The effects of ingested mammalian blood factors on vector arthropod immunity and physiology

Microbes and Infection

Volumn 15, Issue 3, 2013, Pages 243-254

  Pakpour, Nazzy ^a   Akman Anderson, Leyla ^b   Vodovotz, Yoram ^c,d   Luckhart, Shirley ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^d UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Insulin; Macrophage migration inhibitory factor (MIF); Mosquito; Plasmodium; Tick; Transforming growth factor beta (TGF )

Indexed keywords

CARBOXYPEPTIDASE B; CHITINASE; CHITOTRIOSIDASE; HEMOGLOBIN; HYDROGEN PEROXIDE; INSULIN; INTERLEUKIN 6; JANUS KINASE; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; SMAD PROTEIN; SOMATOMEDIN C;

AMBLYOMMA AMERICANUM; ANOPHELES STEPHENSI; BLOOD GROUP; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; HAEMAPHYSALIS LONGICORNIS; HUMAN; HYPERINSULINEMIA; IMMUNE RESPONSE; IMMUNE SYSTEM; INGESTION; INSULIN BLOOD LEVEL; INSULIN RELEASE; INSULIN RESISTANCE; LEISHMANIA TROPICA; LIFESPAN; MALARIA FALCIPARUM; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; ORNITHODOROS MOUBATA; OXIDATIVE STRESS; PARASITE IMMUNITY; PARASITE VECTOR; PARASITOSIS; PLASMODIUM; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRODUCTION; SHORT SURVEY; SIGNAL TRANSDUCTION; TRYPANOSOMA CRUZI;

ANIMALS; ARTHROPOD VECTORS; BLOOD PROTEINS; CULICIDAE; FEEDING BEHAVIOR; HOST-PARASITE INTERACTIONS; HUMANS; TICKS;

ARTHROPODA; INVERTEBRATA; IXODIDA; MAMMALIA; VERTEBRATA;

EID: 84874957518     PISSN: 12864579     EISSN: 1769714X     Source Type: Journal    
DOI: 10.1016/j.micinf.2013.01.003     Document Type: Short Survey

References (129)

1. Darby S.M., Miller M.L., Allen R.O., LeBeau M. A mass spectrometric method for quantitation of intact insulin in blood samples. J. Anal. Toxicol. 2001, 25:8-14.
2. White N.J., Warrell D.A., Chanthavanich P., Looareesuwan S., Warrell M.J., Krishna S., Williamson D.H., Turner R.C. Severe hypoglycemia and hyperinsulinemia in falciparum malaria. N. Engl. J. Med. 1983, 309:61-66.
3. Danquah I., Bedu-Addo G., Mockenhaupt F.P. Type 2 diabetes mellitus and increased risk for malaria infection. Emerg. Infect. Dis. 2010, 16:1601-1604.
4. Whitten M.M., Shiao S.H., Levashina E.A. Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunol. 2006, 28:121-130.
5. Beier M.S., Pumpuni C.B., Beier J.C., Davis J.R. Effects of para-aminobenzoic acid, insulin, and gentamicin on Plasmodium falciparum development in anopheline mosquitoes (Diptera: Culicidae). J. Med. Entomol. 1994, 31:561-565.
6. Surachetpong W., Pakpour N., Cheung K.W., Luckhart S. Reactive oxygen species-dependent cell signaling regulates the mosquito immune response to Plasmodium falciparum. Antioxid. Redox Signal. 2011, 14:943-955.
7. Kang M.A., Mott T.M., Tapley E.C., Lewis E.E., Luckhart S. Insulin regulates aging and oxidative stress in Anopheles stephensi. J. Exp. Biol. 2008, 211:741-748.
8. Drexler A., Nuss A., Hauck E., Glennon E., Cheung K., Brown M., Luckhart S. Human IGF1 extends lifespan and enhances resistance to Plasmodium falciparum infection in the malaria vector Anopheles stephensi. J. Exp. Biol. 2013, 216:208-217.
9. Luckhart S., Riehle M.A. The insulin signaling cascade from nematodes to mammals: insights into innate immunity of Anopheles mosquitoes to malaria parasite infection. Dev. Comp. Immunol. 2007, 31:647-656.
10. Drexler A., Nuss A., Hauck E., Glennon E., Brown M.R., Luckhart S. Human IGF1 extends lifespan and enhances resistance to Plasmodium falciparum infection in the malaria vector Anopheles stephensi. J. Exp. Biol. 2013, 216:208-217.
