Novel transglutaminase-like peptidase and C2 domains elucidate the structure, biogenesis and evolution of the ciliary compartment

Cell Cycle

Volumn 11, Issue 20, 2012, Pages 3861-3875

  Zhang, Dapeng ^a   Aravind, L ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

C2; Ciliogenesis; Ciliopathy; Evolution; Membrane; Origin of eukaryotes; Transglutaminase like; Transition zone; Tubulin tyrosine ligase; Y shaped linkers

Indexed keywords

EID: 84868028170     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.22068     Document Type: Article

References (85)

1. Dentler WL. Microtubule-membrane interactions in cilia and flagella. Int Rev Cytol 1981;72:1-47; PMID:7019129; http://dx.doi.org/10.1016/S0074-7696 (08) 61193-6. (Pubitemid 11043386)
2. Singla V, Reiter J F. The primary cilium as the cell's antenna: signaling at a sensory organelle. Science 2006;313:629-33; PMID:16888132; http://dx.doi.org/10.1126/science.1124534. (Pubitemid 44201133)
3. Goetz SC, Anderson K V. The primary cilium: a signalling centre during vertebrate development. Nat Rev Genet 2010;11:331-44; PMID:20395968; http://dx.doi.org/10.1038/nrg2774.
4. Li JB, Gerdes JM, Haycraft CJ, Fan Y, Teslovich TM, May-Simera H, et al. Comparative genomics identifies a flagellar and basal body proteome that includes the BBS5 human disease gene. Cell 2004;117:541-52; PMID:15137946; http://dx.doi.org/10.1016/S0092-8674 (04) 00450-7. (Pubitemid 38610238)
5. Kim J, Lee JE, Heynen-Genel S, Suyama E, Ono K, Lee K, et al. Functional genomic screen for modulators of ciliogenesis and cilium length. Nature 2010;464:1048-51; PMID:20393563; http://dx.doi.org/10.1038/nature08895.
6. Czarnecki PG, Shah JV. The ciliary transition zone: from morphology and molecules to medicine. Trends Cell Biol 2012;22:201-10; PMID:22401885; http://dx.doi.org/10.1016/j.tcb.2012.02.001.
7. Heuser T, Raytchev M, Krell J, Porter ME, Nicastro D. The dynein regulatory complex is the nexin link and a major regulatory node in cilia and flagella. J Cell Biol 2009;187:921-33; PMID:20008568; http://dx.doi.org/10.1083/ jcb.200908067.
8. Hu Q, Milenkovic L, Jin H, Scott M P, Nachury MV, Spiliotis ET, et al. A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 2010;329:436-9; PMID:20558667; http://dx.doi.org/10.1126/sci-ence.1191054.
9. Kim SK, Shindo A, Park TJ, Oh EC, Ghosh S, Gray RS, et al. Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 2010;329:1337-40; PMID:20671153; http://dx.doi.org/10. 1126/science.1191184.
10. Janke C, Rogowski K, Wloga D, Regnard C, Kajava AV, Strub JM, et al. Tubulin polyglutamylase enzymes are members of the TTL domain protein family. Science 2005;308:1758-62; PMID:15890843; http://dx.doi.org/10.1126/science. 1113010. (Pubitemid 40847998)
11. Jin H, Nachury MV. The BBSome. Curr Biol 2009;19:R472-3; PMID:19549489.
12. Rosenbaum JL, Witman GB. Intraflagellar transport. Nat Rev Mol Cell Biol 2002;3:813-25; PMID:12415299; http://dx.doi.org/10.1038/nrm952. (Pubitemid 35285272)
13. Taschner M, Bhogaraju S, Lorentzen E. Architecture and function of IFT complex proteins in ciliogenesis. Differentiation 2012;83:S12-22; PMID:22118932.
14. Sang L, Miller JJ, Corbit KC, Giles RH, Brauer MJ, Otto EA, et al. Mapping the NPHP-JBTS-MKS protein network reveals ciliopathy disease genes and pathways. Cell 2011;145:513-28; PMID:21565611; http://dx.doi.org/10.1016/j.cell. 2011.04.019.
