Ciliate pellicular proteome identifies novel protein families with characteristic repeat motifs that are common to alveolates

Molecular Biology and Evolution

Volumn 28, Issue 3, 2011, Pages 1319-1331

  Gould, Sven B ^a,c   Kraft, Lesleigh G K ^a   Van Dooren, Giel G ^a   Goodman, Christopher D ^a   Ford, Kristina L ^a   Cassin, Andrew M ^a,b   Bacic, Antony ^a   McFadden, Geoffrey I ^a   Waller, Ross F ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Alveolata; Apicomplexa; Ciliata; cytoskeleton; inner membrane complex; membrane skeleton; repeat motif proteins

Indexed keywords

PROTEOME; PROTOZOAL PROTEIN;

ALVEOLATA; APICOMPLEXA; ARTICLE; CILIATE; CONTROLLED STUDY; HUMAN; HUMAN CELL; MICROBIAL DIVERSITY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN STRUCTURE; STRUCTURAL BIOINFORMATICS; TETRAHYMENA THERMOPHILA; TOXOPLASMA GONDII;

AMINO ACID SEQUENCE; CELL CULTURE TECHNIQUES; CELL MEMBRANE; CLONING, MOLECULAR; EVOLUTION, MOLECULAR; FIBROBLASTS; HUMANS; MALE; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTEOME; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; REPETITIVE SEQUENCES, NUCLEIC ACID; SEQUENCE ALIGNMENT; TETRAHYMENA THERMOPHILA; TOXOPLASMA;

ALVEOLATA; APICOMPLEXA; CILIOPHORA; DINOPHYCEAE; TETRAHYMENA THERMOPHILA; TOXOPLASMA GONDII;

EID: 79952177807     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msq321     Document Type: Article

References (49)

