Genome evolution in trypanosomatid parasites

SUMMARY A decade of genome sequencing has transformed our understanding of how trypanosomatid parasites have evolved and provided fresh impetus to explaining the origins of parasitism in the Kinetoplastida. In this review, I will consider the many ways in which genome sequences have influenced our view of genomic reduction in trypanosomatids; how species-specific genes, and the genomic domains they occupy, have illuminated the innovations in trypanosomatid genomes; and how comparative genomics has exposed the molecular mechanisms responsible for innovation and adaptation to a parasitic lifestyle.

[1]  E. Ullu,et al.  The emerging role of RNA‐binding proteins in the life cycle of Trypanosoma brucei , 2014, Cellular microbiology.

[2]  Mark C. Field,et al.  The Streamlined Genome of Phytomonas spp. Relative to Human Pathogenic Kinetoplastids Reveals a Parasite Tailored for Plants , 2014, PLoS genetics.

[3]  T. Williams,et al.  Reduction and Expansion in Microsporidian Genome Evolution: New Insights from Comparative Genomics , 2013, Genome biology and evolution.

[4]  K. Matthews,et al.  Bloodstream form pre-adaptation to the tsetse fly in Trypanosoma brucei , 2013, Front. Cell. Infect. Microbiol..

[5]  A. Todeschini,et al.  Inhibitory Effects of Trypanosoma cruzi Sialoglycoproteins on CD4+ T Cells Are Associated with Increased Susceptibility to Infection , 2013, PloS one.

[6]  V. Coustou,et al.  Identification of Trans-Sialidases as a Common Mediator of Endothelial Cell Activation by African Trypanosomes , 2013, PLoS pathogens.

[7]  A. Kondrashov,et al.  Paratrypanosoma Is a Novel Early-Branching Trypanosomatid , 2013, Current Biology.

[8]  B. Garat,et al.  Implication of CA repeated tracts on post-transcriptional regulation in Trypanosoma cruzi. , 2013, Experimental parasitology.

[9]  D. Sánchez,et al.  TcTASV-C, a Protein Family in Trypanosoma cruzi that Is Predominantly Trypomastigote-Stage Specific and Secreted to the Medium , 2013, PloS one.

[10]  P. Mieczkowski,et al.  The Genome Sequence of Leishmania (Leishmania) amazonensis: Functional Annotation and Extended Analysis of Gene Models , 2013, DNA research : an international journal for rapid publication of reports on genes and genomes.

[11]  J. Barry,et al.  Mosaic VSGs and the Scale of Trypanosoma brucei Antigenic Variation , 2013, PLoS pathogens.

[12]  L. Flohé,et al.  Trypanothione-based redox metabolism of trypanosomatids. , 2013 .

[13]  Jacqueline A. Keane,et al.  The genomes of four tapeworm species reveal adaptations to parasitism , 2013, Nature.

[14]  Mark C. Field,et al.  A Cell-surface Phylome for African Trypanosomes , 2013, PLoS neglected tropical diseases.

[15]  R. Mortara,et al.  Distinct genomic organization, mRNA expression and cellular localization of members of two amastin sub-families present in Trypanosoma cruzi , 2013, BMC Microbiology.

[16]  E. Ullu,et al.  Developmental Progression to Infectivity in Trypanosoma brucei Triggered by an RNA-Binding Protein , 2012, Science.

[17]  M. Mann,et al.  Comparative Proteomics of Two Life Cycle Stages of Stable Isotope-labeled Trypanosoma brucei Reveals Novel Components of the Parasite's Host Adaptation Machinery* , 2012, Molecular & Cellular Proteomics.

[18]  T. Ochsenreiter,et al.  Proteome remodelling during development from blood to insect-form Trypanosoma brucei quantified by SILAC and mass spectrometry , 2012, BMC Genomics.

[19]  M. Shapira,et al.  Gene duplication in trypanosomatids - two DED1 paralogs are functionally redundant and differentially expressed during the life cycle. , 2012, Molecular and biochemical parasitology.

