Variant surface antigens of malaria parasites: Functional and evolutionary insights from comparative gene family classification and analysis

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Frech, Christian ^a   Chen, Nansheng ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

Author keywords

Comparative genomics; Gene family classification; Malaria parasites; Plasmodium; Vaccine target; Variant surface antigens

Indexed keywords

CHOLESTEROL; ERYTHROCYTE MEMBRANE PROTEIN 1; PARASITE ANTIGEN; SICAVAR PROTEIN; SURFIN; UNCLASSIFIED DRUG; VARIANT SURFACE ANTIGEN;

ARTICLE; BINDING SITE; CHOLESTEROL TRANSPORT; ERYTHROCYTE MEMBRANE; GENE FUNCTION; GENETIC ANALYSIS; GENETIC CONSERVATION; GENETIC LINKAGE; MULTIGENE FAMILY; NONHUMAN; ORTHOLOGY; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; PLASMODIUM FALCIPARUM; PLASMODIUM GALLINACEUM; PLASMODIUM KNOWLESI; PLASMODIUM VIVAX; PLASMODIUM YOELII; PREDICTION; PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, PROTOZOAN; ANTIGENS, SURFACE; CLUSTER ANALYSIS; CONSERVED SEQUENCE; EVOLUTION, MOLECULAR; GENOMICS; INTRACELLULAR SPACE; LIPID METABOLISM; MALARIA; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLASMODIUM; PROTEIN STRUCTURE, TERTIARY; PROTOZOAN PROTEINS; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRYPTOPHAN;

PLASMODIUM FALCIPARUM; PLASMODIUM PARASITES; RODENTIA;

EID: 84879448168     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-427     Document Type: Article

References (87)

1. WHO World Malaria Report 2010 2010, Geneva, Switzerland: World Health Organization, [http://www.who.int/malaria/world_malaria_report_2010/en/index.html], WHO.
2. Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM. Vivax malaria: neglected and not benign. AmJTrop Med Hyg 2007, 77(6 Suppl):79-87.
3. Antinori S, Galimberti L, Milazzo L, Corbellino M. Plasmodium knowlesi: the emerging zoonotic malaria parasite. Acta Trop 2013, 125(2):191-201. 10.1016/j.actatropica.2012.10.008, 23088834.
4. Olotu A, Fegan G, Wambua J, Nyangweso G, Awuondo KO, Leach A, Lievens M, Leboulleux D, Njuguna P, Peshu N, et al. Four-year efficacy of RTS, S/AS01E and its interaction with malaria exposure. N Engl J Med 2013, 368(12):1111-1120. 10.1056/NEJMoa1207564, 23514288.
5. The RTS SCTP A Phase 3 Trial of RTS,S/AS01 Malaria Vaccine in African Infants. N Engl J Med 2012, 367:2284-2295. http://www.nejm.org/doi/full/10.1056/NEJMoa1208394, 10.1056/NEJMoa1208394, 23136909, The RTS SCTP.
6. Patarroyo MA, Calderon D, Moreno-Perez DA. Vaccines against Plasmodium vivax: a research challenge. Expert Rev Vaccines 2012, 11(10):1249-1260. 10.1586/erv.12.91, 23176656.
7. Carlton JM, Angiuoli SV, Suh BB, Kooij TW, Pertea M, Silva JC, Ermolaeva MD, Allen JE, Selengut JD, Koo HL, et al. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 2002, 419(6906):512-519. 10.1038/nature01099, 12368865.
8. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419(6906):498-511. 10.1038/nature01097, 12368864.
9. Hall N, Karras M, Raine JD, Carlton JM, Kooij TW, Berriman M, Florens L, Janssen CS, Pain A, Christophides GK, et al. A comprehensive survey of the Plasmodium life cycle by genomic, transcriptomic, and proteomic analyses. Science 2005, 307(5706):82-86. 10.1126/science.1103717, 15637271.
10. Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H, Caler E, Crabtree J, Angiuoli SV, Merino EF, Amedeo P, et al. Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 2008, 455(7214):757-763. 10.1038/nature07327, 2651158, 18843361.
