Genome-Wide Survey and Evolutionary Analysis of Trypsin Proteases in Apicomplexan Parasites

Apicomplexa are an extremely diverse group of unicellular organisms that infect humans and other animals. Despite the great advances in combating infectious diseases over the past century, these parasites still have a tremendous social and economic burden on human societies, particularly in tropical and subtropical regions of the world. Proteases from apicomplexa have been characterized at the molecular and cellular levels, and central roles have been proposed for proteases in diverse processes. In this work, 16 new genes encoding for trypsin proteases are identified in 8 apicomplexan genomes by a genome-wide survey. Phylogenetic analysis suggests that these genes were gained through both intracellular gene transfer and vertical gene transfer. Identification, characterization and understanding of the evolutionary origin of protease-mediated processes are crucial to increase the knowledge and improve the strategies for the development of novel chemotherapeutic agents and vaccines.

[1]  M. Kenichi,et al.  Cloning, characterization and nucleotide sequences of two cDNAs encoding human pancreatic trypsinogens. , 1986 .

[2]  Masato Yano,et al.  Binding of proteins to the PDZ domain regulates proteolytic activity of HtrA1 serine protease. , 2004, The Biochemical journal.

[3]  Tim Clausen,et al.  Crystal Structure of the DegS Stress Sensor How a PDZ Domain Recognizes Misfolded Protein and Activates a Protease , 2004, Cell.

[4]  H. Neurath,et al.  Evolution of proteolytic enzymes. , 1984, Science.

[5]  S. Petersen,et al.  The Origin of Trypsin: Evidence for Multiple Gene Duplications in Trypsins , 1998, Journal of Molecular Evolution.

[6]  Krystyna A. Kelly,et al.  Epigenomic Modifications Predict Active Promoters and Gene Structure in Toxoplasma gondii , 2007, PLoS pathogens.

[7]  Amos Bairoch,et al.  The PROSITE database, its status in 1999 , 1999, Nucleic Acids Res..

[8]  Kami Kim.  Role of proteases in host cell invasion by Toxoplasma gondii and other Apicomplexa. , 2004, Acta tropica.

[9]  J A Eisen,et al.  Microbial Genes in the Human Genome: Lateral Transfer or Gene Loss? , 2001, Science.

[10]  J. Roach,et al.  The Molecular Evolution of the Vertebrate Trypsinogens , 1997, Journal of Molecular Evolution.

[11]  R. Sinden,et al.  Members of a trypsin gene family in Anopheles gambiae are induced in the gut by blood meal. , 1993, The EMBO journal.

[12]  D. Hickey,et al.  Concerted evolution within a trypsin gene cluster in Drosophila. , 1999, Molecular biology and evolution.

[13]  D. D. Brown,et al.  Developmental and thyroid hormone-dependent regulation of pancreatic genes in Xenopus laevis. , 1990, Genes & development.

[14]  S. Brunak,et al.  Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. , 2000, Journal of molecular biology.

[15]  Geoffrey I. McFadden,et al.  Plastid in human parasites , 1996, Nature.

[16]  Amos Bairoch,et al.  The PROSITE database, its status in 2002 , 2002, Nucleic Acids Res..

[17]  B. White,et al.  A gene family in Drosophila melanogaster coding for trypsin-like enzymes. , 1985, Nucleic acids research.

[18]  Michael J. Stanhope,et al.  Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates , 2001, Nature.

[19]  William W. Cohen,et al.  Evidence for an Active-Center Histidine in Trypsin through Use of a Specific Reagent, 1-Chloro-3-tosylamido-7-amino-2-heptanone, the Chloromethyl Ketone Derived from Nα-Tosyl-L-lysine* , 1965 .

[20]  J. Palmer,et al.  A Plastid of Probable Green Algal Origin in Apicomplexan Parasites , 1997, Science.

[21]  C. Chothia,et al.  Structure, function and evolution of multidomain proteins. , 2004, Current opinion in structural biology.

[22]  C. Ponting,et al.  The natural history of protein domains. , 2002, Annual review of biophysics and biomolecular structure.