15. Williams CL, Li C, Kida K, Inglis PN, Mohan S, Semenec L, et al. MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. J Cell Biol 2011;192:1023-41; PMID:21422230; http://dx.doi.org/10.1083/jcb.201012116.
16. Chih B, Liu P, Chinn Y, Chalouni C, Komuves LG, Hass PE, et al. A ciliopathy complex at the transition zone protects the cilia as a privileged membrane domain. Nat Cell Biol 2012;14:61-72; PMID:22179047; http://dx.doi.org/10.1038/ncb2410.
17. Garcia-Gonzalo FR, Corbit KC, Sirerol-Piquer MS, Ramaswami G, Otto EA, Noriega TR, et al. A transition zone complex regulates mammalian ciliogen-esis and ciliary membrane composition. Nat Genet 2011;43:776-84; PMID:21725307; http://dx.doi.org/10.1038/ng.891.
18. Reiter J F, Blacque OE, Leroux MR. The base of the cili-um: roles for transition fibres and the transition zone in ciliary formation, maintenance and compartmentaliza-tion. EMBO Rep 2012;13:608-18; PMID:22653444; http://dx.doi.org/10.1038/embor.2012.73.
19. Silverman MA, Leroux MR. Intraflagellar transport and the generation of dynamic, structurally and functionally diverse cilia. Trends Cell Biol 2009;19:306-16; PMID:19560357; http://dx.doi.org/10.1016/j. tcb.2009.04.002.
20. Zhao C, Malicki J. Nephrocystins and MKS proteins interact with IFT particle and facilitate transport of selected ciliary cargos. EMBO J 2011;30:2532-44; PMID:21602787; http://dx.doi.org/10.1038/emboj.2011.165.
21. Dawe HR, Smith UM, Cullinane AR, Gerrelli D, Cox P, Badano JL, et al. The Meckel-Gruber Syndrome proteins MKS1 and meckelin interact and are required for primary cilium formation. Hum Mol Genet 2007;16:173-86; PMID:17185389; http://dx.doi.org/10.1093/hmg/ddl459. (Pubitemid 46179000)
22. Jauregui AR, Nguyen KC, Hall DH, Barr MM. The Caenorhabditis elegans nephrocystins act as global modifiers of cilium structure. J Cell Biol 2008;180:973-88; PMID:18316409; http://dx.doi.org/10.1083/jcb.200707090. (Pubitemid 351398423)
23. Ou G, Blacque OE, Snow JJ, Leroux MR, Scholey JM. Functional coordination of intraflagellar transport motors. Nature 2005;436:583-7; PMID:16049494; http://dx.doi.org/10.1038/nature03818. (Pubitemid 41112934)
24. Lechtreck K F, Johnson EC, Sakai T, Cochran D, Ballif BA, Rush J, et al. The Chlamydomonas rein-hardtii BBSome is an IFT cargo required for export of specific signaling proteins from flagella. J Cell Biol 2009;187:1117-32; PMID:20038682; http://dx.doi.org/10.1083/jcb.200909183.
25. Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AG, et al. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic "supergroups". Proc Natl Acad Sci USA 2009;106:3859-64; PMID:19237557; http://dx.doi.org/10.1073/pnas.0807880106.
26. Hodges ME, Scheumann N, Wickstead B, Langdale JA, Gull K. Reconstructing the evolutionary history of the centriole from protein components. J Cell Sci 2010;123:1407-13; PMID:20388734; http://dx.doi.org/10.1242/jcs.064873.
27. Carvalho-Santos Z, Azimzadeh J, Pereira-Leal JB, Bettencourt-Dias M. Evolution: Tracing the origins of centrioles, cilia, and flagella. J Cell Biol 2011;194:165-75; PMID:21788366; http://dx.doi.org/10.1083/jcb.201011152.
28. Jin H, White SR, Shida T, Schulz S, Aguiar M, Gygi S P, et al. The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 2010;141:1208-19; PMID:20603001; http://dx.doi.org/10. 1016/j.cell.2010.05.015.
