Mitosis in the Human Malaria Parasite Plasmodium falciparum

ABSTRACT Malaria is caused by intraerythrocytic protozoan parasites belonging to Plasmodium spp. (phylum Apicomplexa) that produce significant morbidity and mortality, mostly in developing countries. Plasmodium parasites have a complex life cycle that includes multiple stages in anopheline mosquito vectors and vertebrate hosts. During the life cycle, the parasites undergo several cycles of extreme population growth within a brief span, and this is critical for their continued transmission and a contributing factor for their pathogenesis in the host. As with other eukaryotes, successful mitosis is an essential requirement for Plasmodium reproduction; however, some aspects of Plasmodium mitosis are quite distinct and not fully understood. In this review, we will discuss the current understanding of the architecture and key events of mitosis in Plasmodium falciparum and related parasites and compare them with the traditional mitotic events described for other eukaryotes.

[1]  C. Rieder.  Mitosis in vertebrates: the G2/M and M/A transitions and their associated checkpoints , 2011, Chromosome Research.

[2]  Danny W. Wilson,et al.  Super-resolution dissection of coordinated events during malaria parasite invasion of the human erythrocyte. , 2011, Cell host & microbe.

[3]  D. Miranda-Saavedra,et al.  An essential Aurora-related kinase transiently associates with spindle pole bodies during Plasmodium falciparum erythrocytic schizogony , 2011, Molecular microbiology.

[4]  Alex Bateman,et al.  The Systematic Functional Analysis of Plasmodium Protein Kinases Identifies Essential Regulators of Mosquito Transmission , 2010, Cell host & microbe.

[5]  Yixian Zheng.  A membranous spindle matrix orchestrates cell division , 2010, Nature Reviews Molecular Cell Biology.

[6]  N. Waters,et al.  Leveraging cell cycle analysis in anticancer drug discovery to identify novel plasmodial drug targets. , 2010, Infectious disorders drug targets.

[7]  James R. Brown,et al.  Thousands of chemical starting points for antimalarial lead identification , 2010, Nature.

[8]  E. Winzeler,et al.  A Plant-Like Kinase in Plasmodium falciparum Regulates Parasite Egress from Erythrocytes , 2010, Science.

[9]  D. Chakrabarti,et al.  A Plasmodium falciparum Transcriptional Cyclin-Dependent Kinase-Related Kinase with a Crucial Role in Parasite Proliferation Associates with Histone Deacetylase Activity , 2010, Eukaryotic Cell.

[10]  S. Osmani,et al.  Double duty for nuclear proteins--the price of more open forms of mitosis. , 2009, Trends in genetics : TIG.

[11]  A. Vaughan,et al.  Malaria parasite development in the mosquito and infection of the mammalian host. , 2009, Annual review of microbiology.

[12]  R. Ménard,et al.  Signalling in malaria parasites. The MALSIG consortium. , 2009, Parasite.

[13]  R. Sinden.  Malaria, sexual development and transmission: retrospect and prospect , 2009, Parasitology.

[14]  R. Tewari,et al.  An Essential Role for the Plasmodium Nek-2 Nima-related Protein Kinase in the Sexual Development of Malaria Parasites , 2009, The Journal of Biological Chemistry.

[15]  D. Goldberg,et al.  A calpain unique to alveolates is essential in Plasmodium falciparum and its knockdown reveals an involvement in pre-S-phase development , 2009, Proceedings of the National Academy of Sciences.

[16]  L. Aravind,et al.  Centrins, Cell Cycle Regulation Proteins in Human Malaria Parasite Plasmodium falciparum* , 2008, Journal of Biological Chemistry.

[17]  R. Rosenberg.  Malaria: some considerations regarding parasite productivity. , 2008, Trends in parasitology.

[18]  M. Gubbels,et al.  The cell cycle and Toxoplasma gondii cell division: tightly knit or loosely stitched? , 2008, International journal for parasitology.

[19]  A. Scherf,et al.  Differential association of Orc1 and Sir2 proteins to telomeric domains in Plasmodium falciparum , 2008, Journal of Cell Science.

[20]  A. Bell,et al.  Isotype expression, post-translational modification and stage-dependent production of tubulins in erythrocytic Plasmodium falciparum. , 2008, International journal for parasitology.

[21]  J. M. Behnke.  Structure in parasite component communities in wild rodents: predictability, stability, associations and interactions .... or pure randomness? , 2008, Parasitology.

[22]  S. Kyes,et al.  Nuclear Non-coding RNAs Are Transcribed from the Centromeres of Plasmodium falciparum and Are Associated with Centromeric Chromatin* , 2008, Journal of Biological Chemistry.

[23]  D. Ferguson,et al.  MORN1 Has a Conserved Role in Asexual and Sexual Development across the Apicomplexa , 2008, Eukaryotic Cell.

[24]  B. Striepen,et al.  Forward Genetic Analysis of the Apicomplexan Cell Division Cycle in Toxoplasma gondii , 2008, PLoS pathogens.