11. Marquez A.G., Pietri J.E., Smithers H.M., Nuss A., Antonova Y., Drexler A.L., Riehle M.A., Brown M.R., Luckhart S. Insulin-like peptides in the mosquito Anopheles stephensi: identification and expression in response to diet and infection with Plasmodium falciparum. Gen. Comp. Endocrinol. 2011, 173:303-312.
12. Lim J., Gowda D.C., Krishnegowda G., Luckhart S. Induction of nitric oxide synthase in Anopheles stephensi by Plasmodium falciparum: mechanism of signaling and the role of parasite glycosylphosphatidylinositols. Infect. Immun. 2005, 73:2778-2789.
13. Akman-Anderson L., Olivier M., Luckhart S. Induction of nitric oxide synthase and activation of signaling proteins in Anopheles mosquitoes by the malaria pigment, hemozoin. Infect. Immun. 2007, 75:4012-4019.
14. Horton A.A., Wang B., Camp L., Price M.S., Arshi A., Nagy M., Nadler S.A., Faeder J.R., Luckhart S. The mitogen-activated protein kinome from Anopheles gambiae: identification, phylogeny and functional characterization of the ERK, JNK and p38 MAP kinases. BMC Genomics 2011, 12:574.
15. Pakpour N., Corby-Harris V., Green G.P., Smithers H.M., Cheung K.W., Riehle M.A., Luckhart S. Ingested human insulin inhibits the mosquito NF-kappaB-dependent immune response to Plasmodium falciparum. Infect. Immun. 2012, 80:2141-2149.
16. Corby-Harris V., Drexler A., Watkins de Jong L., Antonova Y., Pakpour N., Ziegler R., Ramberg F., Lewis E.E., Brown J.M., Luckhart S., Riehle M.A. Activation of Akt signaling reduces the prevalence and intensity of malaria parasite infection and lifespan in Anopheles stephensi mosquitoes. PLoS Pathog. 2010, 6:e1001003.
17. Antonova Y., Arik A.J., Moore W., Riehle M.R., Brown M.R. Insulin-like peptides: structure, signaling, and function. Insect Endocrinology 2012, 63-92. Elsevier/Academic Press, Waltham, MA. L.I. Gilbert (Ed.).
18. Davis H.H., Dotson E.M., Oliver J.H. Localization of insulin-like immunoreactivity in the synganglion of nymphal and adult Dermacentor variabilis (Acari: Ixodidae). Exp. Appl. Acarol. 1994, 18:111-122.
19. de Abreu L.A., Fabres A., Esteves E., Masuda A., da Silva Vaz I., Daffre S., Logullo C. Exogenous insulin stimulates glycogen accumulation in Rhipicephalus (Boophilus) microplus embryo cell line BME26 via PI3K/AKT pathway. Comp. Biochem. Physiol. B: Biochem. Mol. Biol. 2009, 153:185-190.
20. Surachetpong W., Singh N., Cheung K.W., Luckhart S. MAPK ERK signaling regulates the TGF-beta1-dependent mosquito response to Plasmodium falciparum. PLoS Pathog. 2009, 5:e1000366.
21. Humphries K.M., Szweda P.A., Szweda L.I. Aging: a shift from redox regulation to oxidative damage. Free Radic. Res. 2006, 40:1239-1243.
22. S. Luckhart, C. Giulivi, A.L. Drexler, Y. Antonova-Koch, D. Sakaguchi, E. Napoli, S. Wong, M.S. Price, R. Eigenheer, B.S. Phinney, N. Pakpour, J.E. Pietri, K. Cheung, M. Georgis, M. Riehle, Sustained activation of Akt elicits mitochondrial dysfunction to block Plasmodium falciparum infection in the mosquito host, PLoS Pathog., in press.
23. Luckhart S., Vodovotz Y., Cui L., Rosenberg R. The mosquito Anopheles stephensi limits malaria parasite development with inducible synthesis of nitric oxide. Proc. Natl. Acad. Sci. U. S. A. 1998, 95:5700-5705.
24. Peterson T.M., Gow A.J., Luckhart S. Nitric oxide metabolites induced in Anopheles stephensi control malaria parasite infection. Free Radic. Biol. Med. 2007, 42:132-142.
