The cell cycle and Toxoplasma gondii cell division: Tightly knit or loosely stitched?

International Journal for Parasitology

Volumn 38, Issue 12, 2008, Pages 1343-1358

  Gubbels, Marc Jan ^a   White, Michael ^b   Szatanek, Tomasz ^a  

^a BOSTON COLLEGE   (United States)

^b MONTANA STATE UNIVERSITY   (United States)

Author keywords

Cell cycle; Centrocone; Centrosome; Cytokinesis; Endodyogeny; Endopolygeny; Schizogony; Toxoplasma gondii

Indexed keywords

CYCLIN DEPENDENT KINASE; CYCLINE;

EXPERIMENTAL STUDY; GROWTH RATE; LIFE CYCLE; MAMMAL; PARASITIC DISEASE; PROTOZOAN; REPRODUCTIVE BIOLOGY; VACCINE; VIRULENCE; YEAST;

APICOMPLEXA; BRADYZOITE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL DIVISION; COCCIDIA; CYTOKINESIS; DNA REPLICATION; GENE SEQUENCE; GENETIC ANALYSIS; MITOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE VIRULENCE; POLYPLOIDY; REVIEW; TACHYZOITE; TOXOPLASMA GONDII;

ANIMALS; CELL CYCLE; CELL DIVISION; CYCLINS; CYTOKINESIS; MITOSIS; TOXOPLASMA; TOXOPLASMOSIS;

APICOMPLEXA; EUKARYOTA; MAMMALIA; SACCHAROMYCETALES; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 51249101916     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2008.06.004     Document Type: Review

References (99)

