The biochemical basis of antimicrobial responses in Manduca Sexta

Insect Science

Volumn 15, Issue 1, 2008, Pages 53-66

  Jiang, Haobo ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

Clip domain; Hemolymph protein; Insect immunity; Melanization; plasmatocyte; Serine proteinase cascade; Serpin; Sp tzle; Tobacco hornworm; Toll pathway

Indexed keywords

BACTERIA (MICROORGANISMS); HEXAPODA; INVERTEBRATA; MANDUCA SEXTA; VERTEBRATA;

EID: 44149112551     PISSN: 16729609     EISSN: 17447917     Source Type: Journal    
DOI: 10.1111/j.1744-7917.2008.00187.x     Document Type: Review

References (120)

1. Aizawa, T., Fujitani, N., Hayakawa, Y., Ohnishi, A., Ohkubo, T., Kumake, Y., Kawano, K., Hikichi, K. and Nitta, K. (1999) Solution structure of an insect growth factor, growth-blocking peptide. Journal of Biological Chemistry, 274, 1887-1890.
2. Amaya, K.E., Asgari, S., Jung, R., Hongskula, M. and Beckage, N.E. (2005) Parasitization of Manduca sexta larvae by the parasitoid wasp Cotesia congregata induces an impaired host immune response. Journal of Insect Physiology, 51, 505-512.
3. Ashida, M. and Brey, P.T. (1998) Recent advances on the research of the insect prophenoloxidase cascade. Molecular Mechanisms of Immune Responses in Insects (eds. P.T. Brey & D. Hultmark), pp. 135-172. Chapman & Hall, London.
4. Chen, C., Lampe, D.J., Robertson, H.M. and Nardi, J.B. (1997) Neuroglian is expressed on cells destined to form the prothoracic glands of Manduca embryos as they segregate from surrounding cells and rearrange during morphogenesis. Developmental Biology, 181, 1-13.
5. 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., Müller, 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., Zheng, L., Bork, P. and Kafatos, F.C. (2002) Immunity-related genes and gene families in Anopheles gambiae. Science, 298, 159-165.
6. Dai, H., Rayaprolu, S., Gong, Y., Huang, R., Prakash, O. and Jiang, H. (2008) Solution structure, antibacterial activity, and expression profile of Manduca sexta moricin. Journal of Peptide Science (in press).
7. Dean, P., Potter, U., Richards, E.H., Edwards, J.P., Charnley, A. K. and Reynolds, S.E. (2004) Hyperphagocytic haemocytes in Manduca sexta. Journal of Insect Physiology, 50, 1027-1036.
8. De Gregorio, E., Han, S.J., Lee, W.J., Baek, M.J., Osaki, T., Kawabata, S., Lee, B.L., Iwanaga, S., Lemaitre, B. and Brey, P.T. (2002) An immune-responsive serpin regulates the melanization cascade in Drosophila. Developmental Cell, 3, 581-592.
9. De Gregorio, E., Spellman, P.T., Rubin, G.M. and Lemaitre, B. (2001) Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proceedings of the National Academy of Sciences of the United States of America, 98, 12590-12595.
10. Dickinson, L., Russell, V.W. and Dunn, P.E. (1988) A family of bacteria-regulated cecropin D-like peptides from Manduca sexta. Journal of Biological Chemistry, 263, 19424-19429.
11. Dunn, P.E., Dai, W., Kanost, M.R. and Geng, C.X. (1985) Soluble peptidoglycan fragments stimulate antibacterial protein synthesis by fat body from larvae of Manduca sexta. Developmental and Comparative Immunology, 9, 559-568.
12. Eleftherianos, I., Gokcen, F., Felfoldi, G., Millichap, P.J., Trenczek, T.E., ffrench-Constant, R.H. and Reynolds, S.E. (2007) The immunoglobulin family protein hemolin mediates cellular immune responses to bacteria in the insect Manduca sexta. Cell Microbiology, 9, 1137-1147.
