Insect Hemocytes and Their Role in Immunity

Insect Immunology

Volumn , Issue , 2008, Pages 25-47

  Strand, Michael R ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

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EID: 84882551163     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1016/B978-012373976-6.50004-5     Document Type: Chapter

References (143)

1. H. Agaisse and N. Perrimon (2004) The roles of JAK/STAT signaling in Drosophila immune responses. Immunol. Rev. 198 72-82.
2. H. Agaisse, L.S. Burrack, J.A. Philips, E.J. Rubin, N. Perrimon and D.E. Higgins (2005) Genome-wide RNAi screen for host factors required for intracellular bacterial infection. Science 309 1248-1251.
3. H. Akai and S. Sato (1971) An ultrastructural study of the haemopoietic organs of the silkworm, Bombyx mori. J. Insect Physiol. 17 1665-1676.
4. T.B. Alfonso and B.W. Jones (2002) gcm2 promotes glial cell differentiation and is required with glial cells missing for macrophage development in Drosophila. Dev. Biol. 248 369-383.
5. T.G. Andreadis and D.W. Hall (1976) Neoplectana carpocapsae: Encapsulation in Aedes aegypti and changes in host hemocytes and hemolymph proteins. Exp. Parasitol. 39 252-261.
6. J.W. Arnold and C.F. Hinks (1976) Haemopoiesis in Lepidoptera. I. The multiplication of circulating haemocytes. Can. J. Zool. 54 1003-1012.
7. H. Asha, I. Nagy, G. Kovacs, D. Stetson, I. Ando and C.R. Dearolf (2003) Analysis of Ras-induced overproliferation in Drosophila hemocytes. Genetics 163 203-215.
8. J. Bangham, F. Jiggins and B. Lemaitre (2006) Insect immunity, the post-genomic era. Immunity 25 1-5.
9. L.C. Bartholomay, W.L. Cho, T.A. Rocheleau, J.P. Boyle, E.T. Beck, J.F. Fuchs, P. Liss, M. Rusch, K.M. Butler, R.C.C. Wu, S.P. Lin, F.Y. Kuo, I.Y. Tsao, C.Y. Huang, T.T. Liu, K.J. Hsiao, S.F. Tsai, U.C. Yang, A.J. Nappi, N.T. Perna, C.C. Chen and B.M. Christensen (2004) Description of the transcriptomes of immune response-activated hemocytes from the mosquito vectors Aedes aegypti and Armigeres subalbatus. Infect. Immun. 72 4114-4126.
10. M. Beck and M.R. Strand (2003) RNA interference silences Microplitis demolitor bracovirus genes and implicates glcl.8 in blocking adhesion of infected host cells. Virology 314 521-535.
11. S. Beetz, M. Brinkmann and T. Trenczek (2004) Differences between larval and pupal hemocytes of the tobacco hornworm, Manduca sexta, determined by monoclonal antibodies and density centrifugation. J. Insect Physiol. 50 805-819.
12. G. Bidla, M. Lindren, U. Theopold and M.S. Dushay (2005) Hemolymph coagulation and phenoloxidase in Drosophila larvae. Dev. Comp. Immunol. 29 669-679.
13. S. Blandin and E.A. Levashina (2004) Thioester-containing proteins and insect immunity. Mol. Immunol. 40 903-908.
14. S. Blandin, S. Shiao, L. Moita, C. Janse, A. Waters, F. Kafatos and E. Levashina (2004) Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116 661-670.
15. H.G. Boman (2003) Antibacterial peptides: Basic facts and emerging concepts. J. Intern. Med. 254 197-215.
16. M. Boutros, H. Agaisse and N. Perrimon (2002) Sequential activation of signaling pathways during innate immune responses in Drosophila. Dev. Cell 3 711-722.
17. M. Brehelin and D. Zachary (1986) Insect haemocytes, a new classification to rule out controversy. M. Brehelin (Eds) Immunity in Invertebrates Berlin: Springer Verlag 36-48.
