A comprehensive analysis of the Manduca sexta immunotranscriptome

Developmental and Comparative Immunology

Volumn 39, Issue 4, 2013, Pages 388-398

  Gunaratna, Ramesh T ^a   Jiang, Haobo ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Gene discovery; Hemolymph proteins; Insect immunity; RNA Seq; Transcript profiling

Indexed keywords

JANUS KINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; POLYPEPTIDE ANTIBIOTIC AGENT; STAT PROTEIN; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR; TRANSCRIPTOME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN RECOGNITION; ARTICLE; BLOOD CELL; CONTROLLED STUDY; FAT BODY; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENETIC CODE; GENETIC DIFFERENCE; IMMUNOGENETICS; INNATE IMMUNITY; INSECT GENOME; JANUS KINASE GENE; LARVAL STAGE; MANDUCA SEXTA; MITOGEN ACTIVATED PROTEIN KINASE P38 GENE; NONHUMAN; PRIORITY JOURNAL; PROVOCATION TEST; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; STAT GENE; STRESS ACTIVATED PROTEIN KINASE GENE; TOLL LIKE RECEPTOR GENE; TRANSCRIPTION REGULATION;

EID: 84873742189     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2012.10.004     Document Type: Article

References (117)

1. Abraham J. The Role of Drosophila SUMO Conjugating Enzyme Lesswright in Larval Hematopoiesis: Effects on Cactus, Dorsal and Dorsal-related immunity factor (Dif) 2007, Ohio University, Ohio, Link. .
2. Agaisse H. An adaptive immune response in Drosophila?. Cell Host Microbe 2007, 1:91-93.
3. Altincicek B., Vilcinskas A. Identification of immune-related genes from an apterygote insect, the firebrat Thermobia domestica. Insect Biochem. Mol. Biol. 2007, 37:726-731.
4. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
5. An C., Jiang H., Kanost M.R. Proteolytic activation and function of the cytokine Spatzle in the innate immune response of a lepidopteran insect Manduca sexta. FEBS J. 2010, 277:148-162.
6. An C., Ishibashi J., Ragan E.J., Jiang H., Kanost M.R. Functions of Manduca sexta hemolymph proteinases HP6 and HP8 in two innate immune pathways. J. Biol. Chem. 2009, 284:19716-19726.
7. Aoun R.B., Hetru C., Troxler L., Doucet D., Ferrandon D., Matt N. Analysis of thioester-containing proteins during the innate immune response of Drosophila melanogaster. J. Innate Immun. 2011, 3:52-64.
8. Baeg G.H., Zhou R., Perrimon N. Genome-wide RNAi analysis of JAK/STAT signaling components in Drosophila. Genes Dev. 2005, 19:1861-1870.
9. Bhaskar V., Smith M., Courey A.J. Conjugation of Smt3 to dorsal may potentiate the Drosophila immune response. Mol. Cell. Biol. 2002, 22:492.
10. Bhaskar V., Valentine S.A., Courey A.J. A functional interaction between dorsal and components of the Smt3 conjugation machinery. J. Biol. Chem. 2000, 275:4033-4040.
11. Bhattacharya A., Steward R. The Drosophila homolog of NTF-2, the nuclear transport factor-2, is essential for immune response. EMBO Rep. 2002, 3:378-383.
12. Blandin S., Levashina E.A. Thioester-containing proteins and insect immunity. Mol. Immunol. 2004, 40:903-908.
13. Bokoch G.M. Regulation of innate immunity by Rho GTPases. Trends Cell Biol. 2005, 15:163-171.
14. Boutros M., Agaisse H., Perrimon N. Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell 2002, 3:711-722.
15. Brey P.T., Hultmark D. Molecular Mechanisms of Immune Responses in Insects 1998, Chapman & Hall, London; New York.
16. Chapman A.D. Numbers of Living Species in Australia and the World 2006, Australian Biodiversity Information Services, Australian Govt., Dept. of Environ. Heritage, Canberra, ACT, Australia.
17. Choe K.M., Werner T., Stoven S., Hultmark D., Anderson K.V. Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 2002, 296:359-362.
18. Christensen B.M., Li J., Chen C.C., Nappi A.J. Melanization immune responses in mosquito vectors. Trends Parasitol. 2005, 21:192-199.