25. Sinden R.E., Dawes E.J., Alavi Y., Waldock J., Finney O., Mendoza J., Butcher G.A., Andrews L., Hill A.V., Gilbert S.C., Basanez M.G. Progression of Plasmodium berghei through Anopheles stephensi is density-dependent. PLoS Pathog. 2007, 3:e195.
26. Dandona P., Aljada A., Mohanty P., Ghanim H., Hamouda W., Assian E., Ahmad S. Insulin inhibits intranuclear nuclear factor kappaB and stimulates IkappaB in mononuclear cells in obese subjects: evidence for an anti-inflammatory effect?. J. Clin. Endocrinol. Metab. 2001, 86:3257-3265.
27. Frolet C., Thoma M., Blandin S., Hoffmann J.A., Levashina E.A. Boosting NF-kappaB-dependent basal immunity of Anopheles gambiae aborts development of Plasmodium berghei. Immunity 2006, 25:677-685.
28. Meredith J.M., Munks R.J., Grail W., Hurd H., Eggleston P., Lehane M.J. A novel association between clustered NF-kappaB and C/EBP binding sites is required for immune regulation of mosquito defensin genes. Insect Mol. Biol. 2006, 15:393-401.
29. Vallabhapurapu S., Karin M. Regulation and function of NF-kappaB transcription factors in the immune system. Annu. Rev. Immunol. 2009, 27:693-733.
30. Cirimotich C.M., Dong Y., Garver L.S., Sim S., Dimopoulos G. Mosquito immune defenses against Plasmodium infection. Dev. Comp. Immunol. 2010, 34:387-395.
31. Mohan S., Baylink D.J. IGF-binding proteins are multifunctional and act via IGF-dependent and -independent mechanisms. J. Endocrinol. 2002, 175:19-31.
32. Honegger B., Galic M., Kohler K., Wittwer F., Brogiolo W., Hafen E., Stocker H. Imp-L2, a putative homolog of vertebrate IGF-binding protein 7, counteracts insulin signaling in Drosophila and is essential for starvation resistance. J. Biol. 2008, 7:10.
33. Sajid W., Kulahin N., Schluckebier G., Ribel U., Henderson H.R., Tatar M., Hansen B.F., Svendsen A.M., Kiselyov V.V., Norgaard P., Wahlund P.O., Brandt J., Kohanski R.A., Andersen A.S., De Meyts P. Structural and biological properties of the Drosophila insulin-like peptide 5 show evolutionary conservation. J. Biol. Chem. 2011, 286:661-673.
34. Mulenga A., Khumthong R. Silencing of three Amblyomma americanum (L.) insulin-like growth factor binding protein-related proteins prevents ticks from feeding to repletion. J. Exp. Biol. 2010, 213:1153-1161.
35. Brown M.R., Clark K.D., Gulia M., Zhao Z., Garczynski S.F., Crim J.W., Suderman R.J., Strand M.R. An insulin-like peptide regulates egg maturation and metabolism in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:5716-5721.
36. Andersen L., Jorgensen P.N., Jensen L.B., Walsh D. A new insulin immunoassay specific for the rapid-acting insulin analog, insulin aspart, suitable for bioavailability, bioequivalence, and pharmacokinetic studies. Clin. Biochem. 2000, 33:627-633.
37. Attisano L., Wrana J.L. Signal transduction by the TGF-beta superfamily. Science 2002, 296:1646-1647.
38. Omer F.M., Kurtzhals J.A., Riley E.M. Maintaining the immunological balance in parasitic infections: a role for TGF-beta?. Parasitol. Today 2000, 16:18-23.
39. Moustakas A., Heldin C.H. Non-Smad TGF-beta signals. J. Cell Sci. 2005, 118:3573-3584.
40. Luckhart S., Crampton A.L., Zamora R., Lieber M.J., Dos Santos P.C., Peterson T.M., Emmith N., Lim J., Wink D.A., Vodovotz Y. Mammalian transforming growth factor beta1 activated after ingestion by Anopheles stephensi modulates mosquito immunity. Infect. Immun. 2003, 71:3000-3009.
41. Lieber M.J., Luckhart S. Transforming growth factor-betas and related gene products in mosquito vectors of human malaria parasites: signaling architecture for immunological crosstalk. Mol. Immunol. 2004, 41:965-977.
42. Padgett R.W., Wozney J.M., Gelbart W.M. Human BMP sequences can confer normal dorsal-ventral patterning in the Drosophila embryo. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:2905-2909.
