My major focus is on the physiology of ticks, emphasizing the role of the salivary glands in osmoregulation, the control of salivary fluid secretion, the endocrinological control of salivary gland development and degeneration and the control of vitellogenesis
We work primarily with the tick, Amblyomma hebraeum (Acari: Ixodidae), one of the largest species that can be reared on rabbits in the laboratory.
Three receptors control fluid secretion: (a) catecholamines act via a dopamine (DA)-receptor. (b) Ergot alkaloids are agonists at a receptor distinct from the DA-receptor (Minion & Kaufman, MS in preparation, January 2002). The natural ligand for the 'ergot receptor' is unknown. (c) A g-aminobutyric acid (GABA)-receptor modulates the activity of the first two. Although GABA has little intrinsic activity of its own, in the presence of DA, GABA increases fluid secretion by up to 100% or more. This potentiation can be mimicked by butyrophenone drugs -- a surprising result, because butyrophenones are potent antagonists of some DA-receptors in the mammalian CNS.
Relevant publications:
W. Reuben Kaufman, B. Duff Sloley, Roger J. Tatchell, Geoff Zbitnew, Tom Dieffenbach and Jeff Goldberg (1999) Quantification and cellular localization of dopamine in the salivary gland of the ixodid tick, Amblyomma hebraeum and the effect of organ culture on dopamine content. Experimental and Applied Acarology, 23: 251-265.
Kaufman, W.R. and Sloley, B.D. (1996). Catabolism of dopamine and 5-hydroxytryptamine by monoamine oxidase in the ixodid tick, Amblyomma hebraeum. Insect Biochem. Molec. Biol. 26: 101-109.
Lucien, J., Reiffenstein, R., Zbitnew, G. and Kaufman, W.R. (1995) g-aminobutyric acid (GABA) and other amino acids in tissues of the tick, Amblyomma hebraeum throughout the feeding and reproductive periods. Exp. Appl. Acarol. 19: 617-631.
Lindsay, P.J. and W.R. Kaufman (1986) Potentiation of salivary fluid secretion in ixodid ticks: a new receptor system for g-aminobutyric acid. Can. J. Physiol. Pharmacol. 64: 1119-1126.
Kaufman, W.R. and D.L.-P. Wong (1983) Evidence for multiple receptors mediating fluid secretion in salivary glands of ticks. Eur. J. Pharmacol. 87: 43-52.
Kaufman, W. (1979) Control of salivary fluid secretion in ixodid ticks. pp. 357-363. In: Recent Advances in Acarology (J.G. Rodriguez, Ed.) Vol. I Academic Press, New York.
Kaufman, W. (1978) Actions of some transmitters and their antagonists on salivary secretion in a tick. Am. J. Physiol. 235: R76-R81.
The functional state of the salivary glands depends on the degree of engorgement, there being a 60-fold increase in fluid secretory competence during the first 5-7 days of feeding. Our evidence suggests that a blood-borne factor triggers salivary gland development, although the identity of the factor is not known. However, within a few days following engorgement, the salivary glands atrophy under the influence of a 'tick salivary gland degeneration factor' (TSGDF). The release of TSGDF occurs only after a critical degree of engorgement has been achieved. Moreover, a substance transferred with the semen somehow interacts with stretch receptor information from the abdomen to hasten the release of TSGDF. We do not yet know the identity of the 'male factor' (although it is a protein between 20-100kD) but TSGDF is an ecdysteroid hormone - - probably 20-hydroxyecdysone (20E).
Since 1994 we have been publishing on the ecdysteroid receptor (EcR) in the salivary glands, elucidating the distribution, pharmacological and biochemical properties and ontogeny of these receptors.
Relevant publications:
Weiss, Brian L., Stepczynski, Jadwiga M., Wong Paul and Kaufman, W.R. (2002) Identification and characterization of genes differentially expressed in the testis/vas deferens of the fed male tick, Amblyomma hebraeum. Insect Biochem and Molec. Biol. IN PRESS for 2002.
Weiss, Brian & Kaufman W.R. (2001) The relationship between 'critical weight' and 20-hydroxyecdysone in the female ixodid tick, Amblyomma hebraeum. J. Insect Physiology, 47: 1261-1267.
