Early changes in the pupal transcriptome of the flesh fly Sarcophagha crassipalpis to parasitization by the ectoparasitic wasp, Nasonia vitripennis

Insect Biochemistry and Molecular Biology

Volumn 43, Issue 12, 2013, Pages 1189-1200

  Danneels, Ellen L ^a   Formesyn, Ellen M ^a   Hahn, Daniel A ^b   Denlinger, David L ^c   Cardoen, Dries ^d   Wenseleers, Tom ^d   Schoofs, Liliane ^d   de Graaf, Dirk C ^a  

^a GHENT UNIVERSITY   (Belgium)

^b UNIVERSITY OF FLORIDA   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Ectoparasitoid; Microarray; Nasonia vitripennis; Sarcophaga crassipalpis; Venom

Indexed keywords

VENOM; WASP VENOM;

ANIMAL; ARTICLE; ECTOPARASITOID; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; INSECT; LARVA; MICROARRAY; NASONIA VITRIPENNIS; PARASITOLOGY; PATHOGENICITY; SARCOPHAGA CRASSIPALPIS; SARCOPHAGIDAE; WASP;

ECTOPARASITOID; MICROARRAY; NASONIA VITRIPENNIS; SARCOPHAGA CRASSIPALPIS; VENOM;

ANIMALS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; LARVA; PUPA; SARCOPHAGIDAE; WASP VENOMS; WASPS;

EID: 84887144242     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2013.10.003     Document Type: Article

References (101)

