The skin as interface in the transmission of arthropod-borne pathogens

Cellular Microbiology

Volumn 9, Issue 7, 2007, Pages 1630-1640

  Frischknecht, Freddy ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPLASMA; ANIMAL DISEASE; ANTIBODY RESPONSE; ARTHROPOD; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL TRANSMISSION; CELLULAR IMMUNITY; DEFENSE MECHANISM; DERMIS; DRUG RESEARCH; HORSE DISEASE; HOST PATHOGEN INTERACTION; IMMUNOMODULATION; INFECTION RISK; INNATE IMMUNITY; INSECT; INTERNALIZATION; MORTALITY; NEUTROPHIL; NONHUMAN; PARASITE TRANSMISSION; PARASITE VECTOR; PARASITOSIS; PATHOGENESIS; PLAGUE; PLASMODIUM; PRIORITY JOURNAL; RISK ASSESSMENT; RISK FACTOR; SHORT SURVEY; SKIN FUNCTION; SKIN INFECTION; SKIN PROTECTION; SKIN STRUCTURE; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS REPLICATION; VIRUS STRAIN; VIRUS TRANSMISSION;

ANIMALS; ARTHROPOD VECTORS; BACTERIA; BACTERIAL INFECTIONS; CHILD, PRESCHOOL; HOST-PARASITE RELATIONS; HUMANS; MICE; PARASITES; PARASITIC DISEASES; SKIN; VIRUS DISEASES;

ANIMALIA; ARTHROPODA; BACTERIA (MICROORGANISMS); IXODIDA;

EID: 34250732432     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2007.00955.x     Document Type: Short Survey

References (112)

1. Aga, E., Katschinski, D.M., van Zandbergen, G., Laufs, H., Hansen, B., Muller, K., et al. (2002) Inhibition of the spontaneous apoptosis of neutrophil granulocytes by the intracellular parasite Leishmania major. J Immunol 169: 898-905.
2. Akaki, M., and Dvorak, J.A. (2005) A chemotactic response facilitates mosquito salivary gland infection by malaria sporozoites. J Exp Biol 208: 3211-3218.
3. Akarid, K., Arnoult, D., Micic-Polianski, J., Sif, J., Estaquier, J., and Ameisen, J.C. (2004) Leishmania major-mediated prevention of programmed cell death induction in infected macrophages is associated with the repression of mitochondrial release of cytochrome c. J Leukoc Biol 76: 95-103.
4. Akkoyunlu, M., Malawista, S.E., Anguita, J., and Fikrig, E. (2001) Exploitation of interleukin-8-induced neutrophil chemotaxis by the agent of human granulocytic ehrlichiosis. Infect Immun 69: 5577-5588.
5. Allenbach, C., Zufferey, C., Perez, C., Launois, P., Mueller, C., and Tacchini-Cottier, F. (2006) Macrophages induce neutrophil apoptosis through membrane TNF, a process amplified by Leishmania major. J Immunol 176: 6656-6664.
6. Amino, R., Thiberge, S., Martin, B., Celli, S., Shorte, S., Frischknecht, F., and Menard, R. (2006) Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med 12: 220-224.
7. Amino, R., Franke-Fayard, B., Janse, C.J., Waters, A.P., Menard, R., and Frischknecht, F. (2007) Imaging parasites in vivo. In Imaging Cellular and Molecular Biological Function. Frischknecht, F., and Shorte, S.L. (eds). Heidelberg: Springer (in press).
8. Ansell, J., Hamilton, K.A., Pinder, M., Walraven, G.E., and Lindsay, S.W. (2002) Short-range attractiveness of pregnant women to Anopheles gambiae mosquitoes. Trans R Soc Trop Med Hyg 96: 113-116.
