Injury and immune response: Applying the danger theory to mosquitoes

Frontiers in Plant Science

Volumn 5, Issue SEP, 2014, Pages

  Moreno García, Miguel ^a,d   Recio Tótoro, Benito ^a,b   Claudio Piedras, Fabiola ^a,c   Lanz Mendoza, Humberto ^a  

^a INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^b INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

^c UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^d Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Danger damage; Immune response; Insects; Mosquitoes; Wound

Indexed keywords

EID: 84908181408     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00451     Document Type: Article

References (150)

1. Aderem, A., and Smith, K. D. (2004). A systems approach to dissecting immunity and inflammation. Semin. Immunol. 16, 55-67. doi: 10.1016/j.smim.2003.10.002
2. Al-Olayan, E. M., Williams, G. T., and Hurd, H. (2002). Apoptosis in the malaria protozoan, Plasmodium berghei: a possible mechanism for limiting intensity of infection in the mosquito. Int. J. Parasitol. 32, 1133-1143. doi: 10.1016/S0020-7519(02)00087-5
3. Altincicek, B., Linder, M., Linder, D., Preissner, K., and Vilcinskas, A. (2007). Microbial metalloproteinases mediate sensing of invading pathogens and activate innate immune responses in the Lepidopteran model hostGalleria mellonella. Infect. Immun. 75, 175-183. doi: 10.1128/IAI.01385-06
4. Altincicek, B., and Vilcinskas, A. (2006). Metamorphosis and collagen-IV-fragments stimulate innate immune response in the greater wax moth, Galleria mellonella. Dev. Comp. Immunol. 30, 1108-1118. doi: 10.1016/j.dci.2006.03.002
5. Angrisano, F., Tan, Y-H., Sturm, A., McFadden, G. I., and Baum, J. (2012). Malaria parasite colonization of the mosquito midgut: placing the plasmodium ookinete centre stage. Int. J. Parasitol. 42, 519-527. doi: 10.1016/j.ijpara.2012.02.004
6. Arrighi, R. B. G., Lycett, G., Mahairaki, V., Siden-Kiamos, I., and Louis, C. (2005). Laminin and the malaria parasite's journey through the mosquito midgut. J. Exp. Biol. 208, 2497-2502. doi: 10.1242/jeb.01664
7. Ayyaz, A., and Jasper, H. (2013). Intestinal inflammation and stem cell homeostasis in aging Drosophila melanogaster. Front. Cell. Infect. Microbiol. 3:98. doi: 10.3389/fcimb.2013.00098
8. Babcock, D. T., Brock, A. R., Fish, G. S., Wang, Y., Perrin, L., Krasnow, M. A.,et al. (2008). Circulating blood cells function as a surveillance system for damaged tissue in Drosophila larvae. Proc. Natl. Acad. Sci. U.S.A. 105, 10017-10022. doi: 10.1073/pnas.0709951105
9. Bagley, K. C., Abdelwahab, S. F., Tuskan, R. G., and Lewis, G. K. (2006). Cholera toxin indirectly activates human monocyte-derived dendritic cells in vitro through the production of soluble factors, including prostaglandin E2 and nitric oxide. Clin. Vaccine Immunol. 13, 106-115. doi: 10.1128/CVI.13.1.106-115.2006
10. Bannister, L. H., and Sherman, I. W. (2009). Plasmodium. eLS. doi: 10.1002/9780470015902.a0001970.pub2
11. Baton, L. A., and Ranford-Cartwright, L. C. (2004). Plasmodium falciparum ookinete invasion of the midgut epithelium of Anopheles stephensi is consistent with the time bomb model. Parasitology 129, 663-676. doi: 10.1017/S0031182004005979
12. Baton, L. A., and Ranford-Cartwright, L. C. (2005). How do malaria ookinetes cross the mosquito midgut wall?Trends Parasitol. 21, 22-28. doi: 10.1016/j.pt.2004.11.001
13. Baton, L. A., and Ranford-Cartwright, L. C. (2007). Morphological evidence for proliferative regeneration of theAnopheles stephensi midgut epithelium following Plasmodium falciparum ookinete invasion. J. Invertebr. Pathol.96, 244-254. doi: 10.1016/j.jip.2007.05.005
14. Billingsley, P. F., and Lehane, M. J. (1996). "Structure and ultrastructure of the insect midgut," in Biology of the Insect Midgut, eds M. J. Lehane and P. F. Billingsley (The Netherlands: Springer), 3-30.
