The Comparative Genomics and Phylogenomics of Leishmania amazonensis Parasite

Leishmaniasis is an infectious disease caused by Leishmania species. Leishmania amazonensis is a New World Leishmania species belonging to the Mexicana complex, which is able to cause all types of leishmaniasis infections. The L. amazonensis reference strain MHOM/BR/1973/M2269 was sequenced identifying 8,802 codifying sequences (CDS), most of them of hypothetical function. Comparative analysis using six Leishmania species showed a core set of 7,016 orthologs. L. amazonensis and Leishmania mexicana share the largest number of distinct orthologs, while Leishmania braziliensis presented the largest number of inparalogs. Additionally, phylogenomic analysis confirmed the taxonomic position for L. amazonensis within the “Mexicana complex”, reinforcing understanding of the split of New and Old World Leishmania. Potential non-homologous isofunctional enzymes (NISE) were identified between L. amazonensis and Homo sapiens that could provide new drug targets for development.

[1]  Kary A. C. S. Ocaña,et al.  STINGRAY: system for integrated genomic resources and analysis , 2014, BMC Research Notes.

[2]  J. M. Requena,et al.  Evolution and species discrimination according to the Leishmania heat-shock protein 20 gene. , 2013, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[3]  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.

[4]  S. Eddy,et al.  Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions , 2013, Nucleic acids research.

[5]  E. Dias,et al.  Cluster randomised trial to evaluate the effectiveness of a vaccine against cutaneous leishmaniasis in the Caratinga microregion, south-east Brazil. , 2013, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[6]  M. Samant,et al.  Novel Features of a PIWI-Like Protein Homolog in the Parasitic Protozoan Leishmania , 2012, PloS one.

[7]  C. Laughton,et al.  Synthetic lethal targeting of DNA double‐strand break repair deficient cells by human apurinic/apyrimidinic endonuclease inhibitors , 2012, International journal of cancer.

[8]  D. Sundar,et al.  Epitopic analysis of Potential Vaccine Candidate in Leishmania infantum for Development of Human Vaccine , 2012 .

[9]  N. El-Sayed,et al.  Functional genomics of trypanosomatids , 2012, Parasite immunology.

[10]  S. Teixeira,et al.  Trypanosomatid comparative genomics: Contributions to the study of parasite biology and different parasitic diseases , 2012, Genetics and molecular biology.

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

[12]  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.

[13]  Haiming Wang,et al.  GeneDB—an annotation database for pathogens , 2011, Nucleic Acids Res..

[14]  Susumu Goto,et al.  KEGG for integration and interpretation of large-scale molecular data sets , 2011, Nucleic Acids Res..

[15]  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.

[16]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[17]  C. Muskus,et al.  Transfusion‐transmitted visceral leishmaniasis caused by Leishmania (Leishmania) mexicana in an immunocompromised patient: a case report , 2011, Transfusion.

[18]  M. Gramiccia,et al.  A gold-containing drug against parasitic polyamine metabolism: the X-ray structure of trypanothione reductase from Leishmania infantum in complex with auranofin reveals a dual mechanism of enzyme inhibition , 2011, Amino Acids.

[19]  A. D. de Miranda,et al.  Specific and Nonhomologous Isofunctional Enzymes of the Genetic Information Processing Pathways as Potential Therapeutical Targets for Tritryps , 2011, Enzyme research.

[20]  S. Krungkrai,et al.  Malaria parasite carbonic anhydrase: inhibition of aromatic/heterocyclic sulfonamides and its therapeutic potential. , 2011, Asian Pacific journal of tropical biomedicine.

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

[22]  Kary A. C. S. Ocaña,et al.  Phylogenomics-Based Reconstruction of Protozoan Species Tree , 2011, Evolutionary bioinformatics online.

[23]  L. Dardenne,et al.  Structural modelling and comparative analysis of homologous, analogous and specific proteins from Trypanosoma cruzi versus Homo sapiens: putative drug targets for chagas' disease treatment , 2010, BMC Genomics.

[24]  E. Ullu,et al.  Retention and Loss of RNA Interference Pathways in Trypanosomatid Protozoans , 2010, PLoS pathogens.