19. Christophides G.K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S., Blass C., Brey P.T., Collins F.H., Danielli A., Dimopoulos G., Hetru C., Hoa N.T., Hoffmann J.A., Kanzok S.M., Letunic I., Levashina E.A., Loukeris T.G., Lycett G., Meister S., Michel K., Moita L.F., Muller H.M., Osta M.A., Paskewitz S.M., Reichhart J.M., Rzhetsky A., Troxler L., Vernick K.D., Vlachou D., Volz J., von Mering C., Xu J.N., Zheng L.B., Bork P., Kafatos F.C. Immunity-related genes and gene families in Anopheles gambiae. Science 2002, 298:159-165.
20. 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.
21. De Gregorio E., Spellman P.T., Rubin G.M., Lemaitre B. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. USA 2001, 98:12590-12595.
22. Ding S.W., Li H., Lu R., Li F., Li W.X. RNA silencing: a conserved antiviral immunity of plants and animals. Virus Res. 2004, 102:109-115.
23. Dong C., Davis R.J., Flavell R.A. MAP kinases in the immune response. Annu. Rev. Immunol. 2002, 20:55-72.
24. Dostert C., Jouanguy E., Irving P., Troxler L., Galiana-Arnoux D., Hetru C., Hoffmann J.A., Imler J.L. The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat. Immunol. 2005, 6:946-953.
25. Edgar R.C. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 2004, 32:1792-1797.
26. Engstrom Y. Induction and regulation of antimicrobial peptides in Drosophila. Dev. Comp. Immunol. 1999, 23:345-358.
27. Evans J.D., Aronstein K., Chen Y.P., Hetru C., Imler J.L., Jiang H., Kanost M., Thompson G.J., Zou Z., Hultmark D. Immune pathways and defence mechanisms in honey bees Apis mellifera. Insect Mol. Biol. 2006, 15:645-656.
28. Fauvarque M.O., Williams M.J. Drosophila cellular immunity: a story of migration and adhesion. J. Cell Sci. 2011, 124:1373-1382.
29. Foley E., O'Farrell P.H. Functional dissection of an innate immune response by a genome-wide RNAi screen. PLoS Biol. 2004, 2:E203.
30. Gallo K.A., Johnson G.L. Mixed-lineage kinase control of JNK and p38 MAPK pathways. Nat. Rev. Mol. Cell Biol. 2002, 3:663-672.
31. Geng J.F., Klionsky D.J. The Atg8 and Atg12 ubiquitin-like conjugation systems in macroautophagy. EMBO Rep. 2008, 9:859-864.
32. Gerardo N.M., Altincicek B., Anselme C., Atamian H., Barribeau S.M., De Vos M., Duncan E.J., Evans J.D., Gabaldon T., Ghanim M., Heddi A., Kaloshian I., Latorre A., Moya A., Nakabachi A., Parker B.J., Perez-Brocal V., Pignatelli M., Rahbe Y., Ramsey J.S., Spragg C.J., Tamames J., Tamarit D., Tamborindeguy C., Vincent-Monegat C., Vilcinskas A. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 2010, 11:R21.
33. Gillespie J.P., Kanost M.R., Trenczek T. Biological mediators of insect immunity. Annu. Rev. Entomol. 1997, 42:611-643.
34. Gottar M., Gobert V., Michel T., Belvin M., Duyk G., Hoffmann J.A., Ferrandon D., Royet J. The Drosophila immune response against Gram-negative bacteria is mediated by a peptidoglycan recognition protein. Nature 2002, 416:640-644.
35. 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.
36. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279:509.
37. Han Z.Q.S., Enslen H., Hu X.D., Meng X.J., Wu I.H., Barrett T., Davis R.J., Ip Y.T. A conserved p38 mitogen-activated protein kinase pathway regulates Drosophila immunity gene expression. Mol. Cell. Biol. 1998, 18:3527-3539.
38. Hoffmann J.A. The immune response of Drosophila. Nature 2003, 426:33-38.
39. Hoffmann J.A., Kafatos F.C., Janeway C.A., Ezekowitz R.A.B. Phylogenetic perspectives in innate immunity. Science 1999, 284:1313-1318.