15. Billingsley, P. F., and Rudin, W. (1992). The role of the mosquito peritrophic membrane in bloodmeal digestion and infectivity of Plasmodium species. J. Parasitol. 78, 430-440. doi: 10.2307/3283640
16. Blandin, S., Shiao, S-H., Moita, L. F., Janse, C. J., Waters, A. P., Kafatos, F. C.,et al. (2004). Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae. Cell 116, 661-670. doi: 10.1016/S0092-8674(04)00173-4
17. Burnstock, G., and Verkhratsky, A. (2009). Evolutionary origins of the purinergic signalling system. Acta Physiol.195, 415-447. doi: 10.1111/j.1748-1716.2009.01957.x
18. Burnstock, G., and Verkhratsky, A. (2012). Purinergic Signalling and the Nervous System. Berlin: Springer. doi: 10.1007/978-3-642-28863-0
19. Canning, E. U., and Sinden, R. E. (1973). The organization of the ookinete and observations on nuclear division in oocysts of Plasmodium berghei. Parasitology 67, 29-40. doi: 10.1017/S0031182000046266
20. Chamy, L. E., Leclerc, V., Caldelari, I., and Reichhart, J-M. (2008). Sensing of 'danger signals' and pathogen-associated molecular patterns defines binary signaling pathways 'upstream' of toll. Nat. Immunol. 9, 1165-1170. doi: 10.1038/ni.1643
21. Christophides, G. K., Vlachou, D., and Kafatos, F. C. (2004). Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol. Rev. 198, 127-148. doi: 10.1111/j.0105-2896.2004.0127.x
22. Churcher, T., Dawes, E., Sinden, R., Christophides, G., Koella, J., and Basanez, M-G. (2010). Population biology of malaria within the mosquito: density-dependent processes and potential implications for transmission-blocking interventions. Malar. J. 9, 311. doi: 10.1186/1475-2875-9-311
23. Clayton, A. M., Dong, Y., and Dimopoulos, G. (2014). The Anopheles innate immune system in the defense against malaria infection. J. Innate Immun. 6, 169-181. doi: 10.1159/000353602
24. Contreras-Garduño, J., Rodríguez, M. C., Rodríguez, M. H., Alvarado-Delgado, A., and Lanz-Mendoza, H. (2014). Cost of immune priming within generations: trade-off between infection and reproduction. Microbes Infect. 16, 261-267. doi: 10.1016/j.micinf.2013.11.010
25. Cook, S. P., and McCleskey, E. W. (2002). Cell damage excites nociceptors through release of cytosolic ATP. Pain95, 41-47. doi: 10.1016/S0304-3959(01)00372-4
26. Cooper, E. L. (2010). Evolution of immune systems from self/not self to danger to artificial immune systems (AIS). Phys. Life Rev. 7, 55-78. doi: 10.1016/j.plrev.2009.12.001
27. Cunliffe, J. (1997). Morphostasis: an evolving perspective. Med. Hypotheses 49, 449-459. doi: 10.1016/S0306-9877(97)90062-1
28. DeJong, R. J., Miller, L. M., Molina-Cruz, A., Gupta, L., Kumar, S., and Barillas-Mury, C. (2007). Reactive oxygen species detoxification by catalase is a major determinant of fecundity in the mosquito Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 104, 2121-2126. doi: 10.1073/pnas.0608407104
29. Dembic, Z. (2000). Immune system protects integrity of tissues. Mol. Immunol. 37, 563-569. doi: 10.1016/S0161-5890(00)00084-5
30. Dimopoulos, G., Christophides, G. K., Meister, S., Schultz, J., White, K. P., Barillas-Mury, C.,et al. (2002). Genome expression analysis of Anopheles gambiae: responses to injury, bacterial challenge, and malaria infection. Proc. Natl. Acad. Sci. U.S.A. 99, 8814-8819. doi: 10.1073/pnas.092274999
31. Dimopoulos, G., Seeley, D., Wolf, A., and Kafatos, F. C. (1998). Malaria infection of the mosquito Anopheles gambiae activates immune-responsive genes during critical transition stages of the parasite life cycle. EMBO J. 17, 6115-6123. doi: 10.1093/emboj/17.21.6115
32. Dolezelova, E., Nothacker, H-P., Civelli, O., Bryant, P. J., and Zurovec, M. (2007). A Drosophila adenosine receptor activates cAMP and calcium signaling. Insect Biochem. Mol. Biol. 37, 318-329. doi: 10.1016/j.ibmb.2006.12.003
33. Du Pasquier, L., and Flajnik, M. (1999). "Origin and evolution of the vertebrate immune system," in Fundamental Immunology, ed. W. E. Paul (Philadelphia: Lippincott Williams & Wilkins), 605-650.
34. Ferguson, H. M., and Read, A. F. (2002). Why is the effect of malaria parasites on mosquito survival still unresolved? Trends Parasitol. 18, 256-261. doi: 10.1016/S1471-4922(02)02281-X
35. Foley, D. (1978). "Innate cellular defense by mosquito hemocytes," in Invertebrate Models for Biomedical Research, eds L. Bulla, Jr. and T. Cheng. (New York: Springer), 113-144.
