Pyrosequencing-based expression profiling and identification of differentially regulated genes from Manduca sexta, a lepidopteran model insect

Insect Biochemistry and Molecular Biology

Volumn 41, Issue 9, 2011, Pages 733-746

  Zhang, Shuguang ^a   Gunaratna, Ramesh T ^a   Zhang, Xiufeng ^a   Najar, Fares ^b   Wang, Yang ^a   Roe, Bruce ^b   Jiang, Haobo ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

Author keywords

454 sequencing; Functional genomics; Gene discovery; Hemolymph proteins; Insect immunity; RNA Seq; Transcript profiling

Indexed keywords

INSECT PROTEIN;

ANIMAL; ARTICLE; BLOOD CELL; CHEMISTRY; DNA SEQUENCE; EVALUATION; FAT BODY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LARVA; LEPIDOPTERA; METHODOLOGY;

ANIMALS; FAT BODY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEMOCYTES; INSECT PROTEINS; LARVA; MANDUCA; SEQUENCE ANALYSIS, DNA;

HEXAPODA; MANDUCA SEXTA;

EID: 79959802232     PISSN: 09651748     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ibmb.2011.05.005     Document Type: Article

References (65)

1. Abdel-latief M., Hilker M. Innate immunity: eggs of Manduca sexta are able to respond to parasitism by Trichogramma evanescens. Insect. Biochem. Mol. Biol. 2008, 38:136-145.
2. Altincicek B., Vilcinskas A. Identification of a lepidopteran matrix metalloproteinase with dual roles in metamorphosis and innate immunity. Dev. Comp. Immunol. 2008, 32:400-409.
3. 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.
4. An C., Jiang H., Kanost M.R. Proteolytic activation and function of the cytokine Spätzle in innate immune response of a lepidopteran insect, Manduca sexta. FEBS J. 2010, 277:148-162.
5. Ao J.Q., Ling E., Yu X.Q. A Toll receptor from Manduca sexta is in response to Escherichia coli infection. Mol. Immunol. 2008, 45:543-552.
6. Armstrong P.B. Proteases and protease inhibitors: a balance of activities in host-pathogen interaction. Immunobiology 2006, 211:263-281.
7. Arrese E.L., Soulages J.L. Insect fat body: energy, metabolism, and regulation. Annu. Rev. Entomol. 2010, 55:207-225.
8. Bird P.I. Serpins and regulation of cell death. Results Probl. Cell Differ. 1998, 24:63-89.
9. Bulet P., Stöcklin R., Menin L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 2004, 198:169-184.
10. Costa V., Angelini C., De Feis I., Ciccodicola A. Uncovering the complexity of transcriptomes with RNA-Seq. J. Biomed. Biotechnol. 2010, 853916.
11. Dai H., Rayaprolu S., Gong Y., Huang R., Prakash O., Jiang H. Solution structure, antibacterial activity, and expression profile of Manduca sexta moricin. J. Pept. Sci. 2008, 14:855-863.
12. Dunn P.E., Drake D. Fate of bacteria injected into naive and immunized larvae of the tobacco hornworm, Manduca sexta. J. Invertebr. Pathol. 1983, 41:77-85.
13. Finnerty C.M., Karplus P.A., Granados R.R. The insect immune protein scolexin is a novel serine proteinase homolog. Protein Sci. 1999, 8:242-248.
14. Furukawa S., Tanaka H., Ishibashi J., Imanishi S., Yamakawa M. Functional characterization of a cactus homolog from the silkworm Bombyx mori. Biosci. Biotechnol. Biochem. 2009, 73:2665-2670.
15. Gan H., Wang Y., Jiang H., Mita K., Kanost M.R. A bacteria-induced, intracellular serpin in granular hemocytes of Manduca sexta. Insect Biochem. Mol. Biol. 2001, 31:887-898.
16. Gillespie J.P., Kanost M.R., Trenczek T. Biological mediators of insect immunity. Ann. Rev. Entomol. 1997, 42:611-643.
17. Girard P., Boublik Y., Wheat C.W., Volkoff A.N., Cousserans F., Brehélin M., Escoubas J.M. X-tox: an atypical defensin derived family of immune-related proteins specific to Lepidoptera. Dev. Comp. Immunol. 2008, 32:575-584.
18. Gorman M.J., An C., Kanost M.R. Characterization of tyrosine hydroxylase from Manduca sexta. Insect Biochem. Mol. Biol. 2007, 37:1327-1337.
19. Gupta S., Wang Y., Jiang H. Manduca sexta prophenoloxidase (proPO) activation requires proPO-activating proteinase (PAP) and serine proteinase homologs (SPHs) simultaneously. Insect Biochem. Mol. Biol. 2005, 35:241-248.
