Malaria Parasites: Genomes and Molecular Biology
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Introduction: The Plasmodium falciparum Genome Project
Carucci, Goodwin, Gottlieb and McGovern

No Abstract is available for this chapter, therefore we present the first paragraph of the chapter..

The Birth of the Project
Malaria is responsible for more than a million deaths a year, and up to 500 million people suffer from this disease. In response to this growing global crisis a group of 30 international researchers and funders gathered in May 1996 to discuss an exciting but daunting new project- obtaining the complete genome sequence of a malaria pathogen. At that time only small viral genomes and the bacterium Haemophilus influenzae (1.83Mb) had been completely sequenced. Although there were on-going projects to sequence some larger eukaryotic genomes of model organisms, for example the 12 Mb genome of the yeast Saccharomyces cerevisiae and the 97Mb genome of the nematode worm, Caenorhabditis elegans, their completion required a very large international effort; and in 1996 it was inconceivable that a draft human genome sequence would be available by 2000. Sequencing the 14 chromosomes (30Mb of DNA) of Plasmodium falciparum, the most lethal of the malaria parasites infecting humans, was then a considerable technical challenge because of the AT-rich nature of the DNA, but the potential value of genomic approaches for drug and vaccine development were strong motivators for the multiyear, multimillion-dollar investment. Initially the Burroughs Wellcome Fund (BWF), The National Institute of Allergy and Infectious Diseases (NIAID), the U.S. Department of Defense (DoD) and the Wellcome Trust (WT) agreed to work collaboratively and complementarily on funding the project (Hoffman et al., 1997). The World Health Organization (WHO) joined the project in 1998.


Chapter 1: The Genome of Plasmodium falciparum
Neil Hall and Malcolm J. Gardner

Abstract
The Plasmodium falciparum genome project, initiated in 1996, was the first attempt to sequence a genome of a eukaryotic pathogen. Not only has the genome told us a lot about the biology of the parasite but since the sequence data started to be released onto public web sites, it has changed the way many Plasmodium laboratories have approached their research. Here we outline how the sequencing project was approached, and describe what the major findings have been from being able to look at the unusual genome of P. falciparum. We also attempt to foresee what impact genomics and comparative genomics will have on the field of malaria research.


Chapter 2: The Genome of Model Malaria Parasites, and Comparative Genomics
Jane Carlton, Joana Silva and Neil Hall

Abstract
The field of comparative genomics of malaria parasites has recently come of age with the completion of the whole genome sequences of the human malaria parasite Plasmodium falciparum and a rodent malaria model, Plasmodium yoelii yoelii. With several other genome sequencing projects of different model and human malaria parasite species underway, comparing genomes from multiple species has necessitated the development of improved informatics tools and analyses. Results from initial comparative analyses reveal striking conservation of gene synteny between malaria species within conserved chromosome cores, in contrast to reduced homology within subtelomeric regions, in line with previous findings on a smaller scale. Genes that elicit a host immune response are frequently found to be species-specific, although a large variant multigene family is common to many rodent malaria species and Plasmodium vivax. Sequence alignment of syntenic regions from multiple species has revealed the similarity between species in coding regions to be high relative to non-coding regions, and phylogenetic footprinting studies promise to reveal conserved motifs in the latter. Comparison of non-synonymous substitution rates between orthologous genes is proving a powerful technique for identifying genes under selection pressure, and may be useful for vaccine design. This is a stimulating time for comparative genomics of model and human malaria parasites, which promises to produce useful results for the development of antimalarial drugs and vaccines.


Chapter 3: Getting the Most out of Bioinformatics Resources
Jessica C. Kissinger and David S. Roos

Abstract
The recent publication of a complete reference sequence for the Plasmodium falciparum genome is a momentous event for malaria researchers. In addition, genomic and functional genomics data is now available for six further Plasmodium species and eight non-Plasmodium species of apicomplexan parasites. These datasets can greatly expedite the identification of candidate targets for drug, vaccine and diagnostic development, in addition to enhancing our basic understanding of malaria parasites. But how can researchers most effectively access and exploit genomic-scale data, integrating this information with the results from other experiments? Bioinformatics research is fundamentally no different from 'wet lab' experiments conducted at the bench, requiring an understanding of the starting reagents (databases), the strengths and weaknesses of experimental (computational) methods, and a critical analysis of the results obtained. This chapter discusses the nature and organization of data resources, strategies for data mining, and the interpretation of computational results.