36. Foley, E., and O'Farrell, P. H. (2003). Nitric oxide contributes to induction of innate immune responses to gram-negative bacteria in Drosophila. Genes Dev. 17, 115-125. doi: 10.1101/gad.1018503
37. Forst, C. V. (2006). Host-pathogen systems biology. Drug Discov. Today 11, 220-227. doi: 10.1016/S1359-6446(05)03735-9
38. Fountain, S., and Burnstock, G. (2009). An evolutionary history of P2X receptors. Purinergic Signal. 5, 269-272. doi: 10.1007/s11302-008-9127-x
39. Friend, W. G., and Smith, J. J. B. (1977). Factors affecting feeding by bloodsucking insects. Annu. Rev. Entomol. 22, 309-331. doi: 10.1146/annurev.en.22.010177.001521
40. Gallucci, S., and Matzinger, P. (2001). Danger signals: SOS to the immune system. Curr. Opin. Immunol. 13, 114-119. doi: 10.1016/S0952-7915(00)00191-6
41. Gloire, G., Legrand-Poels, S., and Piette, J. (2006). NF-κB activation by reactive oxygen species: fifteen years later. Biochem. Pharmacol. 72, 1493-1505. doi: 10.1016/j.bcp.2006.04.011
42. Gooding, R. H. (1973). The digestive processes of haematophagous insects: IV. Secretion of trypsin by Aedes aegypti (Diptera: Culicidae). Can. Entomol. 105, 599-603. doi: 10.4039/Ent105599-4
43. Grieco, J. P., Achee, N. L., Briceno, I., King, R., Andre, R., Roberts, D.,et al. (2003). Comparison of life table attributes from newly established colonies of Anopheles albimanus and Anopheles vestitipennis in northern Belize. J. Vector Ecol. 28, 200-207.
44. Han, Y. S., Thompson, J., Kafatos, F. C., and Barillas-Mury, C. (2000). Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes. EMBO J. 19, 6030-6040. doi: 10.1093/emboj/19.22.6030
45. Harvey, W., and Blankemeyer, J. (1975). "Epithelial structure and function," in Invertebrate Immunity. Mechanisms of Invertebrate Vector-Parasite Relations, eds K. Matamorosch and R. Shope (New York: Academic Press), 3-23.
46. Hecker, H. (1977). Structure and function of midgut epithelial cells in culicidae mosquitoes (Insecta, Diptera). Cell Tissue Res. 184, 321-341. doi: 10.1007/BF00219894
47. Heil, M. (2012). Damaged-self recognition as a general strategy for injury detection. Plant Signal. Behav. 7, 576-580. doi: 10.4161/psb.19921
48. Herrera-Ortíz, A., Lanz-Mendoza, H., Martínez-Barnetche, J., Hernández-Martínez, S., Villarreal-Treviño, C., Aguilar-Marcelino, L.,et al. (2004). Plasmodium berghei ookinetes induce nitric oxide production in Anopheles pseudopunctipennis midguts cultured in vitro. Insect Biochem. Mol. Biol. 34, 893-901. doi: 10.1016/j.ibmb.2004.05.007
49. Hernández-Martínez, S., Lanz-Mendoza, H., Martínez-Barnetche, J., and Rodríguez, M. (2013). Antimicrobial properties of Anopheles albimanus pericardial cells. Cell Tissue Res. 351, 127-137. doi: 10.1007/s00441-012-1505-1506
50. Hernández-Martínez, S., Lanz-Mendoza, H., Rodrguez, M. H., González-Ceron, L., and Tsutsumi, V. (2002). Cellular-mediated reactions to foreign organisms inoculated into the hemocoel of Anopheles albimanus (Diptera: Culicidae). J. Med. Entomol. 39, 61-69. doi: 10.1603/0022-2585-39.1.61
51. Herrera-Ortiz, A., Martínez-Barnetche, J., Smit, N., Rodriguez, M. H., and Lanz-Mendoza, H. (2011). The effect of nitric oxide and hydrogen peroxide in the activation of the systemic immune response of Anopheles albimanusinfected with Plasmodium berghei. Dev. Comp. Immunol. 35, 44-50. doi: 10.1016/j.dci.2010.08.004
52. Hillyer, J. F., Barreau, C., and Vernick, K. D. (2007). Efficiency of salivary gland invasion by malaria sporozoites is controlled by rapid sporozoite destruction in the mosquito haemocoel. Int. J. Parasitol. 37, 673-681. doi: 10.1016/j.ijpara.2006.12.007
53. Hillyer, J. F., Schmidt, S. L., and Christensen, B. M. (2003). Rapid phagocytosis and melanization of bacteria andPlasmodium sporozoites by hemocytes of the mosquito Aedes aegypti. J. Parasitol. 89, 62-69. doi: 10.1645/0022-3395(2003)089[0062:RPAMOB]2.0.CO;2
54. Hirschhorn, R., and Candotti, F. (2007). "Immunodeficiency due to defects of purine metabolism," in Primary Immunodeficiency Diseases: A Molecular and Genetic Approach, 2nd Edn, eds H. D. Hans, D. Ochs, E. Smith, and J. M. Puck (Oxford: Oxford University Press), 169-196.