1. Asgari S. MicroRNA functions in insects. Insect Biochem. Mol. Biol. 2013, 43:388-397.
2. Asgari S., Rivers D.B. Venom proteins from endoparasitoid wasp and their role in host-parasite interactions. Annu. Rev. Entomol. 2011, 56:313-335.
3. Aznar S., Lacal J.C. Rho signals to cell growth and apoptosis. Cancer Lett. 2001, 165:1-10.
4. Benes P., Vetvicka V., Fusek M. Cathepsin D-Many functions of one aspartic protease. Crit. Rev. Oncol. Hematol. 2008, 68:12-28.
5. Benjamini Y., Hochberg Y. Controlling the false discovery rate - a practical and powerful approach to multiple testing. J.R. Stat. Soc. Ser. B-Methodolog. 1995, 57:289-300.
6. Berry D.L., Baehrecke E.H. Growth arrest and autophagy are required for salivary gland cell degradation in Drosophila. Cell 2007, 131:1137-1148.
7. Bitra K., Zhang S., Strand M.R. Transcriptomic profiling of Microplitis demolitor bracovirus reveals host, tissue and stage-specific patterns of activity. J.Gen. Virol. 2011, 92:2060-2071.
8. Blanco E., Ruiz-Romero M., Beltran S., Bosch M., Punset A., Serras F., Corominas M. Gene expression following induction of regeneration in Drosophila wing imaginal discs. Expression profile of regenerating wing discs. BMC Develop. Biol. 2010, 10.
9. Brown G.C., Borutaite V. Regulation of apoptosis by the redox state of cytochrome c. Biochim. Biophys. Acta-Bioenerg. 2008, 1777:877-881.
10. 2+ signals in autophagy. Cell Calcium 2012, 52:44-51.
11. Charriere G.M., Ip W.K.E., Dejardin S., Boyer L., Sokolovska A., Cappillino M.P., Cherayil B.J., Podolsky D.K., Kobayashi K.S., Silverman N., Lacy-Hulbert A., Stuart L.M. Identification of Drosophila Yin and PEPT2 as evolutionarily conserved phagosome-associated muramyl dipeptide transporters. J.Biol. Chem. 2010, 285:20147-20154.
12. Chan T.A., Chu C.A., Rauen K.A., Kroiher M., Tatarewicz S.M., Steele R.E. Identification of a gene encoding a novel protein-tyrosine kinase containing Sh2 domains and ankyrin-like repeats. Oncogene 1994, 9:1253-1259.
13. Chang J.H., Pratt J.C., Sawasdikosol S., Kapeller R., Burakoff S.J. The small GTP-binding protein rho potentiates AP-1 transcription in T cells. Mol. Cell Biol. 1998, 18:4986-4993.
14. Chen G.C., Gajowniczek P., Settleman J. Rho-LIM kinase signaling regulates ecdysone-induced gene expression and morphogenesis during Drosophila metamorphosis. Curr. Biol. 2004, 14:309-313.
15. Clark E.A., Golub T.R., Lander E.S., Hynes R.O. Genomic analysis of metastasis reveals an essential role for RhoC. Nature 2000, 406:532-535.
16. Coleman M.L., Olson M.F. Rho GTPase signalling pathways in the morphological changes associated with apoptosis. Cell Death Differ. 2002, 9:493-504.
17. Concannon C.G., Gorman A.M., Samalli A. On the role of Hsp27 in regulating apoptosis. Apoptosis 2003, 8:61-70.
18. Conesa A., Gotz S., Garcia-Gomez J.M., Terol J., Talon M., Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005, 21:3674-3676.
19. Cooper D.M., Mitchell-Foster K. Death for survival: what do we know about innate immunity and cell death in insects?. Invertebr. Surv. J. 2011, 8:162-172.
20. Cox A.D., Der C.J. The dark side of Ras: regulation of apoptosis. Oncogene 2003, 22:8999-9006.
21. Dahlman D.L., Rana R.L., Schepers E.J., Schepers T., Diluna F.A., Webb B.A. Ateratocyte gene from a parasitic wasp that is associated with inhibition of insect growth and development inhibits host protein synthesis. Insect Mol. Biol. 2003, 12:527-534.
22. Danneels E.L., Rivers D.B., de Graaf D.C. Venom proteins of the parasitoid wasp Nasonia vitripennis: recent discovery of an untapped pharmacopee. Toxins. (Basel) 2010, 2:494-516.