[20]  H. Luján,et al.  In silico analysis of trypanosomatids' helicases. , 2012, FEMS microbiology letters.

[21]  R. Soares,et al.  Glycoconjugates in New World species of Leishmania: polymorphisms in lipophosphoglycan and glycoinositolphospholipids and interaction with hosts. , 2012, Biochimica et biophysica acta.

[22]  D. Bartholomeu,et al.  The MASP Family of Trypanosoma cruzi: Changes in Gene Expression and Antigenic Profile during the Acute Phase of Experimental Infection , 2012, PLoS neglected tropical diseases.

[23]  J. Ruiz,et al.  Anatomy and evolution of telomeric and subtelomeric regions in the human protozoan parasite Trypanosoma cruzi , 2012, BMC Genomics.

[24]  Michael A. J. Ferguson,et al.  Comparative SILAC Proteomic Analysis of Trypanosoma brucei Bloodstream and Procyclic Lifecycle Stages , 2012, PLoS ONE.

[25]  A. Frasch,et al.  A 43-Nucleotide U-rich Element in 3′-Untranslated Region of Large Number of Trypanosoma cruzi Transcripts Is Important for mRNA Abundance in Intracellular Amastigotes* , 2012, The Journal of Biological Chemistry.

[26]  D. Salmon,et al.  Cytokinesis of Trypanosoma brucei bloodstream forms depends on expression of adenylyl cyclases of the ESAG4 or ESAG4‐like subfamily , 2012, Molecular microbiology.

[27]  A. Osuna,et al.  Multigene Families in Trypanosoma cruzi and Their Role in Infectivity , 2012, Infection and Immunity.

[28]  Christiane Hertz-Fowler,et al.  Antigenic diversity is generated by distinct evolutionary mechanisms in African trypanosome species , 2012, Proceedings of the National Academy of Sciences.

[29]  J. Donelson,et al.  Mapping of VSG similarities in Trypanosoma brucei. , 2012, Molecular and biochemical parasitology.

[30]  Pawel Herzyk,et al.  Chromosome and gene copy number variation allow major structural change between species and strains of Leishmania. , 2011, Genome research.

[31]  M. Quail,et al.  Whole genome sequencing of multiple Leishmania donovani clinical isolates provides insights into population structure and mechanisms of drug resistance. , 2011, Genome research.

[32]  Anton J. Enright,et al.  Evolutionary and functional insights into Leishmania META1: evidence for lateral gene transfer and a role for META1 in secretion , 2011, BMC Evolutionary Biology.

[33]  G. Rudenko.  African trypanosomes: the genome and adaptations for immune evasion. , 2011, Essays in biochemistry.

[34]  D. Bartholomeu,et al.  Genomic Analyses, Gene Expression and Antigenic Profile of the Trans-Sialidase Superfamily of Trypanosoma cruzi Reveal an Undetected Level of Complexity , 2011, PloS one.

[35]  Mario Stanke,et al.  Genome sequencing of the lizard parasite Leishmania tarentolae reveals loss of genes associated to the intracellular stage of human pathogenic species , 2011, Nucleic acids research.

[36]  Fernán Agüero,et al.  Molecular diversity of the Trypanosoma cruzi TcSMUG family of mucin genes and proteins. , 2011, The Biochemical journal.

[37]  P. Alzari,et al.  Crystal structure of an enzymatically inactive trans-sialidase-like lectin from Trypanosoma cruzi: the carbohydrate binding mechanism involves residual sialidase activity. , 2011, Biochimica et biophysica acta.

[38]  G. Buck,et al.  Identification and Phylogenetic Analysis of Heme Synthesis Genes in Trypanosomatids and Their Bacterial Endosymbionts , 2011, PloS one.

[39]  Jeremy D. DeBarry,et al.  Genome cartography: charting the apicomplexan genome. , 2011, Trends in parasitology.

[40]  A. Alonso,et al.  Proteome Profiling of Leishmania Infantum Promastigotes , 2011, The Journal of eukaryotic microbiology.

[41]  Alejandro Sanchez-Flores,et al.  High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. , 2011, Genome research.