18. J.C. Castillo, A.E. Robertson and M.R. Strand (2006) Characterization of hemocytes from the mosquitoes Anopheles gambiae and Aedes aegypti. Insect Biochem. Mol. Biol. 36 891-903.
19. G.C. Chen, B. Turano, P.J. Ruest, M. Hagel, J. Settleman and S.M. Thomas (2005) Regulation of rho and rac signaling to the actin cytoskeleton by paxillin during Drosophila development. Mol. Cell Biol. 25 979-987.
20. S. Cherry and N. Silverman (2006) Host-pathogen interactions in Drosophila, new tricks from an old friend. Nat. Immunol. 7 911-917.
21. M.Y. Cho, H.S. Lee, K.M. Lee, K. Homma, S. Natori and B.L. Lee (1999) Molecular cloning and functional properties of two early-stage encapsulation-relating proteins from the coleopteran insect, Tenebrio molitor larvae. Eur. J. Biochem. 262 737-744.
22. K.-M. Choe, T. Werner, S. Stoven, D. Hultmark and K.V. Anderson (2002) Requirement for a peptidoglycan recognition protein (PGRP) in Relish activation and antibacterial immune responses in Drosophila. Science 296 359-362.
23. K.D. Clark, L.L. Pech and M.R. Strand (1997) Isolation and identification of a plasmatocyte-spreading peptide from the hemolymph of the lepidopteran insect Pseudoplusia includens. J. Biol. Chem. 272 23440-23447.
24. K.D. Clark, A. Witherell and M.R. Strand (1998) Plasmatocyte spreading peptide is encoded by an mRNA differentially expressed in tissues of the moth Pseudoplusia inciudens. Biochem. Biophys. Res. Comm. 250 479-485.
25. K.D. Clark, S. Garczynski, A. Arora, J. Crim and M.R. Strand (2004) Specific residues in plasmatocyte spreading peptide are required from receptor binding and functional antagonism of insect immune cells. J. Biol. Chem. 279 33246-33252.
26. R. Collins, R. Sakai, K. Vernick, S. Paskewitz, D. Seeley, W. Collins, C. Campbell and R. Gwadz (1986) Genetic selection of a plasmodium-refractory strain of the malaria vector Anopheles gambiae. Science 234 607-610.
27. L. Cornelis and K. Soderhall (2004) The prophenoloxidse-activating system in invertebrates. Immunol. Rev. 198 116-126.
28. M. Crozatier, J.M. Ubeda, A. Vincent and M. Meister (2004) Cellular immune response to parasitization in Drosophila requires the EBF orthologue Collier. PLoS Biol 2 e196.
29. P. Dean, U. Potter, E.H. Richards, J.P. Edwards, A.K. Charnley and S.E. Reynolds (2004) Hyperphagocytic haemocytes in Manduca sexta. J. Insect Physiol. 50(11), 1027-1036.
30. C.R. Dearolf (1998) Fruit fly ‘leukemia’. Intl. J. Biochem. Biophys. Mol. Biol. 1377 M13-M23.
31. E. De Gregorio, S. Han, W. Lee, M. Baek, T. Osaki, S. Kawabata, B. Lee, S. Iwanaga, B. Lemaitre and P.T. Brey (2002) An immune-responsive serpin regulates the melanization cascade in Drosophila. Dev. Cell 3 581-592.
32. G. Dimopoulos, T.L. Casavant, S. Chang, T Scheetz, C. Roberts, M. Donohue, J. Schultz, V. Benes, P. Bork, W. Ansorge, M. Bento Sores and F.C. Kafatos (2000) Anopheles gambiae pilot gene discovery project: Identification of mosquito innate immunity genes from expressed sequence tags generated from immune-competent cell lines. Proc. Natl. Acad. Sci. USA 97 6619-6624.
33. Y.M. Dong, H.E. Taylor and G. Dimopoulos (2006) AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae immune system. PLoS Biol. 4 1137-1146.
34. C. Dostert, E. Jouanguy, P. Irving, L. Troxler, D. Galiana-Arnoux, C. Hetru, J.A. Hoffmann and J.-L. Imler (2005) The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila. Nat. Immunol. 6 946-953.