11. Pain A, Bohme U, Berry AE, Mungall K, Finn RD, Jackson AP, Mourier T, Mistry J, Pasini EM, Aslett MA, et al. The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature 2008, 455(7214):799-803. 10.1038/nature07306, 2656934, 18843368.
12. Frech C, Chen N. Genome comparison of human and non-human malaria parasites reveals species subset-specific genes potentially linked to human disease. PLoS Comput Biol 2011, 7(12):e1002320. 10.1371/journal.pcbi.1002320, 3245289, 22215999.
13. Recker M, Buckee CO, Serazin A, Kyes S, Pinches R, Christodoulou Z, Springer AL, Gupta S, Newbold CI. Antigenic variation in Plasmodium falciparum malaria involves a highly structured switching pattern. PLoS Pathog 2011, 7(3):e1001306. 10.1371/journal.ppat.1001306, 3048365, 21408201.
14. Cunningham D, Lawton J, Jarra W, Preiser P, Langhorne J. The pir multigene family of Plasmodium: antigenic variation and beyond. Mol Biochem Parasitol 2010, 170(2):65-73. 10.1016/j.molbiopara.2009.12.010, 20045030.
15. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, Peterson DS, Ravetch JA, Wellems TE. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 1995, 82(1):89-100. 10.1016/0092-8674(95)90055-1, 7606788.
16. Cheng Q, Cloonan N, Fischer K, Thompson J, Waine G, Lanzer M, Saul A. stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol Biochem Parasitol 1998, 97(1-2):161-176.
17. Winter G, Kawai S, Haeggstrom M, Kaneko O, Von Euler A, Kawazu S, Palm D, Fernandez V, Wahlgren M. SURFIN is a polymorphic antigen expressed on Plasmodium falciparum merozoites and infected erythrocytes. J Exp Med 2005, 201(11):1853-1863. 10.1084/jem.20041392, 2213267, 15939796.
18. Sam-Yellowe TY, Florens L, Johnson JR, Wang T, Drazba JA, Le Roch KG, Zhou Y, Batalov S, Carucci DJ, Winzeler EA, et al. A Plasmodium gene family encoding Maurer's cleft membrane proteins: structural properties and expression profiling. Genome Res 2004, 14(6):1052-1059. 10.1101/gr.2126104, 419783, 15140830.
19. Del Portillo HA, Fernandez-Becerra C, Bowman S, Oliver K, Preuss M, Sanchez CP, Schneider NK, Villalobos JM, Rajandream MA, Harris D, et al. A superfamily of variant genes encoded in the subtelomeric region of Plasmodium vivax. Nature 2001, 410(6830):839-842. 10.1038/35071118, 11298455.
20. Janssen CS, Phillips RS, Turner CM, Barrett MP. Plasmodium interspersed repeats: the major multigene superfamily of malaria parasites. Nucleic Acids Res 2004, 32(19):5712-5720. 10.1093/nar/gkh907, 528792, 15507685.
21. Janssen CS, Barrett MP, Turner CM, Phillips RS. A large gene family for putative variant antigens shared by human and rodent malaria parasites. Proceedings 2002, 269(1489):431-436.
22. Al-Khedery B, Barnwell JW, Galinski MR. Antigenic variation in malaria: a 3′ genomic alteration associated with the expression of a P. knowlesi variant antigen. Mol Cell 1999, 3(2):131-141. 10.1016/S1097-2765(00)80304-4, 10078196.
23. Sargeant TJ, Marti M, Caler E, Carlton JM, Simpson K, Speed TP, Cowman AF. Lineage-specific expansion of proteins exported to erythrocytes in malaria parasites. Genome Biol 2006, 7(2):R12. 10.1186/gb-2006-7-2-r12, 1431722, 16507167.
24. Hiller NL, Bhattacharjee S, Van Ooij C, Liolios K, Harrison T, Lopez-Estrano C, Haldar K. A host-targeting signal in virulence proteins reveals a secretome in malarial infection. Science 2004, 306(5703):1934-1937. 10.1126/science.1102737, 15591203.
25. Marti M, Good RT, Rug M, Knuepfer E, Cowman AF. Targeting malaria virulence and remodeling proteins to the host erythrocyte. Science 2004, 306(5703):1930-1933. 10.1126/science.1102452, 15591202.