43. Newfeld S.J., Mehra A., Singer M.A., Wrana J.L., Attisano L., Gelbart W.M. Mothers against dpp participates in a DDP/TGF-beta responsive serine-threonine kinase signal transduction cascade. Development 1997, 124:3167-3176.
44. Brummel T., Abdollah S., Haerry T.E., Shimell M.J., Merriam J., Raftery L., Wrana J.L., O'Connor M.B. The Drosophila activin receptor baboon signals through dSmad2 and controls cell proliferation but not patterning during larval development. Genes Dev. 1999, 13:98-111.
45. Matsuo T., Cerruto Noya C.A., Taylor D., Fujisaki K. Immunohistochemical examination of PDGF-AB, TGF-beta and their receptors in the hemocytes of a tick, Ornithodoros moubata (Acari: Argasidae). J. Vet. Med. Sci. 2007, 69:317-320.
46. Vodovotz Y., Zamora R., Lieber M.J., Luckhart S. Cross-talk between nitric oxide and transforming growth factor-beta1 in malaria. Curr. Mol. Med. 2004, 4:787-797.
47. Vodovotz Y. Control of nitric oxide production by transforming growth factor-beta1: mechanistic insights and potential relevance to human disease. Nitric Oxide 1997, 1:3-17.
48. Bozza M.T., Martins Y.C., Carneiro L.A., Paiva C.N. Macrophage migration inhibitory factor in protozoan infections. J. Parasitol. Res. 2012, 2012:413052.
49. Jaworski D.C., Jasinskas A., Metz C.N., Bucala R., Barbour A.G. Identification and characterization of a homologue of the pro-inflammatory cytokine macrophage migration inhibitory factor in the tick, Amblyomma americanum. Insect Mol. Biol. 2001, 10:323-331.
50. Umemiya R., Hatta T., Liao M., Tanaka M., Zhou J., Inoue N., Fujisaki K. Haemaphysalis longicornis: molecular characterization of a homologue of the macrophage migration inhibitory factor from the partially fed ticks. Exp. Parasitol. 2007, 115:135-142.
51. Wasala N.B., Jaworski D.C. Dermacentor variabilis: characterization and modeling of macrophage migration inhibitory factor with phylogenetic comparisons to other ticks, insects and parasitic nematodes. Exp. Parasitol. 2012, 130:232-238.
52. Bowen C.J., Jaworski D.C., Wasala N.B., Coons L.B. Macrophage migration inhibitory factor expression and protein localization in Amblyomma americanum (Ixodidae). Exp. Appl. Acarol. 2010, 50:343-352.
53. Jaworski D.C., Bowen C.J., Wasala N.B. Amblyomma americanum (L): tick macrophage migration inhibitory factor peptide immunization lengthens lone star tick feeding intervals in vivo. Exp. Parasitol. 2009, 121:384-387.
54. Rehbein G., Ahmed J.S., Schein E., Horchner F., Zweygarth E. Immunological aspects of Theileria annulata infection calves. 2. Production of macrophage migration inhibition factor (MIF) by sensitized lymphocytes from Theileria annulata-infected calves. Tropenmed. Parasitol. 1981, 32:154-156.
55. Kozaci D.L., Ertug S., Kavak T., Okyay P., Chikanza I.C., Ertabaklar H. Investigation of serum macrophage migration inhibitor factor (MIF) levels in patients with cutaneous leishmaniasis. Turkiye Parazitol Derg 2005, 29:145-148.
56. Nishimura K., Nakaya H., Nakagawa H., Matsuo S., Ohnishi Y., Yamasaki S. Differential effects of Trypanosoma brucei gambiense and Trypanosoma brucei brucei on rat macrophages. J. Parasitol. 2011, 97:48-54.
57. Prieto-Lafuente L., Gregory W.F., Allen J.E., Maizels R.M. MIF homologues from a filarial nematode parasite synergize with IL-4 to induce alternative activation of host macrophages. J. Leukoc. Biol. 2009, 85:844-854.
58. Kamir D., Zierow S., Leng L., Cho Y., Diaz Y., Griffith J., McDonald C., Merk M., Mitchell R.A., Trent J., Chen Y., Kwong Y.K., Xiong H., Vermeire J., Cappello M., McMahon-Pratt D., Walker J., Bernhagen J., Lolis E., Bucala R. A Leishmania ortholog of macrophage migration inhibitory factor modulates host macrophage responses. J. Immunol. 2008, 180:8250-8261.