29. Jékely G. Small GTPases and the evolution of the eukaryotic cell. Bioessays 2003;25:1129-38; PMID:14579253. (Pubitemid 37411772)
30. Mans BJ, Anantharaman V, Aravind L, Koonin EV. Comparative genomics, evolution and origins of the nuclear envelope and nuclear pore complex. Cell Cycle 2004;3:1612-37; PMID:15611647; http://dx.doi.org/10.4161/cc.3.12.1316. (Pubitemid 40521416)
31. Jékely G, Arendt D. Evolution of intraflagellar transport from coated vesicles and autogenous origin of the eukaryotic cilium. Bioessays 2006;28:191-8; PMID:16435301.
32. Kee HL, Dishinger J F, Blasius TL, Liu CJ, Margolis B, Verhey KJ. A size-exclusion permeability barrier and nucleoporins characterize a ciliary pore complex that regulates transport into cilia. Nat Cell Biol 2012;14:431-7; PMID:22388888; http://dx.doi.org/10.1038/ncb2450.
33. Obado SO, Rout M P. Ciliary and nuclear transport: different places, similar routes? Dev Cell 2012;22:693-4; PMID:22516195; http://dx.doi.org/10. 1016/j.dev-cel.2012.04.002.
34. Iyer LM, Leipe DD, Koonin EV, Aravind L. Evolutionary history and higher order classification of AAA+ ATPases. J Struct Biol 2004;146:11-31; PMID:15037234; http://dx.doi.org/10.1016/j. jsb.2003.10.010. (Pubitemid 38369015)
35. Leipe DD, Wolf YI, Koonin EV, Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J Mol Biol 2002;317:41-72; PMID:11916378; http://dx.doi.org/10.1006/jmbi.2001.5378. (Pubitemid 34722199)
36. Yutin N, Koonin EV. Archaeal origin of tubulin. Biol Direct 2012;7:10; PMID:22458654; http://dx.doi.org/10.1186/1745-6150-7-10.
37. Zhang D, Aravind L. Identification of novel families and classification of the C2 domain superfamily elucidate the origin and evolution of membrane targeting activities in eukaryotes. Gene 2010;469:18-30; PMID:20713135; http://dx.doi.org/10.1016/j. gene.2010.08.006.
38. Beatson S, Ponting C P. GIFT domains: linking eukary-otic intraflagellar transport and glycosylation to bacterial gliding. Trends Biochem Sci 2004;29:396-9; PMID:15288869; http://dx.doi.org/10.1016/j. tibs.2004.06.002. (Pubitemid 39061083)
39. Wan H, Li L, Federhen S, Wootton JC. Discovering simple regions in biological sequences associated with scoring schemes. J Comput Biol 2003;10:171-85; PMID:12804090; http://dx.doi.org/10.1089/106652703321825955. (Pubitemid 36623538)
40. Tallila J, Jakkula E, Peltonen L, Salonen R, Kestilä M. Identification of CC2D2A as a Meckel syndrome gene adds an important piece to the ciliopathy puzzle. Am J Hum Genet 2008;82:1361-7; PMID:18513680; http://dx.doi.org/10.1016/j.ajhg.2008.05.004.
41. Tsang WY, Spektor A, Vijayakumar S, Bista BR, Li J, Sanchez I, et al. Cep76, a centrosomal protein that specifically restrains centriole reduplication. Dev Cell 2009;16:649-60; PMID:19460342; http://dx.doi.org/10. 1016/j.devcel.2009.03.004.
42. Yang Y, Cochran DA, Gargano MD, King I, Samhat NK, Burger B P, et al. Regulation of flagellar motil-ity by the conserved flagellar protein CG34110/Ccdc135/FAP50. Mol Biol Cell 2011;22:976-87; PMID:21289096; http://dx.doi.org/10.1091/mbc. E10-04-0331.
43. Anantharaman V, Aravind L. Evolutionary history, structural features and biochemical diversity of the NlpC/P60 superfamily of enzymes. Genome Biol 2003;4:R11; PMID:12620121; http://dx.doi.org/10.1186/gb-2003-4-2-r11.