[25]  E. Cupolillo,et al.  Targeted gene expression profiling in Leishmania braziliensis and Leishmania guyanensis parasites isolated from Brazilian patients with different antimonial treatment outcomes. , 2010, Infection, genetics and evolution : journal of molecular epidemiology and evolutionary genetics in infectious diseases.

[26]  J. Mano,et al.  The Involvement of Lipid Peroxide-Derived Aldehydes in Aluminum Toxicity of Tobacco Roots1[W][OA] , 2009, Plant Physiology.

[27]  M. Walkinshaw,et al.  Crystal structures of Leishmania mexicana phosphoglycerate mutase suggest a one-metal mechanism and a new enzyme subclass. , 2009, Journal of molecular biology.

[28]  Scott Kennedy,et al.  Requirement for the ERI/DICER Complex in Endogenous RNA Interference and Sperm Development in Caenorhabditis elegans , 2009, Genetics.

[29]  W. Degrave,et al.  A new approach for potential drug target discovery through in silico metabolic pathway analysis using Trypanosoma cruzi genome information. , 2009, Memorias do Instituto Oswaldo Cruz.

[30]  D. Aubert,et al.  The role of ATP-binding cassette (ABC) proteins in protozoan parasites. , 2009, Molecular and biochemical parasitology.

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

[32]  Thomas M. Keane,et al.  ABACAS: algorithm-based automatic contiguation of assembled sequences , 2009, Bioinform..

[33]  Thomas D. Otto,et al.  AnEnPi: identification and annotation of analogous enzymes , 2008, BMC Bioinformatics.

[34]  Umakant Sharma,et al.  Insect vectors of Leishmania: distribution, physiology and their control. , 2008, Journal of vector borne diseases.

[35]  Cyrus Chothia,et al.  SUPERFAMILY—sophisticated comparative genomics, data mining, visualization and phylogeny , 2008, Nucleic Acids Res..

[36]  E. Birney,et al.  Velvet: algorithms for de novo short read assembly using de Bruijn graphs. , 2008, Genome research.

[37]  Gary Ruvkun,et al.  The exonuclease ERI-1 has a conserved dual role in 5.8S rRNA processing and RNAi , 2008, Nature Structural &Molecular Biology.

[38]  E. Birney,et al.  Pfam: the protein families database , 2013, Nucleic Acids Res..

[39]  Tim J. P. Hubbard,et al.  Data growth and its impact on the SCOP database: new developments , 2007, Nucleic Acids Res..

[40]  Marta Mattoso,et al.  ProtozoaDB: dynamic visualization and exploration of protozoan genomes , 2007, Nucleic Acids Res..

[41]  K. Wilson,et al.  Crystal structure and DNA repair activities of the AP endonuclease from Leishmania major. , 2007, Journal of molecular biology.

[42]  R. Peeling,et al.  Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? , 2007, Nature Reviews Microbiology.

[43]  P. Bates.  Transmission of Leishmania metacyclic promastigotes by phlebotomine sand flies , 2007, International journal for parasitology.

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

[45]  F. Ayala,et al.  Evolutionary and geographical history of the Leishmania donovani complex with a revision of current taxonomy , 2007, Proceedings of the National Academy of Sciences.

[46]  M. Miles,et al.  Glycoprotein 63 (gp63) genes show gene conversion and reveal the evolution of Old World Leishmania. , 2007, International journal for parasitology.

[47]  T. Hasan,et al.  Clinical manifestations and classification of Old World cutaneous leishmaniasis , 2007, International journal of dermatology.

[48]  E. Ullu,et al.  An unusual Dicer-like1 protein fuels the RNA interference pathway in Trypanosoma brucei. , 2006, RNA.

[49]  G. H. Coombs,et al.  Studies on the CPA cysteine peptidase in the Leishmania infantum genome strain JPCM5 , 2006, BMC Molecular Biology.

[50]  P. Leprohon,et al.  Modulation of Leishmania ABC Protein Gene Expression through Life Stages and among Drug-Resistant Parasites , 2006, Eukaryotic Cell.