35. L. Drif and M. Brehelin (1983) The circulating hemocytes of Culex pipiens and Aedes aegypti Cytology, histochemistry, hemograms, and functions. Dev. Comp. Immunol. 7 687-690.
36. I. Eleftherianos, F. Gokcen, G. Felfoldi, P.J. Millichap, T.E. Trenczek, R.H. French-Constant and S.E. Reynolds (2007) The immunoglobulin family protein Hemolin mediates cellular immune responses to bacteria in the insect Manduca sexta. Cell. Microbiol. 9 1137-1147.
37. M. Elrod-Erickson, S. Mishra and D. Schneider (2000) Interactions between the cellular and humoral immune responses in Drosophila. Curr. Biol. 10 781-784.
38. C.J. Evans, V. Hartenstein and U. Banerjee (2003) Thicker than blood: Conserved mechanisms in Drosophila and vertebrate hematopoiesis. Dev. Cell 5 673-690.
39. D. Eeir (1979) Multiplication of hemocytes. A.P. Gupta (Eds) Insect Hemocytes Cambridge, UK: Cambridge University Press 67-82.
40. S.R. Filipe, A. Tomasz and P. Ligoxygakis (2005) Requirements of peptidoglycan structure that allow detection by the Drosophila Toll pathway. EMBO Rep. 6 327-333.
41. D.A. Foley (1978) Innate cellular defense by mosquito hemocytes. L.A. Bulla, Jr.,T.C. Cheng (Eds) Comparative Pathobiology Vol. 4 New York: Academic Press 114-143.
42. N.C. Franc, P. Heitzler, R.A.B. Ezekowitz and K. White (1999) Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila. Science 284 1991-1994.
43. D. Galiana-Arnoux, C. Dostert, A. Schneemann, J.A. Hoffmann and J.L. Imler (2006) Essential function in vivo for Dicer-2 in host defense against RNA viruses in Drosophila. Nat. Immunol. 7 590-597.
44. E.M.M. Gardiner and M.R. Strand (1999) Monoclonal antibodies bind distinct classes of hemocytes in the moth Pseudoplusia includens. J. Insect Physiol. 45 113-126.
45. E.M.M. Gardiner and M.R. Strand (2000) Hematopoiesis in larval Pseudoplusia includens and Spodoptera frugiperda. Arch. Insect Bich. Physiol. 43 147-164.
46. L.S. Garver, J. Wu and L.P. Wu (2006) The peptidoglycan recognition protein PGRP-SCla is essential for Toll signaling and phagocytosis of Staphylococcus aureus in Drosophila. Proc. Natl. Acad. Sci USA 103 660-665.
47. J.P. Gillespie, M.R. Kanost and T. Trenczek (1997) Biological mediators of insect immunity. Annu. Rev. Entomol. 42 611-643.
48. A.V. Grimstone, S. Rotheram and G.B. Salt (1967) An electron-microscope study of capsule formation by insect blood cells. J. Cell Sci. 2 281-292.
49. A.P. Gupta (1985) Cellular elements in hemolymph. G.A. Kerkut, L.I. Gilbert (Eds) Comprehensive Insect Physiology, Biochemistry and Pharmacology vol. 3 Oxford: Pergamon Press 401-451.
50. J.F. Hillyer and B.M. Christensen (2002) Characterization of hemocytes from the yellow fever mosquito, Aedes aegypti. Histochem. Cell Biol. 117 431-440.
51. C.F. Hinks and J.W. Arnold (1977) Haemopoiesis in Leptidoptera II, the role of haemopoietic organs. Can. J. Zool. 55 1740-1755.
52. J.A. Hoffmann and J.-M. Reichhart (2002) Drosophila innate immunity, an evolutionary perspective. Nat. Immunol. 3 121-126.
53. A. Holz, B. Bossinger, T. Strasser, W. Janning and S. Klapper (2003) The two origins of hemocytes in Drosophila. Development 130 4955-4962.
54. J.-L. Imler and P. Bulet (2005) Antimicrobial peptides in Drosophila, structures, activities and gene regulation. D. Kabelitz, J.M. Schroder (Eds) Mechanisms of Epithelial Defense Vol. 86 Basil: Karger 1-21.