44. Anantharaman V, Koonin E V, Aravind L. Peptide-N-glycanases and DNA repair proteins, Xp-C/Rad4, are, respectively, active and inactivated enzymes sharing a common transglutaminase fold. Hum Mol Genet 2001;10:1627-30; PMID:11487565; http://dx.doi.org/10.1093/hmg/10.16.1627. (Pubitemid 32776291)
45. Iyer LM, Anantharaman V, Wolf MY, Aravind L. Comparative genomics of transcription factors and chromatin proteins in parasitic protists and other eukaryotes. Int J Parasitol 2008;38:1-31; PMID:17949725; http://dx.doi.org/10. 1016/j.ijpa-ra.2007.07.018. (Pubitemid 350251386)
46. Huang J, Gurung B, Wan B, Matkar S, Veniaminova NA, Wan K, et al. The same pocket in menin binds both MLL and JUND but has opposite effects on transcription. Nature 2012;482:542-6; PMID:22327296; http://dx.doi.org/10.1038/ nature10806.
47. Murai MJ, Chruszcz M, Reddy G, Grembecka J, Cierpicki T. Crystal structure of menin reveals binding site for mixed lineage leukemia (MLL) protein. J Biol Chem 2011;286:31742-8; PMID:21757704; http://dx.doi.org/10.1074/ jbc. M111.258186.
48. Hodder AN, Drew DR, Epa VC, Delorenzi M, Bourgon R, Miller SK, et al. Enzymic, phyloge-netic, and structural characterization of the unusual papain-like protease domain of Plasmodium falci-parum SERA5. J Biol Chem 2003;278:48169-77; PMID:13679369; http://dx.doi.org/10.1074/jbc. M306755200. (Pubitemid 37523270)
49. Snider J, Houry WA. MoxR AAA+ ATPases: a novel family of molecular chaperones? J Struct Biol 2006;156:200-9; PMID:16677824; http://dx.doi.org/10. 1016/j.jsb.2006.02.009. (Pubitemid 44488671)
50. Ulbrich C, Diepholz M, Bassler J, Kressler D, Pertschy B, Galani K, et al. Mechanochemical removal of ribo-some biogenesis factors from nascent 60S ribosomal subunits. Cell 2009;138:911-22; PMID:19737519; http://dx.doi.org/10. 1016/j.cell.2009.06.045.
51. Scheele U, Erdmann S, Ungewickell EJ, Felisberto-Rodrigues C, Ortiz-Lombardía M, Garrett RA. Chaperone role for proteins p618 and p892 in the extracellular tail development of Acidianus two-tailed virus. J Virol 2011;85:4812-21; PMID:21367903; http://dx.doi.org/10.1128/JVI.00072-11.
52. Iyer LM, Abhiman S, Maxwell Burroughs A, Aravind L. Amidoligases with ATP-grasp, glutamine synthetase-like and acetyltransferase-like domains: synthesis of novel metabolites and peptide modifications of proteins. Mol Biosyst 2009;5:1636-60; PMID:20023723; http://dx.doi.org/10.1039/b917682a.
53. Alexeyenko A, Schmitt T, Tjärnberg A, Guala D, Frings O, Sonnhammer EL. Comparative interac-tomics with Funcoup 2.0. Nucleic Acids Res 2012;40(Database issue):D821-8; PMID:22110034; http://dx.doi.org/10.1093/nar/ gkr1062.
54. Dowdle WE, Robinson J F, Kneist A, Sirerol-Piquer MS, Frints SG, Corbit KC, et al. Disruption of a ciliary B9 protein complex causes Meckel syndrome. Am J Hum Genet 2011;89:94-110; PMID:21763481; http://dx.doi.org/10.1016/j.ajhg. 2011.06.003.
55. Arts HH, Doherty D, van Beersum SE, Parisi MA, Letteboer SJ, Gorden N T, et al. Mutations in the gene encoding the basal body protein RPGRIP1L, a nephrocystin-4 interactor, cause Joubert syndrome. Nat Genet 2007;39:882-8; PMID:17558407; http://dx.doi.org/10.1038/ng2069. (Pubitemid 47014499)
56. Parisi MA, Bennett CL, Eckert ML, Dobyns WB, Gleeson JG, Shaw DW, et al. The NPHP1 gene deletion associated with juvenile nephronophthisis is present in a subset of individuals with Joubert syndrome. Am J Hum Genet 2004;75:82-91; PMID:15138899; http://dx.doi.org/10.1086/421846. (Pubitemid 38801903)
57. Wiik AC, Wade C, Biagi T, Ropstad EO, Bjerkås E, Lindblad-Toh K, et al. A deletion in nephronophthisis 4 (NPHP4) is associated with recessive cone-rod dystrophy in standard wire-haired dachshund. Genome Res 2008;18:1415-21; PMID:18687878; http://dx.doi.org/10.1101/gr.074302.107.