[42]  J. Donelson,et al.  Differential protein expression throughout the life cycle of Trypanosoma congolense, a major parasite of cattle in Africa , 2011, Molecular and biochemical parasitology.

[43]  G. Van der Auwera,et al.  Comparative Gene Expression Analysis throughout the Life Cycle of Leishmania braziliensis: Diversity of Expression Profiles among Clinical Isolates , 2011, PLoS neglected tropical diseases.

[44]  Songnian Hu,et al.  An evolutionary analysis of trypanosomatid GP63 proteases , 2011, Parasitology Research.

[45]  P. Volf,et al.  The stage-regulated HASPB and SHERP proteins are essential for differentiation of the protozoan parasite Leishmania major in its sand fly vector, Phlebotomus papatasi , 2010, Cellular microbiology.

[46]  D. Horn,et al.  Molecular mechanisms underlying the control of antigenic variation in African trypanosomes , 2010, Current opinion in microbiology.

[47]  P. Bastien,et al.  Targeting essential pathways in trypanosomatids gives insights into protozoan mechanisms of cell death , 2010, Parasites & Vectors.

[48]  V. Parro,et al.  Transcriptomics throughout the life cycle of Leishmania infantum: high down-regulation rate in the amastigote stage. , 2010, International journal for parasitology.

[49]  M. Olivier,et al.  Leishmania-Induced Inactivation of the Macrophage Transcription Factor AP-1 Is Mediated by the Parasite Metalloprotease GP63 , 2010, PLoS pathogens.

[50]  D. Sánchez,et al.  TcTASV: A Novel Protein Family in Trypanosoma cruzi Identified from a Subtractive Trypomastigote cDNA Library , 2010, PLoS neglected tropical diseases.

[51]  G. Rudenko.  Epigenetics and transcriptional control in African trypanosomes. , 2010, Essays in biochemistry.

[52]  D. Depledge,et al.  Leishmania-Specific Surface Antigens Show Sub-Genus Sequence Variation and Immune Recognition , 2010, PLoS neglected tropical diseases.

[53]  T. Samuelsson,et al.  Analysis of Gene Order Conservation in Eukaryotes Identifies Transcriptionally and Functionally Linked Genes , 2010, PloS one.

[54]  Xuning Wang,et al.  Genome-wide analysis of mRNA abundance in two life-cycle stages of Trypanosoma brucei and identification of splicing and polyadenylation sites , 2010, Nucleic acids research.

[55]  M. Quail,et al.  The Genome Sequence of Trypanosoma brucei gambiense, Causative Agent of Chronic Human African Trypanosomiasis , 2010, PLoS neglected tropical diseases.

[56]  O. Gascuel,et al.  New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. , 2010, Systematic biology.

[57]  A. MacLeod,et al.  Digital gene expression analysis of two life cycle stages of the human-infective parasite, Trypanosoma brucei gambiense reveals differentially expressed clusters of co-regulated genes , 2010, BMC Genomics.

[58]  J. Lukeš,et al.  Evolution of the haem synthetic pathway in kinetoplastid flagellates: an essential pathway that is not essential after all? , 2010, International journal for parasitology.

[59]  G. Wei,et al.  Characterization of Major Surface Protease Homologues of Trypanosoma congolense , 2010, Journal of biomedicine & biotechnology.

[60]  R. Mortara,et al.  The TryPIKinome of five human pathogenic trypanosomatids: Trypanosoma brucei, Trypanosoma cruzi, Leishmania major, Leishmania braziliensis and Leishmania infantum--new tools for designing specific inhibitors. , 2009, Biochemical and biophysical research communications.

[61]  K. Gull,et al.  Cell morphogenesis of Trypanosoma brucei requires the paralogous, differentially expressed calpain-related proteins CAP5.5 and CAP5.5V. , 2009, Protist.

[62]  C. Yao.  Major Surface Protease of Trypanosomatids: One Size Fits All? , 2009, Infection and Immunity.

[63]  P. Myler,et al.  Widespread variation in transcript abundance within and across developmental stages of Trypanosoma brucei , 2009, BMC Genomics.