Lomas, L.O. & W.R. Kaufman (1999) What is the meaning of 'critical weight' to female ixodid ticks?: A 'grand unification theory'! In: Acarology IX, Volume 2, Symposia (Eds. G.R. Needham, R. Mitchell, D.J. Horn, and W.C. Welbourn); The Ohio Biological Survey, Columbus Ohio, pp. 481-485.
Lomas, L.O., Gelman, D. and Kaufman, W.R. (1997) Ecdysteroid regulation of salivary gland degeneration in the ixodid tick, Amblyomma hebraeum: A reconciliation of in vivo and in vitro observations. Gen. Comp. Endocrinol. 109: 200-211.
Mao, H & Kaufman, W.R. (1999) Profile of the ecdysteroid hormone and its receptor in the salivary gland of the adult female tick, Amblyomma hebraeum. Insect Biochemistry and Molecular Biology 29: 33-42.
Mao, H & Kaufman, W.R. (1998) DNA binding properties of the ecdysteroid receptor in the salivary gland of the female ixodid tick, Amblyomma hebraeum. Insect Biochemistry and Molecular Biology 28: 947-957.
Kaufman, W.R. and Lomas, L. (1996) 'Male Factors' in ticks: their role in feeding
and egg development. Invertebrate Reproduction and Development 30: 191-198.
Charrois, G., Mao H. and Kaufman, W.R. (1996) Putative ecdysteroid antagonists
and agonists: impact on salivary gland degeneration in the ixodid tick, Amblyomma
hebraeum. Pest. Biochem. Physiol. 55: 140-149.
Lomas, L.O. & W.R. Kaufman (1992) An indirect mechanism by which a protein
from the male gonad hastens salivary gland degeneration in the female ixodid
tick, Amblyomma hebraeum. Arch. Insect Biochem. Physiol. 21: 169-178.
Lomas, L.O., and Kaufman, W.R. (1992) The influence of a factor from the male
genital tract on salivary gland degeneration in the female ixodid tick, Amblyomma
hebraeum. J. Insect Physiol. 38: 595-601.
Although some progress has been made in understanding the endocrinology of egg development in the argasid family of ticks, we know very little about the process in the ixodid family. Ovary transplant experiments on Amblyomma hebraeum have demonstrated that egg development is definitely under hormonal control (Lunke & Kaufman, 1993), and very recent experiments in our lab demonstrate that 20E triggers yolk-synthesis in vivo (Friesen & Kaufman, MS in preparation, December 2001), but 20E is not sufficient on its own to stimulate the whole process: yolk uptake following yolk synthesis. JH and JH-analogues are also ineffective in triggering yolk synthesis or uptake. It intrigues us that the tick ovary has so far shown itself to be refractory to treatments which have traditionally stimulated egg development in other arthropods, and we intend to probe further for haemolymph-borne substances that might stimulate the whole process.
Relevant publications:
Kaufman, W.R. (1999) Chelicerate Arthropods. In: Encyclopedia of Reproduction, (Ernst Knobil and Jimmy D. Neill, Eds) Academic Press, pp. 564-571.
Kaufman, W.R. (1997) ARTHROPODA-Chelicerata. Chapter 7 in: Reproductive Biology of Invertebrates (series editors: K.G. Adiyodi and Rita Adiyodi) Vol. 8 Part A, Progress in Reproductive Endocrinology (Ed. Terrance S. Adams), Oxford and IBH, New Delhi, India, and Wiley, NY, NY, pp. 211-245.
Mao, H., McBlain, W.A. and Kaufman, W.R. (1995) Some properties of the ecdysteroid receptor in the salivary gland of the ixodid tick, Amblyomma hebraeum. Gen. Comp. Endocrinol. 99: 340-348.
Lunke, M.D. and W.R. Kaufman (1993) Hormonal control of ovarian development in the tick Amblyomma hebraeum Koch (Acari: Ixodidae). Invertebrate Reproduction and Development, 23: 25-38.
The avermectins (AVMs) are very potent, broad spectrum antihelmintic drugs that are also effective against ticks. The AVMs potentiate the activity of GABA-pathways in mammals and invertebrates; this interaction with GABA may be responsible for antihelmintic activity, although several recent reports suggest instances in which GABA-pathways may not be involved. The mechanism of action against ticks is not known. We have demonstrated that the AVMs do not influence salivary gland activity, but they do inhibit vitellogenesis, the application of egg-wax, and oviposition. As with many other organisms that are sensitive to the AVMs, high concentrations of the drug induce a general paralysis. AVMs are likely to have several sites of action in ticks, and we are studying how they induce their numerous effects.