1. Acquaviva C., Herzog F., Kraft C., and Pines J. The anaphase promoting complex/cyclosome is recruited to centromeres by the spindle assembly checkpoint. Nat. Cell Biol. 6 (2004) 892-898
2. Allshire R., and Pidoux A. Centromeres. Curr. Biol. 11 (2001) R454
3. Baker D.J., Dawlaty M.M., Galardy P., and van Deursen J.M. Mitotic regulation of the anaphase-promoting complex. Cell. Mol. Life Sci. 64 (2007) 589-600
4. Balasubramanian M.K., Bi E., and Glotzer M. Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr. Biol. 14 (2004) R806-R818
5. Bloom J., and Cross F.R. Multiple levels of cyclin specificity in cell-cycle control. Nat. Rev. 8 (2007) 149-160
6. Brown J.M., Hardin C., and Gaertig J. Rotokinesis, a novel phenomenon of cell locomotion-assisted cytokinesis in the ciliate Tetrahymena thermophila. Cell Biol. Int. 23 (1999) 841-848
7. Castedo M., Perfettini J.L., Roumier T., Andreau K., Medema R., and Kroemer G. Cell death by mitotic catastrophe: a molecular definition. Oncogene 23 (2004) 2825-2837
8. Castedo M., Perfettini J.L., Roumier T., Valent A., Raslova H., Yakushijin K., Horne D., Feunteun J., Lenoir G., Medema R., Vainchenker W., and Kroemer G. Mitotic catastrophe constitutes a special case of apoptosis whose suppression entails aneuploidy. Oncogene 23 (2004) 4362-4370
9. Cerutti L., and Simanis V. Controlling the end of the cell cycle. Curr. Opin. Genet. Dev. 10 (2000) 65-69
10. Chotivanich K., Udomsangpetch R., Simpson J.A., Newton P., Pukrittayakamee S., Looareesuwan S., and White N.J. Parasite multiplication potential and the severity of Falciparum malaria. J. Infect. Dis. 181 (2000) 1206-1209
11. Clarke D.J., and Gimenez-Abian J.F. Checkpoints controlling mitosis. Bioessays 22 (2000) 351-363
12. Colanzi A., and Corda D. Mitosis controls the Golgi and the Golgi controls mitosis. Curr. Opin. Cell Biol. 19 (2007) 386-393
13. Colanzi A., Hidalgo Carcedo C., Persico A., Cericola C., Turacchio G., Bonazzi M., Luini A., and Corda D. The Golgi mitotic checkpoint is controlled by BARS-dependent fission of the Golgi ribbon into separate stacks in G2. EMBO J. 26 (2007) 2465-2476
14. Conde de Felipe M.M., Lehmann M.M., Jerome M.E., and White M.W. Inhibition of Toxoplasma gondii growth by pyrrolidine dithiocarbamate is cell cycle specific and leads to population synchronization. Mol. Biochem. Parasitol. 157 (2008) 22-31
15. Cornelissen A.W., Overdulve J.P., and Van der Ploeg M. Cytochemical studies on nuclear DNA of four eucoccidian parasites, Isospora (Toxoplasma) gondii, Eimeria tenella, Sarcocystis cruzi and Plasmodium berghei. Parasitology 88 Pt 1 (1984) 13-25
16. Cornelissen A.W., and Overdulve J.P. Sex determination and sex differentiation in coccidia: gametogony and oocyst production after monoclonal infection of cats with free-living and intermediate host stages of Isospora (Toxoplasma) gondii. Parasitology 90 Pt 1 (1985) 35-44
17. Cornelissen A.W., and Overdulve J.P. Isospora (Toxoplasma) gondii: induction of sexuality. Cell Biol. Int. Rep. 10 (1986) 735-744
18. de Melo E.J., Mayerhoffer R.O., and de Souza W. Hydroxyurea inhibits intracellular Toxoplasma gondii multiplication. FEMS Microbiol. Lett. 185 (2000) 79-82
19. Delbac F., Sanger A., Neuhaus E.M., Stratmann R., Ajioka J.W., Toursel C., Herm-Gotz A., Tomavo S., Soldati T., and Soldati D. Toxoplasma gondii myosins B/C: one gene, two tails, two localizations, and a role in parasite division. J. Cell Biol. 155 (2001) 613-623
20. Dobbelaere D.A., and Rottenberg S. Theileria-induced leukocyte transformation. Curr. Opin. Microbiol. 6 (2003) 377-382