[64]  J. Ramirez,et al.  Localization and Developmental Regulation of a Dispersed Gene Family 1 Protein in Trypanosoma cruzi , 2009, Infection and Immunity.

[65]  M. Tremblay,et al.  Leishmania GP63 Alters Host Signaling Through Cleavage-Activated Protein Tyrosine Phosphatases , 2009, Science Signaling.

[66]  A. Jackson.  The Evolution of Amastin Surface Glycoproteins in Trypanosomatid Parasites , 2009, Molecular biology and evolution.

[67]  D. B. Weatherly,et al.  The steady-state transcriptome of the four major life-cycle stages of Trypanosoma cruzi , 2009, BMC Genomics.

[68]  D. Horn,et al.  What has DNA sequencing revealed about the VSG expression sites of African trypanosomes? , 2009, Trends in parasitology.

[69]  A. Ivens,et al.  Comparative Expression Profiling of Leishmania: Modulation in Gene Expression between Species and in Different Host Genetic Backgrounds , 2009, PLoS neglected tropical diseases.

[70]  G. Cross,et al.  Epigenetic regulation in African trypanosomes: a new kid on the block , 2009, Nature Reviews Microbiology.

[71]  John P. Overington,et al.  The genome of the blood fluke Schistosoma mansoni , 2009, Nature.

[72]  V. Parro,et al.  Genome-wide analysis reveals increased levels of transcripts related with infectivity in peanut lectin non-agglutinated promastigotes of Leishmania infantum. , 2009, Genomics.

[73]  G J Ebrahim,et al.  Neglected tropical diseases , 2005, BMJ : British Medical Journal.

[74]  F. Bringaud,et al.  Organization and evolution of two SIDER retroposon subfamilies and their impact on the Leishmania genome , 2009, BMC Genomics.

[75]  F. Raymond,et al.  Whole-genome comparative RNA expression profiling of axenic and intracellular amastigote forms of Leishmania infantum. , 2009, Molecular and biochemical parasitology.

[76]  R. Mortara,et al.  Homology, paralogy and function of DGF-1, a highly dispersed Trypanosoma cruzi specific gene family and its implications for information entropy of its encoded proteins. , 2009, Molecular and biochemical parasitology.

[77]  A. Torrecilhas,et al.  GPIomics: global analysis of glycosylphosphatidylinositol-anchored molecules of Trypanosoma cruzi , 2009, Molecular systems biology.

[78]  G. Cerqueira,et al.  Genomic organization and expression profile of the mucin-associated surface protein (masp) family of the human pathogen Trypanosoma cruzi , 2009, Nucleic acids research.

[79]  W. McMaster,et al.  The Leishmania Surface Protease GP63 Cleaves Multiple Intracellular Proteins and Actively Participates in p38 Mitogen-activated Protein Kinase Inactivation* , 2009, Journal of Biological Chemistry.

[80]  B. McGwire,et al.  Trypanosoma cruzi GP63 Proteins Undergo Stage-Specific Differential Posttranslational Modification and Are Important for Host Cell Infection , 2009, Infection and Immunity.

[81]  Michael J. Dagley,et al.  The single mitochondrial porin of Trypanosoma brucei is the main metabolite transporter in the outer mitochondrial membrane. , 2008, Molecular biology and evolution.

[82]  B. Wickstead,et al.  Bioinformatic insights to the ESAG5 and GRESAG5 gene families in kinetoplastid parasites. , 2008, Molecular and biochemical parasitology.

[83]  R. Krauth-Siegel,et al.  Redox control in trypanosomatids, parasitic protozoa with trypanothione-based thiol metabolism. , 2008, Biochimica et biophysica acta.

[84]  Christiane Hertz-Fowler,et al.  Telomeric Expression Sites Are Highly Conserved in Trypanosoma brucei , 2008, PloS one.

[85]  A. Devault,et al.  The promastigote surface antigen gene family of the Leishmania parasite: differential evolution by positive selection and recombination , 2008, BMC Evolutionary Biology.

