIAL, BACTERIAL; CONSERVED SEQUENCE; DNA TRANSPOSABLE ELEMENTS; DNA, INTERGENIC; GENE DUPLICATION; GENETIC VARIATION; GENOME; MICROSATELLITE REPEATS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; REPRODUCIBILITY OF RESULTS; SEGMENTAL DUPLICATIONS, GENOMIC; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; STRONGYLOCENTROTUS PURPURATUS;

EID: 77957900229     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-11-575     Document Type: Article

References (69)

1. Raftos DA, Raison RL. Early vertebrates reveal diverse immune recognition strategies. Immunology and Cell Biology 2008, 86:479-481. 10.1038/icb.2008.38, 18521099.
2. Flajnik MF, Du Pasquier L. Evolution of innate and adaptive immunity: can we draw a line?. Trends in Immunology 2004, 25(12):640-644. 10.1016/j.it.2004.10.001, 15530832.
3. Loker ES, Adema CM, Zhang SM, Kepler TB. Invertebrate immune systems--not homogeneous, not simple, not well understood. Immunological Review 2004, 198:10-24.
4. Messier-Solek C, Buckley KM, Rast JP. Highly diversified innate receptor systems and new forms of animal immunity. Seminars in Immunology 2010, 22(1):39-47. 10.1016/j.smim.2009.11.007, 20022762.
5. Zhang SM, Adema CM, Kepler TB, Loker ES. Diversification of Ig superfamily genes in an invertebrate. Science 2004, 305(5681):251-254. 10.1126/science.1088069, 15247481.
6. Schmucker D, Clemens JC, Shu H, Worby CA, Xiao J, Muda M, Dixon JE, Zipursky SL. Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity. Cell 2000, 101(6):671-684. 10.1016/S0092-8674(00)80878-8, 10892653.
7. Schmucker D, Chen B. Dscam and DSCAM: complex genes in simple animals, complex animals yet simple genes. Genes and Development 2009, 23:147-156. 10.1101/gad.1752909, 19171779.
8. Brites D, McTaggart S, Morris K, Anderson J, Thomas K, Colson I, Fabbro T, Little TJ, Ebert D, Du Pasquier L. The Dscam homologue of the crustacean Daphnia is diversified by alternative splicing like in insects. Molecular Biology and Evolution 2008, 25(7):1429-1439. 10.1093/molbev/msn087, 18403399.
9. Watson FL, Puttmann-Holgado R, Thomas F, Lamar DL, Hughes M, Kondo M, Rebel VI, Schmucker D. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 2005, 309(5742):1874-1878. 10.1126/science.1116887, 16109846.
10. Dong Y, Taylor HE, Dimopoulos G. AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system. PLoS Biology 2006, 4(7):e229. 10.1371/journal.pbio.0040229, 1479700, 16774454.
11. McDowell JM, Simon SA. Molecular diversity at the plant-pathogen interface. Developmental and Comparative Immunology 2008, 32(7):736-744. 10.1016/j.dci.2007.11.005, 18191204.
12. Cannon JP, Haire RN, Litman GW. Identification of diversified genes that contain immunoglobulin-like variable regions in a protochordate. Nature Immunology 2002, 3(12):1200-1207. 10.1038/ni849, 12415263.
13. Cannon JP, Haire RN, Rast JP, Litman GW. The phylogenetic origins of the antigen-binding receptors and somatic diversification mechanisms. Immunolocal Reviews 2004, 200:12-22.
14. Dishaw LJ, Meuller MG, Gwatney N, Cannon JP, Haire RN, Litman RT, Amemiya CT, Ota T, Rowen L, Gluxman G, et al. Genomic complexity of the variable region-containing chitin-binding proteins in amphioxus. MBC Genetics 2008, 9:78.
15. Buckley KM, Smith LC. Extraordinary diversity among members of the large gene family, 185/333, from the purple sea urchin, Strongylocentrotus purpuratus. BMC Molecular Biology 2007, 8:68. 10.1186/1471-2199-8-68, 1988830, 17697382.
16. Ghosh JG, Buckley KM, Nair SV, Raftos DA, Miller C, Majeske AJ, Hibino T, Rast JP, Roth M, Smith LC. Sp185/333: A novel family of genes and proteins involved in the purple sea urchin immune response. Developmental and Comparative Immunology 2010, 34:235-245. 10.1016/j.dci.2009.10.008, 19887082.