20. Jiang H. The biochemical basis of antimicrobial responses in Manduca sexta. Insect Sci. 2008, 15:53-66.
21. Jiang H., Kanost M.R. The clip-domain family of serine proteinases in arthropods. Insect Biochem. Mol. Biol. 2000, 30:95-105.
22. Jiang H., Wang Y., Kanost M.R. Four serine proteinases expressed in Manduca sexta hemocytes. Insect Mol. Biol. 1999, 8:39-53.
23. 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.
24. Jiang H., Wang Y., Ma C., Kanost M.R. Subunit composition of pro-phenol oxidase from Manduca sexta: molecular cloning of subunit proPO-p1. Insect Biochem. Mol. Biol. 1997, 27:835-850.
25. Jiang H., Wang Y., Kanost M.R. Prophenoloxidase-activating proteinase-2 from hemolymph of Manduca sexta: a bacteria-inducible serine proteinase containing two clip domains. J. Biol. Chem. 2003, 278:3552-3561.
26. Jiang H., Wang Y., Yu X.Q., Zhu Y., Kanost M.R. Prophenoloxidase-activating proteinase-3 (PAP-3) from Manduca sexta hemolymph: a clip-domain serine proteinase regulated by serpin-1J and serine proteinase homologs. Insect Biochem. Mol. Biol. 2003, 33:1049-1060.
27. Kanamori Y., Hayakawa Y., Matsumoto H., Yasukochi Y., Shimura S., Nakahara Y., Kiuchi M., Kamimura M. A eukaryotic (insect) tricistronic mRNA encodes three proteins selected by context-dependent scanning. J. Biol. Chem. 2010, 285:36933-36944.
28. Kanost M.R., Nardi J.B. Innate immune responses of Manduca sexta. Molecular Biology and Genetics of Lepidoptera 2010, 271-292. CRC Press, New York. M.R. Goldsmith, F. Marec (Eds.).
29. Kanost M.R., Zepp M.K., Ladendorff N.E., Andersson L.A. Isolation and characterization of a hemocyte aggregation inhibitor from hemolymph of Manduca sexta larvae. Arch. Insect Biochem. Physiol. 1994, 27:123-136.
30. Kanost M.R. Serine proteinase inhibitors in arthropod immunity. Dev. Comp. Immunol. 1999, 23:291-301.
31. Kauppila S., Maaty W.S., Chen P., Tomar R.S., Eby M.T., Chapo J., Chew S., Rathore N., Zachariah S., Sinha S.K., Abrams J.M., Chaudhary P.M. Eiger and its receptor, Wengen, comprise a TNF-like system in Drosophila. Oncogene 2003, 22:4860-4867.
32. Kocks C., Cho J.H., Nehme N., Ulvila J., Pearson A.M., Meister M., Strom C., Conto S.L., Hetru C., Stuart L.M., Stehle T., Hoffmann J.A., Reichhart J.M., Ferrandon D., Rämet M., Ezekowitz R.A. Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 2005, 123:335-346.
33. Kurucz E., Márkus R., Zsámboki J., Folkl-Medzihradszky K., Darula Z., Vilmos P., Udvardy A., Krausz I., Lukacsovich T., Gateff E., Zettervall C.J., Hultmark D., Andó I. Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes. Curr. Biol. 2007, 17:649-654.
34. Ladendorff N.E., Kanost M.R. Bacteria-induced protein P4 (hemolin) from Manduca sexta: a member of the immunoglobulin superfamily which can inhibit hemocyte aggregation. Arch. Insect Biochem. Physiol. 1991, 18:285-300.
35. Lemaitre B., Hoffmann J. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 2007, 25:697-743.
36. Lesch C., Goto A., Lindgren M., Bidla G., Dushay M.S., Theopold U. A role for hemolectin in coagulation and immunity in Drosophila melanogaster. Dev. Comp. Immunol. 2007, 31:1255-1263.
37. Ling E., Rao X.J., Ao J.Q., Yu X.Q. Purification and characterization of a small cationic protein from the tobacco hornworm Manduca sexta. Insect Biochem. Mol. Biol. 2009, 39:263-271.
38. Liu X., Yao Q., Wang Y., Chen K. Proteomic analysis of nucleopolyhedrovirus infection resistance in the silkworm, Bombyx mori. J. Invertebr. Pathol. 2010, 105:84-90.
39. Ma C., Kanost M.R. A beta-1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. J. Biol. Chem. 2000, 275:7505-7514.
40. Marguerat S., Bähler J. RNA-Seq: from technology to biology. Cell Mol. Life Sci. 2010, 67:569-579.
41. Margulies M., Egholm M., Altman W.E., Bader J.S., et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437:376-380.