55. Hoffmann, J., Kafatos, F., Janeway, C., and Ezekowitz, R. (1999). Phylogenetic perspectives in innate immunity. Science 284, 1313-1318. doi: 10.1126/science.284.5418.1313
56. Hurd, H., Grant, K. M., and Arambage, S. C. (2006). Apoptosis-like death as a feature of malaria infection in mosquitoes. Parasitology 132, S33-S47. doi: 10.1017/S0031182006000849
57. Hurd, H., Taylor, P. J., Adams, D., Underhill, A., Eggleston, P., and Koella, J. (2005). Evaluating the costs of mosquito resistance to malaria parasites. Evolution 59, 2560-2572. doi: 10.1554/05-211.1
58. Imamura, M., Yang, J., and Yamakawa, M. (2002). cDNA cloning, characterization and gene expression of nitric oxide synthase from the silkworm, Bombyx mori. Insect Mol. Biol. 11, 257-265. doi: 10.1046/j.1365-2583.2002.00333.x
59. Ivison, S. M., Himmel, M. E., Mayer, M., Yao, Y., Kifayet, A., Levings, M. K.,et al. (2011). The stress signal extracellular ATP modulates antiflagellin immune responses in intestinal epithelial cells. Inflamm. Bowel Dis. 17, 319-333. doi: 10.1002/ibd.21428
60. King, J., and Hillyer, J. (2013). Spatial and temporal in vivo analysis of circulating and sessile immune cells in mosquitoes: hemocyte mitosis following infection. BMC Biol. 11:55. doi: 10.1186/1741-7007-11-55
61. King, J. G., and Hillyer, J. F. (2012). Infection-induced interaction between the mosquito circulatory and immune systems. PLoS Pathog. 8:e1003058. doi: 10.1371/journal.ppat.1003058
62. Klein, J. (1999). Self-nonself discrimination, histoincompatibility, and the concept of immunology. Immunogenetics 50, 116-123. doi: 10.1007/s002510050587
63. Klowden, M. J. (2008). Physiological Systems in Insects. San Diego, CA: Academic Press.
64. Koropatnick, T. A., Engle, J. T., Apicella, M. A., Stabb, E. V., Goldman, W. E., and McFall-Ngai, M. J. (2004). Microbial factor-mediated development in a host-bacterial mutualism. Science 306, 1186-1188. doi: 10.1126/science.1102218
65. Kumar, S., and Barillas-Mury, C. (2005). Ookinete-induced midgut peroxidases detonate the time bomb in anopheline mosquitoes. Insect Biochem. Mol. Biol. 35, 721-727. doi: 10.1016/j.ibmb.2005.02.014
66. Kumar, S., Christophides, G. K., Cantera, R., Charles, B., Han, Y. S., Meister, S.,et al. (2003). The role of reactive oxygen species on Plasmodium melanotic encapsulation in Anopheles gambiae. Proc. Natl. Acad. Sci. U.S.A. 100, 14139-14144. doi: 10.1073/pnas.2036262100
67. Kumar, S., Gupta, L., Han, Y. S., and Barillas-Mury, C. (2004). Inducible peroxidases mediate nitration ofAnopheles midgut cells undergoing apoptosis in response to Plasmodium invasion. J. Biol. Chem. 279, 53475-53482. doi: 10.1074/jbc.M409905200
68. Kurtz, J. (2005). Specific memory within innate immune systems. Trends Immunol. 26, 186-192. doi: 10.1016/j.it.2005.02.001
69. Lackie, A. M. (1988). "Haemocyte behaviour," in Advances in Insect Physiology, eds P. D. Evans and V. B. Wigglesworth (San Diego, CA: Academic Press), 85-178.