[25]  Tomoyuki U. Tanaka,et al.  Kinetochore microtubule interaction during S phase in Saccharomyces cerevisiae. , 2007, Genes & development.

[26]  A. Sicard,et al.  Disruption of the PfPK7 Gene Impairs Schizogony and Sporogony in the Human Malaria Parasite Plasmodium falciparum , 2007, Eukaryotic Cell.

[27]  M. Ferdig,et al.  Quantitative dissection of clone-specific growth rates in cultured malaria parasites. , 2007, International journal for parasitology.

[28]  J. Salisbury.  A mechanistic view on the evolutionary origin for centrin‐based control of centriole duplication , 2007, Journal of cellular physiology.

[29]  L. Bannister,et al.  Vesicle trafficking during sporozoite development in Plasmodium berghei: ultrastructural evidence for a novel trafficking mechanism , 2007, Parasitology.

[30]  F. Gergely,et al.  Aurora-A: the maker and breaker of spindle poles , 2007, Journal of Cell Science.

[31]  A. Cowman,et al.  Re-assessing the locations of components of the classical vesicle-mediated trafficking machinery in transfected Plasmodium falciparum. , 2007, International journal for parasitology.

[32]  S. Osmani,et al.  Mitosis, Not Just Open or Closed , 2007, Eukaryotic Cell.

[33]  M. Bornens,et al.  Structure and duplication of the centrosome , 2007, Journal of Cell Science.

[34]  G. V. van Dooren,et al.  Building the Perfect Parasite: Cell Division in Apicomplexa , 2007, PLoS pathogens.

[35]  Leann Tilley,et al.  Illuminating Plasmodium falciparum-infected red blood cells. , 2007, Trends in parasitology.

[36]  E. Salmon,et al.  The spindle-assembly checkpoint in space and time , 2007, Nature Reviews Molecular Cell Biology.

[37]  L. Schofield.  Intravascular infiltrates and organ‐specific inflammation in malaria pathogenesis , 2007, Immunology and cell biology.

[38]  J. A. Vaughan.  Population dynamics of Plasmodium sporogony. , 2007, Trends in parasitology.

[39]  A. Bell,et al.  Studies on cell-cycle synchronization in the asexual erythrocytic stages of Plasmodium falciparum , 2006, Parasitology.

[40]  Rogerio Amino,et al.  Manipulation of Host Hepatocytes by the Malaria Parasite for Delivery into Liver Sinusoids , 2006, Science.

[41]  B. Striepen,et al.  A MORN-repeat protein is a dynamic component of the Toxoplasma gondii cell division apparatus , 2006, Journal of Cell Science.

[42]  Angus Bell,et al.  Cellular and molecular actions of dinitroaniline and phosphorothioamidate herbicides on Plasmodium falciparum: tubulin as a specific antimalarial target. , 2006, Molecular and biochemical parasitology.

[43]  L. Ranford-Cartwright,et al.  Spreading the seeds of million-murdering death: metamorphoses of malaria in the mosquito. , 2005, Trends in parasitology.

[44]  Matthias Marti,et al.  Re-defining the Golgi complex in Plasmodium falciparum using the novel Golgi marker PfGRASP , 2005, Journal of Cell Science.

[45]  C. Janse,et al.  Plasmodium berghei α-tubulin II: A role in both male gamete formation and asexual blood stages , 2005 .

[46]  Oliver Billker,et al.  A NIMA-related Protein Kinase Is Essential for Completion of the Sexual Cycle of Malaria Parasites* , 2005, Journal of Biological Chemistry.

[47]  B. Striepen,et al.  Plastid segregation and cell division in the apicomplexan parasite Sarcocystis neurona , 2005, Journal of Cell Science.

[48]  Christopher J. Tonkin,et al.  Development of the endoplasmic reticulum, mitochondrion and apicoplast during the asexual life cycle of Plasmodium falciparum , 2005, Molecular microbiology.

[49]  E. Rocha,et al.  The unusually large Plasmodium telomerase reverse-transcriptase localizes in a discrete compartment associated with the nucleolus , 2005, Nucleic acids research.

[50]  D. Carucci,et al.  Molecular approaches to malaria , 2004, Molecular microbiology.

[51]  L. Bannister,et al.  Correlation of structural development and differential expression of invasion-related molecules in schizonts of Plasmodium falciparum , 2004, Parasitology.

[52]  M. Bornens,et al.  Fission yeast cdc31p is a component of the half-bridge and controls SPB duplication. , 2003, Molecular biology of the cell.

[53]  L. Bannister,et al.  The ins, outs and roundabouts of malaria. , 2003, Trends in parasitology.

[54]  J. Endicott,et al.  Cyclin-dependent kinase homologues of Plasmodium falciparum. , 2002, International journal for parasitology.

[55]  S. Krishna,et al.  A brief illustrated guide to the ultrastructure of Plasmodium falciparum asexual blood stages. , 2000, Parasitology today.