42. Matsumoto Y., Oda Y., Uryu M., Hayakawa Y. Insect cytokine growth-blocking peptide triggers a termination system of cellular immunity by inducing its binding protein. J. Biol. Chem. 2003, 278:38579-38585.
43. Morin R.D., Aksay G., Dolgosheina E., Ebhardt H.A., Magrini V., Mardis E.R., Sahinalp S.C., Unrau P.J. Comparative analysis of the small RNA transcriptomes of Pinus contorta and Oryza sativa. Genome Res. 2008, 18:571-584.
44. Mortazavi A., Williams B.A., McCue K., Schaeffer L., Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 2008, 5:621-628.
45. Mulnix A.B., Dunn P.E. Structure and induction of a lysozyme gene from the tobacco hornworm, Manduca sexta. Insect Biochem. Mol. Biol. 1994, 24:271-281.
46. Nardi J.B., Martos R., Walden K.K., Lampe D.J., Robertson H.M. Expression of lacunin, a large multidomain extracellular matrix protein, accompanies morphogenesis of epithelial monolayers in Manduca sexta. Insect Biochem. Mol. Biol. 1999, 29:883-897.
47. Nardi J.B., Zhuang S., Pilas B., Bee C.M., Kanost M.R. Clustering of adhesion receptors following exposure of insect blood cells to foreign surfaces. J. Insect. Physiol. 2005, 51:555-564.
48. Nichol H., Law J.H., Winzerling J.J. Iron metabolism in insects. Ann. Rev. Entomol. 2002, 47:535-559.
49. Noguchi H., Tsuzuki S., Tanaka K., Matsumoto H., Hiruma K., Hayakawa Y. Isolation and characterization of a dopa decarboxylase cDNA and the induction of its expression by an insect cytokine, growth-blocking peptide in Pseudaletia separata. Insect Biochem. Mol. Biol. 2003, 33:209-217.
50. 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.
51. Ragan E.J., An C., Jiang H., Kanost M.R. Roles of hemolymph proteins in antimicrobial defenses of Manduca sexta. Insect Infection and Immunity 2009, 34-48. Oxford University Press. S. Reynolds, J. Rolff (Eds.).
52. Rayaprolu S., Wang Y., Kanost M.R., Hartson S., Jiang H. Functional analysis of four processing products from multiple precursors encoded by a lebocin-related gene from Manduca sexta. Dev. Comp. Immunol. 2010, 34:638-647.
53. Roe B. Shotgun library construction for DNA sequencing. Methods Mol. Biol. 2004, 255:171-187.
54. Shin S.W., Park S.S., Park D.S., Kim M.G., Kim S.C., Brey P.T., Park H.Y. Isolation and characterization of immune-related genes from the fall webworm, Hyphantria cunea, using PCR-based differential display and subtractive cloning. Insect Biochem. Mol. Biol. 1998, 28:827-837.
55. Strand M.R. The insect cellular immune response. Insect Sci. 2008, 15:1-15.
56. 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.
57. Tanaka H., Matsuki H., Furukawa S., Sagisaka A., Kotani E., Mori H., Yamakawa M. Identification and functional analysis of Relish homologs in the silkworm, Bombyx mori. Biochim. Biophys. Acta 2007, 1769:559-568.
58. Vogel B.E., Hedgecock E.M. Hemicentin, a conserved extracellular member of the immunoglobulin superfamily, organizes epithelial and other cell attachments into oriented line-shaped junctions. Development 2001, 128:883-894.
59. Yu X.Q., Jiang H., Wang Y., Kanost M.R. Nonproteolytic serine proteinase homologs involved in phenoloxidase activation in the tobacco hornworm, Manduca sexta. Insect Biochem. Mol. Biol. 2003, 33:197-208.
60. Yu X.Q., Tracy M.E., Ling E., Scholz F.R., Trenczek T. A novel C-type immulectin-3 from Manduca sexta is translocated from hemolymph into the cytoplasm of hemocytes. Insect Biochem. Mol. Biol. 2005, 35:285-295.
61. Zang X., Maizels R.M. Serine proteinase inhibitors from nematodes and the arms race between host and pathogen. Trends Biochem. Sci. 2001, 26:191-197.
62. Zhu Y., Johnson T.J., Myers A.A., Kanost M.R. Identification by subtractive suppression hybridization of bacteria-induced genes expressed in Manduca sexta fat body. Insect Biochem. Mol. Biol. 2003, 33:541-559.
63. Zhu Y., 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.
64. 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.
65. Zou Z., Zhao P., Weng H., Mita K., Jiang H. A comparative analysis of serpin genes in the silkworm genome. Genomics 2009, 93:367-375.