23. de Graaf D.C., Aerts M., Brunain M., Desjardins C.A., Jacobs F.J., Werren J.H., Devreese B. Insights into the venom composition of the ectoparasitoid wasp Nasonia vitripennis from bioinformatic and proteomic studies. Insect Mol. Biol. 2010, 19:11-26.
24. Denlinger D.L. Induction and termination of pupal diapause in Sarcophaga (Diptera-Sarcophagidae). Biol. Bull. 1972, 142:11-24.
25. Denlinger D.L., Zdarek J. Metamorphosis behavior of flies. Annu. Rev. Entomol. 1994, 39:243-266.
26. Edgar A.J., Polak J.M. Molecular cloning of the human and murine 2-amino-3-ketobutyrate coenzyme A ligase cDNAs. Eur. J. Biochem. 2000, 267:1805-1812.
27. Etebari K., Palfreyman R.W., Schlipalius D., Nielsen L.K., Glatz R.V., Asgari S. Deep sequencing-based transcriptome analysis of Plutella xylostella larvae parasitized by Diadegma semiclausum. BMC Genomics 2011, 12:446-463.
28. Etebari K., Hussain M., Asgari S. Identification of microRNAs from Plutella xylostella larvae associated with parasitization by Diadegma semiclausum. Insect Biochem. Mol. Biol. 2013, 43:309-318.
29. Fang Q., Wang L., Zhu J.Y., Li Y.M., Song Q.S., Stanley D.W., Akhtar Z.R., Ye G.Y. Expression of immune-response genes in lepidopteran host is suppressed by venom from an endoparasitoid, Pteromalus puparum. BMC Genomics 2010, 11:484-500.
30. Fiorentini C., Falzano L., Travaglione S., Fabbri A. Hijacking Rho GTPases by protein toxins and apoptosis: molecular strategies of pathogenic bacteria. Cell Death Differ. 2003, 10:147-152.
31. Formesyn E.M., Danneels E.L., de Graaf D.C. Chapter 19-Proteomics of the venom of the parasitoid Nasonia vitripennis. Parasitoid Viruses: Symbionts and Pathogens 2010, 233-246. Elsevier Inc. N.E. Beckage, J.M. Drezen (Eds.).
32. Formesyn E.M., Heyninck K., de Graaf D.C. The role of serine- and metalloproteases in Nasonia vitripennis venom in cell death related processes towards a Spodoptera frugiperda Sf21 cell line. J.Insect Physiol. 2013, 59:795-803.
33. Fullaondo A., Lee S.Y. Identification of putative miRNA involved in Drosophila melanogaster immune response. Develop. Comp. Immunol. 2012, 36:267-273.
34. Ganapathy V., Thangaraju M., Gopal E., Martin P.M., Itagaki S., Miyauchi S., Prasad P.D. Sodium-coupled monocarboxylate transporters in normal tissues and in cancer. AAPS J. 2008, 10:193-199.
35. Gentleman R.C., Carey V.J., Bates D.M., Bolstad B., Dettling M., Dudoit S., Ellis B., Gautier L., Ge Y.C., Gentry J., Hornik K., Hothorn T., Huber W., Iacus S., Irizarry R., Leisch F., Li C., Maechler M., Rossini A.J., Sawitzki G., Smith C., Smyth G., Tierney L., Yang J.Y.H., Zhang J.H. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004, 5:R80.
36. Gerisch B., Antebi A. Hormonal signals produced by DAF-9/cytochrome P450 regulate C.elegans dauer diapause in response to environmental cues. Development 2004, 131:1765-1776.
37. Gillespie J.P., Kanost M.R., Trenczek T. Biological mediators of insect immunity. Annu. Rev. Entomol. 1997, 42:611-643.
38. Glatz R.V., Asgari S., Schmidt O. Evolution of polydnaviruses as insect immune suppressors. Trends Microbiol. 2004, 12:545-554.
39. Gorr T.A., Tomita T., Wappner P., Bunn H.F. Regulation of Drosophila hypoxia-inducible factor (HIF) activity in SL2 cells - identification of a hypoxia-induced variant isoform of the HIF alpha homolog gene similar. J.Biol. Chem. 2004, 279:36048-36058.
40. Gotz S., Garcia-Gomez J.M., Terol J., Williams T.D., Nagaraj S.H., Nueda M.J., Robles M., Talon M., Dopazo J., Conesa A. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008, 36:3420-3435.
