The Tetrahymena thermophila phagosome proteome

Eukaryotic Cell

Volumn 5, Issue 12, 2006, Pages 1990-2000

  Jacobs, Mary Ellen ^a   DeSouza, Leroi V ^b   Samaranayake, Haresha ^a   Pearlman, Ronald E ^b   Siu, K W Michael ^b   Klobutcher, Lawrence A ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; PROTEOME; PROTOZOAL DNA; PROTOZOAL PROTEIN;

ANIMAL; ARTICLE; CHEMISTRY; GENE; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PHAGOCYTOSIS; PHAGOSOME; PHYSIOLOGY; TANDEM MASS SPECTROMETRY; TETRAHYMENA THERMOPHILA;

ANIMALS; BASE SEQUENCE; DNA, PROTOZOAN; GENES, PROTOZOAN; PHAGOCYTOSIS; PHAGOSOMES; PROTEOME; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; TANDEM MASS SPECTROMETRY; TETRAHYMENA THERMOPHILA;

CILIOPHORA; EUKARYOTA; PROTISTA; TETRAHYMENA; TETRAHYMENA THERMOPHILA; VERTEBRATA;

EID: 33845660879     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00195-06     Document Type: Article

References (87)

1. Aderem, A., and D. M. Underhill. 1999. Mechanisms of phagocytosis in macrophages. Annu. Rev. Immunol. 17:593-623.
2. Allen, R. D., and R. W. Wolf. 1979. Membrane recycling at the cytoproct of Tetrahymena. J. Cell Sci. 35:217-227.
3. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
4. Bared, S. M., C. Buechler, A. Boettcher, R. Dajoub, A. Sigruener, M. Grandl, C. Rudolph, A. Dada, and G. Schmitz. 2004. Association of ABCA1 with syntaxin 13 and flotillin-1 and enhanced phagocytosis in tangier cells. Mol. Biol. Cell 15:5399-5407.
5. Batz, W., and F. Wunderlich. 1976. Structural transformation of the phagosomal membrane in Tetrahymena cells endocytosing latex beads. Arch. Microbiol. 109:215-250.
6. Blocker, A., F. F. Severin, J. K. Burkhardt, J. B. Bingham, H. Yu, J.-C. Olivo, T. A. Schroer, A. A. Hyman, and G. Griffiths. 1997. Molecular requirements for bi-directional movement of phagosomes along microtubules. J. Cell Biol. 137:113-129.
7. Bokoch, G. M. 2005. Regulation of innate immunity by Rho GTPases. Trends Cell Biol. 15:163-171.
8. Boldrin, F., G. Santovito, J. Gaertig, D. Wloga, D. Cassidy-Hanley, T. Clark, and E. Piccinni. 2006. Metallothionein gene from Tetrahymena thermophila with a copper-inducible-repressible promoter. Eukaryot. Cell 5:422-425.
9. Bowman, G., N. C. Elde, G. Morgan, M. Winey, and A. P. Turkewitz. 2005. Core formation and the acquisition of fusion competence are linked during secretory granule maturation in Tetrahymena. Traffic 6:303-323.
10. Bowman, G. R., D. G. Smith, K. W. M. Siu, R. E. Pearlman, and A. P. Turkewitz. 2005. Genomic and proteomic evidence for a second family of dense core granule cargo proteins in Tetrahymena thermophila. J. Eukaryot. Microbiol. 52:291-297.
11. Bruns, P. J., and D. Cassidy-Hanley. 2000. Biolistic transformation of macro- and micronuclei. Methods Cell Biol. 62:501-512.
12. Chicoine, L. G., D. Wenkert, R. Richman, C. James, J. C. Wiggins, and C. D. Allis. 1985. Modulation of linker histones during development in Tetrahymena: selective elimination of linker histone during the differentiation of new macronuclei. Dev. Biol. 109:1-8.
13. Chilcoat, N. D., N. C. Elde, and A. P. Turkewitz. 2001. An antisense approach to phenotype-based gene cloning in Tetrahymena. Proc. Natl. Acad. Sci. USA 98:8709-8713.