59. Han C., Lin Y., Shan G., Zhang Z., Sun X., Wang Z., Wei C., Deng Y., Zhang L., Bu L., Shao D., Wang H. Plasma concentration of malaria parasite-derived macrophage migration inhibitory factor in uncomplicated malaria patients correlates with parasitemia and disease severity. Clin. Vaccine Immunol. 2010, 17:1524-1532.
60. Lue H., Kleemann R., Calandra T., Roger T., Bernhagen J. Macrophage migration inhibitory factor (MIF): mechanisms of action and role in disease. Microbes Infect. 2002, 4:449-460.
61. Schindler C., Levy D.E., Decker T. JAK-STAT signaling: from interferons to cytokines. J. Biol. Chem. 2007, 282:20059-20063.
62. Zhou F., Agaisse H. JAK/STAT Signaling and Invertebrate Immune Responses Jak-Stat Signaling: from Basics to Disease 2012, 133-151. Springer, Vienna. T. Decker, M. Müller (Eds.).
63. Gupta L., Molina-Cruz A., Kumar S., Rodrigues J., Dixit R., Zamora R.E., Barillas-Mury C. The STAT pathway mediates late-phase immunity against Plasmodium in the mosquito Anopheles gambiae. Cell Host Microbe 2009, 5:498-507.
64. Souza-Neto J.A., Sim S., Dimopoulos G. An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:17841-17846.
65. Bahia A.C., Kubota M.S., Tempone A.J., Araujo H.R., Guedes B.A., Orfano A.S., Tadei W.P., Rios-Velasquez C.M., Han Y.S., Secundino N.F., Barillas-Mury C., Pimenta P.F., Traub-Cseko Y.M. The JAK-STAT pathway controls Plasmodium vivax load in early stages of Anopheles aquasalis infection. PLoS Negl. Trop. Dis. 2011, 5:e1317.
66. Liu L., Dai J., Zhao Y.O., Narasimhan S., Yang Y., Zhang L., Fikrig E. Ixodes scapularis JAK-STAT pathway regulates tick antimicrobial peptides, thereby controlling the agent of human granulocytic anaplasmosis. J. Infect. Dis. 2012, 206:1233-1241.
67. Lyke K.E., Burges R., Cissoko Y., Sangare L., Dao M., Diarra I., Kone A., Harley R., Plowe C.V., Doumbo O.K., Sztein M.B. Serum levels of the proinflammatory cytokines interleukin-1 beta (IL-1beta), IL-6, IL-8, IL-10, tumor necrosis factor alpha, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect. Immun. 2004, 72:5630-5637.
68. Huang Y.H., Lei H.Y., Liu H.S., Lin Y.S., Liu C.C., Yeh T.M. Dengue virus infects human endothelial cells and induces IL-6 and IL-8 production. Am. J. Trop. Med. Hyg. 2000, 63:71-75.
69. Sigal L.H. Lyme disease: a review of aspects of its immunology and immunopathogenesis. Annu. Rev. Immunol. 1997, 15:63-92.
70. Lavazec C., Bourgouin C. Mosquito-based transmission blocking vaccines for interrupting Plasmodium development. Microbes Infect. 2008, 10:845-849.
71. de la Fuente J., Kocan K.M. Strategies for development of vaccines for control of ixodid tick species. Parasite Immunol. 2006, 28:275-283.
72. Crompton P.D., Pierce S.K., Miller L.H. Advances and challenges in malaria vaccine development. J. Clin. Invest. 2010, 120:4168-4178.
73. Schuijt T.J., Hovius J.W., van der Poll T., van Dam A.P., Fikrig E. Lyme borreliosis vaccination: the facts, the challenge, the future. Trends Parasitol. 2011, 27:40-47.
74. Dinglasan R.R., Jacobs-Lorena M. Flipping the paradigm on malaria transmission-blocking vaccines. Trends Parasitol. 2008, 24:364-370.
75. Dinglasan R.R., Kalume D.E., Kanzok S.M., Ghosh A.K., Muratova O., Pandey A., Jacobs-Lorena M. Disruption of Plasmodium falciparum development by antibodies against a conserved mosquito midgut antigen. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:13461-13466.
76. Ramasamy M.S., Sands M., Kay B.H., Fanning I.D., Lawrence G.W., Ramasamy R. Anti-mosquito antibodies reduce the susceptibility of Aedes aegypti to arbovirus infection. Med. Vet. Entomol. 1990, 4:49-55.