9. Arnoult, D., Akarid, K., Grodet, A., Petit, P.X., Estaquier, J., and Ameisen, J.C. (2002) On the evolution of programmed cell death: apoptosis of the unicellular eukaryote Leishmania major involves cysteine proteinase activation and mitochondrion permeabilization. Cell Death Differ 9: 65-81.
10. Bajenoff, M., Egen, J.G., Koo, L.Y., Laugier, J.P., Brau, F., Glaichenhaus, N., and Germain, R.N. (2006) Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25: 989-1001.
11. Baum, J., Papenfuss, A.T., Baum, B., Speed, T.P., and Cowman, A.F. (2006) Regulation of apicomplexan actin-based motility. Nat Rev Microbiol 4: 621-628.
12. Baylis, M., and Mbwabi, A.L. (1995) Feeding behaviour of tsetse flies (Glossina pallidipes Austen) on Trypanosoma-infected oxen in Kenya. Parasitology 110: 297-305.
13. Beier, J.C. (1998) Malaria parasite development in mosquitoes. Annu Rev Entomol 43: 519-543.
14. Belkaid, Y., and Rouse, B.T. (2005) Natural regulatory T cells in infectious disease. Nat Immunol 6: 353-360.
15. Belkaid, Y., Kamhawi, S., Modi, G., Valenzuela, J., Noben-Trauth, N., Rowton, E., et al. (1998) Development of a natural model of cutaneous leishmaniasis: Powerful effects of vector saliva and saliva preexposure on the long-term outcome of Leishmania major infection in the mouse ear dermis. J Exp Med 188: 1941-1953.
16. Belkaid, Y., Piccirillo, C.A., Mendez, S., Shevach, E.M., and Sacks, D.L. (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420: 502-507.
17. Belongia, E.A. (2002) Epidemiology and impact of coinfections acquired from Ixodes ticks. Vector Borne Zoonotic Dis 2: 265-273.
18. Braks, M.A.H., and Takken, W. (1999) Incubated alkaline human sweat but not fresh acidic sweat attracts the malaria mosquito Anopheles gambiae sensu stricto. J Chem Ecol 25: 663-672.
19. Braks, M.A., Anderson, R.A., and Knols, B.G. (1999) Infochemicals in mosquito host selection: Human skin microflora and Plasmodium parasites. Parasitol Today 15: 409-413.
20. Burke, G., Wikel, S.K., Spielman, A., Telford, S.R., McKay, K., and Krause, P.J. (2005) Hypersensitivity to ticks and Lyme disease risk. Emerg Infect Dis 11: 36-41.
21. Caljon, G., Van Den Abbeele, J., Stijlemans, B., Coosemans, M., De Baetselier, P., and Magez, S. (2006) Tsetse fly saliva accelerates the onset of Trypanosoma brucei infection in a mouse model associated with a reduced host inflammatory response. Infect Immun 74: 6324-6330.
22. Carlyon, J.A., and Fikrig, E. (2003) Invasion and survival strategies of Anaplasma phagocytophilum. Cell Microbiol 5: 743-754.
23. Cohuet, A., Osta, M.A., Morlais, I., Awono-Ambene, P.H., Michel, K., Simard, F., et al. (2006) Anopheles and Plasmodium: From laboratory models to natural systems in the field. EMBO Rep 7: 1285-1289.
24. Demeure, C.E., Brahimi, K., Hacini, F., Marchand, F., Peronet, R., Huerre, M., et al. (2005) Anopheles mosquito bites activate cutaneous mast cells leading to a local inflammatory response and lymph node hyperplasia. J Immunol 174: 3932-3940.
25. Depinay, N., Hacini, F., Beghdadi, W., Peronet, R., and Mecheri, S. (2006) Mast cell-dependent down-regulation of antigen-specific immune responses by mosquito bites. J Immunol 176: 4141-4146.
26. Dogan, E.B., Ayres, J.W., and Rossignol, P.A. (1999) Behavioural mode of action of deet: Inhibition of lactic acid attraction. Med Vet Entomol 13: 97-100.