21. Dondorp A.M., Desakorn V., Pongtavornpinyo W., Sahassananda D., Silamut K., Chotivanich K., Newton P.N., Pitisuttithum P., Smithyman A.M., White N.J., and Day N.P. Estimation of the total parasite biomass in acute falciparum malaria from plasma PfHRP2. PLoS Med. 2 (2005) e204
22. Dubremetz J.F. Ultrastructural study of schizogonic mitosis in the coccidian, Eimeria necatrix (Johnson 1930). J. Ultrastruct. Res. 42 (1973) 354-376
23. Dzierszinski F., Nishi M., Ouko L., and Roos D.S. Dynamics of Toxoplasma gondii differentiation. Eukaryot. Cell 3 (2004) 992-1003
24. Ferguson D.J., Hutchison W.M., Dunachie J.F., and Siim J.C. Ultrastructural study of early stages of asexual multiplication and microgametogony of Toxoplasma gondii in the small intestine of the cat. Acta Pathol. Microbiol. Scand. B Microbiol. Immunol. 82 (1974) 167-181
25. Ferguson D.J., and Hutchison W.M. Comparison of the development of avirulent and virulent strains of Toxoplasma gondii in the peritoneal exudate of mice. Ann. Trop. Med. Parasitol. 75 (1981) 539-546
26. Ferguson D.J., and Hutchison W.M. An ultrastructural study of the early development and tissue cyst formation of Toxoplasma gondii in the brains of mice. Parasitol. Res. 73 (1987) 483-491
27. Ferguson D.J., Huskinson-Mark J., Araujo F.G., and Remington J.S. A morphological study of chronic cerebral toxoplasmosis in mice. comparison of four different strains of Toxoplasma gondii. Parasitol. Res. 80 (1994) 493-501
28. Ferguson D.J. Toxoplasma gondii and sex: essential or optional extra?. Trends Parasitol. 18 (2002) 355-359
29. Ferguson D.J., Campbell S.A., Henriquez F.L., Phan L., Mui E., Richards T.A., Muench S.P., Allary M., Lu J.Z., Prigge S.T., Tomley F., Shirley M.W., Rice D.W., McLeod R., and Roberts C.W. Enzymes of type II fatty acid synthesis and apicoplast differentiation and division in Eimeria tenella. Int. J. Parasitol. 37 (2007) 33-51
30. Ferguson D.J., Sahoo N., Pinches R.A., Bumstead J.M., Tomley F.M., and Gubbels M.J. MORN1 has a conserved role in asexual and sexual development across the Apicomplexa. Eukaryot. Cell 7 (2008) 698-711
31. Frankel M.B., Mordue D.G., and Knoll L.J. Discovery of parasite virulence genes reveals a unique regulator of chromosome condensation 1 ortholog critical for efficient nuclear trafficking. Proc. Nat. Acad. Sci. USA 104 (2007) 10181-10186
32. Gaskins E., Gilk S., DeVore N., Mann T., Ward G., and Beckers C. Identification of the membrane receptor of a class XIV myosin in Toxoplasma gondii. J. Cell Biol. 165 (2004) 383-393
33. Glotzer M. The molecular requirements for cytokinesis. Science (New York, NY) 307 (2005) 1735-1739
34. Gordon, J.L., Beatty, W.L., Sibley, L.D., 2008. A novel actin-related protein is associated with daughter cell formation in Toxoplasma. Eukaryot. Cell.
35. Grallert A., Krapp A., Bagley S., Simanis V., and Hagan I.M. Recruitment of NIMA kinase shows that maturation of the S. Pombe spindle-pole body occurs over consecutive cell cycles and reveals a role for NIMA in modulating SIN activity. Genes. Dev. 18 (2004) 1007-1021
36. Gubbels M.J., Wieffer M., and Striepen B. Fluorescent protein tagging in Toxoplasma gondii: identification of a novel inner membrane complex component conserved among Apicomplexa. Mol. Biochem. Parasitol. 137 (2004) 99-110
37. Gubbels M.J., Vaishnava S., Boot N., Dubremetz J.F., and Striepen B. A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus. J. Cell Sci. 119 (2006) 2236-2245
38. Gubbels M.J., Lehmann M., Muthalagi M., Jerome M.E., Brooks C.F., Szatanek T., Flynn J., Parrot B., Radke J., Striepen B., and White M.W. Forward Genetic Analysis of the Apicomplexan Cell Division Cycle in Toxoplasma gondii. PLoS Pathog. 4 (2008) e36