70. Lanz-Mendoza, H., Hernández-Martínez, S., Ku-López, M., Rodríguez, M. D. C., Herrera-Ortiz, A., and Rodríguez, M. H. (2002). Superoxide anion in Anopheles albimanus hemolymph and midgut is toxic to Plasmodium bergheiookinetes. J. Parasitol. 88, 702-706. doi: 10.1645/0022-3395(2002)088[0702:SAIAAH]2.0.CO;2
71. Lazzaro, B. P., and Rolff, J. (2011). Danger, microbes, and homeostasis. Science 332, 43-44. doi: 10.1126/science.1200486
72. Litman, G. W., and Cooper, M. D. (2007). Why study the evolution of immunity? Nat. Immunol. 8, 547-548. doi: 10.1038/ni0607-547
73. Little, T. J., Hultmark, D., and Read, A. F. (2005). Invertebrate immunity and the limits of mechanistic immunology. Nat. Immunol. 6, 651-654. doi: 10.1038/ni1219
74. Little, T. J., and Kraaijeveld, A. R. (2004). Ecological and evolutionary implications of immunological priming in invertebrates. Trends Ecol. Evol. 19, 58-60. doi: 10.1016/j.tree.2003.11.011
75. Little, T. J., O'Connor, B., Colegrave, N., Watt, K., and Read, A. F. (2003). Maternal transfer of strain-specific immunity in an invertebrate. Curr. Biol. 13, 489-492. doi: 10.1016/S0960-9822(03)00163-5
76. Luckhart, S., Crampton, A. L., Zamora, R., Lieber, M. J., Dos Santos, P. C., Peterson, T. M. L.,et al. (2003). Mammalian transforming growth factor β1 activated after ingestion by Anopheles stephensi modulates mosquito immunity. Infect. Immun. 71, 3000-3009. doi: 10.1128/IAI.71.6.3000-3009.2003
77. Luckhart, S., and Li, K. (2001). Transcriptional complexity of the Anopheles stephensi nitric oxide synthase gene. Insect Biochem. Mol. Biol. 31, 249-256. doi: 10.1016/S0965-1748(00)00144-2
78. Luckhart, S., and Rosenberg, R. (1999). Gene structure and polymorphism of an invertebrate nitric oxide synthase gene. Gene 232, 25-34. doi: 10.1016/S0378-1119(99)00121-3
79. Luckhart, S., Vodovotz, Y., Cui, L., and Rosenberg, R. (1998). The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc. Natl. Acad. Sci. U.S.A. 95, 5700-5705. doi: 10.1073/pnas.95.10.5700
80. Maier, S., Galellis, J., and McDermid, H. (2005). Phylogenetic analysis reveals a novel protein family closely related to adenosine deaminase. J. Mol. Evol. 61, 776-794. doi: 10.1007/s00239-005-0046-y
81. Maier, W. A., Becker-Feldman, H., and Seitz, H. M. (1987). Pathology of malaria-infected mosquitoes. Parasitol. Today 3, 216-218. doi: 10.1016/0169-4758(87)90063-9
82. Márkus, R., Kurucz,É., Rus, F., and Andó, I. (2005). Sterile wounding is a minimal and sufficient trigger for a cellular immune response in Drosophila melanogaster. Immunol. Lett. 101, 108-111. doi: 10.1016/j.imlet.2005.03.021
83. Marois, E. (2011). The multifaceted mosquito anti-Plasmodium response. Curr. Opin. Microbiol. 14, 429-435. doi: 10.1016/j.mib.2011.07.016
84. Martinez-Barnetche, J., Gomez-Barreto, R., Ovilla-Munoz, M., Tellez-Sosa, J., Lopez, D. E., Dinglasan, R.,et al. (2012). Transcriptome of the adult female malaria mosquito vector Anopheles albimanus. BMC Genomics 13:207. doi: 10.1186/1471-2164-13-207
85. Matthews, H., Ali, M., Carter, V., Underhill, A., Hunt, J., Szor, H.,et al. (2012). Variation in apoptosis mechanisms employed by malaria parasites: the roles of inducers, dose dependence and parasite stages. Malar. J. 11, 297. doi: 10.1186/1475-2875-11-297
86. Matuschewski, K. (2006). Getting infectious: formation and maturation of Plasmodium sporozoites in theAnopheles vector. Cell Microbiol. 8, 1547-1556. doi: 10.1111/j.1462-5822.2006.00778.x
87. Matzinger, P. (1994). Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12, 991-1045. doi: 10.1146/annurev.iy.12.040194.005015
88. Matzinger, P., and Kamala, T. (2011). Tissue-based class control: the other side of tolerance. Nat. Rev. Immunol. 11, 221-230. doi: 10.1038/nri2940
89. Medzhitov, R., and Janeway, C. A. (2002). Decoding the patterns of self and nonself by the innate immune system. Science 296, 298-300. doi: 10.1126/science.1068883
90. Medzhitov, R., Schneider, D. S., and Soares, M. P. (2012). Disease tolerance as a defense strategy. Science 335, 936-941. doi: 10.1126/science.1214935
91. Meis, J. F. G. M., Wismans, P. G. P., Jap, P. H. K., Lensen, A. H. W., and Ponnudurai, T. (1992). A scanning electron microscopic study of the sporogonic development of Plasmodium falciparum in Anopheles stephensi. Acta Trop.50, 227-236. doi: 10.1016/0001-706X(92)90079-D
92. Mercurio, F., and Manning, M. (1999). NF-kB as a primary regulator of the stress response. Oncogene 18, 6163-6171. doi: 10.1038/sj.onc.1203174