13. Fabrick, J.A., Baker, J.E. and Kanost, M.R. (2003) Properties of a β-1,3-glucan recognition protein from an insect, Plodia interpunctella. Insect Biochemistry and Molecular Biology, 33, 579-594.
14. Faye, I. and Kanost, M.R. (1998) Function and regulation of hemolin. Molecular Mechanisms of Immune Responses in Insects (eds. P.T. Brey & D. Hultmark), pp.173-188. Chapman & Hall, London.
15. Gan, H., Wang, Y., Jiang, H., Mita, K. and Kanost, M.R. (2001) A bacteria-induced, intracellular serpin in granular hemocytes of Manduca sexta. Insect Biochemistry and Molecular Biology, 31, 887-898.
16. Gettins, P.G. (2002) Serpin structure, mechanism, and function. Chemical Review, 102, 4751-4804.
17. Gillespie, J.P., Kanost, M.R. and Trenczek, T. (1997) Biological mediators of insect immunity. Annual Review of Entomology, 42, 611-643.
18. Gorman, M.J., Kankanala, P. and Kanost, M.R. (2003) Bacterial challenge stimulates innate immune responses in extra-embryonic tissues of tobacco hornworm eggs. Insect Molecular Biology, 13, 19-24.
19. Gorman, M.J., An, C. and Kanost, M.R. (2007a) Characterization of tyrosine hydroxylase from Manduca sexta. Insect Biochemistry and Molecular Biology, 37, 1327-1337.
20. Gorman, M.J., Wang, Y., Jiang, H. and Kanost, M.R. (2007b) Manduca sexta hemolymph proteinase 21 activates prophenoloxidase activating proteinase 3 in an insect innate immune response proteinase cascade. Journal of Biological Chemistry, 282, 11742-11749.
21. Götz, P. (1986) Encapsulation in arthropods. Immunity in Invertebrates: Cells, Molecules and Defense Reactions (ed. M. Brehèlin), pp. 153-170. Springer-Verlag, Berlin.
22. Gupta, S., Wang, Y. and Jiang, H. (2005a) Purification and characterization of Manduca sexta prophenoloxidase-activating proteinase-1 (PAP-1), an enzyme involved in insect immune responses. Protein Expression and Purification, 39, 261-268.
23. Gupta, S., Wang, Y. and Jiang, H. (2005b) Manduca sexta prophenoloxidase (proPO) activation requires proPO-activating proteinase (PAP) and serine proteinase homologs (SPHs) simultaneously. Insect Biochemistry and Molecular Biology, 35, 241-248.
24. Hall, M., Scott, T., Sugumaran, M., Söderhäll, K. and Law, J.H. (1995) Proenzyme of Manduca sexta phenol oxidase: purification, activation, substrate specificity of the active enzyme, and molecular cloning. Proceedings of the National Academy of Sciences of the United States of America, 92, 7764-7768.
25. Hoffmann, J.A., Kafatos, F.C., Janeway, C.A. and Ezekowitz, R. A.B. (1999) Phylogenetic perspectives in innate immunity. Science, 284, 1313-1318.
26. Horohov, D.W. and Dunn, P.E. (1983) Phagocytosis and nodule formation by hemocytes of Manduca sexta larvae following injection of Pseudomonas aeruginosa. Journal of Invertebrate Pathology, 41, 203-213.
27. Huang, R., Lu, Z., Dai, H., Vander Velde, D., Prakash, O. and Jiang, H. (2007) The solution structure of clip domains from Manduca sexta prophenoloxidase activating proteinase-2. Biochemistry, 46, 11431-11439.
28. Hughes, J.A., Hurlbert, R.E., Rupp, R.A. and Spence, K.D. (1983) Bacteria-induced haemolymph proteins of Manduca sexta pupae and larvae. Journal of Insect Physiology, 29, 625-632.
29. Ji, C., Wang, Y., Guo, X., Hartson, S. and Jiang, H. (2004) A pattern recognition serine proteinase triggers the prophenoloxidase activation cascade in the tobacco hornworm, Manduca sexta. Journal of Biological Chemistry, 279, 34101- 34106.