27. Dumler, J.S., Choi, K.S., Garcia-Garcia, J.C., Barat, N.S., Scorpio, D.G., Garyu, J.W., et al. (2005) Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerg Infect Dis 11: 1828-1834.
28. Fallman, M., and Gustavsson, A. (2005) Cellular mechanisms of bacterial internalization counteracted by Yersinia. Int Rev Cytol 246: 135-188.
29. Ferguson, H.M., and Read, A.F. (2004) Mosquito appetite for blood is stimulated by Plasmodium chabaudi infections in themselves and their vertebrate hosts. Malar J 3: 12.
30. Frischknecht, F., Baldacci, P., Martin, B., Zimmer, C., Thiberge, S., Olivo-Marin, J.C., et al. (2004) Imaging movement of malaria parasites during transmission by Anopheles mosquitoes. Cell Microbiol 6: 687-694.
31. Ge, Y., and Rikihisa, Y. (2006) Anaplasma phagocytophilum delays spontaneous human neutrophil apoptosis by modulation of multiple apoptotic pathways. Cell Microbiol 8: 1406-1416.
32. Gokce, H.I., Ross, G., and Woldehiwet, Z. (1999) Inhibition of phagosome-lysosome fusion in ovine polymorphonuclear leucocytes by Ehrlichia (Cytoecetes) phagocytophila. J Comp Pathol 120: 369-381.
33. Gomes, R.B., Brodskyn, C., de Oliveira, C.I., Costa, J., Miranda, J.C., Caldas, A., et al. (2002) Seroconversion against Lutzomyia longipalpis saliva concurrent with the development of anti-Leishmania chagasi delayed-type hypersensitivity. J Infect Dis 186: 1530-1534.
34. Goodman, J.L., Nelson, C.M., Klein, M.B., Hayes, S.F., and Weston, B.W. (1999) Leukocyte infection by the granulocytic ehrlichiosis agent is linked to expression of a selectin ligand. J Clin Invest 103: 407-412.
35. Green, S., and Rothman, A. (2006) Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr Opin Infect Dis 19: 429-436.
36. Heintzelman, M.B. (2006) Cellular and molecular mechanics of gliding locomotion in eukaryotes. Int Rev Cytol 251: 79-129.
37. Henson, P.M., Bratton, D.L., and Fadok, V.A. (2001) The phosphatidylserine receptor: A crucial molecular switch? Nat Rev Mol Cell Biol 2: 627-633.
38. Herron, M.J., Nelson, C.M., Larson, J., Snapp, K.R., Kansas, G.S., and Goodman, J.L. (2000) Intracellular parasitism by the human granulocytic ehrlichiosis bacterium through the P-selectin ligand, PSGL-1. Science 288: 1653-1656.
39. Herron, M.J., Ericson, M.E., Kurtti, T.J., and Munderloh, U.G. (2005) The interactions of Anaplasma phagocytophilum, endothelial cells, and human neutrophils. Ann N Y Acad Sci 1063: 374-382.
40. Hinnebusch, B.J. (2005) The evolution of flea-borne transmission in Yersinia pestis. Curr Issues Mol Biol 7: 197-212.
41. Holden, K., Hodzic, E., Feng, S., Freet, K.J., Lefebvre, R.B., and Barthold, S.W. (2005) Coinfection with Anaplasma phagocytophilum alters Borrelia burgdorferi population distribution in C3H/HeN mice. Infect Immun 73: 3440-3444.
42. Huff, C.G. (1949) Life cycles of malaria parasites with special reference to the newer knowledge of pre-erythrocytic stages. In Malariology. Boyd, M.F. (ed.). Philadelphia: W.B. Saunders, pp. 54-64.
43. Iezzi, G., Frohlich, A., Ernst, B., Ampenberger, F., Saeland, S., Glaichenhaus, N., and Kopf, M. (2006) Lymph node resident rather than skin-derived dendritic cells initiate specific T cell responses after Leishmania major infection. J Immunol 177: 1250-1256.