93. Metchnikoff, E. (1893). Lectures on the Comparative Pathology of Inflammation. London: Kegan Paul.
94. Meyer-Fernandes, J. R., Lanz-Mendoza, H., Gondim, K. C., Willott, E., and Wells, M. A. (2000). Ectonucleotide diphosphohydrolase activities in hemocytes of larval Manduca sexta. Arch. Biochem. Biophys. 382, 152-159. doi: 10.1006/abbi.2000.1980
95. Molina-Cruz, A., Garver, L. S., Alabaster, A., Bangiolo, L., Haile, A., Winikor, J.,et al. (2013). The human malaria parasite PFS47 gene mediates evasion of the mosquito immune system. Science 340, 984-987. doi: 10.1126/science.1235264
96. Moreno-García, M., Condé, R., Bello-Bedoy, R., and Lanz-Mendoza, H. (2014). The damage threshold hypothesis and the immune strategies of insects. Infect. Genet. Evol. 24, 25-33. doi: 10.1016/j.meegid.2014.02.010
97. Moret, Y. (2006). 'Trans-generational immune priming': specific enhancement of the antimicrobial immune response in the mealworm beetle, Tenebrio molitor. Proc. R. Soc. B Biol. Sci. 273, 1399-1405. doi: 10.1098/rspb.2006.3465
98. Mueller, A-K., Kohlhepp, F., Hammerschmidt, C., and Michel, K. (2010). Invasion of mosquito salivary glands by malaria parasites: prerequisites and defense strategies. Int. J. Parasitol. 40, 1229-1235. doi: 10.1016/j.ijpara.2010.05.005
99. Mutai, B., and Waitumbi, J. (2010). Apoptosis stalks Plasmodium falciparum maintained in continuous culture condition. Malar. J. 9(suppl. 3):S6. doi: 10.1186/1475-2875-9-S3-S6
100. Nacer, A., Walker, K., and Hurd, H. (2008). Localisation of laminin within Plasmodium berghei oocysts and the midgut epithelial cells of Anopheles stephensi. Parasites Vectors 1, 33. doi: 10.1186/1756-3305-1-33
101. Nam, H-J., Jang, I-H., You, H., Lee, K-A., and Lee, W-J. (2012). Genetic evidence of a redox-dependent systemic wound response via Hayan protease-phenoloxidase system in Drosophila. EMBO J. 31, 1253-1265. doi: 10.1038/emboj.2011.476
102. Nappi, A., Vass, E., Frey, F., and Carton, Y. (1995). Superoxide anion generation in Drosophila during melanotic encapsulation of parasite. Eur. J. Cell Biol. 68, 450-456.
103. Nappi, A. J., and Vass, E. (1993). Melanogenesis and the generation of cytotoxic molecules during insect cellular immune reactions. Pigment. Cell Res. 6, 117-126. doi: 10.1111/j.1600-0749.1993.tb00590.x
104. Nappi, A. J., and Vass, E. (1998). Hydrogen peroxide production in immune-reactive Drosophila melanogaster. J. Parasitol. 84, 1150-1157. doi: 10.2307/3284664
105. Nappi, A. J., Vass, E., Frey, F., and Carton, Y. (2000). Nitric oxide involvement in Drosophila immunity. Nitric Oxide 4, 423-430. doi: 10.1006/niox.2000.0294
106. Natori, S. (1998). "Relation between insect defense proteins and development of the flesh fly, Sarcophaga peregrina," in Molecular Mechanisms of Immune Responses in Insects, eds P. T. Brey and D. Hultmark (London, UK: Chapman & Hall Ltd), 245-260.
107. Nayar, J. K., and Knight, J. W. (1995). Wounding increases intracellular encapsulation (melanization) of developingBrugia malayi (Nematoda: Filarioidea) larvae in thoracic muscles of Anopheles quadrimaculatus. Comp. Biochem. Physiol. A Physiol. 112, 553-557. doi: 10.1016/0300-9629(95)02027-6
108. Noble, A. (2009). Do we have memory of danger as well as antigen? Trends Immunol. 30, 150-156. doi: 10.1016/j.it.2009.02.001
109. Novakova, M., and Dolezal, T. (2011). Expression of Drosophila adenosine deaminase in immune cells during inflammatory response. PLoS ONE 6:e17741. doi: 10.1371/journal.pone.0017741
110. Oliveira, G. D. A., Lieberman, J., and Barillas-Mury, C. (2012). Epithelial nitration by a peroxidase/NOX5 system mediates mosquito antiplasmodial immunity. Science 335, 856-859. doi: 10.1126/science.1209678
111. Pastor-Pareja, J., Wu, M., and Xu, T. (2008). An innate immune response of blood cells to tumors and tissue damage in Drosophila. Dis. Models Mech. 1, 144-154. doi: 10.1242/dmm.000950
112. Peterson, T. M. L., Gow, A. J., and Luckhart, S. (2007). Nitric oxide metabolites induced in Anopheles stephensicontrol malaria parasite infection. Free Radic. Biol. Med. 42, 132-142. doi: 10.1016/j.freeradbiomed.2006.10.037
113. Pham, L. N., and Schneider, D. S. (2008). "Evidence for specificity and memory in the insect innate immune response," in Insect Immunology, ed. N. E. Beckage (San Diego: Academic Press), 97-127.