30. Jiang, H. and Kanost, M.R. (1997) Characterization and functional analysis of twelve naturally occurring reactive site variants of serpin-1 from Manduca sexta. Journal of Biological Chemistry, 272, 1082-1087.
31. Jiang, H. and Kanost, M.R. (2000) The clip-domain family of serine proteinases in arthropods. Insect Biochemistry and Molecular Biology, 30, 95-105.
32. Jiang, H., Ma, C., Lu, Z. and Kanost, M.R. (2004) β-1,3-Glucan recognition protein-2 (βGRP-2) from Manduca sexta: an acutephase protein that binds β-1,3-glucan and lipoteichoic acid to aggregate fungi and bacteria. Insect Biochemistry and Molecular Biology, 34, 89-100.
33. Jiang, H., Mulnix, A.B. and Kanost, M.R. (1995) Expression and characterization of recombinant Manduca sexta serpin-1B and site-directed mutants that change its inhibitory selectivity. Insect Biochemistry and Molecular Biology, 25, 1093-1100.
34. Jiang, H., Wang, Y., Huang, Y., Mulnix, A.B., Kadel, J., Cole, K. and Kanost, M.R. (1996) Organization of serpin gene-1 from Manduca sexta: evolution of a family of alternate exons encoding the reactive site loop. Journal of Biological Chemistry, 271, 28017-28023.
35. Jiang, H., Wang, Y. and Kanost, M.R. (1994) Mutually exclusive exon use and reactive center diversity in insect serpins. Journal of Biological Chemistry, 269, 55-58.
36. Jiang, H., Wang, Y. and Kanost, M.R. (1998) Pro-phenol oxidase activating proteinase from an insect, Manduca sexta: a bacteria- inducible protein similar to Drosophila easter. Proceedings of the National Academy of Sciences of the United States of America, 95, 12220-12225.
37. Jiang, H., Wang, Y. and Kanost, M.R. (1999) Four serine proteinases expressed in Manduca sexta hemocytes. Insect Molecular Biology, 8, 39-53.
38. Jiang, H., Wang, Y. and Kanost, M.R. (2001) Proteolytic activation of prophenoloxidase in an insect Manduca sexta. Advances in Experimental Medical Biology, 484, 313-317.
39. Jiang, H, Wang, Y., Ma, C. and Kanost, M.R. (1997) Subunit composition of pro-phenol oxidase from Manduca sexta: molecular cloning of subunit proPO-p1. Insect Biochemistry and Molecular Biology, 27, 835-850.
40. Jiang, H., Wang, Y., Yu, X-Q. and Kanost, M.R. (2003a) Prophenoloxidase-activating proteinase-2 (PAP-2) from hemolymph of Manduca sexta: a bacteria-inducible serine proteinase containing two clip domains. Journal of Biological Chemistry, 278, 3552-3561.
41. Jiang, H., Wang, Y., Yu, X-Q., Zhu, Y. and Kanost, M.R. (2003b) Prophenoloxidase-activating proteinase-3 (PAP-3) from Manduca sexta hemolymph: a clip-domain serine proteinase regulated by serpin-1J and serine proteinase homologs. Insect Biochemistry and Molecular Biology, 33, 1049-1060.
42. Jiang, H., Wang, Y., Gu, Y., Guo, X., Zou, Z., Scholz, F., Trenczek, T.E. and Kanost, M.R. (2005) Molecular identification of a bevy of serine proteinases in Manduca sexta hemolymph. Insect Biochemistry and Molecular Biology, 35, 931-943.
43. Kanost, M.R. (1990) Isolation and characterization of four serine proteinase inhibitors (serpins) from hemolymph of Manduca sexta. Insect Biochemistry, 20, 141-147.
44. Kanost, M.R. (1999) Serine proteinase inhibitors in arthropod immunity. Developmental and Comparative Immunology, 23, 291-301.