1. Adl SM, Simpson AG, Farmer MA, et al. (17 co-authors) 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J Eukaryot Microbiol. 52:399-451. (Pubitemid 43923926)
2. Allen RD. 1967. Fine structure, reconstruction and possible functions of components of the cortex of Tetrahymena pyriformis. J Protozool. 14:553-565.
3. Anderson-White BR, Ivey FD, Cheng K, Szatanek T, Lorestani A, Beckers CJ, Ferguson DJP, Sahoo N, Gubbels MJ. 2011. A family of intermediate filament-like proteins is sequentially assembled into the cytoskeleton of Toxoplasma gondii. Cell Microbiol 13:18-31.
4. Baldauf SL, Roger AJ, Wenk-Siefert I, Doolittle WF. 2000. A kingdomlevel phylogeny of eukaryotes based on combined protein data. Science 290:972-977.
5. Baum J, Tonkin CJ, Paul AS, Rug M, Smith BJ, Gould SB, Richard D, Pollard TD, Cowman AF. 2008. A malaria parasite formin regulates actin polymerization and localizes to the parasiteerythrocyte moving junction during invasion. Cell Host Microbe. 3:188-198. (Pubitemid 351325762)
6. Bricheux G, Coffe G, Brugerolle G. 2007. Identification of a new protein in the centrosome-like "atractophore" of Trichomonas vaginalis. Mol Biochem Parasitol. 153:133-140. (Pubitemid 46654249)
7. Bullen HE, Tonkin CJ, O'Donnell RA, Tham WH, Papenfuss AT, Gould SB, Cowman AF, Crabb BS, Gilson PR. 2009. A novel family of apicomplexan glideosome associated proteins with an inner-membrane anchoring role. J Biol Chem. 284:25353-25363.
8. Burki F, Shalchian-Tabrizi K, Minge M, Skjaeveland A, Nikolaev SI, Jakobsen KS, Pawlowski J. 2007. Phylogenomics reshuffles the eukaryotic supergroups. PLoS One. 2: e790.
9. Coffe G, Le Caer JP, Lima O, Adoutte A. 1996. Purification, in vitro reassembly, and preliminary sequence analysis of epiplasmins, the major constituent of the membrane skeleton of Paramecium. Cell Motil Cytoskeleton. 34:137-151.
10. Craig R, Beavis RC. 2004. TANDEM: matching proteins with tandem mass spectra. Bioinformatics 20:1466-1467. (Pubitemid 38931421)
11. Damaj R, Pomel S, Bricheux G, Coffe G, Vigues B, Ravet V, Bouchard P. 2009. Cross-study analysis of genomic data defines the ciliate multigenic epiplasmin family: strategies for functional analysis in Paramecium tetraurelia. BMC Evol Biol. 9:125.
12. Dodge J. 1987. Dinoflagellate ultrastructure and complex organelles. In: Taylor FJ, editor. The biology of dinoflagellates. Oxford: Blackwell. p. 92-142.
13. Eisen JA, Coyne RS, Wu M, et al. (53 co-authors) 2006. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 4: e286.
14. Gaertig J, Kapler G. 2000. Transient and stable DNA transformation of Tetrahymena thermophila by electroporation. In: Asai DJ, Forney JD, editors. Methods in cell biology: Tetrahymena thermophila. San Diego (CA): Academic Press. p. 486-500.
15. Gaskins E, Gilk S, DeVore N, Mann T, Ward G, Beckers C. 2004. Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J Cell Biol. 165:383-393. (Pubitemid 38649913)
16. Gould SB, Tham WH, Cowman AF, McFadden GI, Waller RF. 2008. Alveolins, a new family of cortical proteins that define the protist infrakingdom Alveolata. Mol Biol Evol. 25:1219-1230.
17. Hampl V, Hug L, Leigh JW, Dacks JB, Lang BF, Simpson AG, Roger AJ. 2009. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic "supergroups". Proc Natl Acad Sci U S A. 106:3859-3864.
18. Hausmann K, Bradbury P. 1996. Ciliates: cells as organisms. Jena (Germany): Gustav Fischer Verlag.
19. Heger A, Holm L. 2000. Rapid automatic detection and alignment of repeats in protein sequences. Proteins 41:224-237.
20. Honts JE, Williams NE. 1990. Tetrins: polypeptides that form bundled filaments in Tetrahymena. J Cell Sci. 96 (Pt 2):293):293-302.
21. Hu K, Johnson J, Florens L, Fraunholz M, Suravajjala S, DiLullo C, Yates J, Roos DS, Murray JM. 2006. Cytoskeletal components of an invasion machine-the apical complex of Toxoplasma gondii. PLoS Pathog. 2: e13.
22. Huynh MH, Carruthers VB. 2009. Tagging of endogenous genes in a Toxoplasma gondii strain lacking Ku80. Eukaryot Cell. 8:530-539.
23. Khater EI, Sinden RE, Dessens JT. 2004. A malaria membrane skeletal protein is essential for normal morphogenesis, motility, and infectivity of sporozoites. J Cell Biol. 167:425-432. (Pubitemid 39489051)
24. Kilburn CL, Pearson CG, Romijn EP, Meehl JB, Giddings TH, Culver BP, Yates JR, Winey M. 2007. New Tetrahymena basal body protein components identify basal body domain structure. J Cell Biol. 178:905-912. (Pubitemid 47443315)
25. Mann T, Beckers C. 2001. Characterization of the subpellicular network, a filamentous membrane skeletal component in the parasite Toxoplasma gondii. Mol Biochem Parasitol. 115:257-268. (Pubitemid 32566235)