[86]  A. Khamesipour,et al.  Leishmania surface protein gp63 binds directly to human natural killer cells and inhibits proliferation , 2008, Clinical and experimental immunology.

[87]  Jacques Corbeil,et al.  Genome-wide gene expression profiling analysis of Leishmania major and Leishmania infantum developmental stages reveals substantial differences between the two species , 2008, BMC Genomics.

[88]  Dan Zilberstein,et al.  Post‐translational modification of cellular proteins during Leishmania donovani differentiation , 2008, Proteomics.

[89]  F. Opperdoes,et al.  Retooling Leishmania metabolism: from sand fly gut to human macrophage , 2008, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[90]  Barbara Papadopoulou,et al.  Developmental regulation of gene expression in trypanosomatid parasitic protozoa. , 2007, Current opinion in microbiology.

[91]  J. Huxley-Jones,et al.  The TriTryp Phosphatome: analysis of the protein phosphatase catalytic domains , 2007, BMC Genomics.

[92]  A. Jackson.  Evolutionary consequences of a large duplication event in Trypanosoma brucei: Chromosomes 4 and 8 are partial duplicons , 2007, BMC Genomics.

[93]  J. Donelson,et al.  A Function for a Specific Zinc Metalloprotease of African Trypanosomes , 2007, PLoS pathogens.

[94]  F. Opperdoes,et al.  Horizontal gene transfer in trypanosomatids. , 2007, Trends in parasitology.

[95]  L. Marcello,et al.  Analysis of the VSG gene silent archive in Trypanosoma brucei reveals that mosaic gene expression is prominent in antigenic variation and is favored by archive substructure. , 2007, Genome research.

[96]  Elodie Ghedin,et al.  Members of a Large Retroposon Family Are Determinants of Post-Transcriptional Gene Expression in Leishmania , 2007, PLoS pathogens.

[97]  M. Giardini,et al.  Telomere biology of trypanosomatids: beginning to answer some questions. , 2007, Trends in parasitology.

[98]  Nicola G. Jones,et al.  Variant Surface Glycoprotein gene repertoires in Trypanosoma brucei have diverged to become strain-specific , 2007, BMC Genomics.

[99]  Brian White,et al.  Comparative genomic analysis of three Leishmania species that cause diverse human disease , 2007, Nature Genetics.

[100]  S. Natesan,et al.  Intracellular Trafficking in the Trypanosomatids , 2007, Traffic.

[101]  A. Jackson.  Tandem gene arrays in Trypanosoma brucei: Comparative phylogenomic analysis of duplicate sequence variation , 2007, BMC Evolutionary Biology.

[102]  K. Leifso,et al.  Genomic and proteomic expression analysis of Leishmania promastigote and amastigote life stages: the Leishmania genome is constitutively expressed. , 2007, Molecular and biochemical parasitology.

[103]  P. Myler,et al.  Analysis of the Leishmania donovani transcriptome reveals an ordered progression of transient and permanent changes in gene expression during differentiation. , 2007, Molecular and biochemical parasitology.

[104]  Terry K. Smith,et al.  A novel phospholipase from Trypanosoma brucei , 2007, Molecular microbiology.

[105]  I. Roditi,et al.  A family of stage‐specific alanine‐rich proteins on the surface of epimastigote forms of Trypanosoma brucei , 2007, Molecular microbiology.

[106]  Fernán Agüero,et al.  Two metallocarboxypeptidases from the protozoan Trypanosoma cruzi belong to the M32 family, found so far only in prokaryotes. , 2006, The Biochemical journal.

[107]  W. McMaster,et al.  The major surface‐metalloprotease of the parasitic protozoan, Leishmania, protects against antimicrobial peptide‐induced apoptotic killing , 2006, Molecular microbiology.

[108]  A. Frasch,et al.  Procyclic Trypanosoma brucei Expresses Separate Sialidase and trans-Sialidase Enzymes on Its Surface Membrane* , 2006, Journal of Biological Chemistry.

[109]  K. Gull,et al.  Comparative genomics and concerted evolution of β-tubulin paralogs in Leishmania spp , 2006, BMC Genomics.