44. Jones, L.D., Davies, C.R., Steele, G.M., and Nuttall, P.A. (1987) A novel mode of arbovirus transmission involving a nonviremic host. Science 237: 775-777.
45. de Jong, R., and Knols, B.G. (1995) Olfactory responses of host-seeking Anopheles gambiae s.s. Giles (Diptera: Culicidae). Acta Trop 59: 333-335.
46. Kamhawi, S., Belkaid, Y., Modi, G., Rowton, E., and Sacks, D. (2000) Protection against cutaneous leishmaniasis resulting from bites of uninfected sand flies. Science 290: 1351-1354.
47. Kissenpfennig, A., and Malissen, B. (2006) Langerhans cells - revisiting the paradigm using genetically engineered mice. Trends Immunol 27: 132-139.
48. Knols, B.G.J., Loon, J.J.A., Cork, A., Robinson, R.D., Adam, W., Meijerink, J., et al. (1997) Behavioural and electrophysiological responses of the female malaria mosquitoe Anopheles gambiae (Diptera: Culicidae) to Limburger cheese volatiles. Bull Entomol Res 87: 151-159.
49. Krettli, A.U., and Dantas, L.A. (2000) Which routes do Plasmodium sporozoites use for successful infections of vertebrates? Infect Immun 68: 3064-3065.
50. Labuda, M., and Nuttall, P.A. (2004) Tick-borne viruses. Parasitology 129 (Suppl.): S221-S245.
51. Labuda, M., Austyn, J.M., Zuffova, E., Kozuch, O., Fuchsberger, N., Lysy, J., and Nuttall, P.A. (1996) Importance of localized skin infection in tick-borne encephalitis virus transmission. Virology 219: 357-366.
52. Labuda, M., Kozuch, O., Zuffova, E., Eleckova, E., Hails, R.S., and Nuttall, P.A. (1997) Tick-borne encephalitis virus transmission between ticks cofeeding on specific immune natural rodent hosts. Virology 235: 138-143.
53. Labuda, M., Trimnell, A.R., Lickova, M., Kazimirova, M., Davies, G.M., Lissina, O., et al. (2006) An antivector vaccine protects against a lethal vector-borne pathogen. PLoS Pathog 2: E27.
54. Laskay, T., van Zandbergen, G., and Solbach, W. (2003) Neutrophil granulocytes - Trojan horses for Leishmania major and other intracellular microbes? Trends Microbiol 11: 210-214.
55. Lefevre, T., Koella, J.C., Renaud, F., Hurd, H., Biron, D.G., and Thomas, F. (2006) New prospects for research on manipulation of insect vectors by pathogens. PLoS Pathog 2: E72.
56. Lindova, J., Novotna, M., Havlicek, J., Jozifkova, E., Skallova, A., Kolbekova, P., et al. (2006) Gender differences in behavioural changes induced by latent toxoplasmosis. Int J Parasitol 36: 1485-1492.
57. Lloyd, O.C., and Sommerville, T. (1949) The fate of sporozoites of Plasmodium cynomolgi injected into the skin of rhesus monkeys. Proc Path Soc 61: 144-146.
58. Lorange, E.A., Race, B.L., Sebbane, F., and Joseph Hinnebusch, B. (2005) Poor vector competence of fleas and the evolution of hypervirulence in Yersinia pestis. J Infect Dis 191: 1907-1912.
59. Lozach, P.Y., Burleigh, L., Staropoli, I., Navarro-Sanchez, E., Harriague, J., Virelizier, J.L., et al. (2005) Dendritic cell-specific intercellular adhesion molecule 3-grabbing non-integrin (DC-SIGN)-mediated enhancement of dengue virus infection is independent of DC-SIGN internalization signals. J Biol Chem 280: 23698-23708.