58. Hoover AN, Wynkoop A, Zeng H, Jia J, Niswander LA, Liu A. C2cd3 is required for cilia formation and Hedgehog signaling in mouse. Development 2008;135:4049-58; PMID:19004860; http://dx.doi.org/10.1242/dev. 029835.
59. Dixon-Salazar T, Silhavy JL, Marsh SE, Louie CM, Scott LC, Gururaj A, et al. Mutations in the AHI1 gene, encoding jouberin, cause Joubert syndrome with cortical polymicrogyria. Am J Hum Genet 2004;75:979-87; PMID:15467982; http://dx.doi.org/10.1086/425985. (Pubitemid 39532068)
60. Anantharaman V, Iyer LM, Aravind L. Comparative genomics of protists: new insights into the evolution of eukaryotic signal transduction and gene regulation. Annu Rev Microbiol 2007;61:453-75; PMID:17506670; http://dx.doi.org/10.1146/annurev. micro.61.080706.093309. (Pubitemid 350058217)
61. Seo S, Baye LM, Schulz N P, Beck JS, Zhang Q, Slusarski DC, et al. BBS6, BBS10, and BBS12 form a complex with CCT/TRiC family chaperonins and mediate BBSome assembly. Proc Natl Acad Sci USA 2010;107:1488-93; PMID:20080638; http://dx.doi.org/10.1073/pnas.0910268107.
62. Doré AS, Kilkenny ML, Rzechorzek NJ, Pearl LH. Crystal structure of the rad9-rad1-hus1 DNA damage checkpoint complex-implications for clamp loading and regulation. Mol Cell 2009;34:735-45; PMID:19446481; http://dx.doi.org/10.1016/j.mol-cel.2009.04.027.
63. Smith DM, Benaroudj N, Goldberg A. Proteasomes and their associated ATPases: a destructive combination. J Struct Biol 2006;156:72-83; PMID:16919475; http://dx.doi.org/10.1016/j.jsb.2006.04.012. (Pubitemid 44486067)
64. Coene KL, Mans DA, Boldt K, Gloeckner CJ, van Reeuwijk J, Bolat E, et al. The ciliopathy-associ-ated protein homologs RPGRIP1 and RPGRIP1L are linked to cilium integrity through interaction with Nek4 serine/threonine kinase. Hum Mol Genet 2011;20:3592-605; PMID:21685204; http://dx.doi.org/10.1093/hmg/ddr280.
65. Mahajan B, Selvapandiyan A, Gerald NJ, Majam V, Zheng H, Wickramarachchi T, et al. Centrins, cell cycle regulation proteins in human malaria parasite Plasmodium falciparum. J Biol Chem 2008;283:31871-83; PMID:18693242; http://dx.doi.org/10.1074/jbc. M800028200.
66. Aravind L, Anantharaman V, Zhang D, De Souza RF, Iyer LM. Gene flow and biological conflict systems in the origin and evolution of eukaryotes. Frontiers in Cellular and Infection Microbiology 2012;2.
67. Zhang D, de Souza RF, Anantharaman V, Iyer LM, Aravind L. Polymorphic toxin systems: comprehensive characterization of trafficking modes, processing, mechanisms of action, immunity and ecology using comparative genomics. Biol Direct 2012;7:18; PMID:22731697.
68. Nunoura T, Takaki Y, Kakuta J, Nishi S, Sugahara J, Kazama H, et al. Insights into the evolution of Archaea and eukaryotic protein modifier systems revealed by the genome of a novel archaeal group. Nucleic Acids Res 2011;39:3204-23; PMID:21169198; http://dx.doi.org/10.1093/nar/gkq1228.
69. Burroughs AM, Iyer LM, Aravind L. Functional diversification of the RING finger and other binuclear treble clef domains in prokaryotes and the early evolution of the ubiquitin system. Mol Biosyst 2011;7:2261-77; PMID:21547297; http://dx.doi.org/10.1039/c1mb05061c.