77. de la Fuente J., Almazan C., Blas-Machado U., Naranjo V., Mangold A.J., Blouin E.F., Gortazar C., Kocan K.M. The tick protective antigen, 4D8, is a conserved protein involved in modulation of tick blood ingestion and reproduction. Vaccine 2006, 24:4082-4095.
78. Merino O., Almazan C., Canales M., Villar M., Moreno-Cid J.A., Galindo R.C., de la Fuente J. Targeting the tick protective antigen subolesin reduces vector infestations and pathogen infection by Anaplasma marginale and Babesia bigemina. Vaccine 2011, 29:8575-8579.
79. de la Fuente J., Moreno-Cid J.A., Canales M., Villar M., de la Lastra J.M., Kocan K.M., Galindo R.C., Almazan C., Blouin E.F. Targeting arthropod subolesin/akirin for the development of a universal vaccine for control of vector infestations and pathogen transmission. Vet. Parasitol. 2011, 181:17-22.
80. Bensaci M., Bhattacharya D., Clark R., Hu L.T. Oral vaccination with vaccinia virus expressing the tick antigen subolesin inhibits tick feeding and transmission of Borrelia burgdorferi. Vaccine 2012, 30:6040-6046.
81. Kamhawi S., Ramalho-Ortigao M., Pham V.M., Kumar S., Lawyer P.G., Turco S.J., Barillas-Mury C., Sacks D.L., Valenzuela J.G. A role for insect galectins in parasite survival. Cell 2004, 119:329-341.
82. Gouagna L.C., Bonnet S., Gounoue R., Verhave J.P., Eling W., Sauerwein R., Boudin C. Stage-specific effects of host plasma factors on the early sporogony of autologous Plasmodium falciparum isolates within Anopheles gambiae. Trop. Med. Int. Health 2004, 9:937-948.
83. Healer J., McGuinness D., Hopcroft P., Haley S., Carter R., Riley E. Complement-mediated lysis of Plasmodium falciparum gametes by malaria-immune human sera is associated with antibodies to the gamete surface antigen Pfs230. Infect. Immun. 1997, 65:3017-3023.
84. Fujita T. Evolution of the lectin-complement pathway and its role in innate immunity. Nat. Rev. Immunol. 2002, 2:346-353.
85. Margos G., Navarette S., Butcher G., Davies A., Willers C., Sinden R.E., Lachmann P.J. Interaction between host complement and mosquito-midgut-stage Plasmodium berghei. Infect. Immun. 2001, 69:5064-5071.
86. Tsuboi T., Cao Y.M., Torii M., Hitsumoto Y., Kanbara H. Murine complement reduces infectivity of Plasmodium yoelii to mosquitoes. Infect. Immun. 1995, 63:3702-3704.
87. Breitner-Ruddock S., Wurzner R., Schulze J., Brade V. Heterogeneity in the complement-dependent bacteriolysis within the species of Borrelia burgdorferi. Med. Microbiol. Immunol. 1997, 185:253-260.
88. Stevenson B., El-Hage N., Hines M.A., Miller J.C., Babb K. Differential binding of host complement inhibitor factor H by Borrelia burgdorferi Erp surface proteins: a possible mechanism underlying the expansive host range of Lyme disease spirochetes. Infect. Immun. 2002, 70:491-497.
89. Kurtenbach K., De Michelis S., Etti S., Schafer S.M., Sewell H.S., Brade V., Kraiczy P. Host association of Borrelia burgdorferi sensu lato - the key role of host complement. Trends Microbiol. 2002, 10:74-79.
90. Terra W.R. The origin and functions of the insect peritrophic membrane and peritrophic gel. Arch. Insect Biochem. Physiol. 2001, 47:47-61.
91. Langer R.C., Vinetz J.M. Plasmodium ookinete-secreted chitinase and parasite penetration of the mosquito peritrophic matrix. Trends Parasitol. 2001, 17:269-272.
92. Rogers M.E., Hajmova M., Joshi M.B., Sadlova J., Dwyer D.M., Volf P., Bates P.A. Leishmania chitinase facilitates colonization of sand fly vectors and enhances transmission to mice. Cell. Microbiol. 2008, 10:1363-1372.
93. Walters L.L., Irons K.P., Guzman H., Tesh R.B. Peritrophic envelopes of Lutzomyia spinicrassa (Diptera: Psychodidae). J. Med. Entomol. 1995, 32:711-725.
