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Biochemical perspectives on paralysis and other forms of toxicoses caused by ticks

Published online by Cambridge University Press:  19 April 2005

B. J. MANS ,
R. GOTHE  and
A. W. H. NEITZ
B. J. MANS
Affiliation:
Department of Biochemistry, University of Pretoria, Pretoria, 0002 South Africa
R. GOTHE
Affiliation:
Department of Biochemistry, University of Pretoria, Pretoria, 0002 South Africa
A. W. H. NEITZ
Affiliation:
Department of Biochemistry, University of Pretoria, Pretoria, 0002 South Africa
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Abstract

Tick toxicoses, of which paralysis is the most widespread and dominant form, are important elements of pathogenesis induced by ticks. Tick paralysis is the most widespread and dominant form of tick toxicoses. Non-paralytic forms of tick toxicoses do occur and evidence suggests that these forms of toxicoses are not evolutionary related. While functional significance has been suggested for tick toxins, the advantages for tick survival in general are not clear. This review considers the molecular nature of tick toxins, the possibility that tick toxins have originated more than once independently and whether these toxins could have unrecognized benign functions.

Keywords

Evolutiontick paralysistoxicosestoxins
Type
Research Article
Information
Parasitology , Volume 129 , Issue S1 , October 2004 , pp. S95 - S111
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

ANDREOTTI, R., GOMES, A., MALAVAZI-PIZA, K. C., SASAKI, S. D., SAMPAIO, C. A. M. & TANAKA, A. S. ( 2002). BmTI antigens induce a bovine protective immune response against Boophilus microplus tick. International Immunopharmacology 2, 557–563.CrossRefGoogle Scholar
BEZUIDENHOUT, J. D. & MALHERBE, A. ( 1981). Sweating sickness: A comparative study of virulent and avirulent strains of Hyalomma truncatum. In Tick Biology and Control ( ed. Whitehead, G. B. & Gibson, J. D.), pp. 7–12. Grahamstown, South Africa, Tick Research Unit, Rhodes University.
BRUNK, U. T. & TERMAN, A. ( 2002). The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. European Journal of Biochemistry 269, 1996–2002.CrossRefGoogle Scholar
BURGER, D. B., CRAUSE, J. C., SPICKETT, A. M. & NEITZ, A. W. H. ( 1991). A comparative study of proteins present in sweating-sickness-inducing and non-inducing strains of Hyalomma truncatum ticks. Experimental and Applied Acarology 13, 59–63.CrossRefGoogle Scholar
CAYA, J. G. ( 2001). Clostridium botulinum and the ophthalmologist: a review of botulism, including biological warfare ramifications of botulinum toxin. Survey of Ophthalmology 46, 25–34.CrossRefGoogle Scholar
CHELLAPPA, D. J. ( 1973). Note on spinose ear tick infestation in man and domestic animals in India and its control. Madras Agricultural Journal 60, 656–658.Google Scholar
COOPER, B. J. & SPENCE, I. ( 1976). Temperature-dependent inhibition of evoked acetylcholine release in tick paralysis. Nature 263, 693–695.CrossRefGoogle Scholar
CRAUSE, J. C., VAN WYNGAARDT, S., GOTHE, R. & NEITZ, A. W. H. ( 1994). A shared epitope found in the major paralysis inducing tick species of Africa. Experimental and Applied Acarology 18, 51–59.CrossRefGoogle Scholar
CRAUSE, J. C., VERSCHOOR, J. A., COETZEE, J., HOPPE, H. C., TALJAARD, J. N., GOTHE, R. & NEITZ, A. W. ( 1993). The localization of a paralysis toxin in granules and nuclei of prefed female Rhipicephalus evertsi evertsi tick salivary gland cells. Experimental and Applied Acarology 17, 357–363.CrossRefGoogle Scholar
DALY, J. W., PADGETT, W. L., SAUNDERS, R. L. & COVER, J. F. Jr. ( 1997). Absence of tetrodotoxins in a captive-raised riparian frog, Atelopus varius. Toxicon 35, 705–709.CrossRefGoogle Scholar