40. Hoffmann J.A., Reichhart J.M. Drosophila immunity. Trends Cell Biol. 1997, 7:309-316.
41. Hou X.S., Perrimon N. The JAK-STAT pathway in Drosophila. Trends Genet. 1997, 13:105-110.
42. Huang L., Ohsako S., Tanda S. The lesswright mutation activates Rel-related proteins, leading to overproduction of larval hemocytes in Drosophila melanogaster. Dev. Biol. 2005, 280:407-420.
43. Hultmark D. Immune reactions in Drosophila and other insects: a model for innate immunity. Trends Genet. 1993, 9:178-183.
44. Hultmark D. Drosophila immunity: paths and patterns. Curr. Opin. Immunol. 2003, 15:12-19.
45. Inoue H., Tateno M., Fujimura-Kamada K., Takaesu G., Adachi-Yamada T., Ninomiya-Tsuji J., Irie K., Nishida Y., Matsumoto K. A Drosophila MAPKKK, D-MEKK1, mediates stress responses through activation of p38 MAPK. EMBO J. 2001, 20:5421-5430.
46. Irving P., Troxler L., Heuer T.S., Belvin M., Kopczynski C., Reichhart J.M., Hoffmann J.A., Hetru C. A genome-wide analysis of immune responses in Drosophila. Proc. Natl. Acad. Sci. USA 2001, 98:15119-15124.
47. Jang I.H., Nam H.J., Lee W.J. CLIP-domain serine proteases in Drosophila innate immunity. BMB Rep. 2008, 41:102-107.
48. Jiang H. The biochemical basis of antimicrobial responses in Manduca sexta. Insect Sci. 2008, 15:53-66.
49. Jiang H., Vilcinskas A., Kanost M.R. Immunity in lepidopteran insects. Adv. Exp. Med. Biol. 2010, 708:181-204.
50. Jiang H., Wang Y., Gu Y., Guo X., Zou Z., Scholz F., Trenczek T.E., Kanost M.R. Molecular identification of a bevy of serine proteinases in Manduca sexta hemolymph. Insect Biochem. Mol. Biol. 2005, 35:931-943.
51. Kallio J., Leinonen A., Ulvila J., Valanne S., Ezekowitz R.A., Ramet M. Functional analysis of immune response genes in Drosophila identifies JNK pathway as a regulator of antimicrobial peptide gene expression in S2 cells. Microbes Infect. 2005, 7:811-819.
52. Kaneko T., Goldman W.E., Mellroth P., Steiner H., Fukase K., Kusumoto S., Harley W., Fox A., Golenbock D., Silverman N. Monomeric and polymeric Gram-negative peptidoglycan but not purified LPS stimulate the Drosophila IMD pathway. Immunity 2004, 20:637-649.
53. Kaneko T., Yano T., Aggarwal K., Lim J.H., Ueda K., Oshima Y., Peach C., Erturk-Hasdemir D., Goldman W.E., Oh B.H. PGRP-LC and PGRP-LE have essential yet distinct functions in the Drosophila immune response to monomeric DAP-type peptidoglycan. Nat. Immunol. 2006, 7:715-723.
54. Kanost M.R. Serine proteinase inhibitors in arthropod immunity. Dev. Comp. Immunol. 1999, 23:291-301.
55. Kanost M.R., Gorman M.G. Phenoloxidases in insect immunity. Insect Immunology 2008, 69-96. Academic Press/Elsevier, San Diego. N. Beckage (Ed.).
56. Kanost M.R., Jiang H.B., Wang Y., Yu X.Q., Ma C.C., Zhu Y.F. Hemolymph proteinases in immune responses of Manduca sexta. Phylogenet. Perspect. Vert. Immune Syst. 2001, 484:319-328.
57. Kanost M.R., Jiang H.B., Yu X.Q. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol. Rev. 2004, 198:97-105.
58. Khush R.S., Lemaitre B. Genes that fight infection - what the Drosophila genome says about animal immunity. Trends Genet. 2000, 16:442-449.
59. Kim T., Kim Y.J. Overview of innate immunity in Drosophila. J. Biochem. Mol. Biol. 2005, 38:121-127.
60. Kisseleva T., Bhattacharya S., Braunstein J., Schindler C.W. Signaling through the JAK/STAT pathway, recent advances and future challenges. Gene 2002, 285:1-24.