Chapter 4: Manipulating the Plasmodium Genome
Teresa Gil Carvalho and Robert Ménard

Abstract
Genome manipulation, the primary tool for assigning function to sequence, will be essential for understanding Plasmodium biology and malaria pathogenesis in molecular terms. The first success in transfecting Plasmodium was reported almost ten years ago. Gene-targeting studies have since flourished, as Plasmodium is haploid and integrates DNA only by homologous recombination. These studies have shed new light on the function of many proteins, including vaccine candidates and drug resistance factors. However, many essential proteins, including those involved in parasite invasion of erythrocytes, cannot be characterized in the absence of conditional mutagenesis. Proteins also cannot be identified on a functional basis as random DNA integration has not been achieved. We overview here the ways in which the Plasmodium genome can be manipulated. We also point to the tools that should be established if our goal is to address parasite infectivity in a systematic way and to conduct refined structure-function analysis of selected products.


Chapter 5: Toxoplasma gondii a Model Organism for the Apicomplexans?
Dominique Soldati and Markus Meissner

Abstract
Toxoplasma gondii is closely related to the Plasmodium species sharing with them multiple structural and functional features but differing significantly in their mode of transmission and differentiation. The broad host range specificity and the robust nature of the extracellular form of T. gondii have facilitated its propagation in cell culture and led to the rapid development of genetic tools. Genetic manipulation has also revolutionized the research on Malaria and rather unexpectedly, some genetic properties differ significantly between T. gondii and P. falciparum imposing limits as to which strategies are specifically applicable to each of these parasites. Advantages, constraints are intrinsic to both systems and consequently our understanding of both parasites is not only complementary but also synergistic. The information obtained from the Plasmodium and several other Apicomplexa genomes have led to the identification of exciting new classes of genes that are restricted to the phylum and thus of considerable interest as potential targets for intervention. T. gondii is particularly amenable to ultrastructural and biochemical studies and some important findings regarding the composition and function of subcellular structures and organelles, unique metabolic pathways and mechanisms leading to the establishment of intracellular parasitism are of great significance for the malaria research.


Chapter 6: Microsatellite Markers and Population Genetics in Plasmodium falciparum
Deirdre Joy, Jianbing Mu, and Xin-zhuan Su

Abstract
Microsatellites are short (2-6 bp in length) tandemly repeated sequences. They have been shown to be abundant in the Plasmodium falciparum genome and as such will play a significant role in the study of malaria in the post-genome era. Microsatellites are useful for dissecting gene function, identifying vaccine candidates and drug targets, and elucidating the evolutionary history of the malaria parasite. With the availability of a high-density genetic marker map for P. falciparum, it is now possible to perform genome-wide allelic association studies for genes contribution to such specific phenotypes as drug resistance and virulence. Additionally, the application of a large number of microsatellite markers to field samples promises to reveal important information about population genetic structure, demographic history, and transmission dynamics.


Chapter 7: Chromosome Structure and Dynamics of Plasmodium Subtelomeres
Artur Scherf, Luisa M. Figueiredo and Lúcio H. Freitas-Junior

Abstract
Substantial gene synteny has been observed between malaria species. However, new data on the organization of plasmodial subtelomeres has recently become available and demonstrates that chromosome ends show, unlike the central region, a very dynamic evolution of its DNA sequence. Sequences of the subtelomere elements vary greatly among malaria species. Duplications among subtelomeres have created large families of expressed genes often encoding variable surface antigens. Fluorescence in situ hybridisation (FISH) combined with three-dimensional microscopy has demonstrated that chromosome ends in Plasmodium are not randomly arranged in the nucleus. Telomeres form clusters of 4 to 7 heterologous chromosome ends and are associated with the nuclear periphery. The physical alignment of subtelomeres promotes frequent recombination between members of telomere-associated virulence factor genes in heterologous chromosomes. This has important implications for the parasite survival and its adaptation to environmental stress.


Chapter 8: Gene Expression
Kirk W Deitsch

Abstract
The study of gene expression in malaria parasites has blossomed in recent years with the development and use of reporter gene constructs in transfection experiments and the recent release of the annotated sequence of the P. falciparum genome. The promoters and regulatory regions of many genes from several Plasmodium species have been characterized, however the exact nature of the transcription factors that bind them remain ill-defined. In addition, how expression of the large multigene families found in all Plasmodium genomes is regulated presents a particularly interesting problem. Recent findings with regard to the var gene family of P. falciparum may shed light on the topics of allelic exclusion and transcription switching that are important for understanding how expression of these gene families is controlled.