DE KOCK, G., VAN HEERDEN, C. J., DU TOIT, R. & NEITZ, W. O. ( 1937). Bovine theileriosis in South Africa with special reference to Theileria mutans. Onderstepoort Journal of Veterinary Science and Animal Industry 8, 9–125.Google Scholar
DE MEILLON, B. ( 1942). A toxin from the eggs of South African ticks. South African Journal of Medical Science 7, 226–235.Google Scholar
DOBSON, S. J. & BARKER, S. C. ( 1999). Phylogeny of the hard ticks (Ixodidae) inferred from 18S rRNA indicates that the genus Aponomma is paraphyletic. Molecular Phylogenetics and Evolution 11, 288–295.CrossRefGoogle Scholar
DU TOIT, R. & THEILER, G. ( 1964). Ticks and tick-borne diseases in South Africa. Scientific Bulletin of the Department of Agriculture and Technical Services of the Republic of South Africa Number 364.Google Scholar
EADS, R. B. & CAMPOS, E. G. ( 1984). Human parasitism by Otobius megnini (Acari: Argasidae) in New Mexico, USA. Journal of Medical Entomology 21, 244.CrossRefGoogle Scholar
EMMONS, P. & McLENNAN, H. ( 1980). Some observations on tick paralysis in marmots. Journal of Experimental Biology 37, 355–362.Google Scholar
ESCOUBAS, P., DIOCHOT, S. & CORZO, G. ( 2000). Structure and pharmacology of spider venom neurotoxins. Biochimie 82, 893–907.CrossRefGoogle Scholar
GOTHE, R. ( 1984). Tick paralyses: Reasons for appearing during ixodid and argasid feeding. In Current Topics in Vector Research ( ed. Harris, K. F.), Vol. 2, pp. 199–223. New York, Praeger Publishers.
GOTHE, R. ( 1999). Zecken Toxikosen Hieronyms, Munich, JSBN 3-88751-083-17, 377 pp.
GOTHE, R., HAGER, H., JEHN, E., KUNZE, K. & THOENES, W. ( 1971). Pathological-anatomical studies of peripheral nerves in fowl tick paralysis caused by Argas (Persicargas) persicus larvae. Zeitschrift für Tropenmedizin und Parasitologie 22, 285–291.Google Scholar
GOTHE, R. & KUNZE, K. ( 1971). Stimulus conduction of efferent and afferent peripheral nerve fibers in fowl tick paralysis caused by Argas (Persicargas) persicus larvae. Zeitschrift für Tropenmedizin und Parasitologie 22, 292–296.Google Scholar
GOTHE, R. & KUNZE, K. ( 1982). Action potentials and conduction velocities of the tibial nerve in sheep paralysis caused by Rhipicephalus evertsi evertsi. Zentralblatt für Veterinaermedizin B29, 186–192.Google Scholar
GOTHE, R., KUNZE, K. & HOOGSTRAAL, H. ( 1979). The mechanisms of pathogenicity in tick paralyses. Journal of Medical Entomology 16, 357–369.CrossRefGoogle Scholar
GOTHE, R. & LÄMMLER, M. ( 1982). Sensitivity of laboratory animals to Rhipicephalus evertsi evertsi paralysis. Zentralblatt für Veterinaermedizin B29, 249–252.Google Scholar
GOTHE, R. & NEITZ, A. W. H. ( 1991). Tick paralysis: pathogeneses and etiology. Advances in Disease and Vector Research 8, 177–204.CrossRefGoogle Scholar
GREGSON, J. D. ( 1941). The discovery of an ixovotoxin in Dermacentor andersoni eggs. Proceedings of the Entomological Society of British Columbia 37, 9–10.Google Scholar
GREGSON, J. D. ( 1943). The enigma of tick paralysis. Proceedings of the Entomological Society of British Columbia 40, 19–23.Google Scholar
GREGSON, J. D. ( 1973). Tick paralysis: an appraisal of natural and experimental data. Canadian Department of Agriculture. Monograph No. 9.Google Scholar
HOEPPLI, R. & FENG, L. C. ( 1933). Experimental studies on ticks. Chinese Medical Journal 47, 29–43.Google Scholar
HOLZER, H. & HEINRICH, P. C. ( 1980). Control of proteolysis. Annual Review of Biochemistry 49, 63–91.CrossRefGoogle Scholar
HOOGSTRAAL, H. ( 1956). African Ixodoidea. I. Ticks of the Sudan (with special reference to Equatoria Province and with preliminary reviews of the genera Boophilus, Margaropus and Hyalomma). Research Report NM 005050.29.07, Department of the Navy, 1101.