55. J.-L. Imler and L. Zheng (2005) Biology of Tool receptors, lessons from insects and mammals. J. Leuk. Biol. 74 18-26.
56. P. Irving, J. Ubeda, D. Doucet, L. Trouxler, M. Lagueux, D. Zachary, J. Hoffmann, C. Hetru and M. Meister (2005) New insights into Drosophila larval haemocyte functions through genome-wide analysis. Cell. Microbiol. 7 335-350.
57. H. Jiang, Y. Wang, C. Ma and M.R. Kanost (1997) Subunit composition of pro-phenoloxidase from Manduca sexta, molecular cloning of subunit proPO-P1. Insect Biochem. Mol. Biol. 27 835-850.
58. J.C. Jones (1962) Current concepts concerning insect hemocytes. Am. Zool. 2 209-246.
59. J.C. Jones (1970) Hemocytopoiesis in insects. A.S. Gordon (Eds) Regulation of Hematopoiesis New York: Appleton Press 7-65.
60. S.H. Jung, C.J. Evans, C. Uemura and U. Banerjee (2005) The Drosophila lymph gland as a developmental model of hematopoiesis. Development 132 2521-2533.
61. G.P. Kaaya and N.A. Ratcliffe (1982) Comparative study of hemocytes and associated cells of some medically important dipterans. J. Morph. 173 351-365.
62. T. Kaneko, T. Yano, K. Aggarwall, J. Lim, K. Ueda, Y. Oshima, C. Peach, D. Erturk-Hasdemir, W.E. Goldman, B. Oh, S. Kurata and N. Silverman (2006) PGRP-LC and PGRP-LE have essential yet distinct functions in the Drosophila immune response to monomeric DAP-type peptidoglycan. Nat. Immunol. 7 715-723.
63. K.M. Keene, B.D. Foy, I. Sanchez-Vargas, B.J. Beaty, C.D. Blair and K.E. Olson (2004) RNA interference acts as a natural antiviral response to O'nong-nyong virus (Alphavirus: Togaviridae) infection of Anopheles gambiae. Proc. Natl. Acad. Sci. USA 101 17240-17245.
64. C. Kocks, J.-H. Cho, N. Nehme, J. Ulvila, A.M. Pearson, M. Meister, C. Strom, S.L. Conto, C. Hetru, L.M. Stuart, T. Stehle, J.A. Hoffman, J.-M. Reichhart, D. Ferrandon, M. Ramet and R.A.B. Ezekowitz (2005) Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila. Cell 123 335-346.
65. J. Krzemien, L. Dubois, R. Makki, M. Meister, A. Vincent and M. Crozatier (2007) Control of blood cell homeostasis in Drosophila larvae by the posterior signalling centre. Nature 446 325-328.
66. A.M. Lackie (1988) Haemocyte behaviour. Adv. Insect Physiol. 21 85-178.
67. R. Lanot, D. Zachary, F. Holder and M. Meister (2001) Postembryonic hematopoiesis in Drosophila. Dev. Biol. 230 243-257.
68. M.D. Lavine and M.R. Strand (2001) Surface characteristics of foreign targets that elicit an encapsulation response by the moth Pseudoplusia includens. J. Insect Physiol. 47 965-974.
69. M.D. Lavine and M.R. Strand (2002) Insect hemocytes and their role in cellular immune responses. Insect Biochem. Mol. Biol. 32 1237-1242.
70. M.D. Lavine and M.R. Strand (2003) Hemocytes from Pseudoplusia includens express multiple alpha and beta integrin subunits. Insect Mol. Biol. 12 441-452.
71. M.D. Lavine, G. Chen and M.R. Strand (2005) Immune challenge differentially affects transcript abundance of three antimicrobial peptides in hemocytes from the moth Pseudoplusia includens. Insect Biochem. Mol. Biol. 35 1335-1346.
72. T. Lebestky, T. Chang, V. Hartenstein and U. Banerjee (2000) Specification of Drosophila hematopoietic lineage by conserved transcription factors. Science 288 146-149.