[51]  S. Rafati,et al.  Amastin Peptide-Binding Antibodies as Biomarkers of Active Human Visceral Leishmaniasis , 2006, Clinical and Vaccine Immunology.

[52]  J. L. Martins,et al.  Antileishmanial activity of MDL 28170, a potent calpain inhibitor , 2006, International Journal of Antimicrobial Agents.

[53]  H. Cerutti,et al.  On the origin and functions of RNA-mediated silencing: from protists to man , 2006, Current Genetics.

[54]  B. Snel,et al.  Toward Automatic Reconstruction of a Highly Resolved Tree of Life , 2006, Science.

[55]  Paulo F. Pires,et al.  GARSA: genomic analysis resources for sequence annotation , 2005, Bioinform..

[56]  D. Inzé,et al.  Protection against Photooxidative Injury of Tobacco Leaves by 2-Alkenal Reductase. Detoxication of Lipid Peroxide-Derived Reactive Carbonyls1 , 2005, Plant Physiology.

[57]  K. Gull,et al.  Evolutionary Relationships and Protein Domain Architecture in an Expanded Calpain Superfamily in Kinetoplastid Parasites , 2005, Journal of Molecular Evolution.

[58]  Matthew Berriman,et al.  ACT: the Artemis comparison tool , 2005, Bioinform..

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

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

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

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

[63]  S. Briggs,et al.  Enterococcus faecalis phosphomevalonate kinase , 2005, Protein science : a publication of the Protein Society.

[64]  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.

[65]  K. Katoh,et al.  MAFFT version 5: improvement in accuracy of multiple sequence alignment , 2005, Nucleic acids research.

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

[67]  P. Desjeux.  Leishmaniasis: current situation and new perspectives. , 2004, Comparative immunology, microbiology and infectious diseases.

[68]  P. Myler,et al.  A survey of Leishmania braziliensis genome by shotgun sequencing. , 2004, Molecular and biochemical parasitology.

[69]  James Alexander,et al.  Cysteine peptidases as virulence factors of Leishmania. , 2004, Current opinion in microbiology.

[70]  S. Krungkrai,et al.  Plasmodium falciparum Carbonic Anhydrase is a Possible Target for Malaria Chemotherapy , 2004, Journal of enzyme inhibition and medicinal chemistry.

[71]  P. Bastin,et al.  TbAGO1, an Argonaute protein required for RNA interference, is involved in mitosis and chromosome segregation in Trypanosoma brucei , 2003, BMC Biology.

[72]  J. Donelson,et al.  The major surface protease (MSP or GP63) of Leishmania sp. Biosynthesis, regulation of expression, and function. , 2003, Molecular and biochemical parasitology.

[73]  A. L. Abreu-Silva,et al.  Biological behavior of Leishmania (L.) amazonensis isolated from a human diffuse cutaneous leishmaniasis in inbred strains of mice. , 2003, Histology and histopathology.

[74]  Darren A. Natale,et al.  The COG database: an updated version includes eukaryotes , 2003, BMC Bioinformatics.

[75]  C. Stoeckert,et al.  OrthoMCL: identification of ortholog groups for eukaryotic genomes. , 2003, Genome research.

[76]  S. Beverley,et al.  Improvements in transfection efficiency and tests of RNA interference (RNAi) approaches in the protozoan parasite Leishmania. , 2003, Molecular and biochemical parasitology.

[77]  I. Longden,et al.  EMBOSS: the European Molecular Biology Open Software Suite. , 2000, Trends in genetics : TIG.

[78]  M. Ashburner,et al.  Gene Ontology: tool for the unification of biology , 2000, Nature Genetics.

[79]  J. Stiles,et al.  Genomic organization, transcription, splicing and gene regulation in Leishmania. , 1999, Annals of tropical medicine and parasitology.

[80]  M. Miles,et al.  Genomic diversity in the Leishmania donovani complex , 1999, Parasitology.

[81]  W. Degrave,et al.  Leishmania (Viannia) braziliensis is the predominant species infecting patients with American cutaneous leishmaniasis in the State of Minas Gerais, Southeast Brazil. , 1999, Acta tropica.