39. Guerini M.N., Que X., Reed S.L., and White M.W. Two genes encoding unique proliferating-cell-nuclear-antigens are expressed in Toxoplasma gondii. Mol. Biochem. Parasitol. 109 (2000) 121-131
40. Guerini M.N., Behnke M.S., and White M.W. Biochemical and genetic analysis of the distinct proliferating cell nuclear antigens of Toxoplasma gondii. Mol. Biochem. Parasitol. 142 (2005) 56-65
41. Hammarton T.C., Monnerat S., and Mottram J.C. Cytokinesis in trypanosomatids. Curr. Opin. Microbiol. 10 (2007) 520-527
42. Hammond D.M. The Coccidia: Eimeria, Isospora, Toxoplasma and Related Genera (1973), University Park Press, Baltimore, MD
43. Hartmann J., Hu K., He C.Y., Pelletier L., Roos D.S., and Warren G. Golgi and centrosome cycles in Toxoplasma gondii. Mol. Biochem. Parasitol. 145 (2006) 125-127
44. Hartwell L.H., and Unger M.W. Unequal division in Saccharomyces cerevisiae and its implications for the control of cell division. J. Cell Biol. 75 (1977) 422-435
45. He C.Y., Shaw M.K., Pletcher C.H., Striepen B., Tilney L.G., and Roos D.S. A plastid segregation defect in the protozoan parasite Toxoplasma gondii. EMBO J. 20 (2001) 330-339
46. Hidalgo Carcedo C., Bonazzi M., Spano S., Turacchio G., Colanzi A., Luini A., and Corda D. Mitotic Golgi partitioning is driven by the membrane-fissioning protein CtBP3/BARS. Science (New York, NY) 305 (2004) 93-96
47. Hu K., Mann T., Striepen B., Beckers C.J., Roos D.S., and Murray J.M. Daughter cell assembly in the protozoan parasite Toxoplasma gondii. Mol. Biol. Cell 13 (2002) 593-606
48. Hu K., Roos D.S., Angel S.O., and Murray J.M. Variability and heritability of cell division pathways in Toxoplasma gondii. J. Cell Sci. 117 (2004) 5697-5705
49. Hu K., Johnson J., Florens L., Fraunholz M., Suravajjala S., DiLullo C., Yates J., Roos D.S., and Murray J.M. Cytoskeletal components of an invasion machine - the apical complex of Toxoplasma gondii. PLoS Pathog. 2 (2006) 121-138
50. Hu K. Organizational changes of the daughter basal complex during the parasite replication of Toxoplasma gondii. PLoS Pathog. 4 (2008) e10
51. Janse C.J., van der Klooster P.F., van der Kaay H.J., van der Ploeg M., and Overdulve J.P. DNA synthesis in Plasmodium berghei during asexual and sexual development. Mol. Biochem. Parasitol. 20 (1986) 173-182
52. Janse C.J., Van der Klooster P.F., Van der Kaay H.J., Van der Ploeg M., and Overdulve J.P. Rapid repeated DNA replication during microgametogenesis and DNA synthesis in young zygotes of Plasmodium berghei. Trans. R. Soc. Trop. Med. Hyg. 80 (1986) 154-157
53. Jerome M.E., Radke J.R., Bohne W., Roos D.S., and White M.W. Toxoplasma gondii bradyzoites form spontaneously during sporozoite-initiated development. Infect. Immun. 66 (1998) 4838-4844
54. Kerk D., Templeton G., and Moorhead G.B. Evolutionary radiation pattern of novel protein phosphatases revealed by analysis of protein data from the completely sequenced genomes of humans, green algae, and higher plants. Plant Physiol. 146 (2008) 351-367
55. Kim J., and Kipreos E.T. Control of the Cdc6 replication licensing factor in metazoa: the role of nuclear export and the CUL4 ubiquitin ligase. Cell Cycle 7 (2008) 146-150 (Georgetown Tex)
56. Krien M.J., West R.R., John U.P., Koniaras K., McIntosh J.R., and O'Connell M.J. The fission yeast NIMA kinase Fin1p is required for spindle function and nuclear envelope integrity. EMBO J. 21 (2002) 1713-1722
57. Kvaal C.A., Radke J.R., Guerini M.N., and White M.W. Isolation of a Toxoplasma gondii cyclin by yeast two-hybrid interactive screen. Mol. Biochem. Parasitol. 120 (2002) 187-194
58. Lechtreck K.F. Striated fiber assemblin in apicomplexan parasites. Mol. Biochem. Parasitol. 128 (2003) 95-99