70. Koonin EV, Aravind L. Dynein light chains of the Roadblock/LC7 group belong to an ancient protein superfamily implicated in NTPase regulation. Curr Biol 2000;10:R774-6; PMID:11084347.
71. Miertzschke M, Koerner C, Vetter IR, Keilberg D, Hot E, Leonardy S, et al. Structural analysis of the Ras-like G protein MglA and its cognate GAP MglB and implications for bacterial polarity. EMBO J 2011;30:4185-97; PMID:21847100; http://dx.doi.org/10.1038/emboj.2011.291.
72. Zhang Y, Franco M, Ducret A, Mignot T. A bacterial Ras-like small GTP-binding protein and its cognate GAP establish a dynamic spatial polarity axis to control directed motility. PLoS Biol 2010;8:e1000430; PMID:20652021; http://dx.doi.org/10.1371/journal. pbio.1000430.
73. Oliva MA, Martin-Galiano AJ, Sakaguchi Y, Andreu JM. Tubulin homolog TubZ in a phage-encoded partition system. Proc Natl Acad Sci USA 2012;109:7711-6; PMID:22538818; http://dx.doi.org/10.1073/pnas.1121546109.
74. Busiek KK, Margolin W. Split decision: a thaumarchae-on encoding both FtsZ and Cdv cell division proteins chooses Cdv for cytokinesis. Mol Microbiol 2011;82:535-8; PMID:21895799; http://dx.doi.org/10.1111/j.1365-2958.2011.07833. x.
75. Ni L, Xu W, Kumaraswami M, Schumacher MA. Plasmid protein TubR uses a distinct mode of HTH-DNA binding and recruits the prokaryotic tubulin homolog TubZ to effect DNA partition. Proc Natl Acad Sci USA 2010;107:11763-8; PMID:20534443; http://dx.doi.org/10.1073/pnas.1003817107.
76. Pelve EA, Lindås AC, Martens-Habbena W, de la Torre JR, Stahl DA, Bernander R. Cdv-based cell division and cell cycle organization in the thaumarchae-on Nitrosopumilus maritimus. Mol Microbiol 2011;82:555-66; PMID:21923770; http://dx.doi.org/10.1111/j.1365-2958.2011.07834.x.
77. Burroughs AM, Iyer LM, Aravind L. Comparative genomics and evolutionary trajectories of viral ATP dependent DNA-packaging systems. Genome Dyn 2007;3:48-65; PMID:18753784; http://dx.doi.org/10.1159/000107603.
78. Altschul S F, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389-402; PMID:9254694; http://dx.doi.org/ 10.1093/nar/25.17.3389. (Pubitemid 27359211)
79. Johnson LS, Eddy SR, Portugaly E. Hidden Markov model speed heuristic and iterative HMM search procedure. BMC Bioinformatics 2010;11:431; PMID:20718988; http://dx.doi.org/10.1186/1471-2105-11-431.
80. Lassmann T, Sonnhammer EL. Kalign - an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 2005;6:298; PMID:16343337; http://dx.doi.org/10.1186/1471-2105-6-298. (Pubitemid 41829850)
81. Edgar RC. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004;32:1792-7; PMID:15034147; http://dx.doi.org/10.1093/nar/gkh340. (Pubitemid 38832724)
82. Cuff JA, Clamp ME, Siddiqui AS, Finlay M, Barton GJ. JPred: a consensus secondary structure prediction server. Bioinformatics 1998;14:892-3; PMID:9927721; http://dx.doi.org/10.1093/bioinformatics/14.10.892. (Pubitemid 29041548)
83. Söding J. Protein homology detection by HMM-HMM comparison. Bioinformatics 2005;21:951-60; PMID:15531603; http://dx.doi.org/10.1093/ bioinfor-matics/bti125. (Pubitemid 40467915)
84. Price MN, Dehal PS, Arkin A P. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol Biol Evol 2009;26:1641-50; PMID:19377059; http://dx.doi.org/10.1093/molbev/msp077.
85. Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 2007;24:1596-9; PMID:17488738; http://dx.doi.org/10.1093/molbev/msm092. (Pubitemid 47236692)