Chapter 9: Regulation of rRNA Transcription and Processing During the Plasmodium Life Cycle
Thomas F. McCutchan, Rosalinda van Spaendonk, Chris Janse, Jun Fang, and Andrew P. Waters

Abstract
A remarkable feature of Plasmodium parasites is that they express structurally distinct sets of rRNA in a developmentally specific manner. The expression of three different rRNAs parallels the developmental cycle of the parasite. Parasites missing the rRNA genes predominantly expressed in the mosquito develop at a slower rate than wild type parasites but never the less develop fully. The normal cyclical pattern of expression is influenced by temperature and ambient glucose concentrations and changes in these factors can result in dramatic changes in the parasite's physiology. Variable forms of ribosomes are not unique to Plasmodium species. They are often found in plants and bacteria but alteration in these cases result from changes in the protein complement of the ribosome. Alteration of the rRNA itself occurs in Plasmodium species and presents opportunities to study a novel biochemical property of the parasite and to gain insights into RNA as a functional moiety.


Chapter 10: Cell Cycle Control in Plasmodium falciparum: A Genomics Perspective
Christian Doerig and Debopam Chakrabarti

Abstract
The molecular mechanisms regulating cell proliferation and development in malaria parasites are still largely unknown. Phenomenological observations, pertaining to the organisation of the cell cycle during schizogony or to the signal transduction pathways whose activation is responsible for the developmental stage transitions, can now be complemented with information gathered from genomic databases. The PlasmoDB database has been used extensively to identify putative homologues of a number of eukaryotic cell cycle regulators such as cyclins, cyclin-dependent kinases, factors involved in the control of DNA synthesis, and components of signal transduction pathways. However, gene identification based on sequence homology is limited by the fact that any Plasmodium-specific functional homologue will be missed by this approach. Furthermore, experimental data indicate that the structure of some regulatory pathways (unlike that of metabolic pathways) cannot be deducted directly from database mining. Because of these limitations in the direct exploitation of genomic database, elucidation of the organisation of the signal transduction and cell cycle machineries requires experimental, proteomics-based approaches such as the characterisation of protein complexes containing cell cycle regulators and the establishment of a map of protein-protein interactions involving these elements.


Chapter 11: The Apicoplast
Ross F. Waller and Geoff I. McFadden

Abstract
The apicoplast is a semi-autonomous plastid organelle that is homologous to chloroplasts of plants. It occurs throughout the Apicomplexa and is an ancient feature of this group acquired by the process of endosymbiosis. Like plant chloroplasts, apicoplasts are semi-autonomous with their own genome and expression machinery. In addition, apicoplasts import numerous proteins encoded by nuclear genes. These nuclear genes largely derive from the endosymbiont through a process of intracellular gene relocation. The exact role of a plastid in parasites is uncertain but early clues indicate synthesis of lipids, heme and isoprenoids as possibilities. The various metabolic processes of the apicoplast are potentially excellent targets for drug therapy.


Chapter 12: The Surface of the Plasmodium falciparum-infected Erythrocyte
Joseph D. Smith and Alister G. Craig

Abstract
In order to navigate its complex lifecycle, the malaria parasites must interact with a range of host cells. Examples of this are the invasion of hepatocytes by sporozoites and erythrocyte invasion by merozoites. This requirement for cell recognition brings with it the need to display cognate ligands on the parasite surface, and therefore the capacity of the host to develop defences against the infection. Even at a stage where the intracellular nature of erythrocyte development would appear to offer an opportunity for the parasite to be immunologically "silent", parasite-derived proteins are found on the surface of the infected erythrocyte. This review will discuss the proteins found on or associated with the surface of the infected erythrocyte and the resulting phenotypes.


Chapter 13: Merozoite Cell Biology
Agnieszka E. Topolska, Lina Wang, Casilda G. Black and Ross L. Coppel

Abstract
The merozoite of the asexual stage parasite is adapted for the invasion of the red blood cell. Specific structures of the merozoite such as the filamentous surface coat and the secretory organelles of the rhoptries, micronemes and dense granules participate in this process. The repertoire of proteins in these locations participate in a specific set of receptor-ligand interactions, some still poorly understood, that trigger the secretion of products from specialized organelles and the activation of a molecular motor. There is redundancy in the parasite ligands involved and genomic analysis is revealing a large set of gene products that are potentially involved in invasion.