14. Clarke, M., J. Koehler, Q. Arana, T. Liu, J. Heuser, and G. Gerisch. 2002. Dynamics of the vacuolar H(+)-ATPase in the contractile vacuole complex and the endosomal pathway of Dictyostelium cells. J. Cell Sci. 115:2893-2905.
15. Collins, R. F., A. D. Schreiber, S. Grinstein, and W. S. Trimble. 2002. Syntaxins 13 and 7 function at distinct steps during phagocytosis. J. Immunol. 169:3250-3256.
16. Desjardins, M. 1995. Biogenesis of phagolysosomes: the 'kiss and run' hypothesis. Trends Cell Biol. 5:183-186.
17. Desjardins, M., and G. Griffiths. 2003. Phagocytosis: latex leads the way. Curr. Opin. Cell Biol. 15:498-503.
18. Desjardins, M., M. Houde, and E. Gagnon. 2005. Phagocytosis: the convoluted way from nutrition to adaptive immunity. Immunol. Rev. 207:158-165.
19. Desjardins, M., L. A. Huber, R. G. Parton, and G. Griffiths. 1994. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124:677-688.
20. Doerder, F. P., and R. L. Hallberg. 1989. Identification of a cDNA coding for the SerH3 surface protein of Tetrahymena thermophila. J. Protozool. 36:304-307.
21. Doudna, J. A., and V. L. Rath. 2002. Structure and function of the eukaryotic ribosome: the next frontier. Cell 109:153-156.
22. Eisen, J. A., M. Wu, D. Wu, M. Thiagarajan, J. R. Wortman, J. H. Badger, Q. Ren, P. Amedeo, K. M. Jones, L. J. Tallon, A. L. Delcher, S. L. Salzberg, C. delToro, H. F. Rider, S. C. Williamson, R. A. Barbeau, J. C. Silva, B. J. Haas, W. H. Majoros, M. Farzad, J. M. Carlton, J. Garg, R. E. Pearlman, K. M. Karrer, L. Sun, R. K. Smith, Jr., G. Manning, N. C. Elde, A. P. Turkewitz, D. J. Asai, D. E. Wilkes, Y. Wang, H. Cai, K. Collins, K. Wilamowska, W. L. Ruzzo, Z. Weinberg, B. A. Stewart, S. R. Lee, D. Wloga, K. Rogowski, J. Frankel, J. Gaertig, C.-C. Tsao, M. A. Gorovsky, P. J. Keeling, R. F. Waller, N.J. Patron, M. Cherry, N. A. Stover, C. A. Krieger, E. P. Hamilton, E. Orias, and R. S. Coyne. 2006. Macronuclear genome sequence of the ciliate Tetrahymena thermophila, a model eukaryote. PLoS Biol. 4:e286. doi:10.1371/journal.pbio. 0040286.
23. Eskelinen, E.-L., Y. Tanaka, and P. Saftig. 2003. At the acidic edge: emerging functions for lysosomal membrane proteins. Trends Cell Biol. 13:137-145.
24. Feng, Y., B. Press, and A. Wandinger-Ness. 1995. Rab 7: an important regulator of late endocytic membrane traffic. J. Cell Biol. 13:1435-1452.
25. Foster, T. 2005. Immune evasion by staphylococci. Nat. Rev. Microbiol. 3:948-958.
26. Frankel, J. 2000. Cell biology of Tetrahymena thermophila. Methods Cell Biol. 62:27-125.
27. Gaertig, J., Y. Gao, T. Tishgarten, T. G. Clark, and H. W. Dickerson. 1999. Surface display of a parasite antigen in the ciliate Tetrahymena thermophila. Nat. Biotechnol. 17:462-465.
28. Gaertig, J., and G. Kapler. 2000. Transient and stable DNA transformation of Tetrahymena thermophila by electroporation. Methods Cell Biol. 62:485-500.
29. Gaertig, J., T. H. Thatcher, L. Gu, and M. A. Gorovsky. 1994. Electroporation-mediated replacement of a positively and negatively selectable beta-tubulin gene in Tetrahymena thermophila. Proc. Natl. Acad. Sci. USA 91: 4549-4553.
30. Garin, J., R. Diez, S. Kieffer, J.-F. Dermine, S. Duclos, E. Gagnon, R. Sadoul, C. Rondeau, and M. Desjardins. 2001. The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152:165-180.