60. Ma, J., Chen, T., Mandelin, J., Ceponis, A., Miller, N.E., Hukkanen, M., et al. (2003) Regulation of macrophage activation. Cell Mol Life Sci 60: 2334-2346.
61. McKenzie, F.E., and Bossert, W.H. (1997) Mixed-species Plasmodium infections of Anopheles (Diptera: Culicidae). J Med Entomol 34: 417-425.
62. McLachlan, J.B., Hart, J.P., Pizzo, S.V., Shelburne, C.P., Staats, H.F., Gunn, M.D., and Abraham, S.N. (2003) Mast cell-derived tumor necrosis factor induces hypertrophy of draining lymph nodes during infection. Nat Immunol 4: 1199-1205.
63. Malaviya, R., Ikeda, T., Ross, E., and Abraham, S.N. (1996) Mast cell modulation of neutrophil influx and bacterial clearance at sites of infection through TNF-alpha. Nature 381: 77-80.
64. Marketon, M.M., DePaolo, R.W., DeBord, K.L., Jabri, B., and Schneewind, O. (2005) Plague bacteria target immune cells during infection. Science 309: 1739-1741.
65. Matuschewski, K. (2006) Vaccine development against malaria. Curr Opin Immunol 18: 449-457.
66. Modis, Y., Ogata, S., Clements, D., and Harrison, S.C. (2004) Structure of the dengue virus envelope protein after membrane fusion. Nature 427: 313-319.
67. Moll, H., Fuchs, H., Blank, C., and Rollinghoff, M. (1993) Langerhans cells transport Leishmania major from the infected skin to the draining lymph node for presentation to antigen-specific T cells. Eur J Immunol 23: 1595-1601.
68. Moore, J. (2002) Parasites and the Behaviour of Animals. Oxford: Oxford University Press.
69. Morris, R.V., Shoemaker, C.B., David, J.R., Lanzaro, G.C., and Titus, R.G. (2001) Sandfly maxadilan exacerbates infection with Leishmania major and vaccinating against it protects against L. major infection. J Immunol 167: 5226-5230.
70. Munderloh, U.G., Lynch, M.J., Herron, M.J., Palmer, A.T., Kurtti, T.J., Nelson, R.D., and Goodman, J.L. (2004) Infection of endothelial cells with Anaplasma marginale and A. phagocytophilum. Vet Microbiol 101: 53-64.
71. Murray, H.W., Berman, J.D., Davies, C.R., and Saravia, N.G. (2005) Advances in leishmaniasis. Lancet 366: 1561-1577.
72. Njiru, B.N., Mukabana, W.R., Takken, W., and Knols, B.G. (2006) Trapping of the malaria vector Anopheles gambiae with odour-baited MM-X traps in semi-field conditions in western Kenya. Malar J 5: 39.
73. Nuttall, P.A. (1998) Displaced tick-parasite interactions at the host interface. Parasitology 116 (Suppl.): S65-S72.
74. Nuttall, P.A., and Labuda, M. (2004) Tick-host interactions: saliva-activated transmission. Parasitology 129 (Suppl.): S177-S189.
75. O'Shea, B., Rebollar-Tellez, E., Ward, R.D., Hamilton, J.G., el Naiem, D., and Polwart, A. (2002) Enhanced sandfly attraction to Leishmania-infected hosts. Trans R Soc Trop Med Hyg 96: 117-118.
76. Paul, R.E., Nu, V.A., Krettli, A.U., and Brey, P.T. (2002) Interspecific competition during transmission of two sympatric malaria parasite species to the mosquito vector. Proc Biol Sci 269: 2551-2557.
77. Perry, R.D., and Fetherston, J.D. (1997) Yersinia pestis - etiologic agent of plague. Clin Microbiol Rev 10: 35-66.
78. Prudencio, M., Rodriguez, A., and Mota, M.M. (2006) The silent path to thousands of merozoites: The Plasmodium liver stage. Nat Rev Microbiol 4: 849-856.
