Bracoviruses Contain a Large Multigene Family Coding for Protein Tyrosine Phosphatases

ABSTRACT The relationship between parasitic wasps and bracoviruses constitutes one of the few known mutualisms between viruses and eukaryotes. The virions produced in the wasp ovaries are injected into host lepidopteran larvae, where virus genes are expressed, allowing successful development of the parasite by inducing host immune suppression and developmental arrest. Bracovirus-bearing wasps have a common phylogenetic origin, and contemporary bracoviruses are hypothesized to have been inherited by chromosomal transmission from a virus that originally integrated into the genome of the common ancestor wasp living 73.7 ± 10 million years ago. However, so far no conserved genes have been described among different braconid wasp subfamilies. Here we show that a gene family is present in bracoviruses of different braconid wasp subfamilies (Cotesia congregata, Microgastrinae, and Toxoneuron nigriceps, Cardiochilinae) which likely corresponds to an ancient component of the bracovirus genome that might have been present in the ancestral virus. The genes encode proteins belonging to the protein tyrosine phosphatase family, known to play a key role in the control of signal transduction pathways. Bracovirus protein tyrosine phosphatase genes were shown to be expressed in different tissues of parasitized hosts, and two protein tyrosine phosphatases were produced with recombinant baculoviruses and tested for their biochemical activity. One protein tyrosine phosphatase is a functional phosphatase. These results strengthen the hypothesis that protein tyrosine phosphatases are involved in virally induced alterations of host physiology during parasitism.

[1]  L. Cattolico,et al.  Genome Sequence of a Polydnavirus: Insights into Symbiotic Virus Evolution , 2004, Science.

[2]  A. Lever,et al.  Expression and functions of human endogenous retroviruses in the placenta: an update. , 2004, Placenta.

[3]  P. Falabella,et al.  Physiological and molecular interaction in the host-parasitoid system Heliothis virescens-Toxoneuron nigriceps: current status and future perspectives. , 2004, Insect biochemistry and molecular biology.

[4]  D. O'reilly,et al.  A defective viral genome maintained in Escherichia coli for the generation of baculovirus expression vectors , 2001, Biotechnology Letters.

[5]  B. Webb,et al.  Polydnavirus genes and genomes: emerging gene families and new insights into polydnavirus replication. , 2004, Annual review of entomology.

[6]  W. Smith,et al.  PTTH-stimulated ecdysone secretion is dependent upon tyrosine phosphorylation in the prothoracic glands of Manduca sexta. , 2003, Insect biochemistry and molecular biology.

[7]  S. Okitsu,et al.  Detection of norovirus (GI, GII), Sapovirus and astrovirus in fecal samples using reverse transcription single-round multiplex PCR. , 2003, Journal of virological methods.

[8]  Y. P. Chen,et al.  Quantitation of a Glyptapanteles indiensis polydnavirus gene expressed in parasitized host, Lymantria dispar, by real-time quantitative RT-PCR. , 2003, Journal of virological methods.

[9]  E. Herniou,et al.  The genome sequence and evolution of baculoviruses. , 2003, Annual review of entomology.

[10]  M. Strand,et al.  Haemocytes from Pseudoplusia includens express multiple α and β integrin subunits , 2003, Insect molecular biology.

[11]  S. Dupas,et al.  Diversifying selection in a parasitoid's symbiotic virus among genes involved in inhibiting host immunity , 2003, Immunogenetics.

[12]  Y. P. Chen,et al.  Quantitative expression analysis of a Glyptapanteles indiensis polydnavirus protein tyrosine phosphatase gene in its natural lepidopteran host, Lymantria dispar , 2003, Insect molecular biology.

[13]  R. Glatz,et al.  Characterization of a Novel Protein with Homology to C-type Lectins Expressed by the Cotesia rubecula Bracovirus in Larvae of the Lepidopteran Host, Pieris rapae* , 2003, Journal of Biological Chemistry.

[14]  S. Asgari,et al.  Virus or not? Phylogenetics of polydnaviruses and their wasp carriers. , 2003, Journal of insect physiology.

[15]  Y. Bigot,et al.  Origin and evolution of polydnaviruses by symbiogenesis of insect DNA viruses in endoparasitic wasps. , 2003, Journal of insect physiology.

[16]  L. Cattolico,et al.  Polydnavirus genome: integrated vs. free virus. , 2003, Journal of insect physiology.