94. Welburn S.C., Arnold K., Maudlin I., Gooday G.W. Rickettsia-like organisms and chitinase production in relation to transmission of trypanosomes by tsetse flies. Parasitology 1993, 107(Pt 2):141-145.
95. Malaguarnera L. Chitotriosidase: the yin and yang. Cell. Mol. Life Sci. 2006, 63:3018-3029.
96. Barone R., Simpore J., Malaguarnera L., Pignatelli S., Musumeci S. Plasma chitotriosidase activity in acute Plasmodium falciparum malaria. Clin. Chim. Acta 2003, 331:79-85.
97. Di Luca M., Romi R., Severini F., Toma L., Musumeci M., Fausto A.M., Mazzini M., Gambellini G., Musumeci S. High levels of human chitotriosidase hinder the formation of peritrophic membrane in anopheline vectors. Parasitol. Res. 2007, 100:1033-1039.
98. Hollak C.E., van Weely S., van Oers M.H., Aerts J.M. Marked elevation of plasma chitotriosidase activity. A novel hallmark of Gaucher disease. J. Clin. Invest. 1994, 93:1288-1292.
99. Graca-Souza A.V., Maya-Monteiro C., Paiva-Silva G.O., Braz G.R., Paes M.C., Sorgine M.H., Oliveira M.F., Oliveira P.L. Adaptations against heme toxicity in blood-feeding arthropods. Insect Biochem. Mol. Biol. 2006, 36:322-335.
100. Ivanov V.T., Karelin A.A., Philippova M.M., Nazimov I.V., Pletnev V.Z. Hemoglobin as a source of endogenous bioactive peptides: the concept of tissue-specific peptide pool. Biopolymers 1997, 43:171-188.
101. Bulet P., Stocklin R., Menin L. Anti-microbial peptides: from invertebrates to vertebrates. Immunol. Rev. 2004, 198:169-184.
102. Fogaca A.C., da Silva P.I., Miranda M.T., Bianchi A.G., Miranda A., Ribolla P.E., Daffre S. Antimicrobial activity of a bovine hemoglobin fragment in the tick Boophilus microplus. J. Biol. Chem. 1999, 274:25330-25334.
103. Sonenshine D.E., Hynes W.L., Ceraul S.M., Mitchell R., Benzine T. Host blood proteins and peptides in the midgut of the tick Dermacentor variabilis contribute to bacterial control. Exp. Appl. Acarol. 2005, 36:207-223.
104. Nakajima Y., Ogihara K., Taylor D., Yamakawa M. Antibacterial hemoglobin fragments from the midgut of the soft tick, Ornithodoros moubata (Acari: Argasidae). J. Med. Entomol. 2003, 40:78-81.
105. Fraidenraich D., Pena C., Isola E.L., Lammel E.M., Coso O., Anel A.D., Pongor S., Baralle F., Torres H.N., Flawia M.M. Stimulation of Trypanosoma cruzi adenylyl cyclase by an alpha D-globin fragment from Triatoma hindgut: effect on differentiation of epimastigote to trypomastigote forms. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:10140-10144.
106. Garcia E.S., Gonzalez M.S., de Azambuja P., Baralle F.E., Fraidenraich D., Torres H.N., Flawia M.M. Induction of Trypanosoma cruzi metacyclogenesis in the gut of the hematophagous insect vector, Rhodnius prolixus, by hemoglobin and peptides carrying alpha D-globin sequences. Exp. Parasitol. 1995, 81:255-261.
107. Parish C.A., Jiang H., Tokiwa Y., Berova N., Nakanishi K., McCabe D., Zuckerman W., Xia M.M., Gabay J.E. Broad-spectrum antimicrobial activity of hemoglobin. Bioorg. Med. Chem. 2001, 9:377-382.
108. Poole R.K., Hughes M.N. New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol. Microbiol. 2000, 36:775-783.
109. Winterbourn C.C. Reconciling the chemistry and biology of reactive oxygen species. Nat. Chem. Biol. 2008, 4:278-286.
110. Meshnick S.R., Chang K.P., Cerami A. Heme lysis of the bloodstream forms of Trypanosoma brucei. Biochem. Pharmacol. 1977, 26:1923-1928.