17. Nair SV, Del Valle H, Gross PS, Terwilliger DP, Smith LC. Macroarray analysis of coelomocyte gene expression in response to LPS in the sea urchin. Identification of unexpected immune diversity in an invertebrate. Physiological Genomics 2005, 22(1):33-47. 10.1152/physiolgenomics.00052.2005, 15827237.
18. Terwilliger DP, Buckley KM, Brockton V, Ritter NJ, Smith LC. Distinctive expression patterns of 185/333 genes in the purple sea urchin, Strongylocentrotus purpuratus: an unexpectedly diverse family of transcripts in response to LPS, beta-1,3-glucan, and dsRNA. BMC Molecular Biology 2007, 8:16. 10.1186/1471-2199-8-16, 1831783, 17331248.
19. Terwilliger DP, Buckley KM, Mehta D, Moorjani PG, Smith LC. Unexpected diversity displayed in cDNAs expressed by the immune cells of the purple sea urchin, Strongylocentrotus purpuratus. Physiological Genomics 2006, 26(2):134-144. 10.1152/physiolgenomics.00011.2006, 16837652.
20. Rast JP, Pancer Z, Davidson EH. New approaches towards an understanding of deuterostome immunity. Current Topics in Microbiology and Immunology 2000, 248:3-16.
21. Dheilly NM, Nair SV, Smith LC, Raftos DA. Highly variable immune-response proteins (185/333) from the sea urchin Strongylocentrotus purpuratus: Proteomic analysis identifies diversity within and between individuals. Journal of Immunology 2009, 182:2203-2212.
22. Buckley KM, Munshaw S, Kepler TB, Smith LC. The 185/333 gene family is a rapidly diversifying host-defense gene cluster in the purple sea urchin, Strongylocentrotus purpuratus. Journal of Molecular Biology 2008, 379:912-928. 10.1016/j.jmb.2008.04.037, 18482736.
23. Cameron RA, Samanta M, Yuan A, He D, Davidson E. SpBase: the sea urchin genome database and web site. Nucleic Acids Research 2009, (37 Database):D750-D754. 10.1093/nar/gkn887, 2686435, 19010966.
24. Hoskins RA, Carlson JW, Kennedy C, Acevedo D, Evans-Holm M, Frise E, Wan KH, Park S, Mendez-Lago M, Rossi F, et al. Sequence finishing and mapping of Drosophila melanogaster heterochromatin. Science 2007, 316(5831):1625-1628. 10.1126/science.1139816, 2825053, 17569867.
25. Mendez-Lago M, Wild J, Whitehead SL, Tracey A, de Pablos B, Rogers J, Szybalski W, Villasante A. Novel sequencing strategy for repetitive DNA in a Drosophila BAC clone reveals that the centromeric region of the Y chromosome evolved from a telomere. Nucleic Acids Research 2009, 37(7):2264-2273. 10.1093/nar/gkp085, 2673431, 19237394.
26. Strathmann M, Hamilton BA, Mayeda CA, Simon MI, Meyerowitz EM, Palazzolo MJ. Transposon-facilitated DNA sequencing. Proc Natl Acad Sci 1990, 88:1247-1250.
27. She X, Jiang Z, Clark RA, Liu G, Cheng Z, Tuzun E, Church DM, Sutton G, Halpern AL, Eichler EE. Shotgun sequence assembly and recent segmental duplications within the human genome. Nature 2004, 431(7011):927-930. 10.1038/nature03062, 15496912.
28. Medvedev P, Brudno M. Maximum likelihood genome assembly. Journal of Computational Biology 2009, 16(8):1101-1116. 10.1089/cmb.2009.0047, 19645596.
29. Drost DR, Novaes E, Boaventura-Novaes C, Benedict CI, Brown RS, Yin T, Tuskan GA, Kirst M. A microarray-based genotyping and genetic mapping approach for highly heterozygous outcrossing species enables localization of a large fraction of the unassembled Populus trichocarpa genome sequence. Plant Journal 2009, 58(6):1054-1067. 10.1111/j.1365-313X.2009.03828.x, 19220791.
30. Cameron RA, Mahairas G, Rast JP, Martinez P, Biondi TR, Swartzell S, Wallace JC, Poustka AJ, Livingston BT, Wray GA, et al. A sea urchin genome project: sequence scan, virtual map, and additional resources. Proc Natl Acad Sci USA 2000, 97(17):9514-9518. 10.1073/Proceedings of the National Academy of Sciences.160261897, 16896, 10920195.