59. Mann T., Gaskins E., and Beckers C. Proteolytic Processing of TgIMC1 during Maturation of the Membrane Skeleton of Toxoplasma gondii. J. Biol. Chem. 277 (2002) 41240-41246
60. McDonald V., Shirley M.W., and Bellatti M.A. Eimeria maxima: characteristics of attenuated lines obtained by selection for precocious development in the chicken. Exp. Parasitol. 61 (1986) 192-200
61. McDonald V., and Shirley M.W. The endogenous development of virulent strains and attenuated precocious lines of Eimeria tenella and E. Necatrix. J. Parasitol. 73 (1987) 993-997
62. Meissner M., Breinich M.S., Gilson P.R., and Crabb B.S. Molecular genetic tools in Toxoplasma and Plasmodium: achievements and future needs. Curr. Opin. Microbiol. 10 (2007) 349-356
63. Merckx A., Le Roch K., Nivez M.P., Dorin D., Alano P., Gutierrez G.J., Nebreda A.R., Goldring D., Whittle C., Patterson S., Chakrabarti D., and Doerig C. Identification and initial characterization of three novel cyclin-related proteins of the human malaria parasite Plasmodium falciparum. J. Biol. Chem. 278 (2003) 39839-39850
64. Moon S.K., Jung S.Y., Choi Y.H., Lee Y.C., Patterson C., and Kim C.H. PDTC, metal chelating compound, induces G1 phase cell cycle arrest in vascular smooth muscle cells through inducing p21Cip1 expression: involvement of p38 mitogen activated protein kinase. J. Cell. Physiol. 198 (2004) 310-323
65. Morrissette N.S., and Sibley L.D. Disruption of microtubules uncouples budding and nuclear division in Toxoplasma gondii. J. Cell Sci. 115 (2002) 1017-1025
66. Nagamune K., Hicks L.M., Fux B., Brossier F., Chini E.N., and Sibley L.D. Abscisic acid controls calcium-dependent egress and development in Toxoplasma gondii. Nature 451 (2008) 207-210
67. Nishi M., Hu K., Murray J.M., and Roos D.S. Organellar dynamics during the cell cycle of Toxoplasma gondii. J. Cell Sci. (2008) 1559-1568
68. Nurse P.M. Nobel Lecture. Cyclin dependent kinases and cell cycle control. Biosci. Rep. 22 (2002) 487-499
69. O'Regan L., Blot J., and Fry A.M. Mitotic regulation by NIMA-related kinases. Cell Div. 2 (2007) 25
70. Pelletier L., Stern C.A., Pypaert M., Sheff D., Ngo H.M., Roper N., He C.Y., Hu K., Toomre D., Coppens I., Roos D.S., Joiner K.A., and Warren G. Golgi biogenesis in Toxoplasma gondii. Nature 418 (2002) 548-552
71. Pfefferkorn E.R., and Pfefferkorn L.C. Toxoplasma gondii: isolation and preliminary characterization of temperature-sensitive mutants. Exp. Parasitol. 39 (1976) 365-376
72. Piekarski G., Pelster B., and Witte H.M. Endopolygeny in Toxoplasma gondii. Zeitschrift fur Parasitenkunde 36 (1971) 122-130
73. Radke J.R., and White M.W. A cell cycle model for the tachyzoite of Toxoplasma gondii using the Herpes simplex virus thymidine kinase. Mol. Biochem. Parasitol. 94 (1998) 237-247
74. Radke J.R., Guerini M.N., and White M.W. Toxoplasma gondii: characterization of temperature-sensitive tachyzoite cell cycle mutants. Exp. Parasitol. 96 (2000) 168-177
75. Radke J.R., Striepen B., Guerini M.N., Jerome M.E., Roos D.S., and White M.W. Defining the cell cycle for the tachyzoite stage of Toxoplasma gondii. Mol. Biochem. Parasitol. 115 (2001) 165-175
76. Radke J.R., Guerini M.N., Jerome M., and White M.W. A change in the premitotic period of the cell cycle is associated with bradyzoite differentiation in Toxoplasma gondii. Mol. Biochem. Parasitol. 131 (2003) 119-127
77. Reilly H.B., Wang H., Steuter J.A., Marx A.M., and Ferdig M.T. Quantitative dissection of clone-specific growth rates in cultured malaria parasites. Int. J. Parasitol. 37 (2007) 1599-1607
78. Rieder C.L., Khodjakov A., Paliulis L.V., Fortier T.M., Cole R.W., and Sluder G. Mitosis in vertebrate somatic cells with two spindles: implications for the metaphase/anaphase transition checkpoint and cleavage. Proc. Natl. Acad. Sci. USA 94 (1997) 5107-5112