Relevant publications:
Lunke, M.D., and Kaufman, W.R. (1992) Effects of the avermectin analogue MK-243 on vitellogenesis and reproduction in the ixodid tick, Amblyomma hebraeum. Exptl. Appl. Acarol. 13: 249-259.
Lomas, L.O., and Kaufman W.R. (1991) Ivermectin is not an agonist at a GABA-receptor in tick salivary glands. Expt. Appl. Acarol. 12: 129-133.
Kaufman, W.R., S.G. Ungarian and A.E. Noga (1986) The effect of avermectins on feeding, salivary fluid secretion and fecundity in some ixodid ticks. Exp. Appl. Acarol. 2: 1-18.
Since 1990, I have collaborated with Dr. Patricia Nuttall at the NERC Institute of Virology and Environmental Microbiology, Oxford England. The overall theme of our project is to explore how pathogens exploit the physiology of the tick to gain access to the host. The model we work with is Thogoto virus and its tick vectors (Amblyomma variegatum and Rhipicephalus appendiculatus) in laboratory hosts (primarily the guinea pig). We have provided definitive data that virus is transmitted via saliva actively (i.e., by naturally infected ticks) and passively (i.e., following injection of virus into the haemocoel). We have also demonstrated that the tick does not simply act like a "needle and syringe": acquiring virus from one host and transmitting it to another. Rather, the salivary glands participate actively via a protein ('saliva activated transmission (SAT)-factor') that markedly facilitates the movement of virus among ticks and through the host. SAT-factor may have its effect on the host's immune system, although the physiological function of the protein to the tick remains obscure.
Relevant publications:
KAUFMAN, W.R., BOWMAN, A.S. AND NUTTALL P.A. Salivary fluid secretion in the ixodid tick Rhipicephalus appendiculatus is inhibited by Thogoto virus infection. Exptl. Appl. Acarol. IN PRESS, 2001.
WANG, H., W. R. KAUFMAN, W. W. CUI and P. A. NUTTALL (2001) Molecular individuality and adaptation of the tick Rhipicephalus appendiculatus (Ixodidae) in changed feeding environments. Medical & Veterinary Entomology, 15: 1-9.
Kaufman, W.R. & Nuttall P. (2000) Secretion of Thogoto virus by in vitro salivary glands of Rhipicephalus appendiculatus. (Proceedings of 3rd International Conference on Ticks and Tick-borne Pathogens : Into the 21st Century. Eds: M. Kazimirova, M. Labuda & P.A. Nuttall, Institute of Zoology, Slovak Academy of Sciences.
Wang, H., Kaufman, W.R., Nuttall, P. (1999) Molecular individuality: polymorphism of salivary gland proteins in three species of ixodid ticks. Experimental and Applied Acarology 23: 969-975.
Kaufman, W.R. and P.A. Nuttall (1999), Secretion of Thogoto virus by salivary glands of Amblyomma variegatum. In: Acarology IX, Volume 2, Symposia (Eds. G.R. Needham, R. Mitchell, D.J. Horn, and W.C. Welbourn); The Ohio Biological Survey, Columbus Ohio, pp. 427-431.
Kaufman, W.R and Nuttall, P. (1996) Amblyomma variegatum (Acari: Ixodidae): Mechanism and control of arbovirus secretion in tick saliva. Exptl. Parasitol. 82: 316-323.
Nuttall, P.A., L.D. Jones, M. Labuda and W.R. Kaufman (1994) Adaptations of
arboviruses to ticks. J. Med. Entomol. 31: 1-9
Dharampaul, S, W.R. Kaufman and M. Belosevic (1993) Differential recognition
of saliva antigens from the ixodid tick Amblyomma hebraeum by sera from infested
and immunized rabbits. J. Med. Entomol. 30: 262-266.
Nuttall, P.A., L.D. Jones, M. Labuda and W.R. Kaufman (1992) Interactions between arboviruses and their tick vectors. Invited Symposium paper, First International Conference on Tick-Borne Pathogens at the Host-Vector Interface: An Agenda for Research, St. Paul Minnesota, 15-18 September, 1992: 37-41.
Jones, L.D, W.R. Kaufman, and P.A. Nuttall. (1992) Feeding site modification
by tick saliva resulting in enhanced virus transmission. Experientia 48: 779-782.
Last updated: 12 December 2001