41. Gruenewald C., Botella J.A., Bayersdorfer F., Navarro J.A., Schneuwly S. Hyperoxia-induced neurodegeneration as a tool to identify neuroprotective genes in Drosophila melanogaster. Free Radic. Biol. Med. 2009, 46:1668-1676.
42. Guicciardi M.E., Leist M., Gores G.J. Lysosomes in cell death. Oncogene 2004, 23:2881-2890.
43. Guppy M., Withers P. Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol. Rev. Cambridge Phil. Soc. 1999, 74:1-40.
44. Hahn D.A., Ragland G.J., Shoemaker D.D., Denlinger D.L. Gene discovery using massively parallel pyrosequencing to develop ESTs for the flesh fly Sarcophaga crassipalpis. BMC Genomics 2009, 10:234-242.
45. Hayashi H., Nakagami H., Takeichi M., Shimamura M., Koibuchi N., Oiki E., Sato N., Koriyama H., Mori M., Araujo R.G., Maeda A., Morishita R., Tamai K., Kaneda Y. HIG1, a novel regulator of mitochondrial gamma-secretase, maintains normal mitochondrial function. FASEB J. 2012, 26:2306-2317.
46. Kroemer G., Levine B. Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell Biol. 2008, 9:1004-1010.
47. Labrosse C., Carton Y., Dubuffet A., Drezen J.M., Poirie M. Active suppression of D.melanogaster immune response by long gland products of the parasitic wasp Leptopilina boulardi. J.Insect Physiol. 2003, 49:513-522.
48. Lee I.H., Kawai Y., Fergusson M.M., Rovira I.I., Bishop A.J.R., Motoyama N., Cao L., Finkel T. Atg7 modulates p53 activity to regulate cell cycle and survival during metabolic stress. Science 2012, 336:225-228.
49. Levy F., Bulet P., Ehret-Sabatier L. Proteomic analysis of the systemic immune response of Drosophila. Mol. Cell Proteomics 2004, 3:156-166.
50. Lin C.J., Lee C.C., Shih Y.L., Lin C.H., Wang S.H., Chen T.H., Shih C.M. Inhibition of mitochondria- and endoplasmic reticulum stress-mediated autophagy augments temozolomide-induced apoptosis in glioma cells. PloS One 2012, 7.
51. Ling D.J., Salvaterra P.M. Robust RT-qPCR data normalization: validation and selection of internal reference genes during post-experimental data analysis. PloS One 2011, 6.
52. Mahadav A., Gerling D., Gottlieb Y., Czosnek H., Ghanim M. Parasitization by the wasp Eretmocerus mundus induces transcription of genes related to immune response and symbiotic bacteria proliferation in the whitefly Bemisia tabaci. BMC Genomics 2008, 9:342-352.
53. Masova A., Sanda M., Jiracek J., Selicharova I. Changes in the proteomes of the hemocytes and fat bodies of the flesh fly Sarcophaga bullata larvae after infection by Escherichia coli. Proteome Sci. 2010, 8:1-11.
54. Michaud M.R., Denlinger D.L. Shifts in the carbohydrate, polyol, and amino acid pools during rapid cold-hardening and diapause-associated cold-hardening in flesh flies (Sarcophaga crassipalpis): a metabolomic comparison. J.Comp. Physiol. B-Biochem. Syst. Environ. Physiol. 2007, 177:753-763.
55. Motley A.M., Hettema E.H., Ketting R., Plasterk R., Tabak H.F. Caenorhabditis elegans has a single pathway to target matrix proteins to peroxisomes. Embo Rep. 2000, 1:40-46.
56. Nakamatsu Y., Tanaka T. Venom of ectoparasitoid, Euplectrus sp near plathypenae (Hymenoptera: Eulophidae) regulates the physiological state of Pseudaletia separata (Lepidoptera: Noctuidae) host as a food resource. J.Insect Physiol. 2003, 49:149-159.
57. Nakamatsu Y., Tanaka T. Venom of Euplectrus separatae causes hyperlipidemia by lysis of host fat body cells. J.Insect Physiol. 2004, 50:267-275.