61. Kleino A., Valanne S., Ulvila J., Kallio J., Myllymaki H., Enwald H., Stoven S., Poidevin M., Ueda R., Hultmark D., Lemaitre B., Ramet M. Inhibitor of apoptosis 2 and TAK1-binding protein are components of the Drosophila Imd pathway. EMBO J. 2005, 24:3423-3434.
62. Krishnakumar S., Burton D., Rasco J., Chen X.Y., O'Donnell J. Functional interactions between GTP cyclohydrolase I and tyrosine hydroxylase in Drosophila. J. Neurogenet. 2000, 14:1-23.
63. Kurata S., Ariki S., Kawabata S. Recognition of pathogens and activation of immune responses in Drosophila and horseshoe crab innate immunity. Immunobiology 2006, 211:237-249.
64. Lavine M.D., Strand M.R. Insect hemocytes and their role in immunity. Insect Biochem. Mol. Biol. 2002, 32:1295-1309.
65. Lee K.Z., Ferrandon D. Negative regulation of immune responses on the fly. EMBO J. 2011, 30:988-990.
66. Lemaitre B., Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25:697-743.
67. Lemaitre B., Nicolas E., Michaut L., Reichhart J.M., Hoffmann J.A. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86:973-983.
68. LeMosy E.K., Hong C.C., Hashimoto C. Signal transduction by a protease cascade. Trends Cell Biol. 1999, 9:102-107.
69. Mabb A.M., Miyamoto S. SUMO and NF-κB ties. Cell. Mol. Life Sci. 2007, 64:1979-1996.
70. Marmaras V.J., Lampropoulou M. Regulators and signalling in insect haemocyte immunity. Cell. Signal. 2009, 21:186-195.
71. Myhre S., Tveit H., Mollestad T., Laegreid A. Additional gene ontology structure for improved biological reasoning. Bioinformatics 2006, 22:2020-2027.
72. Nappi A., Christensen B. Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochem. Mol. Biol. 2005, 35:443-459.
73. Nappi A.J., Vass E., Frey F., Carton Y. Nitric oxide involvement in Drosophila immunity. Nitric Oxide Biol. Chem. 2000, 4:423-430.
74. Nardi J.B., Pilas B., Bee C.M., Zhuang S., Garsha K., Kanost M.R. Neuroglian-positive plasmatocytes of Manduca sexta and the initiation of hemocyte attachment to foreign surfaces. Dev. Comp. Immunol. 2006, 30:447-462.
75. Pace K.E., Baum L.G. Insect galectins: roles in immunity and development. Glycoconj. J. 2004, 19:607-614.
76. Park J.M., Brady H., Ruocco M.G., Sun H., Williams D., Lee S.J., Kato T., Richards N., Chan K., Mercurio F., Karin M., Wasserman S.A. Targeting of TAK1 by the NF-κB protein Relish regulates the JNK-mediated immune response in Drosophila. Genes Dev. 2004, 18:584-594.
77. Pauchet Y., Wilkinson P., Vogel H., Nelson D.R., Reynolds S.E., Heckel D.G., ffrench-Constant R.H. Pyrosequencing the Manduca sexta larval midgut transcriptome: messages for digestion, detoxification and defence. Insect Mol. Biol. 2010, 19:61-75.
78. Petersen U.M., Kadalayil L., Rehorn K.P., Hoshizaki D.K., Reuter R., Engstrom Y. Serpent regulates Drosophila immunity genes in the larval fat body through an essential GATA motif. EMBO J. 1999, 18:4013-4022.
79. Pham L.N., Dionne M.S., Shirasu-Hiza M., Schneider D.S. A specific primed immune response in Drosophila is dependent on phagocytes. PLoS Path. 2007, 3:e26.
80. Quevillon E., Silventoinen V., Pillai S., Harte N., Mulder N., Apweiler R., Lopez R. InterProScan: protein domains identifier. Nucleic Acids Res. 2005, 33:W116-W120.
81. Ragab A., Buechling T., Gesellchen V., Spirohn K., Boettcher A.L., Boutros M. Drosophila Ras/MAPK signalling regulates innate immune responses in immune and intestinal stem cells. EMBO J. 2011, 30:1123-1136.