Chapter 14: Sexual Development of Malaria Parasites
C.J. Janse and A.P. Waters,

Abstract
Malaria parasites switch from asexual proliferation to a sexual cycle of development in the blood of a vertebrate host in order to transmit between the vertebrate and mosquito host. The central role of sexual development in the life cycle and transmission of Plasmodium parasites make the sexual stages, such as the gametes and zygotes, attractive targets for interruption strategies to prevent transmission of the disease (for example transmission blocking vaccines). Here we review the knowledge on the cellular and molecular processes involved in sexual differentiation, i.e. the development of gametocytes and gametes, fertilization and zygote formation. In contrast to rapidly expanding molecular knowledge of asexual multiplication of malaria parasites, the molecular mechanisms of sexual differentiation are still largely unknown. However, with the availability of the genome sequence of different Plasmodium species combined with post-genomic technologies this situation will change. Insight into molecular processes underlying sexual development and the proteins involved will maximise numbers of candidate proteins available for consideration as transmission blocking vaccine candisdates and will allow researchers and policy makers to make rational, informed decisions about the proteins considered for components of a multi-stage vaccine.


Chapter 15: Ookinete Cell Biology
R.E. Sinden, Y.I.H. Alavi, G.A. Butcher, J.T. Dessens, J.D. Raine, and H.E. Trueman

Abstract
Recent advances in our understanding of the molecular and morphological development of the malarial zygote into a mature invasive ookinete are described. The similarities and more particularly the differences of this development to sporozoite and merozoite differentiation are emphasised. Notable differences include the absences rhoptries, the formation of just one apical complex during meiosis, and the formation of a pore-containing inner pellicular complex. The impact of both vertebrate and mosquito components of the bloodmeal on ookinete development are discussed. The destructive events of invasion of the midgut wall and oocyst differentiation are described and the potential interactions between the parasite and the mosquito immune system outlined. The very successful efforts to develop vaccines targeted to the ookinete are summarised. The contrasting lack of drugs that block transmission through the vector is highlighted.


Chapter 16: Molecular and Cellular Biology of Chloroquine Resistance in Plasmodium falciparum
Karena L. Waller, Sylvia Lee and David A. Fidock

Abstract
For decades, the 4-aminoquinoline chloroquine (CQ1) was the mainstay of antimalarial chemotherapy, with its characteristic properties of rapid efficacy, safety and affordability. However, resistance to this drug has now become prevalent in the majority of malaria-endemic countries and is severely limiting its use as an effective antimalarial. CQ is believed to act against CQ sensitive (CQS) malaria parasites by accumulating inside the digestive vacuole (DV) of the intra-erythrocytic parasite, where CQ binds to heme (ferriprotoporphyrin IX, or FPIX) that is liberated during hemoglobin degradation. The resulting impairment in heme detoxification results in parasite death. Chloroquine resistance (CQR) in Plasmodium falciparum is defined in vitro by elevated CQ IC50 values, reduced CQ accumulation and the ability of verapamil (VP) to reverse (or "chemosensitize") these two traits. Molecular genetic and epidemiological investigations have recently revealed an association between P. falciparum CQR and the presence of multiple amino acid mutations in the DV transmembrane protein PfCRT (P. falciparum chloroquine resistance transporter). Allelic exchange experiments have now definitively demonstrated that mutant pfcrt alleles present in different malaria-endemic continents can confer CQR to CQS parasites. Investigations into other candidate genetic determinants have demonstrated that mutations in the parasite protein Pgh1 (P. falciparum P-glycoprotein homologue 1, also localized to the parasite DV membrane and encoded by the pfmdr1 gene) can modulate the CQR phenotype of parasites, but are not sufficient to confer CQR in vitro. Recent clinical studies demonstrate an increased risk of CQ treatment failure in patients harboring parasites with CQR-associated mutations in pfcrt and sometimes pfmdr1. Other factors, including host immunity, are also important in determining clinical outcome. In vitro, the CQR phenotype may be intimately associated with changes in the physiological processes of the DV, such as altered DV pH. These changes may critically impact the access of CQ to hematin dimers that act as a drug receptor in the DV. Alternatively, mutant PfCRT may contribute to CQR by physically interacting with CQ, leading to increased drug efflux. Ongoing studies, bolstered by recent advances in Plasmodium genetics, genomics and proteomics, can be expected to significantly deepen our understanding of the genetic basis of P. falciparum CQR, the relationship between CQR and DV physiology, and the effect of CQR on the parasite response to other heme-binding antimalarials. The knowledge gained from these studies will be of greatest benefit when they can be translated into new therapies to treat drug-resistant malaria.


1 ADQ, amodiaquine; AO, acridine orange; CQ, chloroquine; CQS, chloroquine sensitive; CQR, chloroquine resistance (or chloroquine resistant); DV, digestive vacuole; FPIX, ferriprotoporphyrin IX; iRBC, infected red blood cells; Pgh1, P-glycoprotein; RBC, red blood cells, SP, sulfadoxine-pyrimethamine; UTR, untranslated region; WHO, World Health Organization.

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