26. Frech C, Chen N. Genome-wide comparative gene family classification. PLoS One 2010, 5(10):e13409. 10.1371/journal.pone.0013409, 2955529, 20976221.
27. Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 2009, 37:D539-D543. Database issue, 10.1093/nar/gkn814, 2686598, 18957442.
28. Loewenstein Y, Portugaly E, Fromer M, Linial M. Efficient algorithms for accurate hierarchical clustering of huge datasets: tackling the entire protein space. Bioinformatics 2008, 24(13):i41-i49. 10.1093/bioinformatics/btn174, 2718652, 18586742.
29. Chen F, Mackey AJ, Stoeckert CJ, Roos DS. OrthoMCL-DB: querying a comprehensive multi-species collection of ortholog groups. Nucleic Acids Res 2006, 34:D363-D368. Database issue, 10.1093/nar/gkj123, 1347485, 16381887.
30. Finn RD, Clements J, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Res 2011, 39:W29-W37. Web Server issue, 10.1093/nar/gkr367, 3125773, 21593126.
31. Anantharaman V, Iyer LM, Balaji S, Aravind L. Adhesion molecules and other secreted host-interaction determinants in Apicomplexa: insights from comparative genomics. Int Rev Cytol 2007, 262:1-74.
32. Wasmuth J, Daub J, Peregrin-Alvarez JM, Finney CA, Parkinson J. The origins of apicomplexan sequence innovation. Genome Res 2009, 19(7):1202-1213. 10.1101/gr.083386.108, 2704437, 19363216.
33. Gough J, Karplus K, Hughey R, Chothia C. Assignment of homology to genome sequences using a library of hidden Markov models that represent all proteins of known structure. J Mol Biol 2001, 313(4):903-919. 10.1006/jmbi.2001.5080, 11697912.
34. Loewenstein Y, Linial M. Connect the dots: exposing hidden protein family connections from the entire sequence tree. Bioinformatics 2008, 24(16):i193-i199. 10.1093/bioinformatics/btn301, 18689824.
35. Lavazec C, Sanyal S, Templeton TJ. Expression switching in the stevor and Pfmc-2TM superfamilies in Plasmodium falciparum. Mol Microbiol 2007, 64(6):1621-1634. 10.1111/j.1365-2958.2007.05767.x, 17555442.
36. Tsarukyanova I, Drazba JA, Fujioka H, Yadav SP, Sam-Yellowe TY. Proteins of the Plasmodium falciparum two transmembrane Maurer's cleft protein family, PfMC-2TM, and the 130 kDa Maurer's cleft protein define different domains of the infected erythrocyte intramembranous network. Parasitol Res 2009, 104(4):875-891. 10.1007/s00436-008-1270-3, 19130087.
37. Kall L, Krogh A, Sonnhammer EL. Advantages of combined transmembrane topology and signal peptide prediction--the Phobius web server. Nucleic Acids Res 2007, 35:W429-W432. Web Server issue, 10.1093/nar/gkm256, 1933244, 17483518.
38. Merino EF, Fernandez-Becerra C, Durham AM, Ferreira JE, Tumilasci VF, D'Arc-Neves J, Da Silva-Nunes M, Ferreira MU, Wickramarachchi T, Udagama-Randeniya P, et al. Multi-character population study of the vir subtelomeric multigene superfamily of Plasmodium vivax, a major human malaria parasite. Mol Biochem Parasitol 2006, 149(1):10-16. 10.1016/j.molbiopara.2006.04.002, 16730808.
39. Waller KL, Cooke BM, Nunomura W, Mohandas N, Coppel RL. Mapping the binding domains involved in the interaction between the Plasmodium falciparum knob-associated histidine-rich protein (KAHRP) and the cytoadherence ligand P. falciparum erythrocyte membrane protein 1 (PfEMP1). J Biol Chem 1999, 274(34):23808-23813. 10.1074/jbc.274.34.23808, 10446142.
40. Mayer C, Slater L, Erat MC, Konrat R, Vakonakis I. Structural analysis of the Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) intracellular domain reveals a conserved interaction epitope. J Biol Chem 2012, 287(10):7182-7189. 10.1074/jbc.M111.330779, 3293552, 22249178.