45. Kanost, M.R., Dai, W. and Dunn, P.E. (1988) Peptidoglycan fragments elicit antibacterial protein synthesis in larvae of Manduca sexta. Archives of Insect Biochemistry and Physiology, 8, 147-164.
46. Kanost, M.R., Kawooya, J.K., Law, J.H., Ryan, R.O., Van Heusden, M.C. and Ziegler, R. (1990) Insect hemolymph proteins. Advances in Insect Physiology, 22, 299-396.
47. Kanost, M.R., Jiang, H., Wang, Y., Yu, X-Q., Ma, C. and Zhu, Y. (2001) Hemolymph proteinases in immune responses of Manduca sexta. Advances in Experimental Medical Biology, 484, 319-328.
48. Kanost, M.R., Jiang, H. and Yu, X-Q. (2004) Innate immune responses of a lepidopteran insect, Manduca sexta. Immunological Review, 198, 97-105.
49. Kanost, M.R., Prasad, S.V., Huang, Y. and Willott, E. (1995) Regulation of serpin gene-1 in Manduca sexta. Insect Biochemistry and Molecular Biology, 25, 285-291.
50. Kanost, M.R., Prasad, S.V. and Wells, M.A. (1989) Primary structure of a member of the serpin superfamily of proteinase inhibitors from an insect, Manduca sexta. Journal of Biological Chemistry, 264, 965-972.
51. Kanost, M.R., Zepp, M.K., Ladendorff, N.E. and Andersson, L. A. (1994) Isolation and characterization of a hemocyte aggregation aggregation inhibitor from hemolymph of Manduca sexta larvae. Archives of Insect Biochemistry and Physiology, 27, 123-136.
52. Ladendorff, N.E. and Kanost, M.R. (1990) Isolation and characterization of bacteria-induced protein P4 from hemolymph of sexta. Archives of Insect Biochemistry and Physiology, 15, 33-41.
53. Ladendorff, N.E. and Kanost, M.R. (1991) Bacteria-induced protein P4 (hemolin) from Manduca sexta: a member of the immunoglobulin superfamily which can inhibit hemocyte aggregation. Archives of Insect Biochemistry and Physiology, 18, 285-300.
54. Lavine, M.D. and Strand, M.R. (2002) Insect hemocytes and their role in immunity. Insect Biochemistry and Molecular Biology, 32, 1295-1309.
55. Lee, K.Y., Horodyski, F.M., Valaitis, A.P. and Denlinger, D.L. (2002) Molecular characterization of the insect immune protein hemolin and its high induction during embryonic diapause in the gypsy moth, Lymantria dispar. Insect Biochemistry and Molecular Biology, 32, 1457-1467.
56. Lee, S.Y., Cho, M.Y., Hyun, J.H., Lee, K.M., Homma, K.I., Natori, S., Kawabata, S.I., Iwanaga, S. and Lee, B.L. (1998) Molecular cloning of cDNA for prophenoloxidase-activating factor I, a serine protease is induced by lipopolysaccharide or 1,3-beta-glucan in coleopteran insect, Holotrichia diomphalia larvae. European Journal of Biochemistry, 257, 615-621.
57. Lee, S.Y., Wang, R. and Söderhäll, K. (2000) A lipopolysaccharide and β-1,3-glucan binding protein from hemocytes of the freshwater crayfish Pacifastacus leniusculus: purification, characterization, and cDNA cloning. Journal of Biological Chemistry, 275, 1337-1343.
58. Levin, D.M., Breuer, L.N., Zhuang, S., Anderson, S.A., Nardi, J. B. and Kanost, M.R. (2005) A hemocyte-specific integrin required for hemocytic encapsulation in the tobacco hornworm, Manduca sexta. Insect Biochemistry and Molecular Biology, 35, 369-380.
59. Li, J., Wang, Z., Canagarajah, B., Jiang, H., Kanost, M.R. and Goldsmith, E.J. (1999) The structure of active serpin K from Manduca sexta and a model for serpin-protease complex formation. Structure, 7, 103-109.