114. Philip, N., and Waters, A. P. (2013). Unveiling the malaria parasite's cloak of invisibility? Science 340, 936-937. doi: 10.1126/science.1239146
115. Pinto, S. B., Kafatos, F. C., and Michel, K. (2008). The parasite invasion marker SRPN6 reduces sporozoite numbers in salivary glands of Anopheles gambiae. Cell Microbiol. 10, 891-898. doi: 10.1111/j.1462-5822.2007.01091.x
116. Pollitt, L., Colegrave, N., Khan, S., Sajid, M., and Reece, S. (2010). Investigating the evolution of apoptosis in malaria parasites: the importance of ecology. Parasit. Vectors 3, 105. doi: 10.1186/1756-3305-3-105
117. Ramirez, J. L., Garver, L. S., Brayner, F. A., Alves, L. C., Rodrigues, J., Molina-Cruz, A.,et al. (2014). The role of hemocytes in Anopheles gambiae antiplasmodial immunity. J. Innate Immun. 6, 119-128. doi: 10.1159/000353765
118. Rivkin, H., Kroemer, J. A., Bronshtein, A., Belausov, E., Webb, B. A., and Chejanovsky, N. (2006). Response of immunocompetent and immunosuppressed Spodoptera littoralis larvae to baculovirus infection. J. Gen. Virol. 87, 2217-2225. doi: 10.1099/vir.0.81918-81910
119. Rizki, R. M., and Rizki, T. M. (1980). Hemocyte response to implanted tissues in Drosophila melanogaster larvae. Wilhem Roux's Arch. 189, 207-213. doi: 10.1007/BF00868679
120. Rodrigues, J., Brayner, F. A., Alves, L. C., Dixit, R., and Barillas-Mury, C. (2010). Hemocyte differentiation mediates innate immune memory in Anopheles gambiae mosquitoes. Science 329, 1353-1355. doi: 10.1126/science.1190689
121. Rodriguez, M. H., and Hernández-Hernández, F. D. L. C. (2004). Insect-malaria parasites interactions: the salivary gland. Insect Biochem. Mol. Biol. 34, 615-624. doi: 10.1016/j.ibmb.2004.03.014
122. Rosenberg, R., and Rungsiwongse, J. (1991). The number of sporozoites produced by individual malaria oocysts. Am. J. Trop. Med. Hyg. 45, 574-577.
123. Ross, R. (1902). Researches on malaria. Nobel Lect. 25-116.
124. Rossignol, P. A., Ribeiro, J. M. C., and Spielman, A. (1984). Increased intradermal probing time in sporozoite-infected mosquitoes. Am. J. Trop. Med. Hyg. 33, 17-20.
125. Rutault, K., Alderman, C., Chain, B. M., and Katz, D. R. (1999). Reactive oxygen species activate human peripheral blood dendritic cells. Free Radic. Biol. Med. 26, 232-238. doi: 10.1016/S0891-5849(98)00194-4
126. Salt, G. (1970). The Cellular Reactions of Insects. Cambridge, UK: Cambridge University Press. doi: 10.1017/CBO9780511721960
127. Sanders, H. R., Foy, B. D., Evans, A. M., Ross, L. S., Beaty, B. J., Olson, K. E.,et al. (2005). Sindbis virus induces transport processes and alters expression of innate immunity pathway genes in the midgut of the disease vector,Aedes aegypti. Insect Biochem. Mol. Biol. 35, 1293-1307. doi: 10.1016/j.ibmb.2005.07.006
128. Serrano-Pinto, V., Acosta-Pérez, M., Luviano-Bazán, D., Hurtado-Sil, G., Batista, C. V. F., Martínez-Barnetche, J.,et al. (2010). Differential expression of proteins in the midgut of Anopheles albimanus infected with Plasmodium berghei. Insect Biochem. Mol. Biol. 40, 752-758. doi: 10.1016/j.ibmb.2010.07.011
129. Sinden, R., Dawes, E. J., Alavi, Y., Waldock, J., Finney, O., Mendoza, J.,et al. (2007). Progression of Plasmodium berghei through Anopheles stephensi is density-dependent. PLoS Pathog. 3:e195. doi: 10.1371/journal.ppat.0030195
130. Sinden, R. E. (1974). Excystment by sporozoites of malaria parasites. Nature 252, 314-314. doi: 10.1038/252314a0
131. Sinden, R. E., and Billingsley, P. F. (2001). Plasmodium invasion of mosquito cells: hawk or dove? Trends Parasitol.17, 209-211. doi: 10.1016/S1471-4922(01)01928-6
132. Sinden, R. E., and Strong, K. (1978). An ultrastructural study of the sporogonic development of Plasmodium falciparum in Anopheles gambiae. Trans. R. Soc. Trop. Med. Hygiene 72, 477-491. doi: 10.1016/0035-9203(78)90167-90160
133. Sitkovsky, M. V., and Ohta, A. (2005). The 'danger' sensors that STOP the immune response: the A2 adenosine receptors? Trends Immunol. 26, 299-304. doi: 10.1016/j.it.2005.04.004
134. Smith, R. C., and Jacobs-Lorena, M. (2010). "Plasmodium-mosquito interactions: a tale of roadblocks and detours," in Advances in Insect Physiology, ed. J. S. Stephen (Academic Press), 119-149.