73. T. Lebestky, S. Jung and U. Banerjee (2003) Serrate-expressing signaling center controls Drosophila hematopoiesis. Genes Dev. 17 348-353.
74. E.A. Levashina, L.F. Moita, S. Blandin, G. Vriend, M. Lagueux and F.C. Kafatos (2001) Conserved role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell 104 709-718.
75. D.M. Levin, L.N. Breuer, S.F. Zhuang, S.A. Anderson, J.B. Nardi and M.R. Kanost (2005) A hemocyte-specific integrin required for hemocytic encapsulation in the tobacco hornworm, Manduca sexta. Insect Biochem. Mol. Biol. 35 369-380.
76. W. Li, H. Li, R. Lu, F. Li, M. Dus, P. Atkinson, E.W.A. Brydon, K.L. Johnson, A. García-Sastre, L.A. Ball, P. Palese and S. Ding (2004) Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc. Natl. Acad. Sci. USA 101 1350-1355.
77. E. Ling, K. Shirai, R. Kanekatsu and K. Kiguchi (2005) Hemocyte differentiation in the hematopoietic organs of the silkworm, Bombyx mori: Prohemocytes have the function of phagocytosis. Cell Tissue Res. 320 535-543.
78. E.J. Ling and X.Q. Yu (2006) Cellular encapsulation and melanization are enhanced by immulectins, pattern recognition receptors from the tobacco hornworm Manduca sexta. Dev. Comp. Immunol. 30 289-299.
79. C.T. Liu, R.F. Hou and C.C. Chen (1998) Formation of basement membrane-like structure terminates the cellular encapsulation of microfilariae in the haemocoel of Anopheles quadrimaculatus. Parasitology 116 511-518.
80. C Lowenberger (2001) Innate immune response of Aedes aegypti. Insect Biochem. Mol. Biol. 31 219-229.
81. L. Mandal, J.A. Martinez-Agosto, C.J. Evans, V. Hartenstein and U. Banerjee (2007) A Hedgehog- and Antennapedia-dependent niche maintains Drosophila hematopoietic precursors. Nature 446 320-324.
82. K. Michel, A. Budd, S. Pinto, T. Gibson and F. Kafatos (2005) Anopheles gambiae SRPN2 facilitates mid gut invasion by the malaria parasite Plasmodium berghei. EMBO Rep. 6 891-897.
83. K. Michel, C. Suwanchaichinda, I. Morlais, L. Lambrechts, A. Cohuet, P.H. Awono-Ambene, F. Simard, D. Fontenille, M.R. Kanost and F.C. Kafatos (2006) Increased melanizing activity in Anopheles gambiae does not affect development of Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 103 16858-16863.
84. L.F. Moita, R. Wang-Stattler, K. Michel, T. Zimmermann, S. Blandin, E.A. Levashina and F.C. Kafatos (2005) In vivo identification of novel regulators and conserved pathways of phagocytosis in A. gambiae. Immunity 23 65-73.
85. A.I. Munier, D. Doucet, E. Perrodou, D. Zchary, M. Meister, J.A. Hoffmann, C.A. Janeway Jr. and M. Lagueux (2002) PVF2. A PDGF/VEGF-like growth factor, induces hemocyte proliferation in Drosophila larvae. EMBO Rep. 3 195-1200.
86. Y. Nakahara, Y. Kanamori, M. Kiuchi and M. Kamimura (2003) In vitro studies of hematopoiesis in the silkworm, cell proliferation in and hemocyte discharge from the hematopoietic organ. J. Insect Physiol. 49 907-916.
87. Y. Nakahara, H. Matsumoto, Y. Kanamori, H. Kataoka, A. Mizoguchi, M. Kiuchi and M. Kamimura (2006) Insulin signaling is involved in hematopoietic regulation in an insect hematopoietic organ. J. Insect Physiol. 52 105-111.
88. A.J. Nappi and B.M. Christensen (2005) Melanogenisis and associated cytotoxic reactions, applications to insect innate immunity. Insect Biochem. Mol. Biol. 35 443-459.
