SALIVARY GLAND EXTRACTS OF CULICOIDES SONORENSIS INHIBIT MURINE LYMPHOCYTE PROLIFERATION AND NO PRODUCTION BY MACROPHAGES

JEANETTE V. BISHOP Department of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado; Arthropod-Borne Animal Diseases Research Laboratory, USDA–ARS, Laramie, Wyoming; SCYNEXIS, Research Triangle Park, North Carolina; Florida Medical Entomology Laboratory, Department of Entomology and Nematology, University of Florida, IFAS, Vero Beach, Florida

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J. SANTIAGO MEJIA Department of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado; Arthropod-Borne Animal Diseases Research Laboratory, USDA–ARS, Laramie, Wyoming; SCYNEXIS, Research Triangle Park, North Carolina; Florida Medical Entomology Laboratory, Department of Entomology and Nematology, University of Florida, IFAS, Vero Beach, Florida

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ADALBERTO A. PÉREZ DE LEÓN Department of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado; Arthropod-Borne Animal Diseases Research Laboratory, USDA–ARS, Laramie, Wyoming; SCYNEXIS, Research Triangle Park, North Carolina; Florida Medical Entomology Laboratory, Department of Entomology and Nematology, University of Florida, IFAS, Vero Beach, Florida

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WALTER J. TABACHNICK Department of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado; Arthropod-Borne Animal Diseases Research Laboratory, USDA–ARS, Laramie, Wyoming; SCYNEXIS, Research Triangle Park, North Carolina; Florida Medical Entomology Laboratory, Department of Entomology and Nematology, University of Florida, IFAS, Vero Beach, Florida

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RICHARD G. TITUS Department of Microbiology, Immunology and Pathology, College of Veterinary Medicine and Biomedical Sciences, Colorado State University, Fort Collins, Colorado; Arthropod-Borne Animal Diseases Research Laboratory, USDA–ARS, Laramie, Wyoming; SCYNEXIS, Research Triangle Park, North Carolina; Florida Medical Entomology Laboratory, Department of Entomology and Nematology, University of Florida, IFAS, Vero Beach, Florida

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Culicoides biting midges serve as vectors of pathogens affecting humans and domestic animals. Culicoides sonorensis is a vector of several arboviruses in North American that cause substantial economic losses to the US livestock industry. Previous studies showed that C. sonorensis saliva, like the saliva of many hematophagous arthropods, contains numerous pharmacological agents that affect hemostasis and early events in the inflammatory response, which may enhance the infectivity of Culicoides-borne pathogens. This paper reports on the immunomodulatory properties of C. sonorensis salivary gland extracts on murine immune cells and discusses the possible immunomodulatory role of C. sonorensis saliva in vesicular stomatitis virus infection of vertebrate hosts. Splenocytes treated with C. sonorensis mitogens were significantly affected in their proliferative response, and peritoneal macrophages secreted significantly less NO. A 66-kDa glycoprotein was purified from C. sonorensis salivary gland extract, which may be in part responsible for these observations and may be considered as a vaccine candidate.

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  • 1

    Mercer DR, Castillo-Pizango MJ, 2005. Changes in relative species compositions of biting midges (Diptera: ceratopogonidae) and an outbreak of Oropouche virus in Iquitos, Peru. J Med Entomol 42 :554–558.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Tabachnick WJ, 1996. Culicoides variipennis and bluetongue—virus epidemiology in the United States. Annu Rev Entomol 41 :23–43.

  • 3

    Price DA, Hardy WT, 1954. Isolation of the bluetongue virus from Texas sheep—Culicoides shown to be a vector. J Am Vet Med Assoc 124 :255–258.

  • 4

    Titus RG, Bishop JV, Mejia JS, 2006. The immunomodulatory factors of arthropod saliva and the potential for these factors to serve as vaccine targets to prevent pathogen transmission. Parasite Immunol 28 :131–141.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Andersen JF, Gudderra NP, Francischetti IM, Ribeiro JM, 2005. The role of salivary lipocalins in blood feeding by Rhodnius prolixus. Arch Insect Biochem Physiol 58 :97–105.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Champagne DE, 2004. Antihemostatic strategies of blood-feeding arthropods. Curr Drug Targets Cardiovasc Haematol Disord 4 :375–396.

  • 7

    de Almeida MC, Vilhena V, Barral A, Barral-Netto M, 2003. Leishmanial infection: analysis of its first steps. A review. Mem Inst Oswaldo Cruz 98 :861–870.

  • 8

    Nuttall PA, Labuda M, 2003. Dynamics of infection in tick vectors and at the tick-host interface. Review. Adv Virus Res 60 :233–272.

  • 9

    Ribeiro JM, Francischetti IM, 2003. Role of arthropod saliva in blood feeding: sialome and post-sialome perspectives. Annu Rev Entomol 48 :73–88.

  • 10

    Schoeler GB, Wikel SK, 2001. Modulation of host immunity by haematophagous arthropods. Ann Trop Med Parisitol 95 :755–771.

  • 11

    Tabachnick WJ, 2000. Pharmacological factors in the saliva of blood-feeding insects. Ann N Y Acad Sci 916 :444–452.

  • 12

    Kamhawi S, 2000. The biological and immunomodulatory properties of sand fly saliva and its role in the establishment of Leishmania infections. Microbes Infect 2 :1765–1773.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Bowman AS, Coons LB, Needham GR, Sauer JR, 1997. Tick saliva: Recent advances and implications for vector competence. Med Vet Entomol 11 :277–285.