82. Ramet M., Manfruelli P., Pearson A., Mathey-Prevot B., Ezekowitz R.A. Functionalgenomic analysis of phagocytosis and identification of a Drosophila receptor for E. coli. Nature 2002, 416:644-648.
83. Ramet M., Lanot R., Zachary D., Manfruelli P. JNK signaling pathway is required for efficient wound healing in Drosophila. Dev. Biol. 2002, 241:145-156.
84. Remillieux-Leschelle N., Santamaria P., Randsholt N.B. Regulation of larval hematopoiesis in Drosophila melanogaster: a role for the multi sex combs gene. Genetics 2002, 162:1259-1274.
85. Rolff J., Reynolds S.E. Insect Infection and Immunity: Evolution, Ecology and Mechanisms 2009, Oxford University Press, Oxford.
86. Sackton T.B., Lazzaro B.P., Schlenke T.A., Evans J.D., Hultmark D., Clark A.G. Dynamic evolution of the innate immune system in Drosophila. Nat. Genet. 2007, 39:1461-1468.
87. Sansonetti P.J. The innate signaling of dangers and the dangers of innate signaling. Nat. Immunol. 2006, 7:1237-1242.
88. Shintani T., Klionsky D.J. Autophagy in health and disease: a double-edged sword. Science 2004, 306:990-995.
89. Sieg D.J., Hauck C.R., Schlaepfer D.D. Required role of focal adhesion kinase (FAK) for integrin-stimulated cell migration. J. Cell Sci. 1999, 112:2677.
90. Silverman N., Maniatis T. NF-κB signaling pathways in mammalian and insect innate immunity. Genes Dev. 2001, 15:2321-2342.
91. Silverman N., Zhou R., Erlich R.L., Hunter M., Bernstein E., Schneider D., Maniatis T. Immune activation of NF-κB and JNK requires Drosophila TAK1. J. Biol. Chem. 2003, 278:48928-48934.
92. Stoven S., Silverman N., Junell A., Hedengren-Olcott M., Erturk D., Engstrom Y., Maniatis T., Hultmark D. Caspase-mediated processing of the Drosophila NF-κB factor Relish. Proc. Natl. Acad. Sci. USA 2003, 100:5991-5996.
93. Strand M.R. The insect cellular immune response. Insect Sci. 2008, 15:1-14.
94. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
95. Tanaka H., Ishibashi J., Fujita K., Nakajima Y., Sagisaka A., Tomimoto K., Suzuki N., Yoshiyama M., Kaneko Y., Iwasaki T., Sunagawa T., Yamaji K., Asaoka A., Mita K., Yamakawa M. A genome-wide analysis of genes and gene families involved in innate immunity of Bombyx mori. Insect Biochem. Mol. Biol. 2008, 38:1087-1110.
96. Valanne S., Wang J.H., Ramet M. The Drosophila Toll signaling pathway. J. Immunol. 2011, 186:649-656.
97. Vilmos P., Kurucz E. Insect immunity: evolutionary roots of the mammalian innate immune system. Immunol. Lett. 1998, 62:59-66.
98. Vogel H., Altincicek B., Glockner G., Vilcinskas A. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics 2011, 12:308.
99. Wajant H., Scheurich P. Analogies between Drosophila and mammalian TRAF pathways. Prog. Mol. Subcell. Biol. 2004, 34:47-72.
100. Wang X.H., Aliyari R., Li W.X., Li H.W., Kim K., Carthew R., Atkinson P., Ding S.W. RNA interference directs innate immunity against viruses in adult Drosophila. Science 2006, 312:452-454.
101. Wang Y., Jiang H. Reconstitution of a branch of the Manduca sexta prophenoloxidase activation cascade in vitro: snake-like hemolymph proteinase 21 (HP21) cleaved by HP14 activates prophenoloxidase-activating proteinase-2 precursor. Insect Biochem. Mol. Biol. 2007, 37:1015-1025.