111. Orjih A.U., Banyal H.S., Chevli R., Fitch C.D. Hemin lyses malaria parasites. Science 1981, 214:667-669.
112. Droge W. Free radicals in the physiological control of cell function. Physiol. Rev. 2002, 82:47-95.
113. Bogdan C., Rollinghoff M., Diefenbach A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr. Opin. Immunol. 2000, 12:64-76.
114. Pan X., Zhou G., Wu J., Bian G., Lu P., Raikhel A.S., Xi Z. Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E23-E31.
115. Baton L.A., Ranford-Cartwright L.C. Plasmodium falciparum ookinete invasion of the midgut epithelium of Anopheles stephensi is consistent with the Time Bomb model. Parasitology 2004, 129:663-676.
116. Leslie N.R., Bennett D., Lindsay Y.E., Stewart H., Gray A., Downes C.P. Redox regulation of PI 3-kinase signalling via inactivation of PTEN. EMBO J. 2003, 22:5501-5510.
117. Gopalakrishna R., Jaken S. Protein kinase C signaling and oxidative stress. Free Radic. Biol. Med. 2000, 28:1349-1361.
118. Oliveira J.H., Goncalves R.L., Lara F.A., Dias F.A., Gandara A.C., Menna-Barreto R.F., Edwards M.C., Laurindo F.R., Silva-Neto M.A., Sorgine M.H., Oliveira P.L. Blood meal-derived heme decreases ROS levels in the midgut of Aedes aegypti and allows proliferation of intestinal microbiota. PLoS Pathog. 2011, 7:e1001320.
119. Riehle M.A., Brown J.M. Characterization of phosphatase and tensin homolog expression in the mosquito Aedes aegypti: six splice variants with developmental and tissue specificity. Insect Mol. Biol. 2007, 16:277-286.
120. de Assis R.R., Ibraim I.C., Nogueira P.M., Soares R.P., Turco S.J. Glycoconjugates in New World species of Leishmania: polymorphisms in lipophosphoglycan and glycoinositolphospholipids and interaction with hosts. Biochim. Biophys. Acta 2012, 1820:1354-1365.
121. Ropert C., Gazzinelli R.T. Signaling of immune system cells by glycosylphosphatidylinositol (GPI) anchor and related structures derived from parasitic protozoa. Curr. Opin. Microbiol. 2000, 3:395-403.
122. Krishnegowda G., Hajjar A.M., Zhu J., Douglass E.J., Uematsu S., Akira S., Woods A.S., Gowda D.C. Induction of proinflammatory responses in macrophages by the glycosylphosphatidylinositols of Plasmodium falciparum: cell signaling receptors, glycosylphosphatidylinositol (GPI) structural requirement, and regulation of GPI activity. J. Biol. Chem. 2005, 280:8606-8616.
123. Arrighi R.B., Debierre-Grockiego F., Schwarz R.T., Faye I. The immunogenic properties of protozoan glycosylphosphatidylinositols in the mosquito Anopheles gambiae. Dev. Comp. Immunol. 2009, 33:216-223.
124. Guther M.L., Lee S., Tetley L., Acosta-Serrano A., Ferguson M.A. GPI-anchored proteins and free GPI glycolipids of procyclic form Trypanosoma brucei are nonessential for growth, are required for colonization of the tsetse fly, and are not the only components of the surface coat. Mol. Biol. Cell 2006, 17:5265-5274.
125. Kitano H. Systems biology: a brief overview. Science 2002, 295:1662-1664.
126. Drexler A.L., Vodovotz Y., Luckhart S. Plasmodium development in the mosquito: biology bottlenecks and opportunities for mathematical modeling. Trends Parasitol. 2008, 24:333-336.
127. Fruh K., Finlay B., McFadden G. On the road to systems biology of host-pathogen interactions. Future Microbiol. 2010, 5:131-133.
128. da Silva-Nunes M., Moreno M., Conn J.E., Gamboa D., Abeles S., Vinetz J.M., Ferreira M.U. Amazonian malaria: asymptomatic human reservoirs, diagnostic challenges, environmentally driven changes in mosquito vector populations, and the mandate for sustainable control strategies. Acta Trop. 2012, 121:281-291.
129. Trott K.A., Chau J.Y., Hudgens M.G., Fine J., Mfalila C.K., Tarara R.P., Collins W.E., Sullivan J., Luckhart S., Abel K. Evidence for an increased risk of transmission of simian immunodeficiency virus and malaria in a rhesus macaque coinfection model. J. Virol. 2011, 85:11655-11663.