  • 14

    Cupp EW, Cupp MS, 1997. Black fly (Diptera: Simuliidae) salivary secretions importance in vector competence and disease. J Med Entomol 34 :87–94.

  • 15

    Drolet BS, Campbell CL, Stuart MA, Wilson WC, 2005. Vector competence of Culicoides sonorensis (Diptera:Ceratopogonidae) for vesicular stomatitis virus. J Med Entomol 42 :409–418.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Nunamaker RA, Pérez de León AA, Campbell CL, Lonning SM, 2000. Oral infection of Culicoides sonorensis (Diptera:Ceratopogonidae) by vesicular stomatitis virus. J Med Entomol 37 :784–786.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Pérez de León AA, Tabachnick WJ, 2006a. Transmission of vesicular stomatitis virus to cattle by the biting midge, Culicoides sonorensis (Diptera: Ceratopogonidae). J Med Entomol 43 :323–329.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Pérez de León AA, O’Toole D, Tabachnick WJ, 2006. Infection of guinea pigs with vesicular stomatitis virus transmitted by the biting midge, Culicoides sonorensis (Diptera: Ceratopogonidae). J Med Entomol 43 :568–573.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Pérez de León AA, Ribeiro JM, Tabachnick WJ, Valenzuela JG, 1997. Identification of a salivary vasodilator in the primary North American vector of bluetongue viruses, Culicoides variipennis. Am J Trop Med Hyg 57 :375–381.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Pérez de León AA, Valenzuela JG, Tabachnick WJ, 1998. Anticoagulant activity in salivary glands of the insect vector Culicoides variipennis sonorensis by an inhibitor of factor Xa. Exp Parasitol 88 :121–130.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Pérez de León AA, Tabachnick WJ, 1996. Apyrase activity and adenosine diphosphate induced platelet aggregation inhibition by the salivary gland proteins of Culicoides variipennis, the North American vector of bluetongue viruses. Vet Parasitol 61 :327–338.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Pérez de León AA, O’Toole TD, Schmidtmann ET, Titus RG, Tabachnick WJ, 1997. Insect blood-feeding and the transmission of arboviruses and vesiculoviruses. Proc US Animal Health Assoc 101 :29–34.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Hunt G, 1994. A procedural manual for the large-scale rearing of the biting midge, Culicoides variipennis (Diptera: Ceratopogonidae). US Dep Agric Research Service Tech Bull 121 :1–68.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Urioste S, Hall LR, Telford SR, Titus RG, 1994. Saliva of the Lyme disease vector, Ixodes dammini, blocks cell activation by a nonprostaglandin E2-dependent mechanism. J Exp Med 180 :1077–1086.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Titus RG, Kelso A, Louis JA, 1984. Intracellular destruction of Leishmania tropica by macrophages activated with macrophage activating factor/interferon. Clin Exp Immunol 55 :157–165.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Chakkalath HR, Titus RG, 1994. Leishmania major-parasitized macrophages augment Th2-type T cell activation. J Immunol 153 :4378–4387.

  • 27

    Green SJ, Nacy CA, Meltzer MS, 1991. Cytokine-induced synthesis of nitrogen oxides in macrophages: A protective host response to Leishmania and other intracellular pathogens. J Leukoc Biol 50 :93–103.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Liew FY, Cox FE, 1991. Nonspecific defense mechanism: The role of nitric oxide. Immunol Today 12 :A17–A21.

  • 29

    Mauel J, Corradin SB, Buchmuller Rouiller Y, 1991. Nitrogen and oxygen metabolites and the killing of Leishmania by activated murine macrophages. Res Immunol 142 :577–580.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Morris RV, Shoemaker CB, David JR, Lanzaro GC, Titus RG, 2001. Sandfly maxadilan exacerbates infection with Leishmania major and vaccinating against it protects against L. major infection. J Immunol 167 :5226–5230.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Wikel SK, Ramachandra RN, Bergman DK, Burkot TR, Piesman J, 1997. Infestation with pathogen-free nymphs of the tick Ixodes scapularis induces host resistance to transmission of Borrelia burgdorferi by ticks. Infect Immun 65 :335–338.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Davies CR, Mazloumi Gavgani AS, 1999. Age, acquired immunity and the risk of visceral leishmaniasis: a prospective study in Iran. Parasitology 119 :247–257.

  • 33

    Gomes RB, Brodskyn C, de Oliveira CI, Costa J, Miranda JC, Caldas A, Valenzuela JG, Barral-Netto M, Barral A, 2002. Seroconversion against Lutzomyia longipalpis saliva concurrent with the development of anti-Leishmania chagasi delayed-type hypersensitivity. J Infect Dis 186 :1530–1534.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Gallucci S, Lolkema M, Matzinger P, 1999. Natural adjuvants: Endogenous activators of dendritic cells. Nat Med 5 :1249–1255.

  • 35

    Shi Y, Zheng W, Rock KL, 2000. Cell injury releases endogenous adjuvants that stimulate cytotoxic T cell responses. Proc Natl Acad Sci USA 97 :14590–14595.

  • 36

    Scaffidi P, Misteli T, Bianchi ME, 2002. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418 :191–195.

  • 37

    Hollister J, Grabenhorst E, Nimtz M, Conradt H, Jarvis DL, 2002. Engineering the protein N-glycosylation pathway in insect cells for production of biantennary, complex N-glycans. Biochemistry 41 :15093–15104.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Dinglasan RR, Valenzuela JG, Azad AF, 2005. Sugar epitopes as potential universal disease transmission blocking targets. Insect Biochem Mol Biol 35 :1–10.

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