79. Rahman, M.M., and McFadden, G. (2006) Modulation of tumor necrosis factor by microbial pathogens. PLoS Pathog 2: E4.
80. Ramamoorthi, N., Narasimhan, S., Pal, U., Bao, F., Yang, X.F., Fish, D., et al. (2005) The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 436: 573-577.
81. Randolph, G.J., Angeli, V., and Swartz, M.A. (2005) Dendritic-cell trafficking to lymph nodes through lymphatic vessels. Nat Rev Immunol 5: 617-628.
82. Reneer, D.V., Kearns, S.A., Yago, T., Sims, J., Cummings, R.D., McEver, R.P., and Carrlyon, J.A. (2006) Characterization of a sialic acid- and P-selectin glycoprotein ligand-1-independent adhesin activity in the granulocytotropic bacterium Anaplasma phagocytophilum. Cell Microbiol 8: 1972-1984.
83. Ribeiro, J.M., and Francischetti, I.M. (2003) Role of arthropod saliva in blood feeding: Sialome and post-sialome perspectives. Annu Rev Entomol 48: 73-88.
84. Ribeiro, J.M., Rossignol, P.A., and Spielman, A. (1984) Role of mosquito saliva in blood vessel location. J Exp Biol 108: 1-7.
85. Rikihisa, Y. (2006) Ehrlichia subversion of host innate responses. Curr Opin Microbiol 9: 95-101.
86. Rogers, M.E., Ilg, T., Nikolaev, A.V., Ferguson, M.A., and Bates, P.A. (2004) Transmission of cutaneous leishmaniasis by sand flies is enhanced by regurgitation of fPPG. Nature 430: 463-467.
87. Rogers, M.E., Sizova, O.V., Ferguson, M.A., Nikolaev, A.V., and Bates, P.A. (2006) Synthetic glycovaccine protects against the bite of leishmania-infected sand flies. J Infect Dis 194: 512-518.
88. Rossignol, P.A., Ribeiro, J.M., and Spielman, A. (1984) Increased intradermal probing time in sporozoite-infected mosquitoes. Am J Trop Med Hyg 33: 17-20.
89. Rossignol, P.A., Ribeiro, J.M., Jungery, M., Turell, M.J., Spielman, A., and Bailey, C.L. (1985) Enhanced mosquito blood-finding success on parasitemic hosts: Evidence for vector-parasite mutualism. Proc Natl Acad Sci USA 82: 7725-7727.
90. Sakuntabhai, A., Turbpaiboon, C., Casademont, I., Chuansumrit, A., Lowhnoo, T., Kajaste-Rudnitski, A., et al. (2005) A variant in the CD209 promoter is associated with severity of dengue disease. Nat Genet 37: 507-513.
91. Schaub, G.A. (2006) Parasitogenic alterations of vector behaviour. Int J Med Microbiol 296 (Suppl. 40): 37-40.
92. Sebbane, F., Jarrett, C.O., Gardner, D., Long, D., and Hinnebusch, B.J. (2006) Role of the Yersinia pestis plasminogen activator in the incidence of distinct septicemic and bubonic forms of flea-borne plague. Proc Natl Acad Sci USA 103: 5526-5530.
93. Shaha, C. (2006) Apoptosis in Leishmania species & its relevance to disease pathogenesis. Indian J Med Res 123: 233-244.
94. Sharp, L.L., Jameson, J.M., Witherden, D.A., Komori, H.K., and Havran, W.L. (2005) Dendritic epidermal T-cell activation. Crit Rev Immunol 25: 1-18.
95. Shirai, O., Tsuda, T., Kitagawa, S., Naitoh, K., Seki, T., Kamimura, K., and Morohashi, M. (2002) Alcohol ingestion stimulates mosquito attraction. J Am Mosq Control Assoc 18: 91-96.