[110]  S. Schaeffer,et al.  The ornithine decarboxylase gene of Trypanosoma brucei: Evidence for horizontal gene transfer from a vertebrate source. , 2006, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[111]  A. Simpson,et al.  The evolution and diversity of kinetoplastid flagellates. , 2006, Trends in parasitology.

[112]  Timothy R Holzer,et al.  Expression profiling by whole-genome interspecies microarray hybridization reveals differential gene expression in procyclic promastigotes, lesion-derived amastigotes, and axenic amastigotes in Leishmania mexicana. , 2006, Molecular and biochemical parasitology.

[113]  A. Frasch,et al.  Trypanosoma cruzi surface mucins: host-dependent coat diversity , 2006, Nature Reviews Microbiology.

[114]  F. Opperdoes,et al.  The presence of four iron-containing superoxide dismutase isozymes in trypanosomatidae: characterization, subcellular localization, and phylogenetic origin in Trypanosoma brucei. , 2006, Free radical biology & medicine.

[115]  D. Rigden,et al.  Autophagy and Related processes in Trypanosomatids: Insights from Genomic and Bioinformatic Analyses , 2006, Autophagy.

[116]  D. Tweardy,et al.  INFECTION AND IMMUNITY , 2006, Infection and Immunity.

[117]  C. Slamovits,et al.  Causes and effects of nuclear genome reduction. , 2005, Current opinion in genetics & development.

[118]  W. Degrave,et al.  Trypanosoma cruzi proline racemases are involved in parasite differentiation and infectivity , 2005, Molecular microbiology.

[119]  Mark C. Field.  Signalling the genome: the Ras-like small GTPase family of trypanosomatids. , 2005, Trends in parasitology.

[120]  M. Parsons,et al.  Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi , 2005, BMC Genomics.

[121]  B. Haas,et al.  The Genome Sequence of Trypanosoma cruzi, Etiologic Agent of Chagas Disease , 2005, Science.

[122]  David M. A. Martin,et al.  The Genome of the African Trypanosome Trypanosoma brucei , 2005, Science.

[123]  F. Opperdoes,et al.  The Trypanosoma cruzi Proteome , 2005, Science.

[124]  Heather J Munden,et al.  The Genome of the Kinetoplastid Parasite, Leishmania major , 2005, Science.

[125]  Daniel Nilsson,et al.  Comparative Genomics of Trypanosomatid Parasitic Protozoa , 2005, Science.

[126]  M. Bergeron,et al.  Characterization and developmental gene regulation of a large gene family encoding amastin surface proteins in Leishmania spp. , 2005, Molecular and biochemical parasitology.

[127]  J. Dujardin,et al.  Complexity of the major surface protease (msp) gene organization in Leishmania (Viannia) braziliensis: evolutionary and functional implications , 2005, Parasitology.

[128]  P. Myler,et al.  Telomere and subtelomere of Trypanosoma cruzi chromosomes are enriched in (pseudo)genes of retrotransposon hot spot and trans-sialidase-like gene families: the origins of T. cruzi telomeres. , 2005, Gene.

[129]  Erin E. Gill,et al.  Early evolution within kinetoplastids (euglenozoa), and the late emergence of trypanosomatids. , 2004, Protist.

[130]  J. Donelson,et al.  Genetic complementation of Leishmania deficient in PSA (GP46) restores their resistance to lysis by complement. , 2004, Molecular and biochemical parasitology.

[131]  D. Moreira,et al.  An updated view of kinetoplastid phylogeny using environmental sequences and a closer outgroup: proposal for a new classification of the class Kinetoplastea. , 2004, International journal of systematic and evolutionary microbiology.

[132]  G. Stormo,et al.  Expression profiling using random genomic DNA microarrays identifies differentially expressed genes associated with three major developmental stages of the protozoan parasite Leishmania major. , 2004, Molecular and biochemical parasitology.

[133]  E. Chao,et al.  Ribosomal RNA Phylogeny of Bodonid and Diplonemid Flagellates and the Evolution of Euglenozoa , 2004, The Journal of eukaryotic microbiology.