31. 2+/calmodulin and p85 cooperatively regulate an initiation of cytokinesis in Tetrahymena. J. Cell Sci. 112:3619-3626.
32. 2+/calmodulin-binding proteins are involved in Tetrahymena thermophila phagocytosis. Cell Struct. Funct. 25:243-251.
33. Gorvel, J.-P., P. Chavrier, M. Zerial, and J. Gruenberg. 1991. RabS controls early endosome fusion in vitro. Cell 64:915-925.
34. Gotthardt, D., H. J. Warnatz, O. Henschel, F. Bruckert, M. Schleicher, and T. Soldati. 2002. High-resolution dissection of phagosome maturation reveals distinct membrane trafficking phases. Mol. Biol. Cell 13:3508-3520.
35. Gregory, D. J., and M. Olivier. 2005. Subversion of host cell signalling by the protozoan parasite Leishmania. Parasitology 130:S27-S35.
36. Gross, S. R., and T. G. Kinzy. 2005. Translation elongation factor 1A is essential for regulation of the actin cytoskeleton and cell morphology. Nat. Struct. Mol. Biol. 12:772-778.
37. Harrison, R. E., C. Bucci, O. V. Vieira, T. A. Schroer, and S. Grinstein. 2003. Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol. Cell. Biol. 23:6494-6506.
38. I hypersecretory mutants of Tetrahymena thermophila. Appl. Microbiol. Biotechnol. 54:390-396.
39. Hosein, R. E., S. A. Williams, and R. H. Gavin. 2005. Directed motility of phagosomes in Tetrahymena thermophila requires actin and Myo1p, a novel unconventional myosin. Cell Motil. Cytoskelet. 61:49-60.
40. Ikonen, E., and M. Hölttä-Vuori. 2004. Cellular pathology of Niemann-Pick type C disease. Semin. Cell Dev. Biol. 15:445-454.
41. Jacobs, M. E., D. E. Cortezzo, and L. A. Klobutcher. 2004. Assessing the effectiveness of coding and non-coding regions in antisense ribosome inhibition of gene expression in Tetrahymena. J. Eukaryot. Microbiol. 51:536-541.
42. Karten, B., R. B. Campenot, D. E. Vance, and J. E. Vance. 2006. The Niemann-Pick C1 protein in recycling endosomes of pre-synaptic nerve terminals. J. Lipid Res. 47:504-514.
43. Kawasaki-Nishi, S., T. Nishi, and M. Forgac. 2003. Proton translocation driven by ATP hydrolysis in V-ATPases. FEBS Lett. 545:76-85.
44. Kitajima, Y., and J. G. A. Thompson. 1977. Differentiation of food vacuolar membranes during endocytosis in Tetrahymena. J. Cell Biol. 75:436-445.
45. Kjeken, R., M. Egeberg, A. Haberman, M. Kuehnel, P. Peyron, M. Floetenmeyer, P. Walther, A. Jahraus, H. Defacque, S. A. Kuznetsov, and G. Griffiths. 2004. Fusion between phagosomes, early and late endosomes: a role for actin in fusion between late, but not early endocytic organelles. Mol. Biol. Cell 15:345-358.
46. Klobutcher, L. A., K. Ragkousi, and P. Setlow. 2006. The Bacillus subtilis spore coat provides "eat resistance" during phagocytic predation by the protozoan Tetrahymena thermophila. Proc. Natl. Acad. Sci. USA 103:165-170.
47. Lee, S., J. C. Wisniewski, W. L. Dentier, and D. J. Asai. 1999. Gene knockouts reveal separate functions for two cytoplasmic dyneins in Tetrahymena thermophila. Mol. Biol. Cell 10:771-784.
48. Lemmon, S. K., and L. M. Traub. 2000. Sorting in the endosomal system in yeast and animal cells. Curr. Opin. Cell Biol. 12:457-466.
49. Maicher, M. T., and A. Tiedtke. 1999. Biochemical analysis of membrane proteins from an early maturation stage of phagosomes. Electrophoresis 20:1011-1016.