96. Sidjanski, S., and Vanderberg, J.P. (1997) Delayed migration of Plasmodium sporozoites from the mosquito bite site to the blood. Am J Trop Med Hyg 57: 426-429.
97. Sodeinde, O.A., Subrahmanyam, Y.V., Stark, K., Quan, T., Bao, Y., and Goguen, J.D. (1992) A surface protease and the invasive character of plague. Science 258: 1004-1007.
98. Takken, W., and Knols, B.G. (1999) Odor-mediated behavior of Afrotropical malaria mosquitoes. Annu Rev Entomol 44: 131-157.
99. Tassaneetrithep, B., Burgess, T.H., Granelli-Piperno, A., Trumpfheller, C., Finke, J., Sun, W., et al. (2003) DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J Exp Med 197: 823-829.
100. Thomas, V., Anguita, J., Barthold, S.W., and Fikrig, E. (2001) Coinfection with Borrelia burgdorferi and the agent of human granulocytic ehrlichiosis alters murine immune responses, pathogen burden, and severity of Lyme arthritis. Infect Immun 69: 3359-3371.
101. Titus, R.G., and Ribeiro, J.M. (1988) Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239: 1306-1308.
102. Turell, M.J., Rossignol, P.A., Spielman, A., Rossi, C.A., and Bailey, C.L. (1984) Enhanced arboviral transmission by mosquitoes that concurrently ingested microfilariae. Science 225: 1039-1041.
103. Urban, C.F., Lourido, S., and Zychlinsky, A. (2006) How do microbes evade neutrophil killing? Cell Microbiol 8: 1687-1696.
104. Valenzuela, J.G., Belkaid, Y., Garfield, M.K., Mendez, S., Kamhawi, S., Rowton, E.D., et al. (2001) Toward a defined anti-Leishmania vaccine targeting vector antigens: Characterization of a protective salivary protein. J Exp Med 194: 331-342.
105. Vanderberg, J.P., and Frevert, U. (2004) Intravital microscopy demonstrating antibody-mediated immobilisation of Plasmodium berghei sporozoites injected into skin by mosquitoes. Int J Parasitol 34: 991-996.
106. Vaughan, J.A., and Turell, M.J. (1996) Facilitation of Rift Valley fever virus transmission by Plasmodium berghei sporozoites in Anopheles stephensi mosquitoes. Am J Trop Med Hyg 55: 407-409.
107. Vaughan, J.A., Scheller, L.F., Wirtz, R.A., and Azad, A.F. (1999) Infectivity of Plasmodium berghei sporozoites delivered by intravenous inoculation versus mosquito bite: Implications for sporozoite vaccine trials. Infect Immun 67: 4285-4289.
108. Wanderley, J.L., Benjamin, A., Real, F., Bonomo, A., Moreira, M.E., and Barcinski, M.A. (2005) Apoptotic mimicry: An altruistic behavior in host/ Leishmania interplay. Braz J Med Biol Res 38: 807-812.
109. Wu, S.J., Grouard-Vogel, G., Sun, W., Mascola, J.R., Brachtel, E., Putvatana, R., et al. (2000) Human skin Langerhans cells are targets of dengue virus infection. Nat Med 6: 816-820.
110. van Zandbergen, G., Klinger, M., Mueller, A., Dannenberg, S., Gebert, A., Solbach, W., and Laskay, T. (2004) Cutting edge: Neutrophil granulocyte serves as a vector for Leishmania entry into macrophages. J Immunol 173: 6521-6525.
111. van Zandbergen, G., Bollinger, A., Wenzel, A., Kamhawi, S., Voll, R., Klinger, M., et al. (2006) Leishmania disease development depends on the presence of apoptotic promastigotes in the virulent inoculum. Proc Natl Acad Sci USA 103: 13837-13842.
112. Zwiebel, L.J., and Takken, W. (2004) Olfactory regulation of mosquito-host interactions. Insect Biochem Mol Biol 34: 645-652.