31. Multerer KA, Smith LC. Two cDNAs from the purple sea urchin, Strongylocentrotus purpuratus, encoding mosaic proteins with domains found in factor H, factor I, and complement components C6 and C7. Immunogenetics 2004, 56(2):89-106. 10.1007/s00251-004-0665-2, 15088130.
32. Sodergren E, Weinstock GM, Davidson EH, Cameron RA, Gibbs RA, Angerer RC, Angerer LM, Arnone MI, Burgess DR, Burke RD, et al. The genome of the sea urchin, Strongylocentrotus purpuratus. Science 2006, 314(5801):941-952. 10.1126/science.1133609, 17095691.
33. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE, Li PW, Hoskins RA, Galle RF, et al. The genome sequence of Drosophila melanogaster. Science 2000, 287(5461):2185-2195. 10.1126/science.287.5461.2185, 10731132.
34. Schatz MC, Phillippy AM, Shneiderman B, Salzberg SL. Hawkeye: an interactive visual analytics tool for genome assemblies. Genome Biology 2007, 8(3):R34. 10.1186/gb-2007-8-3-r34, 1868940, 17349036.
35. Rebeiz M, Posakony JW. GenePalette: a universal software tool for genome sequence visualization and analysis. Developmental Biology 2004, 271(2):431-438. 10.1016/j.ydbio.2004.04.011, 15223345.
36. Hall TA. BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series: 1999 1999, 95-98.
37. Kumar S, Dudley J, Nei M, Tamura K. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Briefings in Bioinformatics 2008, 9:299-306. 10.1093/bib/bbn017, 2562624, 18417537.
38. Toth G, Deak G, Barta E, Kiss GB. PLOTREP: a web tool for defragmentation and visual analysis of dispersed genomic repeats. Nucleic Acids Res 2006, (34 Web Server):W708-W713. 10.1093/nar/gkl263, 1538846, 16845104.
39. Britten RJ, Cetta A, Davidson EH. The single-copy DNA sequence polymorphism of the sea urchin Strongylocentrotus purpuratus. Cell 1978, 15(4):1175-1186. 10.1016/0092-8674(78)90044-2, 728997.
40. Green P. Phrap documentation. 1996, , http://www.phrap.org/phredphrap/phrap.html
41. Havlak P, Chen R, Durbin KJ, Egan A, Ren Y, Song XZ, Weinstock GM, Gibbs RA. The Atlas genome assembly system. Genome Research 2004, 14(4):721-732. 10.1101/gr.2264004, 383319, 15060016.
42. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al. Initial sequencing and analysis of the human genome. Nature 2001, 409(6822):860-921. 10.1038/35057062, 11237011.
43. Myers EW, Sutton GG, Delcher AL, Dew IM, Fasulo DP, Flanigan MJ, Kravitz SA, Mobarry CM, Reinert KH, Remington KA, et al. A whole-genome assembly of Drosophila. Science 2000, 287(5461):2196-2204. 10.1126/science.287.5461.2196, 10731133.
44. Kapitonov VV, Jurka J. Harbinger transposons and an ancient HARBI1 gene derived from a transposase. DNA Cell Biology 2004, 23(5):311-324.
45. Li B, Xia Q, Lu C, Zhou Z, Xiang Z. Analysis on frequency and density of microsatellites in coding sequences of several eukaryotic genomes. Genomics Proteomics Bioinformatics 2004, 2(1):24-31.
46. Schlötterer C, Wiehe T. Microsatellites, a neutral marker to infer selective sweeps. Microsatellites: Evolution and Applications 1999, 238-247. Oxford: Oxford University Press.
47. Schlotterer C. Evolutionary dynamics of microsatellite DNA. Chromosoma 2000, 109:365-371. 10.1007/s004120000089, 11072791.
48. Bagshaw AT, Pitt JP, Gemmell NJ. High frequency of microsatellites in S. cerevisiae meiotic recombination hotspots. BMC Genomics 2008, 9:49. 10.1186/1471-2164-9-49, 2267716, 18226240.
49. Kong A, Gudbjartsson DF, Sainz J, Jonsdottir GM, Gudjonsson SA, Richardsson B, Sigurdardottir S, Barnard J, Hallbeck B, Masson G, et al. A high-resolution recombination map of the human genome. Nature Genetics 2002, 31(3):241-247.
50. Myers S, Bottolo L, Freeman C, McVean G, Donnelly P. A fine-scale map of recombination rates and hotspots across the human genome. Science 2005, 310(5746):321-324. 10.1126/science.1117196, 16224025.