50. Medzihradszky, K. F., X. Zhang, R. J. Chalkley, S. Guan, M. A. McFarland, M. J. Chalmers, A. G. Marshall, R. L. Diaz, C. D. Allis, and A. L. Burlingame. 2004. Characterization of Tetrahymena histone H2B variants and post-translational populations by electron capture dissociation (ECD) Fourier transform ion cyclotron mass spectrometry (FT-ICR MS). Mol. Cell. Proteomics 3:872-886.
51. Melia, S. M., E. S. Cole, and A. P. Turkewitz. 1998. Mutational analysis of regulated exocytosis in Tetrahymena. J. Cell Sci. 111:131-140.
52. Meyer, M., T. Mayer, and A. Tiedtke. 1998. Maturation of phagosomes is accompanied by specific patterns of small GTPases. Electrophoresis 19: 2528-2535.
53. Müller-Taubenberger, A., A. N. Lupas, H. Li, M. Ecke, E. Simmeth, and G. Gerisch. 2001. Calreticulin and calnexin in the endoplasmic reticulum are important for phagocytosis. EMBO J. 20:6772-6782.
54. Nilsson, J. R. 1977. On food vacuoles in Tetrahymena pyriformis GL. J. Protozool. 24:502-507.
55. Nilsson, J. R. 1987. Structural aspects of digestion of Escherichia coli in Tetrahymena. J. Protozool. 34:1-6.
56. Nimmerjahn, F., and J. V. Ravetch. 2006. Fcγ receptors: old friends and new family members. Immunity 24:19-28.
57. Ogden, C., and K. Elkon. 2006. Role of complement and other innate immune mechanisms in the removal of apoptotic cells. Curr. Dir. Autoimmun. 9:120-142.
58. Okada, M., C. D. Huston, B. J. Mann, W. A. J. Petri, K. Kita, and T. Nozaki. 2005. Proteomic analysis of phagocytosis in the enteric protozoan parasite Entamoeba histolytica. Eukaryot. Cell 4:827-831.
59. Okada, M., and T. Nozaki. 2006. New insights into molecular mechanisms of phagocytosis in Entamoeba histolytica by proteomic analysis. Arch. Med. Res. 37:244-252.
60. Quan, L., and M. Wilkinson. 1991. DNA fragment purification from LMP agarose. BioTechniques 10:737-738.
61. Rampoldi, L., C. Dobson-Stone, J. P. Rubio, A. Danek, R. M. Chalmers, N. W. Wood, C. Verellen, X. Ferrer, A. Malandrini, G. M. Fabrizi, R. Brown, J. Vance, M. Pericak-Vance, G. Rudolf, S. Carrè, E. Alonso, M. Manfredi, A. H. Németh, and A. P. Monaco. 2001. A conserved sorting-associated protein is mutant in chorea-acanthocytosis. Nat. Genet. 28:119-120.
62. Rasmussen, C., and C. Wiebe. 1999. Cloning of a Schizosaccharomyces pombe homologue of elongation factor 1 alpha by two-hybrid selection of calmodulin-binding proteins. Biochem. Cell Biol. 77:421-430.
63. Rasmussen, L., and E. Orias. 1975. Tetrahymena: growth without phagocytosis. Science 190:464-465.
64. Rezabek, B. L., J. M. Rodriguez-Paris, J. A. Cardelli, and C. P. Chia. 1997. Phagosomal proteins of Dictyostelium discoideum. J. Eukaryot. Microbiol. 44:284-292.
65. Rosenberger, C. M., and B. B. Finlay. 2003. Phagocyte sabotage: disruption of macrophage signalling by bacterial pathogens. Nat. Rev. Mol. Cell Biol. 4:385-396.
66. Rossi, V., D. K. Banfield, M. Vacca, L. E. P. Dietrich, C. Ungermann, M. D'Esposito, T. Galli, and F. Filippini. 2004. Longins and their longin domains: regulated SNAREs and multifunctional SNARE regulators. Trends Biochem. Sci. 29:682-688.
67. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
68. Schirle, M., M. A. Heurtier, and B. Kuster. 2003. Profiling core proteomes of human cell lines by one-dimensional PAGE and liquid chromatography-tandem mass spectrometry. Mol. Cell. Proteomics 12:1297-1305.