[82]  K. Gull,et al.  Double-stranded RNA induces mRNA degradation in Trypanosoma brucei. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[83]  P. Green,et al.  Base-calling of automated sequencer traces using phred. I. Accuracy assessment. , 1998, Genome research.

[84]  P Green,et al.  Base-calling of automated sequencer traces using phred. II. Error probabilities. , 1998, Genome research.

[85]  A. Barrett,et al.  Nomenclature Committee of the International Union of Biochemistry and Molecular Biology (NC-IUBMB). Enzyme Nomenclature. Recommendations 1992. Supplement 4: corrections and additions (1997). , 1997, European journal of biochemistry.

[86]  D. Morrison,et al.  Evolution of the genus Leishmania revealed by comparison of DNA and RNA polymerase gene sequences. , 1997, Molecular and biochemical parasitology.

[87]  D. Lipman,et al.  A genomic perspective on protein families. , 1997, Science.

[88]  P. Desjeux.  Leishmaniasis: Public health aspects and control , 1996 .

[89]  N. Saravia,et al.  Natural history, clinical evolution, and the host-parasite interaction in New World cutaneous Leishmaniasis. , 1996, Clinics in dermatology.

[90]  A. Fairlamb,et al.  Trypanothione reductase from Leishmania donovani. Purification, characterisation and inhibition by trivalent antimonials. , 1995, European journal of biochemistry.

[91]  A. Fairlamb,et al.  Trypanothione Reductase from Leishmania donovani , 1995 .

[92]  S. Eresh,et al.  Identification and diagnosis of Leishmania mexicana complex isolates by polymerase chain reaction , 1994, Parasitology.

[93]  T. Blundell,et al.  Comparative protein modelling by satisfaction of spatial restraints. , 1993, Journal of molecular biology.

[94]  William R. Taylor,et al.  The rapid generation of mutation data matrices from protein sequences , 1992, Comput. Appl. Biosci..

[95]  R. Badaró,et al.  Leishmaniasis in Bahia, Brazil: evidence that Leishmania amazonensis produces a wide spectrum of clinical disease. , 1991, The American journal of tropical medicine and hygiene.

[96]  D. Wirth,et al.  Characterization of a RNA virus from the parasite Leishmania. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[97]  T. Lindahl,et al.  Suicide inactivation of the E. coli O6‐methylguanine‐DNA methyltransferase. , 1982, The EMBO journal.

[98]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[99]  Martin J. Simard,et al.  Argonaute proteins: key players in RNA silencing , 2008, Nature Reviews Molecular Cell Biology.

[100]  J. Wiesner,et al.  Isoprenoid biosynthesis of the apicoplast as drug target. , 2007, Current drug targets.

[101]  F. Prugnolle,et al.  Leishmania and the leishmaniases: a parasite genetic update and advances in taxonomy, epidemiology and pathogenicity in humans. , 2007, Advances in parasitology.

[102]  R. Pearson,et al.  Atypical American visceral leishmaniasis caused by disseminated Leishmania amazonensis infection presenting with hepatitis and adenopathy. , 2006, Transactions of the Royal Society of Tropical Medicine and Hygiene.

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

[104]  William Saurin,et al.  Getting In or Out: Early Segregation Between Importers and Exporters in the Evolution of ATP-Binding Cassette (ABC) Transporters , 1999, Journal of Molecular Evolution.

[105]  Gapped BLAST and PSI-BLAST: A new , 1997 .

[106]  K. Tipton,et al.  Nomenclature Committee of the International Union of Biochemistry and Molecular Biology (NC-IUBMB). Enzyme nomenclature. Recommendations 1992. Supplement: corrections and additions. , 1994, European journal of biochemistry.

[107]  G. Grimaldi,et al.  Leishmaniasis and its etiologic agents in the New World: an overview. , 1991, Progress in clinical parasitology.

[108]  P. Marsden.  Mucosal leishmaniasis ("espundia" Escomel, 1911). , 1986, Transactions of the Royal Society of Tropical Medicine and Hygiene.