60. Ligoxygakis, P., Pelte, N., Ji, C., Leclerc, V., Duvic, B., Belvin, M., Jiang, H., Hoffmann, J.A. and Reichhart, J.M. (2002) A serpin mutant links Toll activation to melanization in the host defense of Drosophila. EMBO Journal, 21, 6330-6337.
61. Lu, Z. and Jiang, H. (2007) Regulation of phenoloxidase activity by high- and low-molecular- weight inhibitors from the larval hemolymph of Manduca sexta. Insect Biochemistry and Molecular Biology, 37, 478-485.
62. Lu, Z. and Jiang, H. (2008) Expression of Manduca sexta serine proteinase homolog precursors in insect cells and their proteolytic activation. Insect Biochemistry and Molecular Biology, 38, 89-98.
63. Ma, C. and Kanost, M.R. (2000) A β-1,3-glucan recognition protein from an insect, Manduca sexta, agglutinates microorganisms and activates the phenoloxidase cascade. Journal of Biological Chemistry, 275, 7505-7514.
64. Mulnix, A.B. and Dunn, P.E. (1994) Structure and induction of a lysozyme gene from the tobacco hornworm, Manduca sexta. Insect Biochemistry and Molecular Biology, 24, 271-281.
65. Nappi, A.J. and Christensen, B.M. (2005) Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity. Insect Biochemistry and Molecular Biology, 35, 443-459.
66. Nardi, J.B., Martos, R., Walden, K.K., Lampe, D.J. and Robertson, H.M. (1999) Expression of lacunin, a large multidomain extracellular matrix protein, accompanies morphogenesis of epithelial monolayers in Manduca sexta. Insect Biochemistry and Molecular Biology, 29, 883-897.
67. Nardi, J.B., Pilas, B., Bee, C.M., Zhuang, S., Garsha, K. and Kanost, M.R. (2006) Neuroglian-positive plasmatocytes of Manduca sexta and initiation of hemocyte attachment to foreign surfaces. Developmental and Comparative Immunology, 30, 447-462.
68. Nardi, J.B., Zhuang, S., Pilas, B., Bee, C.M. and Kanost, M.R. (2005) Clustering of adhesion receptors following exposure of insect blood cells to foreign surfaces. Journal of Insect Physiology, 51, 555-564.
69. Ochiai, M. and Ashida, M. (1988) Purification of a β-1,3-glucan recognition protein in the prophenoloxidase activating system from hemolymph of the silkworm, Bombyx mori. Journal of Biological Chemistry, 263, 12056-12062.
70. Ochiai, M. and Ashida, M. (1999) A pattern recognition protein for peptidoglycan: cloning the cDNA and the gene of the silkworm, Bombyx mori. Journal of Biological Chemistry, 274, 11854-11858.
71. Ochiai, M. and Ashida, M. (2000) A pattern recognition protein for β-1,3-glucan. Journal of Biological Chemistry, 275, 4995- 5002.
72. Rasmuson, T. and Boman, H.G. (1979) Insect immunity V. Purification and some properties of immune protein P4 from hemolymph of Hyalophora cecropia pupae. Insect Biochemistry, 9, 259-264.
73. RodrÍguez-Pérez, M.A., Dumpit, R.F., Lenz, J.M., Powell, E.N., Tam, S.Y. and Beckage, N.E. (2005) Host refractoriness of the tobacco hornworm, Manduca sexta, to the braconid endoparasitoid Cotesia flavipes. Archives of Insect Biochemistry and Physiology, 60, 159-171.
74. Ross, J., Jiang, H., Kanost, M.R. and Wang, Y. (2003) Serine proteases and their homologs in the Drosophila melanogaster genome: an initial analysis of sequence conservation and phylogenetic relationship. Gene, 304, 117-131.