69. Scott, C. C., R. J. Botelho, and S. Grinstein. 2003. Phagosome maturation: a few bugs in the system. J. Membr. Biol. 193:137-152.
70. Shevchenko, A., M. Wilm, O. Vorm, and M. Mann. 1996. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels. Anal. Chem. 68:850-858.
71. Smith, J. C., J. G. Northey, J. Garg, R. E. Pearlman, and K. W. M. Siu. 2005. Robust method for proteome analysis by MS/MS using an entire translated genome: demonstration on the ciliome of Tetrahymena thermophila. J. Proteome Res. 4:909-919.
72. Stenmark, H., and V. M. Olkkonen. 2001. The Rab GTPase family. Genome Biol. 2:1-7.
73. Stover, N. A., C. J. Krieger, G. Binkley, Q. Dong, D. G. Fisk, R. Nash, A. Sethuraman, S. Weng, and J. M. Cherry. 2006. Tetrahymena Genome Database (TGD): a new genomic resource for Tetrahymena thermophila research. Nucleic Acids Res. 34:D500-D503.
74. Tirumalai, R. S., K. C. Chan, D. A. Prieto, H. J. Issaq, T. P. Conrads, and T. D. Veenstra. 2003. Characterization of the low molecular weight human serum proteome. Mol. Cell. Proteomics 2:1096-1103.
75. Tse, S. M., W. Furuya, E. Gold, A. D. Schreiber, K. Sandvig, R. D. Inman, and S. Grinstein. 2003. Differential role of actin, clathrin, and dynamin in Fcγ receptor-mediated endocytosis and phagocytosis. J. Biol. Chem. 278: 3331-3338.
76. Turk, V., B. Turk, and D. Turk. 2001. Lysosomal cysteine proteases: facts and opportunities. EMBO J. 20:4629-4633.
77. Turkewitz, A. P. 2004. Out with a bang! Tetrahymena as a model system to study secretory granule biogenesis. Traffic 5:63-68.
78. Turkewitz, A. P., E. Orias, and G. Kapler. 2002. Functional genomics: the coming of age for Tetrahymena thermophila. Trends Genet. 18:35-40.
79. Ueno, S.-I., Y. Maruki, M. Nakamura, Y. Tomemori, K. Kamae, H. Tanabe, Y. Yamashita, S. Matsuda, S. Kaneko, and A. Sano. 2001. The gene encoding a newly discovered protein, chorein, is mutated in chorea-acanthocytosis. Nat. Genet. 28:121-122.
80. Velayos-Baeza, A., A. Vettori, R. R. Copley, C. Dobson-Stone, and A. P. Monaco. 2004. Analysis of the human VPS13 gene family. Genomics 84:536-549.
81. Vergne, I., J. Chua, S. B. Singh, and V. Deretic. 2004. Cell biology of Mycobacterium tuberculosis phagosome. Annu. Rev. Cell Dev. Biol. 20:367-394.
82. Vieira, O. V., R. J. Botelho, and S. Grinstein. 2002. Phagosome maturation: aging gracefully. Biochem. J. 366:689-704.
83. Vosskuehler, C., and A. Tiedtke. 1993. Magnetic separation of phagosomes of denned age from Tetrahymena thermophila. J. Eukaryot. Microbiol. 40: 556-562.
84. Weidenbach, A. L., and G. A. Thompson, Jr. 1974. Studies of membrane formation in Tetrahymena pyriformis. VIII. On the origin of membranes surrounding food vacuoles. J. Protozool. 21:745-751.
85. Williams, S. A., R. E. Hosein, J. A. Garces, and R. H. Gavin. 2000. MYO1, a novel, unconventional myosin gene affects endocytosis and macronuclear elongation in Tetrahymena thermophila. J. Eukaryot. Microbiol. 47:561-568.
86. Wolters, D. A., M. P. Washburn, and J. R. Yates III. 2001. An automated multidimensional protein identification technology for shotgun proteomics. Anal. Chem. 73:5683-5690.
87. Yan, M., R. F. Collins, S. Grinstein, and W. S. Trimble. 2005. Coronin-1 function is required for phagosome formation. Mol. Biol. Cell 16:3077-3087.