The art of stealing blood requires that arthropods have the ability to circumvent the efficient mechanisms vertebrates have in place to maintain hemostasis, including platelet aggregation, vasoconstriction, and clotting. This is accomplished using a remarkable array of salivary proteins. We have taken a comparative approach to the study of these salivary components, working with saliva from mosquitoes, triatomine bugs, and ticks. Novel proteins and peptides identified to date include apyrases (ATP/ADP diphosphohydrolases), lipocalin-type proteins that inhibit platelet responses to collagen and ADP, tachykinin peptides which closely mimic endogenous vasodilators, and a family of nitrophorins that function as a storage and transport system for nitric oxide. Our focus also includes the immune response that develops in the host in response to salivary antigens. This response is also manipulated by components of the saliva, and we are currently characterizing these immunomodulators. We believe that the vector modifies the environment of the bite site in a variety of ways that tend to favor parasite or pathogen entry into the host, and we anticipate that identification of the salivary components involved and their mode of action will lead to novel strategies for blocking transmission.

Courses Taught

ENTO 3650 Medical Entomology

This undergraduate survey course introduces students to the concepts and principles of medical and veterinary entomology. The major groups of arthropods associated with disease are discussed. Laboratory exercises emphasize the recognition and identification of medically important arthropods. This course is offered every spring semester.

ENTO 8650 Vector Biology
This course emphasizes recent advances in the understanding of vector physiology, vector-host interactions, and vector-parasite interactions. Selected topics are introduced in an overview lecture, and recent papers are provided for critical discussion. The application of molecular biology techniques to problems in vector biology is highlighted. This course is offered in alternating years.

ENTO 8570 Molecular Entomology
This course is team taught with Drs. M. Brown, M. Adang, and J. Willis. After an introductory lecture students are provided with recent papers for critical discussion. Discussions are student-led. Critical advances in all aspects of insect molecular biology are emphasized. This course alternates with Vector Biology.

ENTO 8590 Medical and Urban Entomology
This course is team taught with Dr. Brian Forschler. We will survey the major arthropod groups involved in causing disease or otherwise impacting quality of life, particularly in the urban environment. A format of lectures and assigned readings will be followed, including laboratory exercises in the identification and control of relevant arthropods. An insect collection will be required. This course is offered fall semester even numbered years.

Selected Publications

Ribeiro, J. M. C., J. M. H. Hazzard, R. H. Nussenzveig, D. E. Champagne, and F. A. Walker. 1993. Reversible binding of nitric oxide by a salivary heme protein from a bloodsucking insect. Science 260: 539-541.

Champagne, D. E. and J. M. C. Ribeiro. 1994. Sialokinin I and II: Vasodilatory tachykinins from the yellow fever mosquito Aedes aegypti. Proceedings of the National Academy of Science U.S.A. 91: 138-142.

Champagne, D. E. 1994. The role of salivary vasodilators in bloodfeeding and parasite transmission. Parasitology Today 10: 430-433.

Champagne, D. E., R. H. Nussenzveig, and J. M. C. Ribeiro. 1995. Purification, partial characterization, and cloning of nitric oxide-carrying heme proteins (Nitrophorins) from salivary glands of the blood-sucking insect Rhodnius prolixus. Journal of Biological Chemistry 270: 8691-8695.

Champagne, D. E., C. T. Smartt, A. A. James, and J. M. C. Ribeiro. 1995. The salivary gland-specific apyrase of the mosquito Aedes aegypti is a member of the 5'-nucleotidase family. Proceedings of the National Academy of Science U. S. A. 92: 694-698.

Abebe, M., M. S. Cupp, D. E. Champagne, and E. W. Cupp. 1995. Simulidin: a black fly (Simulium vittatum) salivary gland protein with anti-thrombin activity. Journal of Insect Physiology 41: 1001-1006.

Andersen, J. F., D. E. Champagne, A. Weichsel, J. M. Ribeiro, C. A. Balfour, V. Dress, and W. R. Montfort. 1997. Nitric oxide binding and crystallization of recombinant nitrophorin I, a nitric oxide transport protein from the blood-sucking bug Rhodnius prolixus. Biochemistry 36: 4423-4428.

Brown, M. R., R. Graf, K. M. Swiderek, D. Fendley, T. H. Stracker, D. E. Champagne, and A. O. Lea. 1998. Identification of a steroidogenic neurohormone in female mosquitoes. Journal of Biological Chemistry 273: 3967-3971.

Weichsel, A., J. F. Andersen, D. E. Champagne, F. A. Walker, and W. R. Montfort. 1998. Crystal structures of a nitric oxide transport protein from a blood-sucking insect. Nature Structural Biology 5: 304-309.

Cupp, M. S., J. M. Ribeiro, D. E. Champagne, and E. W. Cupp. 1998. Analyses of cDNA and recombinant protein for a potent vasoactive protein in saliva of a blood-feeding black fly, Simulium vittatum. Journal of Experimental Biology 201: 1553-1561.

Andersen, J. F., A. Weichsel, C. A. Balfour, D. E. Champagne, and W. R. Montfort. 1998. The crystal structure of nitrophorin 4 at 1.5 A resolution: transport of nitric oxide by a lipocalin-based heme protein. Structure 6: 1315-1327.

Beerntsen, B. T., D. E. Champagne, J. L. Coleman, Y. A. Campos, and A. A. James. 1999. Characterization of the Sialokinin I gene encoding the salivary vasodilator of the yellow fever mosquito, Aedes aegypti. Insect Molecular Biology 8: 459-467.

Francischetti, I. M., J. M. Ribeiro, D. Champagne, and J. Andersen. 2000. Purification, cloning, expression, and mechanism of action of a novel platelet aggregation inhibitor from the salivary gland of the blood-sucking bug, Rhodnius prolixus. Journal of Biological Chemistry 275:12639-12650.

Andersen, J. F., X. D. Ding, C. Balfour, T. K. Shokhireva, D. E. Champagne, F. A. Walker, and W. R. Montfort. 2000. Kinetics and equilibria in ligand binding by nitrophorins 1-4: evidence for stabilization of a nitric oxide-ferriheme complex through a ligand-induced conformational trap. Biochemistry 39(33): 10118-10131.