75. Satoh, D., Horii, A., Ochiai, M. and Ashida, M. (1999) Prophenoloxidase-activating enzyme of the silkworm, Bombyx mori: purification, characterization and cDNA cloning. Journal of Biological Chemistry, 274, 7441-7453.
76. Saul, S.J. and Sugumaran, M. (1987) Protease mediated prophenoloxidase activation in the hemolymph of the tobacco hornworm, Manduca sexta. Archives of Insect Biochemistry and Physiology, 5, 1-11.
77. Shin, S.W., Park, S-S, Park, D-S, Kim, M.G., Kim, S.C., Brey, P. T. and Park, H-Y. (1998) Isolation and characterization of immune-related genes from the fall webworm, Hyphantria cunea, using PCR-based differential display and subtractive cloning. Insect Biochemistry and Molecular Biology, 28, 827- 837.
78. Skinner, W., Dennis, P., Li, J., Summerfelt, R., Carney, R. and Quistad, G. (1991) Isolation and identification of paralytic peptides from hemolymph of the lepidopteran insects Manduca sexta, Spodoptera exigua, and Heliothis virescens. Journal of Biological Chemistry, 266, 12873-12877.
79. Söderhäll, K., Rogener, W., Söderhäll, I., Newton, R.P. and Ratcliffe, N.A. (1988) The properties and purification of a Blaberus craniifer plasma protein which enhances the activation of hemocyte prophenoloxidase by a β-1,3-glucan. Insect Biochemistry, 18, 323-330.
80. Stevens, J.M. (1962) Bactericidal activity of the blood of actively immunized wax moth larvae. Canadian Journal of Microbiology, 8, 491-499.
81. Strand, M.R., Hayakawa, Y. and Clark, K.D. (2000) Plasmatocyte spreading peptide (PSP1) and growth blocking peptide (GBP) are multifunctional homologs. Journal of Insect Physiology, 46, 817-824.
82. Su, X-D, Gastinel, L.N., Vaughn, D.E., Faye, I., Poon, P. and Bjorkman, P.J. (1998) Crystal structure of hemolin: A horseshoe shape with implications for homophilic adhesion. Science, 281, 991-995.
83. Tong, Y., Jiang, H. and Kanost, M.R. (2005) Identification of plasma proteases inhibited by Manduca sexta serpin-4 and serpin-5 and their association with components of the prophenol oxidase activation pathway. Journal of Biological Chemistry, 280, 14932-14942.
84. Tong, Y. and Kanost, M.R. (2005) Manduca sexta serpin-4 and serpin-5 inhibit the prophenol oxidase activation pathway: cDNA cloning, protein expression, and characterization. Journal of Biological Chemistry, 280, 14923-14931.
85. Vasta, G.R., Quesenberry, M., Ahmed, H. and O'Leary, N. (1999) C-type lectins and galectins mediate innate and adaptive immune functions: their roles in the complement activation pathway. Developmental and Comparative Immunology, 23, 401-420.
86. Volkman, B.F., Anderson, M.E., Clark, K.D., Hayakawa, Y., Strand, M.R. and Markley, J.L. (1999) Structure of the insect cytokine peptide plasmatocyte-spreading peptide 1 from Pseudoplusia includens. Journal of Biological Chemistry, 274, 4493-4496.
87. Wang, Y., Chen, T., Rayaprolu, S., Zou, Z., Xia, Q., Xiang, Z. and Jiang, H. (2007) Proteolytic activation of pro-spätzle is re quired for the induced transcription of antimicrobial peptide genes in lepidopteran insects. Developmental and Comparative Immunology, 31, 1002-1012.
88. Wang, Y. and Jiang, H. (2004a) Prophenoloxidase (PPO) activation in Manduca sexta: an initial analysis of molecular interactions among PPO, PPO-activating proteinase-3 (PAP-3), and a cofactor. Insect Biochemistry and Molecular Biology, 34, 731-742.
89. Wang, Y. and Jiang, H. (2004b) Purification and characterization of Manduca sexta serpin-6: a serine proteinase inhibitor that selectively inhibits prophenoloxidase-activating proteinase-3. Insect Biochemistry and Molecular Biology, 34, 387-395.