[134]  A. Frasch,et al.  The Surface Coat of the Mammal-dwelling Infective Trypomastigote Stage of Trypanosoma cruzi Is Formed by Highly Diverse Immunogenic Mucins* , 2004, Journal of Biological Chemistry.

[135]  Samuel V. Angiuoli,et al.  Gene synteny and evolution of genome architecture in trypanosomatids. , 2004, Molecular and biochemical parasitology.

[136]  D. Sánchez,et al.  gp63 Homologues in Trypanosoma cruzi: Surface Antigens with Metalloprotease Activity and a Possible Role in Host Cell Infection , 2003, Infection and Immunity.

[137]  J. Donelson,et al.  Expression and Function of the Trypanosoma brucei Major Surface Protease (GP63) Genes* , 2003, Journal of Biological Chemistry.

[138]  N. Hall,et al.  The architecture of variant surface glycoprotein gene expression sites in Trypanosoma brucei. , 2002, Molecular and biochemical parasitology.

[139]  M. Ouellette,et al.  Pterin transport and metabolism in Leishmania and related trypanosomatid parasites. , 2002, International journal for parasitology.

[140]  R. Litaker,et al.  Molecular Taxonomy of the Suborder Bodonina (Order Kinetoplastida), Including the Important Fish Parasite, Ichthyobodo necator , 2002, The Journal of eukaryotic microbiology.

[141]  K. Gull,et al.  CAP5.5, a life-cycle-regulated, cytoskeleton-associated protein is a member of a novel family of calpain-related proteins in Trypanosoma brucei. , 2001, Molecular and biochemical parasitology.

[142]  I. C. Almeida,et al.  The mucin-like glycoprotein super-family of Trypanosoma cruzi: structure and biological roles. , 2001, Molecular and biochemical parasitology.

[143]  E Pays,et al.  The VSG expression sites of Trypanosoma brucei: multipurpose tools for the adaptation of the parasite to mammalian hosts. , 2001, Molecular and biochemical parasitology.

[144]  M. Lynch,et al.  The evolutionary fate and consequences of duplicate genes. , 2000, Science.

[145]  A. Coutinho,et al.  A B-cell mitogen from a pathogenic trypanosome is a eukaryotic proline racemase , 2000, Nature Medicine.

[146]  J. Barry,et al.  A structural and transcription pattern for variant surface glycoprotein gene expression sites used in metacyclic stage Trypanosoma brucei. , 1999, Molecular and biochemical parasitology.

[147]  I. D. Algranati,et al.  Trypanosoma cruzi epimastigotes lack ornithine decarboxylase but can express a foreign gene encoding this enzyme , 1999, FEBS letters.

[148]  A. Furger,et al.  Unravelling the procyclin coat of Trypanosoma brucei. , 1998, Molecular and biochemical parasitology.

[149]  D. Nolan,et al.  Characterization of the ligand‐binding site of the transferrin receptor in Trypanosoma brucei demonstrates a structural relationship with the N‐terminal domain of the variant surface glycoprotein , 1997, The EMBO journal.

[150]  M. Ferguson.  The surface glycoconjugates of trypanosomatid parasites. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[151]  T. Wellems,et al.  Shared themes of antigenic variation and virulence in bacterial, protozoal, and fungal infections. , 1997, Microbiology and molecular biology reviews : MMBR.

[152]  L. Hardy,et al.  The Roles of Pteridine Reductase 1 and Dihydrofolate Reductase-Thymidylate Synthase in Pteridine Metabolism in the Protozoan Parasite Leishmania major* , 1997, The Journal of Biological Chemistry.

[153]  R. Cappai,et al.  The Leishmania promastigote surface antigen 2 complex is differentially expressed during the parasite life cycle. , 1995, Molecular and biochemical parasitology.

[154]  M. Kavanaugh,et al.  A Family of Putative Receptor-Adenylate Cyclases from Leishmania donovani(*) , 1995, The Journal of Biological Chemistry.

[155]  L. Vanhamme,et al.  Control of gene expression in trypanosomes. , 1995, Microbiological reviews.