58. Nayak B., Kondeti V.K., Xie P., Lin S., Viswakarma N., Raparia K., Kanwar Y.S. Transcriptional and post-translational modulation of myo-Inositol oxygenase by high glucose and related pathobiological stresses. J.Biol. Chem. 2011, 286:27594-27611.
59. Nguyen T.T.A., Boudreault S., Michaud D., Cloutier C. Proteomes of theaphid Macrosiphum euphorbiae in its resistance and susceptibility responses to differently compatible parasitoids. Insect Biochem. Mol. Biol. 2008, 38:730-739.
60. Nicolas E., Nappi A.J., Lemaitre B. Expression of antimicrobial peptide genes after infection by parasitoid wasps in Drosophila. Develop. Comp. Immunol. 1996, 20:175-181.
61. Nurullahoglu Z.U., Uckan F., Sak O., Ergin E. Total lipid and fatty acid composition of Apanteles galleriae and its parasitized host. Ann. Entomol. Soc. Am. 2004, 97:1000-1006.
62. O'Connell R.M., Rao D.S., Chaudhuri A.A., Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 2010, 10:111-122.
63. O'Prey J., Skommer J., Wilkinson S., Ryan K.M. Analysis of DRAM-related proteins reveals evolutionarily conserved and divergent roles in the control of autophagy. Cell Cycle 2009, 8:2260-2265.
64. Olesnicky E.C., Desplan C. Distinct mechanisms for mRNA localization during embryonic axis specification in the wasp Nasonia. Develop. Biol. 2007, 306:134-142.
65. Pagarigan K.T., Bunn B.W., Goodchild J., Rahe T.K., Weis J.F., Saucedo L.J. Drosophila PRL-1 is a growth inhibitor that counteracts the function of the Src oncogene. PloS One 2013, 8.
66. Pedraza L.G., Stewart R.A., Li D.M., Xu T. Drosophila Src-family kinases function with Csk to regulate cell proliferation and apoptosis. Oncogene 2004, 23:4754-4762.
67. Pennacchio F., Strand M.R. Evolution of developmental strategies in parasitic Hymenoptera. Annu. Rev. Entomol. 2006, 51:233-258.
68. Provost B., Jouan V., Hilliou F., Delobel P., Bernardo P., Ravallec M., Cousserans F., Wajnberg E., Darboux I., Fournier P., Strand M.R., Volkoff A.N. Lepidopteran transcriptome analysis following infection by phylogenetically unrelated polydnaviruses highlights differential and common responses. Insect Biochem. Mol. Biol. 2011, 41:582-591.
69. Ragland G.J., Denlinger D.L., Hahn D.A. Mechanisms of suspended animation are revealed by transcript profiling of diapause in the flesh fly. Proc. Natl. Acad. Sci. U S A 2010, 107:14909-14914.
70. Rane M.J., Pan Y., Singh S., Powell D.W., Wu R., Cummins T., Chen Q., McLeish K.R., Klein J.B. Heat shock protein 27 controls apoptosis by regulating Akt activation. J.Biol. Chem. 2003, 278:27828-27835.
71. Rewitz K.F., Yamanaka N., Gilbert L.I., O'Connor M.B. The insect neuropeptide PTTH activates receptor tyrosine kinase Torso to initiate metamorphosis. Science 2009, 326:1403-1405.
72. Richards E.H., Dani M.P., Bradish H. Immunosuppressive properties of a protein (rVPr1) from the venom of the endoparasitic wasp, Pimpla hypochondriaca: mechanism of action and potential use for improving biological control strategies. J. Insect Physiol. 2013, 59:213-222.
73. Rivers D.B., Brogan A. Venom glands from the ectoparasitoid Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) produce a calreticulin-like protein that functions in developmental arrest and cell death in the flesh fly host, Sarcophaga bullata Parker (Diptera: Sarcophagidae). Insect Physiology: New Research 2008, 259-278. Nova Science Publishers, New York. R.P. Maes (Ed.).
74. Rivers D.B., Denlinger D.L. Redirection of metabolism in the flesh fly, Sarcophaga Bullata, following envenomation by the ectoparasitoid Nasonia vitripennis and correlation of metabolic effects with the diapause status of the host. J.Insect Physiol. 1994, 40:207-215.