90. Wang, Y. and Jiang, H. (2006) Interaction of β-1,3-glucan with its recognition protein activates hemolymph proteinase 14, an initiation enzyme of the prophenoloxidase activation system in Manduca sexta. Journal of Biological Chemistry, 281, 9271- 9278.
91. Wang, Y. and Jiang, H. (2007) Reconstitution of a branch of Manduca sexta prophenoloxidase activation cascade in vitro: Snake-like hemolymph proteinase 21 cleaved by HP14 activates prophenoloxidase-activating proteinase-2 precursor. Insect Biochemistry and Molecular Biology, 37, 1015-1025.
92. Wang, Y., Jiang, H. and Kanost, M.R. (2001) Expression and purification of Manduca sexta prophenoloxidase-activating proteinase precursor (proPAP) from baculovirus-infected insect cells. Protein Expression and Purification, 23, 328- 337.
93. Wang, Y., Jiang, H. and Kanost, M.R. (1999) Biological activity of Manduca sexta paralytic and plasmatocyte spreading peptide and primary structure of its hemolymph precursor. Insect Biochemistry and Molecular Biology, 29, 1075-1086.
94. Wang, Y., Willott, E. and Kanost, M.R. (1995) Organization and expression of the hemolin gene, a member of the immunoglobulin superfamily in an insect, Manduca sexta. Insect Molecular Biology, 4, 113-123.
95. Wang, Y., Zou, Z. and Jiang, H. (2006) An expansion of the dual clip-domain serine proteinase family in Manduca sexta: gene organization, expression, and evolution of prophenoloxidaseactivating proteinase-2, hemolymph proteinase 12, and other related proteinases. Genomics, 87, 399-409.
96. Weis, W.I., Taylor, M.E. and Drickamer, K. (1998) The C-type superfamily in the immune system. Immunological Review, 163, 19-34.
97. Ye, S. and Goldsmith, E.J. (2001) Serpins and other covalent protease inhibitors. Current Opinions in Structural Biology, 11, 740-745.
98. Ye, S, Cech, A.L., Belmares, R., Bergstrom, R.C., Tong, Y., Corey, D.R., Kanost, M.R. and Goldsmith, E.J. (2001) The structure of a Michaelis serpin-protease complex. Nature Structural Biology, 8, 979-983.
99. Yoshida, H., Kinoshita, K. and Ashida, M. (1996) Purification of a peptidoglycan recognition protein from hemolymph of the silkworm, Bombyx mori. Journal of Biological Chemistry, 271, 13854-13860.
100. Yu, X-Q. and Kanost, M.R. (1999) Developmental expression of Manduca sexta hemolin. Archives of Insect Biochemistry and Physiology, 42, 198-212.
101. Yu, X-Q. and Kanost, M.R. (2000) Immulectin-2, a lipopolysaccharide- specific lectin from an insect, Manduca sexta, is induced in response to Gram-negative bacteria. Journal of Biological Chemistry, 275, 37373-37381.
102. Yu, X-Q. and Kanost, M.R. (2002) Binding of hemolin to microbial lipopolysaccharide and lipoteichoic acid: an immunoglobulin superfamily member from insects as a pattern recognition receptor. European Journal of Biochemistry, 269, 1827-1834.
103. Yu, X.-Q. and Kanost, M.R. (2003) Manduca sexta lipopolysaccharide- specific immulectin-2 protects larvae from bacterial infection. Developmental and Comparative Immunology, 27, 189-196.
104. Yu, X-Q., Gan, H. and Kanost, M.R. (1999a) Immulectin, an inducible C-type lectin from an insect, Manduca sexta, stimulates activation of plasma prophenol oxidase. Insect Biochemistry and Molecular Biology, 29, 585-597.
105. Yu, X-Q., Jiang, H., Wang, Y. and Kanost, M.R. (2003) Nonproteolytic serine proteinase homologs are involved in prophenoloxidase activation in the tobacco hornworm, Manduca sexta. Insect Biochemistry and Molecular Biology, 33, 197-208.