89. J.B. Nardi (2004) Embryonic origins of the two main classes of hemocytes—granular cells and plasmatocytes in Manduca sexta. Dev. Genes Evol. 214 19-28.
90. J.B. Nardi, E. Ujhelyi, B. Pilas, K. Garsha and M.R. Kanost (2003) Hematopoietic organs of Manduca sexta and hemocyte lineages. Dev. Genes Evol. 213 477-491.
91. J.B. Nardi, B. Pilas, C.M. Bee, S. Zhuang, K. Garsha and M.R. Kanost (2006) Neuroglian-positive plasmatocytes of Manduca sexta and the initiation of hemocyte attachment to foreign surfaces. Dev. Comp. Immunol. 30 447-462.
92. R.E. Nelson, L.I. Fessler, Y. Takagi, B. Blumberg, D.R. Keene, P.F. Olson, C.G. Parker and J.H. Fessler (1994) Peroxidasin: A novel enzyme-matrix protein of Drosophila development. EMBO J. 13 3438-3447.
93. M.A. Osta, G.K. Christophides and F.C. Kafatos (2004) Effects of mosquito genes on Plasmodium development. Science 303 2030-2032.
94. J.T. Parsons (2003) Focal adhesion kinase, the first ten years. J. Cell Sci. 116 1409-1416.
95. A.M. Pearson, K. Baksa, M. Rämet, M. Protas, M. McKee, D. Brown and R.A.B. Ezekowitz (2003) Identification of cytoskeletal regulatory proteins required for efficient phagocytosis in Drosophila. Microbes Infect 5 815-824.
96. L.L. Pech and M.R. Straud (1996) Granular cells are required for encapsulation of foreign targets by insect haemocytes. J. Cell Sci. 109 2053-2060.
97. L.L. Pech and M.R. Strand (2000) Plasmatocytes from the moth Pseudoplusia includens induce apoptosis of granular cells. J. Insect Physiol. 46 1565-1573.
98. J.A. Philips, E.J. Rubin and N. Perrimon (2005) Drosophila RNAi screen reveals C35 family member required for mycobacterial infection. Science 309 1248-1251.
99. H.J. Popham, K.S. Shelby, S.L. Brandt and T.A. Coudron (2004) Potent virucidal activity in larval Heliothis virescens plasma against Helicoverpa zea single capsid nucleopolyhedrovirus. J. Gen. Virol. 85 2255-2261.
100. F. Radtke, A. Wilson and H.R. MacDonald (2005) Notch signaling in hematopoiesis and lymphopoiesis: Lessons from Drosophila. Bioessays 27 1117-1128.
101. M. Ramet, A. Pearson, P. Manfruelli, X. Li, H. Koziel, V. Gobel, E. Chung, M. Krieger and R.A.B. Ezekowitz (2001) Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria. Immunity 15 1027-1038.
102. M. Ramet, P. Manfruelli, A. Pearson, B. Mathey-Prevot and R.A.B. Ezekowitz (2002) Functional genomic analysis and identification of a Drosophila receptor for E. coli. Nature 416 644-648.
103. N.A. Ratcliffe and S.J. Gagen (1976) Cellular defense reactions of insect hemocytes in vivo, nodule formation and development in Galleria mellonella and Pieris brassicae larvae. J. Invert. Pathol. 28 373-382.
104. N.A. Ratcliffe and S.J. Gagen (1977) Studies on the in vivo cellular reactions of insects, an ultrastructural analysis of nodule formation in Galleria mellonella. Tissue Cell 9 73-85.
105. N.A. Ratcliffe, A.F. Rowley, S.W. Fitzgerald and C.P. Rhodes (1985) Invertebrate immunity—basic concepts and recent advances. Intl. Rev. Cytol. 97 183-350.
106. E.P. Reeves, H. Lu, H.L. Jacobs, C.G. Messina, S. Bolsover, G. Gabella, E.O. Potma, A. Warley, J. Roes and A.W. Segal (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416 291-297.