[56]  S. Krishna,et al.  Ultrastructure of rhoptry development in Plasmodium falciparum erythrocytic schizonts , 2000, Parasitology.

[57]  M. Bornens,et al.  A Role for Centrin 3 in Centrosome Reproduction , 2000, The Journal of cell biology.

[58]  K. Gull,et al.  The Plasmodium cell-cycle: facts and questions. , 1998, Annals of tropical medicine and parasitology.

[59]  V. Sinou,et al.  Host Cell and Malarial Targets for Docetaxel (Taxotere™) during the Erythrocytic Development of Plasmodium falciparum , 1998, The Journal of eukaryotic microbiology.

[60]  J. E. Hyde,et al.  On malaria and the cell cycle. , 1997, Parasitology today.

[61]  H. Rubin,et al.  Malaria and the cell cycle. , 1996, Parasitology today.

[62]  J. E. Hyde,et al.  Microtubular organization visualized by immunofluorescence microscopy during erythrocytic schizogony in Plasmodium falciparum and investigation of post-translational modifications of parasite tubulin , 1993, Parasitology.

[63]  R. Rosenberg,et al.  The number of sporozoites produced by individual malaria oocysts. , 1991, The American journal of tropical medicine and hygiene.

[64]  M. van der Ploeg,et al.  DNA synthesis in gametocytes of Plasmodium falciparum , 1988, Parasitology.

[65]  C. Slomianny,et al.  The karyotype of Plasmodium falciparum determined by ultrastructural serial sectioning and 3D reconstruction. , 1986, The Journal of parasitology.

[66]  M. van der Ploeg,et al.  DNA synthesis in Plasmodium berghei during asexual and sexual development. , 1986, Molecular and biochemical parasitology.

[67]  R. Sinden,et al.  Gametocyte and gamete development in Plasmodium falciparum , 1978, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[68]  J. Schrével,et al.  Etude ultrastructurale des mitoses multiples au cours de la sporogonie du Plasmodium b. berghei , 1977 .

[69]  M. Aikawa.  Plasmodium: The fine structure of malarial parasites , 1971 .

[70]  M. Aikawa,et al.  STUDIES ON NUCLEAR DIVISION OF A MALARIAL PARASITE UNDER PYRIMETHAMINE TREATMENT , 1968, The Journal of cell biology.

[71]  P. G. Shute,et al.  Pre-erythrocytic Stage of Plasmodium Falciparum , 1949, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[72]  D. Arnot,et al.  The progression of the intra-erythrocytic cell cycle of Plasmodium falciparum and the role of the centriolar plaques in asynchronous mitotic division during schizogony. , 2011, International journal for parasitology.

[73]  C. Janse,et al.  Plasmodium berghei alpha-tubulin II: a role in both male gamete formation and asexual blood stages. , 2005, Molecular and biochemical parasitology.

[74]  O. Billker,et al.  Gametocytes and Gametes , 2005 .

[75]  C. Rieder,et al.  Re-staging mitosis: a contemporary view of mitotic progression , 2001, Nature Cell Biology.

[76]  T. Mitchison,et al.  Mitosis: a history of division , 2001, Nature Cell Biology.

[77]  J. Beier,et al.  Malaria parasite development in mosquitoes. , 1998, Annual review of entomology.

[78]  Irwin W. Sherman,et al.  Malaria : parasite biology, pathogenesis, and protection , 1998 .

[79]  J. Salisbury.  Centrin, centrosomes, and mitotic spindle poles. , 1995, Current opinion in cell biology.

[80]  R. Sinden,et al.  Mitosis and meiosis in malarial parasites. , 1991, Acta Leidensia.

[81]  A. van Belkum,et al.  Plasmodium falciparum: studies on mature exoerythrocytic forms in the liver of the chimpanzee, Pan troglodytes. , 1990, Experimental parasitology.

[82]  M. van der Ploeg,et al.  Rapid repeated DNA replication during microgametogenesis and DNA synthesis in young zygotes of Plasmodium berghei. , 1986, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[83]  P. Garnham,et al.  The life-cycle of primate malaria parasites. , 1982, British medical bulletin.

[84]  I. Heath.  Variant mitoses in lower eukaryotes: indicators of the evolution of mitosis. , 1980, International review of cytology.

[85]  J. Schrével,et al.  [Ultrastructural study of multiple mitoses during sporogony of Plasmodium b. berghei]. , 1977, Journal of ultrastructure research.

[86]  J. Dubremetz.  [Ultrastructural study of schizogonic mitosis in the coccidian, Eimeria necatrix (Johnson 1930)]. , 1973, Journal of ultrastructure research.

[87]  J. Dubremetz.  Etude ultrastructurale de la mitose schizogonique chez la coccidie Eimeria necatrix (Johnson 1930. , 1973 .

[88]  M. Aikawa.  Parasitological review. Plasmodium: the fine structure of malarial parasites. , 1971, Experimental parasitology.