106. Yu, X-Q., Ling, E., Tracy, M.E. and Zhu, Y. (2006) Immulectin- 4 from the tobacco hornworm Manduca sexta binds to lipopolysaccharide and lipoteichoic acid. Insect Molecular Biology, 15, 119-128.
107. Yu, X-Q., Prakash, O. and Kanost, M.R. (1999b) Structure of a paralytic peptide from an insect, Manduca sexta. Journal of Peptide Research, 54, 256-261.
108. Yu, X-Q., Prakash, O. and Kanost, M.R. (2001) Insect ENF family peptides with diverse biological activities display similar core structures in solution. Medicinal Chemical Research, 10, 493-501.
109. Yu, X-Q., Tracy, M.E., Ling, E., Scholz, F.R. and Trenczek, T. (2005) A novel C-type immulectin-3 from Manduca sexta is translocated from hemolymph into the cytoplasm of hemocytes. Insect Biochemistry and Molecular Biology, 35, 285-295.
110. Yu, X-Q., Zhu, Y., Ma, C., Fabrick, J.A. and Kanost, M.R. (2002) Pattern recognition proteins in Manduca sexta plasma. Insect Biochemistry and Molecular Biology, 32, 1287-1293.
111. Zhao, L. and Kanost, M.R. (1996) In search of a function for hemolin, a hemolymph protein from the immunoglobulin superfamily. Journal of Insect Physiology, 42, 73-79.
112. Zhao, P., Li, J., Wang, Y. and Jiang, H. (2007) Broad-spectrum antimicrobial activity of the reactive compounds generated in vitro by Manduca sexta phenoloxidase. Insect Biochemistry and Molecular Biology, 37, 952-959.
113. Zhu, Y., Johnson, T. and Kanost, M.R. (2003a) Identification of differentially expressed genes in the immune response of the tobacco hornworm, Manduca sexta. Insect Biochemistry and Molecular Biology, 33, 541-559.
114. Zhu, Y., Wang, Y., Gorman, M.J., Jiang, H. and Kanost, M.R. (2003b) Manduca sexta serpin-3 regulates prophenoloxidase activation in response to infection by inhibiting prophenoloxidase-activating proteinases. Journal of Biological Chemistry, 278, 46556-46564.
115. Zhuang, S., Kelo, L., Nardi, J.B. and Kanost, M.R. (2007a) Neuroglian on hemocyte surfaces is involved in homophilic and heterophilic interactions of the innate immune system of Manduca sexta. Developmental and Comparative Immunology, 31, 1159-1167.
116. Zhuang, S., Kelo, L., Nardi, J.B. and Kanost, M.R. (2007b) An integrin-tetraspanin interaction required for cellular innate immune responses of an insect, Manduca sexta. Journal of Biological Chemistry, 282, 22563-22572.
117. Zhuang, S., Kelo, L., Nardi, J.B. and Kanost, M.R. (2008) Multiple β?subunits of integrin are involved in cell-mediated responses of the Manduca immune system. Developmental and Comparative Immunology, 32, (in press).
118. Zou, Z. and Jiang, H. (2005a) Gene structure and expression profile of Manduca sexta prophenoloxidase-activating proteinase- 3 (PAP-3), an immune protein containing two clip domains. Insect Molecular Biology, 14, 433-442.
119. Zou, Z. and Jiang, H. (2005b) Manduca sexta serpin-6 regulates immune serine proteinases PAP-3 and HP8: cDNA cloning, protein expression, inhibition kinetics, and function elucidation. Journal of Biological Chemistry, 280, 14341-14348.
120. Zou, Z., Wang, Y. and Jiang, H. (2005) Manduca sexta prophenoloxidase activating proteinase-1 (PAP-1) gene: organization, expression, and regulation by immune and hormonal signals. Insect Biochemistry and Molecular Biology, 35, 627-636.