[156]  L. Hardy,et al.  PTR1: a reductase mediating salvage of oxidized pteridines and methotrexate resistance in the protozoan parasite Leishmania major. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[157]  K. Ziegelbauer,et al.  Organization of two invariant surface glycoproteins in the surface coat of Trypanosoma brucei , 1993, Infection and immunity.

[158]  D. Jackson,et al.  The identification, purification, and characterization of two invariant surface glycoproteins located beneath the surface coat barrier of bloodstream forms of Trypanosoma brucei. , 1993, The Journal of biological chemistry.

[159]  J. Beck,et al.  Nutritional requirements of wild-type and folate transport-deficient Leishmania donovani for pterins and folates. , 1990, Molecular and biochemical parasitology.

[160]  D. Nelson,et al.  Purine metabolism in Leishmania donovani and Leishmania braziliensis. , 1978, Biochimica et biophysica acta.

[161]  K. Chang,et al.  Heme biosynthesis in bacterium-protozoon symbioses: enzymic defects in host hemoflagellates and complemental role of their intracellular symbiotes. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[162]  Dr. Susumu Ohno.  Evolution by Gene Duplication , 1970, Springer Berlin Heidelberg.

[163]  A. Todeschini,et al.  Trypanosoma cruzi Trans-sialidase: structural features and biological implications. , 2014, Sub-cellular biochemistry.

[164]  J. Lukeš,et al.  Diversity and phylogeny of insect trypanosomatids: all that is hidden shall be revealed. , 2013, Trends in parasitology.

[165]  Purificación López-García,et al.  Phylogenomic analysis of kinetoplastids supports that trypanosomatids arose from within bodonids. , 2011, Molecular biology and evolution.

[166]  S. Goldenberg,et al.  Aspects of Trypanosoma cruzi stage differentiation. , 2011, Advances in parasitology.

[167]  S. T. ´. E. G. Uindon,et al.  New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML , 2010 .

[168]  Terry K. Smith,et al.  Genome-wide expression profiling of in vivo- derived bloodstream parasite stages and dynamic analysis of mRNA alterations during synchronous differentiation in Trypanosoma brucei , 2009, BMC Genomics.

[169]  G. Cerqueira,et al.  Sequence diversity and evolution of multigene families in Trypanosoma cruzi. , 2008, Molecular and biochemical parasitology.

[170]  T. Holzer,et al.  Coordinate regulation of a family of promastigote-enriched mRNAs by the 3'UTR PRE element in Leishmania mexicana. , 2008, Molecular and biochemical parasitology.

[171]  D. Sánchez,et al.  Metacaspases of Trypanosoma cruzi: possible candidates for programmed cell death mediators. , 2006, Molecular and biochemical parasitology.

[172]  A. Fairlamb,et al.  Trypanothione biosynthesis in Leishmania major. , 2005, Molecular and biochemical parasitology.

[173]  T. Aoki,et al.  The Origin of Dihydroorotate Dehydrogenase Genes of Kinetoplastids, with Special Reference to Their Biological Significance and Adaptation to Anaerobic, Parasitic Conditions , 2004, Journal of Molecular Evolution.

[174]  J. Barry,et al.  Why are parasite contingency genes often associated with telomeres? , 2003, International journal for parasitology.

[175]  Shu-Kun Lin,et al.  What is molecular diversity? , 2003, Molecular diversity.

[176]  J. Donelson,et al.  The Genome of the African Trypanosome , 2002 .

[177]  E. Camargo,et al.  Phytomonas and other trypanosomatid parasites of plants and fruit. , 1999, Advances in parasitology.

[178]  ScienceDirect.  Molecular and biochemical parasitology , 1980 .

[179]  W. Gutteridge,et al.  A re-examination of purine and pyrimidine synthesis in the three main forms of Trypanosoma cruzi. , 1979, The International journal of biochemistry.

[180]  Edinburgh Research Explorer Developmental regulation and extracellular release of a VSG expression-site-associated gene product from Trypanosoma brucei bloodstream forms , 2022 .