79. Salisbury J.L., Baron A.T., and Sanders M.A. The centrin-based cytoskeleton of Chlamydomonas reinhardtii: distribution in interphase and mitotic cells. J. Cell Biol. 107 (1988) 635-641
80. Schrevel J., Asfaux-Foucher G., and Bafort J.M. Ultrastructural study of multiple mitoses during sporogony of Plasmodium b. Berghei. J. Ultrastruct. Res. 59 (1977) 332-350
81. Senaud J. Contribution a l'etude de Sarcospridies et des Toxoplasmes (Toxoplasmea). Protistologica 3 (1967) 167-232
82. Shaw M.K., Compton H.L., Roos D.S., and Tilney L.G. Microtubules, but not actin filaments, drive daughter cell budding and cell division in Toxoplasma gondii. J. Cell Sci. 113 Pt 7 (2000) 1241-1254
83. Shaw M.K., Roos D.S., and Tilney L.G. DNA replication and daughter cell budding are not tightly linked in the protozoan parasite Toxoplasma gondii. Microbes Infect. 3 (2001) 351-362
84. Sheffield H.G., and Melton M.L. The fine structure and reproduction of Toxoplasma gondii. J. Parasitol. 54 (1968) 209-226
85. Simanis V. Events at the end of mitosis in the budding and fission yeasts. J. Cell Sci. 116 (2003) 4263-4275
86. Sinden R.E. Mitosis and meiosis in malarial parasites. Acta Leidensia 60 (1991) 19-27
87. Stokkermans T.J., Schwartzman J.D., Keenan K., Morrissette N.S., Tilney L.G., and Roos D.S. Inhibition of Toxoplasma gondii replication by dinitroaniline herbicides. Exp. Parasitol. 84 (1996) 355-370
88. Striepen B., Jordan C.N., Reiff S., and van Dooren G.G. Building the perfect parasite: cell division in apicomplexa. PLoS Pathog. 3 (2007) e78
89. Su J.Y., and Maller J.L. Cloning and expression of a Xenopus gene that prevents mitotic catastrophe in fission yeast. Mol. Gen. Genet. 246 (1995) 387-396
90. Tan A.L., Rida P.C., and Surana U. Essential tension and constructive destruction: the spindle checkpoint and its regulatory links with mitotic exit. Biochem. J. 386 (2005) 1-13
91. Taylor S., Barragan A., Su C., Fux B., Fentress S.J., Tang K., Beatty W.L., Hajj H.E., Jerome M., Behnke M.S., White M., Wootton J.C., and Sibley L.D. A secreted serine-threonine kinase determines virulence in the eukaryotic pathogen Toxoplasma gondii. Science 314 (2006) 1776-1780
92. Timms R., Colegrave N., Chan B.H., and Read A.F. The effect of parasite dose on disease severity in the rodent malaria Plasmodium chabaudi. Parasitology 123 (2001) 1-11
93. Trinkle-Mulcahy L., and Lamond A.I. Mitotic phosphatases: no longer silent partners. Curr. Opin. Cell. Biol. 18 (2006) 623-631
94. Vaishnava S., Morrison D.P., Gaji R.Y., Murray J.M., Entzeroth R., Howe D.K., and Striepen B. Plastid segregation and cell division in the apicomplexan parasite Sarcocystis neurona. J. Cell Sci. 118 (2005) 3397-3407
95. Vivier E., and Petitprez A. The outer membrane complex and its development at the time of the formation of daughter cells in Toxoplasma gondii. J. Cell Biol. 43 (1969) 329-342
96. Vivier E. Further observations on the asexual reproduction of Toxoplasma gondii and considerations on the concept of endogenesis. C. R. Hebd. Seances Acad. Sci. 271 (1970) 2123-2126
97. Ward P., Equinet L., Packer J., and Doerig C. Protein kinases of the human malaria parasite Plasmodium falciparum: the kinome of a divergent eukaryote. BMC Genomics 5 (2004) 79
98. White M.W., Jerome M.E., Vaishnava S., Guerini M., Behnke M., and Striepen B. Genetic rescue of a Toxoplasma gondii conditional cell cycle mutant. Mol. Microbiol. 55 (2005) 1060-1071
99. White M.W., Radke J., Conde de Felipe M., and Lehmann M. Cell Cycle Control/Parasite Division (2007), Horizon Scientific Press, Norwich, UK