[23]  C P Ponting,et al.  Evidence for PDZ domains in bacteria, yeast, and plants , 1997, Protein science : a publication of the Protein Society.

[24]  I. Charles,et al.  PDZ Domains Facilitate Binding of High Temperature Requirement Protease A (HtrA) and Tail-specific Protease (Tsp) to Heterologous Substrates through Recognition of the Small Stable RNA A (ssrA)-encoded Peptide* , 2002, The Journal of Biological Chemistry.

[25]  Lokesh P. Tripathi,et al.  Cross genome comparisons of serine proteases in Arabidopsis and rice , 2006, BMC Genomics.

[26]  J. Palmer,et al.  Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Sean R. Eddy,et al.  Profile hidden Markov models , 1998, Bioinform..

[28]  J. Thompson,et al.  CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. , 1994, Nucleic acids research.

[29]  O. Hagenbüchle,et al.  Sequence organisation and transcriptional regulation of the mouse elastase II and trypsin genes. , 1986, Nucleic acids research.

[30]  S. Brunak,et al.  Improved prediction of signal peptides: SignalP 3.0. , 2004, Journal of molecular biology.

[31]  L. Hood,et al.  The complete 685-kilobase DNA sequence of the human beta T cell receptor locus. , 1996, Science.

[32]  B. Hartley.  Amino-Acid Sequence of Bovine Chymotrypsinogen-A , 1964, Nature.

[33]  M. Pallen,et al.  The HtrA family of serine proteases , 1997, Molecular microbiology.

[34]  M. Nei,et al.  MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. , 2007, Molecular biology and evolution.

[35]  M. Blackman,et al.  Proteases involved in erythrocyte invasion by the malaria parasite: function and potential as chemotherapeutic targets. , 2000, Current drug targets.

[36]  Neil D. Rawlings,et al.  MEROPS: the peptidase database , 2009, Nucleic Acids Res..

[37]  R. Beynon,et al.  Proteolytic Enzymes: A Practical Approach , 2001 .

[38]  J. Boothroyd,et al.  Pulling together: an integrated model of Toxoplasma cell invasion. , 2007, Current opinion in microbiology.

[39]  C. Elvin,et al.  Isolation of a trypsin‐like serine protease gene family from the sheep blowfly Lucilia cuprina , 1994, Insect molecular biology.

[40]  L. Hood,et al.  The Complete 685-Kilobase DNA Sequence of the Human β T Cell Receptor Locus , 1996, Science.

[41]  K Matsubara,et al.  Cloning, characterization and nucleotide sequences of two cDNAs encoding human pancreatic trypsinogens. , 1986, Gene.

[42]  Amos Bairoch,et al.  The PROSITE database, its status in 1997 , 1997, Nucleic Acids Res..

[43]  J Schultz,et al.  SMART, a simple modular architecture research tool: identification of signaling domains. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[44]  C. Plowe.  Antimalarial drug resistance in Africa: strategies for monitoring and deterrence. , 2005, Current topics in microbiology and immunology.

[45]  S. Kano.  [Drug resistant malaria]. , 2003, Nihon rinsho. Japanese journal of clinical medicine.

[46]  Inyoul Y. Lee,et al.  Isolation and characterization of the chicken trypsinogen gene family. , 1995, The Biochemical journal.

[47]  Jessica C Kissinger,et al.  A first glimpse into the pattern and scale of gene transfer in Apicomplexa. , 2004, International journal for parasitology.

[48]  D. Roos,et al.  Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. , 2001, Molecular biology and evolution.

[49]  Charles F. Delwiche,et al.  Tracing the Thread of Plastid Diversity through the Tapestry of Life , 1999, The American Naturalist.

[50]  Søren Brunak,et al.  Non-classical protein secretion in bacteria , 2005, BMC Microbiology.

[51]  H. Neurath,et al.  Peptides combined with 14C-diisopropyl phosphoryl following degradation of 14C-DIP-trypsin with alpha-chymotrypsin. , 1956, Biochimica et biophysica acta.