[17]  H. Matsumoto,et al.  Expression of Cotesia kariyai polydnavirus genes in lepidopteran hemocytes and Sf9 cells. , 2003, Journal of insect physiology.

[18]  A. Volkoff,et al.  Two Hyposoter didmator ichnovirus genes expressed in the lepidopteran host encode secreted or membrane-associated serine and threonine rich proteins in segments that may be nested. , 2003, Journal of insect physiology.

[19]  S. Asgari,et al.  Persistence and expression of Cotesia congregata polydnavirus in host larvae of the tobacco hornworm, Manduca sexta. , 2003, Journal of insect physiology.

[20]  M. Cusson,et al.  Three related TrIV genes: comparative sequence analysis and expression in host larvae and Cf-124T cells. , 2003, Journal of insect physiology.

[21]  F. Blank,et al.  Fate of polydnavirus DNA of the egg-larval parasitoid Chelonus inanitus in the host Spodoptera littoralis. , 2003, Journal of insect physiology.

[22]  A. Haeseler,et al.  Maximum‐Likelihood Analysis Using TREE‐PUZZLE , 2003 .

[23]  P. Falabella,et al.  Toxoneuron nigriceps polydnavirus encodes a putative aspartyl protease highly expressed in parasitized host larvae , 2003, Insect molecular biology.

[24]  R. Hilgarth,et al.  Evidence for a conserved polydnavirus gene family: ichnovirus homologs of the CsIV repeat element genes. , 2002, Virology.

[25]  W. Pearson,et al.  Current Protocols in Bioinformatics , 2002 .

[26]  E. Huguet,et al.  Polydnavirus replication: the EP1 segment of the parasitoid wasp Cotesia congregata is amplified within a larger precursor molecule. , 2002, The Journal of general virology.

[27]  F. Lemeunier,et al.  Visualization of Polydnavirus Sequences in a Parasitoid Wasp Chromosome , 2002, Journal of Virology.

[28]  J. Whitfield Estimating the age of the polydnavirus/braconid wasp symbiosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  B. Lanzrein,et al.  Characterization of two genes of the polydnavirus of Chelonus inanitus and their stage-specific expression in the host Spodoptera littoralis. , 2002, The Journal of general virology.

[30]  L. Gilbert,et al.  Control and biochemical nature of the ecdysteroidogenic pathway. , 2002, Annual review of entomology.

[31]  B. Webb,et al.  Perspectives on polydnavirus origins and evolution. , 2002, Advances in virus research.

[32]  A. Gruber,et al.  Characterization of Chelonus inanitus polydnavirus segments: sequences and analysis, excision site and demonstration of clustering. , 2002, The Journal of general virology.

[33]  P G Drake,et al.  Structural and Evolutionary Relationships among Protein Tyrosine Phosphatase Domains , 2001, Molecular and Cellular Biology.

[34]  P. Najarro,et al.  Vaccinia Virus Blocks Gamma Interferon Signal Transduction: Viral VH1 Phosphatase Reverses Stat1 Activation , 2001, Journal of Virology.

[35]  R. Weaver,et al.  Endocrine interactions of insect parasites and pathogens , 2001 .

[36]  D. Kordis,et al.  Adaptive evolution of animal toxin multigene families. , 2000, Gene.

[37]  T Ohta Evolution of gene families. , 2000, Gene.

[38]  M. Strand,et al.  Characterization of two novel Microplitis demolitor polydnavirus mRNAs expressed in Pseudoplusia includens haemocytes. , 2000, The Journal of general virology.

[39]  A. Austin,et al.  Hymenoptera: Evolution, Biodiversity and Biological Control , 2000 .

[40]  G. Cornelis,et al.  How to survive in the host: the Yersinia lesson. , 2000, Microbes and infection.

[41]  J. Ernst Bacterial inhibition of phagocytosis , 2000, Cellular microbiology.

[42]  F. Pennacchio,et al.  Regulation of host endocrine system by the endophagous braconid cardiochiles nigriceps and its polydnavirus , 2000 .

[43]  A. Austin,et al.  Phylogeny of microgastroid braconid wasps, and what it tells us about polydnavirus evolution. , 2000 .

[44]  B. Finlay,et al.  Phosphatases and kinases delivered to the host cell by bacterial pathogens. , 2000, Trends in microbiology.

[45]  P. Falabella,et al.  Cardiochiles nigriceps polydnavirus: molecular characterization and gene expression in parasitized Heliothis virescens larvae. , 1999, Insect biochemistry and molecular biology.