26. Mann T, Gaskins E, Beckers C. 2002. Proteolytic processing of TgIMC1 during maturation of the membrane skeleton of Toxoplasma gondii. J Biol Chem. 277:41240-41246. (Pubitemid 35215716)
27. Marrs JA, Bouck GB. 1992. The two major membrane skeletal proteins (articulins) of Euglena gracilis define a novel class of cytoskeletal proteins. J Cell Biol. 118:1465-1475.
28. Meszoely CA, Erbe EF, Steere RL, Pacheco ND, Beaudoin RL. 1982. Plasmodium berghei: architectural analysis by freeze-fracturing of the intraoocyst sporozoite's pellicular system. Exp Parasitol. 53:229-241. (Pubitemid 12093285)
29. Morrissette NS, Murray JM, Roos DS. 1997. Subpellicular microtubules associate with an intramembranous particle lattice in the protozoan parasite Toxoplasma gondii. J Cell Sci. 110 (Pt 1):35):35-42. (Pubitemid 27057942)
30. Morrissette NS, Sibley LD. 2002. Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev. 66:21-38. (Pubitemid 34213967)
31. Nahon P, Coffe G, Le Guyader H, Darmanaden-Delorme J, Jeanmaire-Wolf F, Clerot J-C, Adoutte A. 1993. Identification of the epiplasmins, a new set of cortical proteins of the membrane cytoskeleton in Paramecium. J Cell Sci. 104:975-990. (Pubitemid 23154305)
32. Natera SH, Ford KL, Cassin AM, Patterson JH, Newbigin EJ, Bacic A. 2008. Analysis of the Oryza sativa plasma membrane proteome using combined protein and peptide fractionation approaches in conjunction with mass spectrometry journal of proteome reserach. J Proteome Res. 7:1159-1187.
33. Newman AM, Cooper JB. 2007. XSTREAM: a practical algorithm for identification and architecture modeling of tandem repeats in protein sequences. BMC Bioinformatics. 8:382.
34. Numata O, Hanyu K, Takeda T, Watanabe Y. 2000. Tetrahymena calcium-binding proteins, TCBP-25 and TCBP-23. In: Asai DJ, Forney JD, editors. Tetrahymena thermophila. San Diego (CA): Academic Press. p. 455-465.
35. Pazour GJ, Agrin N, Leszyk J, Witman GB. 2005. Proteomic analysis of a eukaryotic cilium. J Cell Biol. 170:103-113. (Pubitemid 40994100)
36. Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. 1999. Probabilitybased protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20:3551-3567. (Pubitemid 30007252)
37. Pomel S, Diogon M, Bouchard P, Pradel L, Ravet V, Coffe G, Vigues B. 2006. The membrane skeleton in Paramecium: molecular characterization of a novel epiplasmin family and preliminary GFP expression results. Protist. 157:61-75. (Pubitemid 43220717)
38. Radivojac P, Iakoucheva LM, Oldfield CJ, Obradovic Z, Uversky VN, Dunker AK. 2007. Intrinsic disorder and functional proteomics. Biophys J. 92:1439-1456. (Pubitemid 46393458)
39. Santos JM, Lebrun M, Daher W, Soldati D, Dubremetz JF. 2009. Apicomplexan cytoskeleton and motors: key regulators in morphogenesis, cell division, transport and motility. Int J Parasitol. 39:153-162.
40. Satir BH, Wissig SL. 1982. Alveolar sacs of Tetrahymena: ultrastructural characteristics and similarities to subsurface cisterns of muscle and nerve. J Cell Sci. 55:13-33. (Pubitemid 12025318)
41. Shang Y, Song X, Bowen J, Corstanje R, Gao Y, Gaertig J, Gorovsky MA. 2008. A robust inducible-repressible promoter greatly facilitates gene knockouts, conditional expression, and overexpression of homologous and heterologous genes in Tetrahymena thermophila. Proc Natl Acad Sci. U S A. 99:3734-3739.
42. Shilov IV, Seymour SL, Patel AA, Loboda A, Tang WH, Keating SP, Hunter CL, Nuwaysir LM, Schaeffer DA. 2007. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics. 6:1638-1655. (Pubitemid 47506173)
43. Tremp AZ, Khater EI, Dessens JT. 2008. IMC1b is a putative membrane skeleton protein involved in cell shape, mechanical strength, motility, and infectivity of malaria ookinetes. J Biol Chem. 283:27604-27611.
44. van Dooren GG, Reiff SB, Tomova C, Meissner M, Humbel BM, Striepen B. 2009. A novel dynamin-related protein has been recruited for apicoplast fission in Toxoplasma gondii. Curr Biol. 19:267-276.
45. Williams NE. 2004. The epiplasm gene EPC1 influences cell shape and cortical pattern in Tetrahymena thermophila. J Eukaryot Microbiol. 51:201-206. (Pubitemid 38503858)
46. Williams NE, Honts JE, Dress VM, Nelsen EM, Frankel J. 1995. Monoclonal antibodies reveal complex structure in the membrane skeleton of Tetrahymena. J Eukaryot Microbiol. 42:422-427.
47. Williams NE, Honts JE, Jaeckel-Williams RF. 1987. Regional differentiation of the membrane skeleton in Tetrahymena. J Cell Sci. 87 (Pt 3):457):457-463.
48. Williams NE, Honts JE, Kaczanowska J. 1990. The formation of basal body domains in the membrane skeleton of Tetrahymena. Development 109:935-942.
49. Wolters J. 1991. The troublesome parasites-molecular and morphological evidence that Apicomplexa belong to the dinoflagellate-ciliate clade. Biosystems 25:75-83.