HOOGSTRAAL, H. ( 1985). Argasid and Nuttalliellid ticks as parasites and vectors. Advances in Parasitology 24, 135–238.CrossRefGoogle Scholar
HOWELL, C. J. ( 1966). Collection of salivary gland secretion from the argasid Ornithodoros savignyi Audouin (1827) by the use of a pharmacological stimulant. Journal of the South African Veterinary Medical Association 37, 236–239.Google Scholar
HOWELL, C. J., NEITZ, A. W. H. & POTGIETER, D. J. J. ( 1975). Some toxic and chemical properties of the oral secretion of the sand tampan, Ornithodoros savignyi Audouin (1825). Onderstepoort Journal of Veterinary Research 43, 99–102.Google Scholar
KASSIS, I., IOFFE-USPENSKY, I., USPENSKY, I. & MUMCUOGLU, K. Y. ( 1997). Human toxicosis caused by the tick Ixodes redikorzevi in Israel. Israel Journal of Medical Science 33, 760–761.Google Scholar
KELLER, P. M., WAXMAN, L., ARNOLD, B. A., SCHULTZ, L. D., CONDRA, C. & CONNOLLY, T. M. ( 1993). Cloning of the cDNA and expression of moubatin, an inhibitor of platelet aggregation. Journal of Biological Chemistry 268, 5450–5456.Google Scholar
KLOMPEN, J. S. H., BLACK IV, W. C., KEIRANS, J. E. & NORRIS, D. E. ( 2000). Systematic and biogeography of hard ticks, a total evidence approach. Cladistics 16, 79–102.CrossRefGoogle Scholar
KLOMPEN, J. S. H., BLACK IV, W. C., KEIRANS, J. E. & OLIVER, J. H. ( 1996). Evolution of ticks. Annual Reviews in Entomology 41, 141–161.CrossRefGoogle Scholar
KONE, K. ( 1948). Accidents mortels chez les zébus causés par des piqûres d'Ornithodores. Bulletin des Services de l'Elevage et des Industries de l'AOF 2, 25–26.Google Scholar
LINDQUIST, E. E. ( 1984). Current theories on the evolution of major groups of Acari and on their relationships with other groups of Arachnida, with consequent implications for their classification. In Acarology VI (Volume 1) ( ed. Griffiths, D. A. & Bowman, C. E.), pp. 28–62. New York, John Wiley & Sons.
MADIGAN, J. E., VALBERG, S. J., RAGLE, C. & MOODY, J. L. ( 1995). Muscle spasms associated with ear tick (Otobius megnini) infestations in five horses. Journal of the American Veterinary and Medical Association 207, 74–76.Google Scholar
MANS, B. J., LOUW, A. I. & NEITZ, A. W. H. ( 2003). The major tick salivary gland proteins and toxins from the soft tick, Ornithodoros savignyi, are part of the lipocalin family: implications for the origins of tick toxicoses. Molecular Biology and Evolution 20, 1158–1167.CrossRefGoogle Scholar
MANS, B. J., STEINMANN, C. M., VENTER, J. D., LOUW, A. I. & NEITZ, A. W. H. ( 2002). Pathogenic mechanisms of sand tampan toxicoses induced by the tick, Ornithodoros savignyi. Toxicon 40, 1007–1016.CrossRefGoogle Scholar
MANS, B. J., VENTER, J. D., VREY, P. J., LOUW, A. I. & NEITZ, A. W. H. ( 2001). Identification of putative proteins involved in granule biogenesis of tick salivary glands. Electrophoresis 22, 1739–1746.3.0.CO;2-7>CrossRefGoogle Scholar
MARITZ, C., LOUW, A. I., GOTHE, R. & NEITZ, A. W. ( 2000). Detection and micro-scale isolation of a low molecular mass paralysis toxin from the tick, Argas (Persicargas) walkerae. Experimental and Applied Acarology 24, 615–630.CrossRefGoogle Scholar
MARITZ, C., LOUW, A. I., GOTHE, R. & NEITZ, A. W. ( 2001). Neuropathogenic properties of Argas (Persicargas) walkerae larval homogenates. Comparative Biochemistry and Physiology A 128, 233–239.CrossRefGoogle Scholar
MASINA, S. & BROADY, K. W. ( 1999). Tick paralysis: development of a vaccine. International Journal for Parasitology 29, 535–541.CrossRefGoogle Scholar
MÊNEZ, A. ( 1998). Functional architectures of animal toxins: a clue to drug design? Toxicon 36, 1557–7152.Google Scholar
MURNAGHAN, M. F. & O'ROUKE, F. J. ( 1978). Tick paralysis. In Arthropod Venoms ( ed. Bettini, S.), pp. 419–464. Handbook of Experimental Pharmacology 48, Berlin, Springer Verlag.CrossRef