102. Waterhouse R.M., Kriventseva E.V., Meister S., Xi Z.Y., Alvarez K.S., Bartholomay L.C., Barillas-Mury C., Bian G.W., Blandin S., Christensen B.M., Dong Y.M., Jiang H.B., Kanost M.R., Koutsos A.C., Levashina E.A., Li J.Y., Ligoxygakis P., MacCallum R.M., Mayhew G.F., Mendes A., Michel K., Osta M.A., Paskewitz S., Shin S.W., Vlachou D., Wang L.H., Wei W.Q., Zheng L.B., Zou Z., Severson D.W., Raikhel A.S., Kafatos F.C., Dimopoulos G., Zdobnov E.M., Christophides G.K. Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 2007, 316:1738-1743.
103. Watson F.L., Puttmann-Holgado R., Thomas F., Lamar D.L., Hughes M., Kondo M., Rebel V.I., Schmucker D. Extensive diversity of Ig-superfamily proteins in the immune system of insects. Science 2005, 309:1874-1878.
104. Weber A.N., Tauszig-Delamasure S., Hoffmann J.A., Lelievre E., Gascan H., Ray K.P., Morse M.A., Imler J.L., Gay N.J. Binding of the Drosophila cytokine Spatzle to Toll is direct and establishes signaling. Nat. Immunol. 2003, 4:794-800.
105. Williams M.J. Drosophila hemopoiesis and cellular immunity. J. Immunol. 2007, 178:4711-4716.
106. Williams M.J., Wiklund M.L., Wikman S., Hultmark D. Rac1 signalling in the Drosophila larval cellular immune response. J. Cell Sci. 2006, 119:2015-2024.
107. Xu H., Hao W., He D., Xu Y. Smt3 is required for the immune response of silkworm, Bombyx mori. Biochimie 2010, 92:1306-1314.
108. Yu X.Q., Zhu Y.F., Ma C., Fabrick J.A., Kanost M.R. Pattern recognition proteins in Manduca sexta plasma. Insect Biochem. Mol. Biol. 2002, 32:1287-1293.
109. Zettervall C.J., Anderl I., Williams M.J., Palmer R., Kurucz E., Ando I., Hultmark D. A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl. Acad. Sci. USA 2004, 101:14192-14197.
110. Zhang F.J., Guo H.Y., Zheng H.J., Zhou T., Zhou Y.J., Wang S.Y., Fang R.X., Qian W., Chen X.Y. Massively parallel pyrosequencing-based transcriptome analyses of small brown planthopper (Laodelphax striatellus), a vector insect transmitting rice stripe virus (RSV). BMC Genomics 2010, 11:303.
111. Zhang S., Gunaratna R.T., Zhang X., Najar F., Wang Y., Roe B., Jiang H. Pyrosequencing-based expression profiling and identification of differentially regulated genes from Manduca sexta, a lepidopteran model insect. Insect Biochem. Mol. Biol. 2011, 41:733-746.
112. Zhu Y.F., Ragan E.J., Kanost M.R. Leureptin: a soluble, extracellular leucine-rich repeat protein from Manduca sexta that binds lipopolysaccharide. Insect Biochem. Mol. Biol. 2010, 40:713-722.
113. Zhuang S.F., Kelo L., Nardi J.B., Kanost M.R. Neuroglian on hemocyte surfaces is involved in homophilic and heterophilic interactions of the innate immune system of Manduca sexta. Dev. Comp. Immunol. 2007, 31:1159-1167.
114. Zhuang S.F., Kelo L.S., Nardi J.B., Kanost M.R. An integrin-tetraspanin interaction required for cellular innate immune responses of an insect, Manduca sexta. J. Biol. Chem. 2007, 282:22563-22572.
115. Zhuang S.F., Nardi J.B., Kanost M.R. An integrin, neuroglian, and a tetraspanin modulate adhesion in hemocytes of an insect Manduca sexta. FASEB J. 2005, 19:A1061-A1062.
116. Zou Z., Evans J.D., Lu Z.Q., Zhao P.C., Williams M., Sumathipala N., Hetru C., Hultmark D., Jiang H.B. Comparative genomic analysis of the Tribolium immune system. Genome Biol. 2007, 8:R177.
117. Zou Z., Najar F., Wang Y., Roe B., Jiang H. Pyrosequence analysis of expressed sequence tags for Manduca sexta hemolymph proteins involved in immune responses. Insect Biochem. Mol. Biol. 2008, 38:677-682.