41. Fernandez-Becerra C, Yamamoto MM, Vencio RZ, Lacerda M, Rosanas-Urgell A, Del Portillo HA. Plasmodium vivax and the importance of the subtelomeric multigene vir superfamily. Trends Parasitol 2009, 25(1):44-51. 10.1016/j.pt.2008.09.012, 19036639.
42. Neafsey DE, Galinsky K, Jiang RH, Young L, Sykes SM, Saif S, Gujja S, Goldberg JM, Young S, Zeng Q, et al. The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. Nat Genet 2012, 44(9):1046-1050. 10.1038/ng.2373, 3432710, 22863733.
43. Bozdech Z, Mok S, Hu G, Imwong M, Jaidee A, Russell B, Ginsburg H, Nosten F, Day NP, White NJ, et al. The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proc Natl Acad Sci USA 2008, 105(42):16290-16295. 10.1073/pnas.0807404105, 2571024, 18852452.
44. Bustamante LY, Bartholdson SJ, Crosnier C, Campos MG, Wanaguru M, Nguon C, Kwiatkowski DP, Wright GJ, Rayner JC. A full-length recombinant Plasmodium falciparum PfRH5 protein induces inhibitory antibodies that are effective across common PfRH5 genetic variants. Vaccine 2012,
45. Crosnier C, Bustamante LY, Bartholdson SJ, Bei AK, Theron M, Uchikawa M, Mboup S, Ndir O, Kwiatkowski DP, Duraisingh MT, et al. Basigin is a receptor essential for erythrocyte invasion by Plasmodium falciparum. Nature 2011, 480(7378):534-537. 3245779, 22080952.
46. Kemp DJ, Coppel RL, Anders RF. Repetitive proteins and genes of malaria. Annu Rev Microbiol 1987, 41:181-208. 10.1146/annurev.mi.41.100187.001145, 3318667.
47. Scherf A, Lopez-Rubio JJ, Riviere L. Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 2008, 62:445-470. 10.1146/annurev.micro.61.080706.093134, 18785843.
48. Wiser MF, Giraldo LE, Schmitt-Wrede HP, Wunderlich F. Plasmodium chabaudi: immunogenicity of a highly antigenic glutamate-rich protein. Exp Parasitol 1997, 85(1):43-54. 10.1006/expr.1996.4126, 9024201.
49. Wunderlich F, Brenner HH, Helwig M. Plasmodium chabaudi malaria: protective immunization with surface membranes of infected erythrocytes. Infect Immun 1988, 56(12):3326-3328. 259746, 3182084.
50. Wunderlich F, Helwig M, Schillinger G, Speth V, Wiser MF. Expression of the parasite protein Pc90 in plasma membranes of erythrocytes infected with Plasmodium chabaudi. Eur J Cell Biol 1988, 47(2):157-164.
51. Fonager J, Pasini EM, Braks JA, Klop O, Ramesar J, Remarque EJ, Vroegrijk IO, Van Duinen SG, Thomas AW, Khan SM, et al. Reduced CD36-dependent tissue sequestration of Plasmodium-infected erythrocytes is detrimental to malaria parasite growth in vivo. J Exp Med 2012, 209(1):93-107. 10.1084/jem.20110762, 3260870, 22184632.
52. Cernetich-Ott A, Daly TM, Vaidya AB, Bergman LW, Burns JM. Remarkable stability in patterns of blood-stage gene expression during episodes of non-lethal Plasmodium yoelii malaria. Malar J 2012, 11(1):265. 10.1186/1475-2875-11-265, 3489522, 22866913.
53. Clark BJ, Wells J, King SR, Stocco DM. The purification, cloning, and expression of a novel luteinizing hormone-induced mitochondrial protein in MA-10 mouse Leydig tumor cells. Characterization of the steroidogenic acute regulatory protein (StAR). J Biol Chem 1994, 269(45):28314-28322.
54. Liu J, Rone MB, Papadopoulos V. Protein-protein interactions mediate mitochondrial cholesterol transport and steroid biosynthesis. J Biol Chem 2006, 281(50):38879-38893. 10.1074/jbc.M608820200, 17050526.