MURREL, A., CAMPBELL, N. J. H. & BARKER, S. C. ( 2001). A total-evidence phylogeny of ticks provides insights into the evolution of life cycles and biogeography. Molecular Phylogenetics and Evolution 21, 244–258.CrossRefGoogle Scholar
NEITZ, W. O. ( 1954). Hyalomma transiens Schulze: A vector of sweating sickness. Journal of the South African Veterinary and Medical Association 25, 19–20.Google Scholar
NEITZ, W. O. ( 1956). Studies on the aetiology of sweating sickness. Onderstepoort Journal of Veterinary Research 27, 197–203.Google Scholar
NEITZ, W. O. ( 1959). Sweating sickness: The present state of our knowledge. Onderstepoort Journal of Veterinary Research 28, 3–38.Google Scholar
NEITZ, W. O. ( 1962). The different forms of tick toxicoses: a review. Second meeting of the FAO/OIE expert panel on tick-borne diseases of livestock. Cairo, U.A.R., 3–10 December.
NEITZ, A. W. H. ( 1976). Biochemical investigation into the toxic salivary secretion of the tick Ornithodoros savignyi. DSc (Agric) thesis, University of Pretoria, South Africa.
NEITZ, A. W. H., BEZUIDENHOUT, J. D., VERMEULEN, N. M. J., POTGIETER, D. J. J. & HOWELL, C. J. ( 1983). In search of the causal agents of tick toxicoses. Toxicon S3, 317–320.CrossRefGoogle Scholar
NEITZ, A. W. & GOTHE, R. ( 1986). Changes in the protein pattern in the salivary glands of paralysis inducing female Rhipicephalus evertsi evertsi during infestation. Journal of Veterinary Medicine B 33, 213–220.CrossRefGoogle Scholar
NEITZ, A. W. H., HOWELL, C. J. & POTGIETER, D. J. J. ( 1969). Purification of the toxic component in the oral secretion of the sand tampan Ornithodoros savignyi Audouin (1827). Journal of the South African Chemical Industry 22, 142–149.Google Scholar
NEITZ, A. W. H., PROZESKY, L., BEZUIDENHOUT, J. D., PUTTERILL, J. F. & POTGIETER, D. J. ( 1981). An investigation into the toxic principle in eggs of the tick Amblyomma hebraeum. Onderstepoort Journal of Veterinary Research 48, 109–117.Google Scholar
OSWALD, B. ( 1938). A review of work published in Yugoslavia on the tick problem and research on toxins in the eggs of ticks. Annales de Parasitologie Humaine et Comparee 16, 548–559.CrossRefGoogle Scholar
PAESEN, G. C., ADAMS, P. L., HARLOS, K., NUTTALL, P. A. & STUART, D. I. ( 1999). Tick histamine-binding proteins: isolation, cloning, and three-dimensional structure. Molecular Cell 3, 661–671.CrossRefGoogle Scholar
PAESEN, G. C., ADAMS, P. L., NUTTALL, P. A. & STUART, D. L. ( 2000). Tick histamine-binding proteins: lipocalins with a second binding cavity. Biochimica et Biophysica Acta 1482, 92–101.CrossRefGoogle Scholar
PEACOCK, P. B. ( 1958). Tick paralysis or poliomyelitis. South African Medical Journal 32, 201–202.Google Scholar
RASH, L. D. & HODGSON, W. C. ( 2002). Pharmacology and biochemistry of spider venoms. Toxicon 40, 225–254.CrossRefGoogle Scholar
REGENDANZ, P. & REICHENOW, E. ( 1931). Über zeckengift und zeckenparalyse. Archiv für Schiffs-und Tropen-Hygiene 35, 255–273.Google Scholar
RICH, G. B. ( 1957). The ear tick, Otobius megnini (Dugès) (Acarina: Argasidae), and its record in British Columbia. Candian Journal of Comparative Medicine 21, 415–418.Google Scholar
RIEK, R. F. ( 1957). Studies on the reactions of animals to infestation with ticks. Australian Journal of Agricultural Research 8, 215–223.CrossRefGoogle Scholar
RIEK, R. F. ( 1958). Studies on the reactions of animals to infestation with ticks. Australian Journal of Agricultural Research 9, 830–841.CrossRefGoogle Scholar
RIEK, R. F. ( 1959). Studies on the reactions of animals to infestation with ticks. Australian Journal of Agricultural Research 10, 604–613.CrossRefGoogle Scholar
ROUSSELOT, R. ( 1956). Meeting report No. 1956/18. Report of the joint FAO/OIE meeting on the control of tick-borne diseases of livestock, Rome 83.