135. Sun, S-C., and Faye, I. (1995). Transcription of immune genes in the giant silkmoth, Hyalophora cecropia, is augmented by H2O2 and diminished by thiol reagents. Eur. J. Biochem. 231, 93-98. doi: 10.1111/j.1432-1033.1995.0093f.x
136. Tanada, Y., and Kaya, H. K. (1993). Insect Pathology. San Diego: Academic Press.
137. Tidbury, H. J., Pedersen, A. B., and Boots, M. (2011). Within and transgenerational immune priming in an insect to a DNA virus. Proc. R. Soc. B Biol. Sci. 278, 871-876. doi: 10.1098/rspb.2010.1517
138. Trautmann, A. (2009). Extracellular ATP in the immune system: more than just a "danger signal". Sci. Signal. 2, pe6. doi: 10.1126/scisignal.256pe6
139. Tripet, F., Aboagye-Antwi, F., and Hurd, H. (2008). Ecological immunology of mosquito-malaria interactions. Trends Parasitol. 24, 219-227. doi: 10.1016/j.pt.2008.02.008
140. Virchow, R. L. K. (1863). Cellular Pathology as Based Upon Physiological and Pathological Histology./by Rudolf Virchow. Translated from the 2nd edition of the original by Frank Chance. With notes and numerous emendations, principally from MS. Notes of the author. Philadelphia: J. B. Lippincott.
141. Vlachou, D., Schlegelmilch, T., Runn, E., Mendes, A., and Kafatos, F. C. (2006). The developmental migration ofPlasmodium in mosquitoes. Curr. Opin. Genet. Dev. 16, 384-391. doi: 10.1016/j.gde.2006.06.012
142. Vlachou, D., Zimmermann, T., Cantera, R., Janse, C. J., Waters, A. P., and Kafatos, F. C. (2004). Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion. Cell Microbiol. 6, 671-685. doi: 10.1111/j.1462-5822.2004.00394.x
143. Vodovotz, Y. (2006). Deciphering the complexity of acute inflammation using mathematical models. Immunol. Res. 36, 237-245. doi: 10.1385/IR:36:1,237
144. Wallach, D., Kang, T-B., and Kovalenko, A. (2014). Concepts of tissue injury and cell death in inflammation: a historical perspective. Nat. Rev. Immunol. 14, 51-59. doi: 10.1038/nri3561
145. Warburg, A., Shtern, A., Cohen, N., and Dahan, N. (2007). Laminin and a Plasmodium ookinete surface protein inhibit melanotic encapsulation of Sephadex beads in the hemocoel of mosquitoes. Microbes Infect. 9, 192-199. doi: 10.1016/j.micinf.2006.11.006
146. Whitten, M. M. A., Shiao, S. H., and Levashina, E. A. (2006). Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunol. 28, 121-130. doi: 10.1111/j.1365-3024.2006.00804.x
147. Yurchenco, P. D., and O’Rear, J. (1993). "Supramolecular organization of basement membranes," in Molecular and Cellular Aspects of Basement Membrane, eds D. H. Rohrbach and R. Timpl (New York: Academic Press), 19-47.
148. Zeiser, R., Penack, O., Holler, E., and Idzko, M. (2011). Danger signals activating innate immunity in graft-versus-host disease. J. Mol. Med. 89, 833-845. doi: 10.1007/s00109-011-0767-x
149. Zieler, H., and Dvorak, J. A. (2000). Invasion in vitro of mosquito midgut cells by the malaria parasite proceeds by a conserved mechanism and results in death of the invaded midgut cells. Proc. Natl. Acad. Sci. U.S.A. 97, 11516-11521. doi: 10.1073/pnas.97.21.11516
150. Zurovec, M., Dolezal, T., Gazi, M., Pavlova, E., and Bryant, P. J. (2002). Adenosine deaminase-related growth factors stimulate cell proliferation in Drosophila by depleting extracellular adenosine. Proc. Natl. Acad. Sci. U.S.A.99, 4403-4408. doi: 10.1073/pnas.062059699