107. C. Ribeiro and M. Brehelin (2006) Insect haemocytes: What type of cell is what? J. Insect Physiol. 52 417-429.
108. M.M. Riehle, K. Markianos, O. Niare, J.N. Xu, J. Li, A.M. Toure, B. Podiougou, F. Oduol, S. Diawara, M. Diallo, B. Coulibaly, A. Ouatara, L. Kruglyak, S.F. Traore and K.D. Vernick (2006) Natural malaria infection in Anopheles gambiae is regulated by a single genomic control region. Science 312 577-579.
109. M.-C. Saleh, R.P. Rij R.P. van, A. Hekele, A. Gillis, E. Foley, P.H. O'Farrell and R. Andino (2006) The endocytic pathway mediates cell entry of dsRNA to induce RNAi silencing. Nat. Cell Biol. 8 793-802.
110. G.B. Salt (1970) The Cellular Defense Reactions in Insects Cambridge: Cambridge University Press
111. C. Scherfer, M.R. Qazi, K. Takahashi, R. Ueda, M.S. Dushay, U. Theopold and B. Lemaitre (2006) The Toll immune-regulated Drosophila protein Fondue is involved in hemolymph clotting and puparium formation. Dev. Biol. 295 156-163.
112. O. Schmidt, U. Theopold and M.R. Strand (2001) Innate immunity and evasion by insect parasitoids. Bioessays 23 344-351.
113. M.E. Selsted and A.J. Ouellette (1995) Defensins in granules of phagocytic and non-phagocytic cells. Trends Cell Biol. 5 114-119.
114. R.P. Sorrentino, Y. Carton and S. Govind (2002) Cellular immune response to parasite infection in the Drosophila lymph gland is developmentally regulated. Dev. Biol. 243 65-80.
115. R.P. Sorrentino, J.P. Melk and S. Govind (2004) Genetic analysis of contributions of dorsal group and JAK-Stat92E pathway genes to larval hemocyte concentration and the egg encapsulation response in Drosophila. Genetics 166 1343-1356.
116. B. Stramer, W. Wood, M.J. Galko, M.J. Redd, A. Jacinto, S.M. Parkhurst and P. Martin (2005) Live imaging of wound inflammation in Drosophila embryos reveals key roles for small GTPases during in vivo cell migration. J. Cell. Biol. 168 567-573.
117. M.R. Strand and K.D. Clark (1999) Plasmatocyte spreading peptide induces spreading of plasmatocytes but represses spreading of granulocytes. Arch. Insect. Bich. Physiol. 42 213-223.
118. M.R. Strand, M.H. Beck and M.D. Lavine (2006) Microplitis demolitor bracovirus inhibits phagocytosis by hemocytes from Pseudoplusia includens. Arch. Insect Bich. Physiol. 61 134-145.
119. M.R. Strand and L.L. Pech (1995) Immunological basis for compatibility in parasitoid-host relationships. Annu. Rev. Entomol. 40 31-56.
120. S.L. Stroschein-Stevenson, E. Foley, P.H. O'Farrell and A.D. Johnson (2006) Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol 4 87-99.
121. L.M. Stuart and R.A. Ezekowitz (2005) Phagocytosis: Elegant complexity. Immunity 22 539-550.
122. L.M. Stuart, J. Boulais, G.M. Charriere, E.J. Hennessy, S. Brunet, I. Jutras, G. Goyette, C. Rondeau, S. Letarte, H. Huang, P. Ye, F. Morales, C. Kocks, J.S. Bader, M. Desjardins and R.A. Ezekowitz (2007) A systems biology analysis of the Drosophila phagosome. Nature 445 95-101.
123. K. Taniai, J.H. Lee and I.H. Lee (2006) Bombyx mori cell line as a model of immune system organs. Insect Mol. Biol. 15 269-279.
124. S. Tauszig, E. Jouanguy, J.A. Hoffmann and J.-L. Imler (2000) Toll-related receptors and the control of antimicrobial peptide expression in Drosophila. Proc. Natl. Acad. Sci. USA 99 10520-10525.
125. U. Tepass, L.I. Fessler, A. Aziz and V. Hartenstein (1994) Embryonic origin of hemocytes and their relationship to cell death in Drosophila. Development 120 1829-1837.