SHULTZ, J. W. ( 1990). Evolutionary morphology and phylogeny of Arachnida. Cladistics 6, 1–38.Google Scholar
SONENSHINE, D. E. ( 1993). Tick paralysis and other tick-borne toxicoses. In Biology of Ticks, 2, 320–332. Oxford, Oxford University Press.
SPICKETT, A. M., BURGER, D. B., CRAUSE, J. C., ROUX, E. M. & NEITZ, A. W. H. ( 1991). Sweating sickness: Relative curative effect of hyperimmune serum and precipitated immunoglobin suspension and immunoblot identification of proposed immunodominant tick salivary gland proteins. Onderstepoort Journal of Veterinary Research 58, 223–226.Google Scholar
STAMPA, S. ( 1959). Tick paralysis in the Karoo areas of South Africa. Onderstepoort Journal of Veterinary Research 28, 169–227.Google Scholar
STANDBURY, J. B. & HUYCK, J. H. ( 1945). Tick paralysis: a critical review. Medicine (Baltimore) 24, 219–242.CrossRefGoogle Scholar
STEINHAUS, E. A. ( 1942). Note on a toxic principle in eggs of the tick, Dermacentor andersoni Stiles. United States Public Health Report 57, 1310–1312.CrossRefGoogle Scholar
STONE, B. F. & BINNINGTON, K. C. ( 1986). The paralyzing toxin and other immunogens of the tick I. holocyclus and the role of the salivary glands in their biosyntheses. In Morphology, Physiology and Behavioral Biology of Ticks ( ed. Sauer, J. R. & Hair, J. A.), pp. 75–99. Chichester, Ellis Horwood.
STONE, B. F., BINNINGTON, K. C., GAUCI, M. & AYLWARD, J. H. ( 1989). Tick/host interactions for Ixodes holocyclus: role, effects, biosynthesis and nature of its toxic and allergenic oral secretions. Experimental and Applied Acarology 7, 59–69.CrossRefGoogle Scholar
STONE, B. F., DOUBE, B. F. & BINNINGTON, K. C. ( 1979). Toxins of the Australian paralysis tick Ixodes holocyclus. Recent Advances in Acarology 1, 347–356.CrossRefGoogle Scholar
TANAKA, A. S., ANDREOTTI, R., GOMES, A., TORQUATO, R. J., SAMPAIO, M. U. & SAMPAIO, C. A. ( 1999). A double headed serine proteinase inhibitor-human plasma kallikrein and elastase inhibitor from Boophilus microplus larvae. Immunopharmacology 45, 171–177.CrossRefGoogle Scholar
THOMAS, A. D. & NEITZ, W. O. ( 1958). Rhipicephaline tick toxicoses in cattle. Its possible aggravating effects on certain diseases. Journal of the South African Veterinary and Medical Association 29, 29–50.Google Scholar
THURN, M. J., GOOLEY, A. & BROADY, K. W. ( 1992). Identification of the neurotoxin from the paralysis tick, Ixodes holocyclus. In Recent Advances in Toxicology Research, 2 ( ed. Gopalakrishnakone, P. & Tan, C. K.), pp. 243–256. Singapore, Venom and Toxin Research Group, National University of Singapore.