55. Sherman IW. Biochemistry of Plasmodium (malarial parasites). Microbiol Rev 1979, 43(4):453-495. 281489, 94424.
56. Maguire PA, Sherman IW. Phospholipid composition, cholesterol content and cholesterol exchange in Plasmodium falciparum-infected red cells. Mol Biochem Parasitol 1990, 38(1):105-112. 10.1016/0166-6851(90)90210-D, 2157152.
57. Sein KK, Aikawa M. The prime role of plasma membrane cholesterol in the pathogenesis of immune evasion and clinical manifestations of falciparum malaria. Medical hypotheses 1998, 51(2):105-110. 10.1016/S0306-9877(98)90102-5, 9881815.
58. Deleersnijder W, Prasomsitti P, Tungpradubkul S, Hendrix D, Hamers-Casterman C, Hamers R. Structure of a Plasmodium chabaudi acidic phosphoprotein that is associated with the host erythrocyte membrane. Mol Biochem Parasitol 1992, 56(1):59-68. 10.1016/0166-6851(92)90154-C, 1475002.
59. Templeton TJ. The varieties of gene amplification, diversification and hypervariability in the human malaria parasite, Plasmodium falciparum. Mol Biochem Parasitol 2009, 166(2):109-116. 10.1016/j.molbiopara.2009.04.003, 19375460.
60. Lavazec C, Sanyal S, Templeton TJ. Hypervariability within the Rifin, Stevor and Pfmc-2TM superfamilies in Plasmodium falciparum. Nucleic Acids Res 2006, 34(22):6696-6707. 10.1093/nar/gkl942, 1751529, 17148488.
61. Korir CC, Galinski MR. Proteomic studies of Plasmodium knowlesi SICA variant antigens demonstrate their relationship with P. falciparum EMP1. Infect Genet Evol 2006, 6(1):75-79. 10.1016/j.meegid.2005.01.003, 16376842.
62. Hora R, Bridges DJ, Craig A, Sharma A. Erythrocytic casein kinase II regulates cytoadherence of Plasmodium falciparum-infected red blood cells. J Biol Chem 2009, 284(10):6260-6269. 2649111, 19131328.
63. Oh SS, Voigt S, Fisher D, Yi SJ, LeRoy PJ, Derick LH, Liu S, Chishti AH. Plasmodium falciparum erythrocyte membrane protein 1 is anchored to the actin-spectrin junction and knob-associated histidine-rich protein in the erythrocyte skeleton. Mol Biochem Parasitol 2000, 108(2):237-247. 10.1016/S0166-6851(00)00227-9, 10838226.
64. Voigt S, Hanspal M, LeRoy PJ, Zhao PS, Oh SS, Chishti AH, Liu SC. The cytoadherence ligand Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) binds to the P. falciparum knob-associated histidine-rich protein (KAHRP) by electrostatic interactions. Mol Biochem Parasitol 2000, 110(2):423-428. 10.1016/S0166-6851(00)00281-4, 11071296.
65. Waller KL, Nunomura W, Cooke BM, Mohandas N, Coppel RL. Mapping the domains of the cytoadherence ligand Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) that bind to the knob-associated histidine-rich protein (KAHRP). Mol Biochem Parasitol 2002, 119(1):125-129. 10.1016/S0166-6851(01)00395-4, 11755194.
66. Glenister FK, Fernandez KM, Kats LM, Hanssen E, Mohandas N, Coppel RL, Cooke BM. Functional alteration of red blood cells by a megadalton protein of Plasmodium falciparum. Blood 2009, 113(4):919-928. 10.1182/blood-2008-05-157735, 2630277, 18832660.
67. Hodder AN, Maier AG, Rug M, Brown M, Hommel M, Pantic I, Puig-de-Morales-Marinkovic M, Smith B, Triglia T, Beeson J, et al. Analysis of structure and function of the giant protein Pf332 in Plasmodium falciparum. Mol Microbiol 2009, 71(1):48-65. 10.1111/j.1365-2958.2008.06508.x, 2680261, 19007413.
68. Waller KL, Stubberfield LM, Dubljevic V, Buckingham DW, Mohandas N, Coppel RL, Cooke BM. Interaction of the exported malaria protein Pf332 with the red blood cell membrane skeleton. Biochim Biophys Acta 2010, 1798(5):861-871. 10.1016/j.bbamem.2010.01.018, 20132790.