75. Rivers D.B., Denlinger D.L. Developmental fate of the flesh fly, Sarcophaga bullata, envenomated by the pupal ectoparasitoid, Nasonia vitripennis. J.Insect Physiol. 1994, 40:121-127.
76. Rivers D.B., Denlinger D.L. Venom-induced alterations in fly lipid-metabolism and its impact on larval development of the ectoparasitoid Nasonia vitripennis (Walker) (Hymenoptera, Pteromalidae). J.Invertebr. Pathol. 1995, 66:104-110.
77. Rivers D.B., Rocco M.M., Frayha A.R. Venom from the ectoparasitic wasp Nasonia vitripennis increases Na+ influx and activates phospholipase C and phospholipase A(2) dependent signal transduction pathways in cultured insect cells. Toxicon 2002, 40:9-21.
78. Rivers D.B., Ruggiero L., Hayes M. The ectoparasitic wasp Nasonia vitripennis (Walker) (Hymenoptera: Pteromalidae) differentially affects cells mediating the immune response of its flesh fly host, Sarcophaga bullata Parker (Diptera: Sarcophagidae). J.Insect Physiol. 2002, 48:1053-1064.
79. Rivers D.B., Uckan F., Ergin E., Keefer D.A. Pathological and ultrastructural changes in cultured cells induced by venom from the ectoparasitic wasp Nasonia vitripennis (Walker) (Hymenoptera Pteromalidae). J.Insect Physiol. 2010, 56:1935-1948.
80. Rivers D.B., Yoder J.A., Ruggiero L. Venom from Nasonia vitripennis: a model for understanding the roles of venom during parasitism by ectoparasitoids. Trends Entomol. 1999, 2:1-17.
81. Ross D.R., Dunn P.E. Effect of parasitism by Cotesia congregata on the susceptibility of Manduca sexta larvae to bacterial infection. Develop. Comp. Immunol. 1989, 13:205-216.
82. Rossman K.L., Der C.J., Sondek J. GEF means go: turning on Rho GTPaseswith guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 2005, 6:167-180.
83. Scharlaken B., de Graaf D.C., Goossens K., Brunain M., Peelman L.J., Jacobs F.J. Reference gene selection for insect expression studies using quantitative real-time PCR: the head of the honeybee, Apis mellifera, after a bacterial challenge. J.Insect Sci. 2008, 8:33-43.
84. Schlenke T.A., Morales J., Govind S., Clark A.G. Contrasting infection strategies in generalist and specialist wasp parasitoids of Drosophila melanogaster. PloS Pathog. 2007, 3:1486-1501.
85. Smyth G. Limma: Linear Models for Microarray Data. Bioinformatics and Computational Biology Solutions using Rand Bioconductor 2005, 397-420. Springer, New York.
86. Song K.H., Jung M.K., Eum J.H., Hwang I.C., Han S.S. Proteomic analysis of parasitized Plutella xylostella larvae plasma. J.Insect Physiol. 2008, 54:1271-1280.
87. Strand M.R. The insect cellular immune response. Insect Sci. 2008, 15:1-14.
88. Tatusov R.L., Galperin M.Y., Natale D.A., Koonin E.V. The COG database: a tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Res. 2000, 28:33-36.
89. Untergasser A., Nijveen H., Rao X., Bisseling T., Geurts R., Leunissen J.A.M. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Res. 2007, 35:W71-W74.
90. Van den Assem J., Jachmann F. Changes in male perseverance in courtship and female readiness to mate in a strain of the parasitic wasp Nasonia vitripennis over a period of 20+years. Neth. J. Zoolog. 1999, 49:125-137.
91. Visser B., Le Lann C., den Blanken F.J., Harvey J.A., van Alphen J.J.M., Ellers J. Loss of lipid synthesis as an evolutionary consequence of a parasitic lifestyle. Proc. Natl. Acad. Sci. U S A 2010, 107:8677-8682.
92. Visser B., Roelofs D., Hahn D.A., Teal P.E.A., Marien J., Ellers J. Transcriptional changes associated with lack of lipid synthesis in parasitoids. Genome Biol. Evol. 2012, 4:864-874.