126. O. Terenius, R. Bettencourt, S.Y. Lee, W. Li, K. Soderhall and I. Faye (2007) RNA interference of Hemolin causes depletion of phenoloxidase activity in Hyalophora cecropia. Dev. Comp. Immunol. 31 571-575.
127. U. Theopold, O. Schmidt, K. Soderhall and M.S. Dushay (2004) Coagulation in arthropods, defence, wound closure and healing. Trends Immunol 25 289-294.
128. D. Traver and L.I. Zon (2002) Walking the walk: Migration and other common themes in blood and vascular development. Cell 108 731-734.
129. D. Trudeau, J.O. Washburn and L.E. Volkman (2001) Central role of hemocytes in Autographa californica M nucleopolyhedrovirus pathogenesis in Heliothis virescens and Helicoverpa zea. J. Virol. 75 996-1003.
130. C.C. Tydell, J. Yuan, P. Tran and M.E. Selsted (2006) Bovine peptidoglycan recognition protein-S, antimicrobial activity, localization, secretion, and binding properties. J. Immunol. 176 1154-1162.
131. X. Wang, R. Aliyari, W. Li, H. Li, K. Kim, R. Carthew, P. Atkinson and S. Ding (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science 312 45-454.
132. B. Wertheim, A.R. Kraaijeveld, E. Schuster, E. Blanc, M. Hopkins, S.D. Pletcher, M.R. Strand, H.C.J. Godfray and L. Partridge (2005) Genome wide expression in response to parasitoid attack in Drosophila. Genome Biol. 6(R94), 1-20.
133. M.M. Whitten, S.H. Shiao and E.A. Levashina (2006) Mosquito midguts and malaria: Cell biology, compartmentalization and immunology. Parasite Immunol. 28 121-130.
134. C. Wiegand, D. Levin, J.P. Gillespie, E. Willott, M.R. Kanost and T. Trenczek (2000) Monoclonal antibody M13 identifies a plasmatocyte membrane protein and inhibits encapsulation and spreading reactions of Manduca sexta hemocytes. Arch. Insect Bich. Physiol. 45 95-108.
135. M.J. Williams, M.L. Wiklund, S. Wikman and D. Hultmark (2006) Racl signalling in the Drosophila larval cellular immune response. J. Cell Sci. 119 2015-2024.
136. E. Willott, T. Trenczek, L.W. Thrower and M.R. Kanost (1994) Immunochemical identification of insect hemocyte populations: Monoclonal antibodies distinguish four major hemocyte types in Manduca sexta. Eur. J. Cell Biol. 65 417-423.
137. W. Wood, C. Faria and A. Jacinto (2006) Distinct mechanisms regulate hemocyte chemotaxis during development and wound healing in Drosophila melanogaster. J. Cell Biol. 173 405-416.
138. Y. Yamano, M. Matsumoto, K. Inoue, T. Kawabata and I. Morishima (1994) Cloning of cDNAs for cecropins A and B, and expression of the genes in the silkworm, Bombyx mori. Biosci. Biotech. Biochem. 58 1476-1478.
139. M. Yamashita and K. Iwabuchi (2001) Bombyx mori prohemocyte division and differentiation in individual microcultures. J. Insect Physiol. 47 325-331.
140. X.Q. Yu and M.R. Kanost (2004) Immulectin-2, a pattern recognition receptor that stimulates hemocyte encapsulation and melanization in the tobacco hornworm, Manduca sexta. Dev. Comp. Immunol. 28 891-900.
141. R.A. Zambon, V.N. Vakharia and L.P. Wu (2006) RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell. Microbiol. 8 880-889.
142. C. Zettervall, I. Anderl, M.J. Williams, R. Palmer, E. Kurucz, I. Ando and D. Hultmark (2004) A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl. Acad. Sci. USA 101 14192-14197.
143. S. Zhuang, L. Kelo, J.B. Nardi and M.R. Kanost (2007) An integrin-tetraspanin interaction required for cellular innate immune responses of an inset. Manduca sexta. J. Biol. Chem. (in press).