69. Benian GM, Kiff JE, Neckelmann N, Moerman DG, Waterston RH. Sequence of an unusually large protein implicated in regulation of myosin activity in C. elegans. Nature 1989, 342(6245):45-50. 10.1038/342045a0, 2812002.
70. She R, Chu JS, Uyar B, Wang J, Wang K, Chen N. genBlastG: using BLAST searches to build homologous gene models. Bioinformatics 2011, 27(15):2141-2143. 10.1093/bioinformatics/btr342, 21653517.
71. Uyar B, Chu JS, Vergara IA, Chua SY, Jones MR, Wong T, Baillie DL, Chen N. RNA-seq analysis of the C. briggsae transcriptome. Genome Res 2012, 22(8):1567-1580. 10.1101/gr.134601.111, 3409270, 22772596.
72. Birney E, Clamp M, Durbin R. GeneWise and Genomewise. Genome Res 2004, 14(5):988-995. 10.1101/gr.1865504, 479130, 15123596.
73. Frith MC. A new repeat-masking method enables specific detection of homologous sequences. Nucleic Acids Res 2011, 39(4):e23. 10.1093/nar/gkq1212, 3045581, 21109538.
74. Thompson JD, Gibson TJ, Higgins DG, et al. Multiple sequence alignment using ClustalW and ClustalX. Current protocols in bioinformatics 2002, Baxevanis AD, Chapter 2:Unit 2 3.
75. Di Tommaso P, Moretti S, Xenarios I, Orobitg M, Montanyola A, Chang JM, Taly JF, Notredame C. T-Coffee: a web server for the multiple sequence alignment of protein and RNA sequences using structural information and homology extension. Nucleic Acids Res 2011, 39:W13-W17. Web Server issue), 10.1093/nar/gkr245, 3125728, 21558174.
76. Nicholas KB, Nicholas HB, Deerfield DW. GeneDoc: Analysis and Visualization of Genetic Variation. EMBNEW.NEWS 1997, 4:14. http://www.nrbsc.org/gfx/genedoc/gdfeedb.htm.
77. Eddy SR. Accelerated Profile HMM Searches. PLoS Comput Biol 2011, 7(10):e1002195. 10.1371/journal.pcbi.1002195, 3197634, 22039361.
78. Wilson D, Pethica R, Zhou Y, Talbot C, Vogel C, Madera M, Chothia C, Gough J. SUPERFAMILY--sophisticated comparative genomics, data mining, visualization and phylogeny. Nucleic Acids Res 2009, 37:D380-D386. Database issue, 10.1093/nar/gkn762, 2686452, 19036790.
79. Frech C, Choo C, Chen N. FeatureStack: Perl module for comparative visualization of gene features. Bioinformatics 2012, 28(23):3137-3138. 10.1093/bioinformatics/bts572, 23023981.
80. Roy A, Kucukural A, Zhang Y. I-TASSER: a unified platform for automated protein structure and function prediction. Nat Protoc 2010, 5(4):725-738. 10.1038/nprot.2010.5, 2849174, 20360767.
81. Zhang Y. I-TASSER server for protein 3D structure prediction. BMC Bioinforma 2008, 9:40.
82. Zhang Y, Skolnick J. TM-align: a protein structure alignment algorithm based on the TM-score. Nucleic Acids Res 2005, 33(7):2302-2309. 10.1093/nar/gki524, 1084323, 15849316.
83. Krogh A, Larsson B, Von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001, 305(3):567-580. 10.1006/jmbi.2000.4315, 11152613.
84. Cole C, Barber JD, Barton GJ. The Jpred 3 secondary structure prediction server. Nucleic Acids Res 2008, 36:W197-W201. Web Server issue, 10.1093/nar/gkn238, 2447793, 18463136.
85. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28(10):2731-2739. 10.1093/molbev/msr121, 3203626, 21546353.
86. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K, et al. The Pfam protein families database. Nucleic Acids Res 2010, 38:D211-D222. Database issue, 10.1093/nar/gkp985, 2808889, 19920124.
87. Carlton JM, Escalante AA, Neafsey D, Volkman SK. Comparative evolutionary genomics of human malaria parasites. Trends Parasitol 2008, 24(12):545-550. 10.1016/j.pt.2008.09.003, 18938107.