51. Jensen-Seaman MI, Furey TS, Payseur BA, Lu Y, Roskin KM, Chen CF, Thomas MA, Haussler D, Jacob HJ. Comparative recombination rates in the rat, mouse, and human genomes. Genome Research 2004, 14(4):528-538. 10.1101/gr.1970304, 383296, 15059993.
52. Trifonov EN. Tuning function of tandemly repeating sequences: a molecular device for fast adaptation. Evolutionary theory and processes: modern horizons, papers in honor of Eviatar Nevo 2003, 1-24. Amsterdam, The Netherlands: Kluwer Academic Publishers, Wassser SP.
53. Gendrel C-G, Boulet A, Dutreix M. (CA/GT)n microsatellites affect homologous recombination during yeast meiosis. Genes and Development 2000, 14:1261-1268. 316615, 10817760.
54. Payen C, Koszul R, Dujon B, Fischer G. Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms. PLoS Genetics 2008, 4(9):e1000175. 10.1371/journal.pgen.1000175, 2518615, 18773114.
55. Wahls WP, Wallace LJ, Moore PD. The Z-DNA motif d(TG)30 promotes reception of information during gene conversion events while stimulating homologous recombination in human cells in culture. Molecular and Cellular Biology 1990, 10(2):785-793. 360879, 2405255.
56. Napierala M, Dere R, Vetcher A, Wells RD. Structure-dependent recombination hot spot activity of GAA.TTC sequences from intron 1 of the Friedreich's ataxia gene. Journal of Biological Chemistry 2004, 279(8):6444-6454. 10.1074/jbc.M309596200, 14625270.
57. Murphy KE, Stringer JR. RecA independent recombination of poly[d(GT)-d(CA)] in pBR322. Nucleic Acids Research 1986, 14:7325-7340. 10.1093/nar/14.18.7325, 311754, 3020512.
58. Bullock P, Miller J, Botchan M. Effects of poly[d(pGpT).d(pApC)] and poly[d(pCpG).d(pCpG)] repeats on homologous recombination in somatic cells. Molecular and Cellular Biology 1986, 6(11):3948-3953. 367158, 3025620.
59. Traherne JA. Human MHC architecture and evolution: implications for disease association studies. International Journal of Immunogenetics 2008, 35(3):179-192. 10.1111/j.1744-313X.2008.00765.x, 2408657, 18397301.
60. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 2003, 15(4):809-834. 10.1105/tpc.009308, 152331, 12671079.
61. Richly E, Kurth J, Leister D. Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Molecular Biology and Evolution 2002, 19(1):76-94.
62. Hibino T, Loza-Coll M, Messier C, Majeske AJ, Cohen A, Terwilliger DP, Buckley KM, Brockton V, Nair S, Berney K, et al. The immune gene repertoire encoded in the purple sea urchin genome. Developmental Biology 2006, 300:349-365. 10.1016/j.ydbio.2006.08.065, 17027739.
63. Boothroyd CE, Dreesen O, Leonova T, Ly KI, Figueiredo LM, Cross GA, Papavasiliou FN. A yeast-endonuclease-generated DNA break induces antigenic switching in Trypanosoma brucei. Nature 2009, 459(7244):278-281. 10.1038/nature07982, 2688456, 19369939.
64. Leister D. Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance gene. Trends in Genetics 2004, 20(3):116-122. 10.1016/j.tig.2004.01.007, 15049302.
65. Li E. Chromatin modification and epigenetic reprogramming in mammalian development. Nature Reviews Genetics 2002, 3:662-673. 10.1038/nrg887, 12209141.
66. Rast JP, Messier-Solek C. Marine invertebrate genome sequences and our evolving understanding of animal immunity. Biological Bulletin 2008, 214:274-283. 10.2307/25470669, 18574104.
67. Gilad Y, Man O, Paabo S, Lancet D. Human specific loss of olfactory receptor genes. Proc Natl Acad Sci USA 2003, 100(6):3324-3327. 10.1073/Proceedings of the National Academy of Sciences.0535697100, 152291, 12612342.
68. Buckley KM, Terwilliger DP, Smith LC. Sequence variations between the 185/333 genes and messages from the purple sea urchin suggest post-transcriptional modifications. Journal of Immunology 2008, 181(12):2203-2212.
69. Brockton V, Henson JH, Raftos DA, Majeske AJ, Kim YO, Smith LC. Localization and diversity of 185/333 proteins from the purple sea urchin - unexpected protein-size range and protein expression in a new coelomocyte type. Journal of Cell Science 2008, 121(3):339-348. 10.1242/jcs.012096, 18198192.