TOMALSKI, M. D., HUTCHINSON, K., TODD, J. & MILLER, L. K. ( 1993). Identification and characterization of tox21A: a mite cDNA encoding a paralytic neurotoxin related to TxP-I. Toxicon 31, 319–326.CrossRefGoogle Scholar
TOMALSKI, M. D. & MILLER, L. K. ( 1991). Insect paralysis by baculovirus-mediated expression of a mite neurotoxin gene. Nature 352, 82–75.CrossRefGoogle Scholar
VERMEULEN, N. M. J. & NEITZ, A. W. H. ( 1987). Biochemical studies on the eggs of Amblyomma hebrauem. Onderstepoort Journal of Veterinary Research 54, 451–459.Google Scholar
VERMEULEN, N. M. J., NEITZ, A. W. H., POTGIETER, D. J. J. & BEZUIDENHOUT, J. D. ( 1984). Anti-protease from Amblyomma hebraeum. Insect Biochemistry 14, 705–711.CrossRefGoogle Scholar
VERMEULEN, N. M. J., VILJOEN, G. J., BEZUIDENHOUT, J. D., VISSER, L. & NEITZ, A. W. H. ( 1988). Kinetic properties of toxic protease inhibitors isolated from tick eggs. International Journal of Biochemistry 20, 621–631.CrossRefGoogle Scholar
VILJOEN, G. J., BEZUIDENHOUT, J. D., OBEREM, P. T., VERMEULEN, N. M., VISSER, L., GOTHE, R. & NEITZ, A. W. H. ( 1986). Isolation of a neurotoxin from the salivary glands of female Rhipicephalus evertsi evertsi. Journal of Parasitology 72, 865–874.CrossRefGoogle Scholar
VILJOEN, G. J., NEITZ, A. W. H., PROZESKY, L., BEZUIDENHOUT, J. D. & VERMEULEN, N. M. J. ( 1985). Purification and properties of tick egg toxic proteins. Insect Biochemistry 15, 475–482.CrossRefGoogle Scholar
VILJOEN, G. J., VAN WYNGAARDT, S., GOTHE, R., VISSER, L., BEZUIDENHOUT, J. D. & NEITZ, A. W. ( 1990). The detection and isolation of a paralysis toxin present in Argas (Persicargas) walkerae. Onderstepoort Journal of Veterinary Research 57, 163–168.Google Scholar
WALTER, D. E. & PROCTOR, H. C. ( 1998). Feeding behaviour and phylogeny: observations on early derivative Acari. Experimental and Applied Acarology 22, 39–50.CrossRefGoogle Scholar
WANG, H. & NUTTALL, P. A. ( 1994). Excretion of host immunoglobulin in tick saliva and detection of IgG-binding proteins in tick haemolymph and salivary glands. Parasitology 109, 525–30.CrossRefGoogle Scholar
WAXMAN, L. & CONNOLLY, T. M. ( 1993). Isolation of an inhibitor selective for collagen-stimulated platelet aggregation from the soft tick Ornithodoros moubata. Journal of Biological Chemistry 268, 5445–5449.Google Scholar
WIKEL, S. K. ( 1984). Tick and mite toxicoses and allergy. In Handbook of Natural Toxins. Volume 2. Insect Poisons, Allergens and Other Invertebrate Venoms ( ed. Anthony T. Tu), pp. 371–396. New York, Marcel Dekker, Inc.
WILLADSEN, P. & McKENNA, R. V. ( 1983). Trypsin-chymotrypsin inhibitors from the tick, Boophilus microplus. Australian Journal of Experimental Biology and Medical Science 61, 231–238.CrossRefGoogle Scholar
WILLADSEN, P. & RIDING, G. A. ( 1979). Characterization of a proteolytic-enzyme inhibitor with allergenic activity. Multiple functions of a parasite-derived protein. Biochemical Journal 177, 41–47.Google Scholar
WILLADSEN, P. & RIDING, G. ( 1980). On the biological role of a proteolytic-enzyme inhibitor from the ectoparasitic tick Boophilus microplus. Biochemical Journal 189, 295–303.CrossRefGoogle Scholar
YOTSU, M., YAMAZAKI, T., MEGURO, Y., ENDO, A., MURATA, M., NAOKI, H. & YASUMOTO, T. ( 1987). Production of tetrodotoxin and its derivatives by Pseudomonas sp. isolated from the skin of a pufferfish. Toxicon 25, 225–228.Google Scholar