[46]  Sirlester A. Parker,et al.  The Second Domain of the CD45 Protein Tyrosine Phosphatase Is Critical for Interleukin-2 Secretion and Substrate Recruitment of TCR-ζ in Vivo* , 1998, Journal of Biological Chemistry.

[47]  P. Falabella,et al.  Prothoracic gland inactivation in Heliothis virescens (F.) (Lepidoptera:Noctuidae) larvae parasitized by Cardiochiles nigriceps Viereck (Hymenoptera:Braconidae). , 1998, Journal of insect physiology.

[48]  N. Beckage,et al.  Production of early expressed parasitism-specific proteins in alternate sphingid hosts of the braconid wasp Cotesia congregata. , 1998, Journal of invertebrate pathology.

[49]  D. A. Reed,et al.  Effects of parasitization by Cotesia congregata on the brain-prothoracic gland axis of its host, Manduca sexta. , 1998, Journal of insect physiology.

[50]  B. Neel,et al.  Genetic analysis of protein tyrosine phosphatases. , 1998, Current opinion in genetics & development.

[51]  J. Whitfield,et al.  Phylogeny and evolution of host-parasitoid interactions in hymenoptera. , 1998, Annual review of entomology.

[52]  J. Thompson,et al.  The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. , 1997, Nucleic acids research.

[53]  J. Drezen,et al.  Excision of the polydnavirus chromosomal integrated EP1 sequence of the parasitoid wasp Cotesia congregata (Braconidae, Microgastinae) at potential recombinase binding sites. , 1997, The Journal of general virology.

[54]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[55]  B. Neel,et al.  Protein tyrosine phosphatases in signal transduction. , 1997, Current opinion in cell biology.

[56]  D. Barford,et al.  Development of "substrate-trapping" mutants to identify physiological substrates of protein tyrosine phosphatases. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[57]  D. Schümperli,et al.  Polydnavirus of the parasitic wasp Chelonus inanitus (Braconidae): characterization, genome organization and time point of replication. , 1994, The Journal of general virology.

[58]  J. Davis,et al.  An abundantly expressed hemolymph glycoprotein isolated from newly parasitized Manduca sexta larvae is a polydnavirus gene product. , 1994, Virology.

[59]  D. Barford,et al.  Crystal structure of human protein tyrosine phosphatase 1B. , 1994, Science.

[60]  N. Beckage,et al.  Characterization and biological effects of cotesia congregata polydnavirus on host larvae of the tobacco hornworm, manduca sexta , 1994 .

[61]  M. Kanost,et al.  Isolation and characterization of a hemocyte aggregation inhibitor from hemolymph of Manduca sexta larvae. , 1994, Archives of insect biochemistry and physiology.

[62]  R. F. Weaver,et al.  Transcription mapping and functional analysis of the protein tyrosine/serine phosphatase (PTPase) gene of the Autographa californica nuclear polyhedrosis virus. , 1993, Virology.

[63]  J. Dixon,et al.  A protein phosphatase related to the vaccinia virus VH1 is encoded in the genomes of several orthopoxviruses and a baculovirus. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[64]  H. Charbonneau,et al.  The baculovirus Autographa californica encodes a protein tyrosine phosphatase. , 1993, The Journal of biological chemistry.

[65]  I. Buron,et al.  Lack of Prothoracic Gland Degeneration in Developmentally Arrested Host Larvae of Manduca sexta Parasitized by the Braconid Wasp Cotesia congregata , 1993 .

[66]  Swethaa S. Ballakrishnen,et al.  ‘Families’ , 1992, Accidental Feminism.

[67]  D. O'reilly,et al.  Baculovirus expression vectors: a laboratory manual. , 1992 .

[68]  M. Summers,et al.  Polydnavirus DNA is integrated in the DNA of its parasitoid wasp host. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[69]  D. Stoltz Evidence for chromosomal transmission of polydnavirus DNA. , 1990, The Journal of general virology.

[70]  D. Theilmann,et al.  Molecular analysis of Campoletis sonorensis virus DNA in the lepidopteran host Heliothis virescens. , 1986, The Journal of general virology.

[71]  J. Felsenstein CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[72]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[73]  P. Krell,et al.  Unusual Baculovirus of the Parasitoid Wasp Apanteles melanoscelus: Isolation and Preliminary Characterization , 1979, Journal of virology.