93. Voet D., Voet J. Biochemistry 2011, John Wiley & Sons, Inc. fourth ed.
94. Werren J.H., Richards S., Desjardins C.A., Niehuis O., Gadau J., Colbourne J.K., Beukeboom L.W., Desplan C., Elsik C.G., Grimmelikhuijzen C.J.P., Kitts P., Lynch J.A., Murphy T., Oliveira D.C.S.G., Smith C.D., van de Zande L., Worley K.C., Zdobnov E.M., Aerts M., Albert S., Anaya V.H., Anzola J.M., Barchuk A.R., Behura S.K., Bera A.N., Berenbaum M.R., Bertossa R.C., Bitondi M.M.G., Bordenstein S.R., Bork P., Bornberg-Bauer E., Brunain M., Cazzamali G., Chaboub L., Chacko J., Chavez D., Childers C.P., Choi J.H., Clark M.E., Claudianos C., Clinton R.A., Cree A.G., Cristino A.S., Dang P.M., Darby A.C., de Graaf D.C., Devreese B., Dinh H.H., Edwards R., Elango N., Elhaik E., Ermolaeva O., Evans J.D., Foret S., Fowler G.R., Gerlach D., Gibson J.D., Gilbert D.G., Graur D., Grunder S., Hagen D.E., Han Y., Hauser F., Hultmark D., Hunter H.C., Jhangian S.N., Jiang H.Y., Johnson R.M., Jones A.K., Junier T., Kadowaki T., Kamping A., Kapustin Y., Kechavarzi B., Kim J., Kim J., Kiryutin B., Koevoets T., Kovar C.L., Kriventseva E.V., Kucharski R., Lee H., Lee S.L., Lees K., Lewis L.R., Loehlin D.W., Logsdon J.M., Lopez J.A., Lozado R.J., Maglott D., Maleszka R., Mayampurath A., Mazur D.J., McClure M.A., Moore A.D., Morgan M.B., Muller J., Munoz-Torres M.C., Muzny D.M., Nazareth L.V., Neupert S., Nguyen N.B., Nunes F.M.F., Oakeshott J.G., Okwuonu G.O., Pannebakker B.A., Pejaver V.R., Peng Z.G., Pratt S.C., Predel R., Pu L.L., Ranson H., Raychoudhury R., Rechtsteiner A., Reese J.T., Reid J.G., Riddle M., Robertson I.M., Romero-Severson J., Rosenberg M., Sackton T.B., Sattelle D.B., Schluns H., Schmitt T., Schneider M., Schuler A., Schurko A.M., Shuker D.M., Simoes Z.L.P., Sinha S., Smith Z., Solovyev V., Souvorov A., Springauf A., Stafflinger E., Stage D.E., Stanke M., Tanaka Y., Telschow A., Trent C., Vattathil S., Verhulst E.C., Viljakainen L., Wanner K.W., Waterhouse R.M., Whitfield J.B., Wilkes T.E., Williamson M., Willis J.H., Wolschin F., Wyder S., Yamada T., Yi S.V., Zecher C.N., Zhang L., Gibbs R.A. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 2010, 327:343-348.
95. Wertheim B., Kraaijeveld A.R., Hopkins M.G., Boer M.W., Godfray H.C.J. Functional genomics of the evolution of increased resistance to parasitism in Drosophila. Mol. Ecol. 2011, 20:932-949.
96. Wertheim B., Kraaijeveld A.R., Schuster E., Blanc E., Hopkins M., Pletcher S.D., Strand M.R., Partridge L., Godfray H.C.J. Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biol. 2005, 6:R94.
97. Whiting A.R. Biology of parasitic wasp Mormoniella vitripennis [=Nasonia brevicornis] (Walker). Q.Rev. Biol. 1967, 42:333-406.
98. Wu C.G., Yan L., Depre C., Dhar S.K., Shen Y.T., Sadoshima J., Vatner S.F., Vatner D.E. Cytochrome c oxidase III as a mechanism for apoptosis in heart failure following myocardial infarction. Am. J. Physiol.-Cell Physiol. 2009, 297:C928-C934.
99. Zapata J.M., Matsuzawa S., Godzik A., Leo E., Wasserman S.A., Reed J.C. The Drosophila tumor necrosis factor receptor-associated factor-1 (DTRAF1) interacts with Pelle and regulates NF kappa B activity. J.Biol. Chem. 2000, 275:12102-12107.
100. Zera A.J. Microevolution of intermediary metabolism: evolutionary genetics meets metabolic biochemistry. J.Exp. Biol. 2011, 214:179-190.
101. Zhu J.Y., Ye G.Y., Fang Q., Hu C. Proteome changes in the plasma of Papilio xuthus (Lepidoptera: Papilionidae): effect of parasitization by the endoparasitic wasp Pteromalus puparum (Hymenoptera: Pteromalidae). J.Zhejiang Univ.-Sci. B 2009, 10:445-453.