Skip to main content
SpringerLink
Log in

Ultrastructural localization of acetylcholinesterase in the synganglion of the tick, Dermacentor variabilis (Say)

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

Light- and electron-microscopic enzyme cytochemistry was used to localize acetylcholinesterase (AChE) activity in the synganglion (brain) of the tick Dermacentor variabilis. High AChE activity was observed throughout the neuropil as well as adjacent to most neuronal perikarya. Intracellular activity was not observed by light microscopy. By electron microscopy, reaction product was localized at the plasma membrane of glia and neurons. Enzyme activity was not associated with the olfactory globuli neurons. In other types of neurons, small amounts of reaction product were observed in the Golgi apparatus and nuclear envelope. Large neurosecretory neurons contained activity that appeared to be associated with deep invaginations of the plasma membrane as well as intracellular membranes. AChE activity was also associated with processes of both neurons and glia. In most peripheral nerves AChE activity was associated with virtually all axons. Clearly then, AChE is associated with glia and non-cholinergic neurons as well as with presumed cholinergic neurons. The widespread localization and large amounts of AChE in the tick brain exceeds that reported for other invertebrates and vertebrates. As has been suggested for other animals, AChE in the tick brain may have functions in addition to its known role in cholinergic neurotransmission.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Brzin M, Tennyson VM, Dettbarn W-D (1975) Cytochemical localization of cholinesterase activity at the giant synapse of the squid. Histochemistry 43:305–311

    Google Scholar 

  • Chubb IW, Ranieri E, White GH, Hodgson AJ (1983) The enkephalins are amongst the peptides hydrolyzed by acetylcholinesterase. Neuroscience 10:1369–1377

    Google Scholar 

  • Chubb IW, White GH, Hodgson AJ (1980) Acetylcholinesterase hydrolyzes substance P. Neuroscience 5:2065–2072

    Google Scholar 

  • Colhoun EH (1958) Distribution of choline acetylase in insect nervous tissue. Nature (London) 182:1378

    Google Scholar 

  • Coons LB, Roshdy MA, Axtell RC (1974) Fine structure of the central nervous system of Dermacentor variabilis (Say), Amblyomma americanum (L.), and Argas arboreus Kaiser, Hoogstraal, and Kohls (Ixodoidea). J Parasitol 60:687–698

    Google Scholar 

  • Czubaj A (1979) Ultrastructural distribution of AChE in Catenula leptocephala (Nuttycombe 1956). Histochemistry 61:189–198

    Google Scholar 

  • Dalton AJ (1955) A chrome-osmium fixative for electron microscopy. Anat Rec 121:281

    Google Scholar 

  • DeLorenzo AJD, Dettbarn WD, Brzin M (1969) Fine structural localization of acetylcholinesterase in single axons. J Ultrastruc Res 28:27–40

    Google Scholar 

  • Emson PC, Bush BMH, Joseph MH (1976) Transmitter metabolizing enzymes and free amino acid levels in sensory and motor nerves and ganglia of the shore crab (Carcinus maenas). J Neurochem 26:779–783

    Google Scholar 

  • Frontali N, Piazza R, Scopelliti R (1971) Localization of acetylcholinesterase in the brain of Periplaneta americana. J Insect Physiol 17:1833–1842

    Google Scholar 

  • Giller E, Schwartz JH (1971) Acetylcholinesterase in identified neurons of abdominal ganglion of Aplysia californica. J Neurophysiol 34:108–117

    Google Scholar 

  • Goh SL, Davey KG (1976) Acetylcholinesterase and synapses in the nervous system of Phocanema decipiens (Nematoda): A histochemical and ultrastructural study. Can J Zool 54:752–771

    Google Scholar 

  • Hart RJ, Beadle DJ, Wilson RG (1984) Comparative pharmacology of insect and tick nerve-muscle synapse. In: Borkovec AB, Kelly TJ (eds) Insect neurochemistry and neurophysiology. Plenum, New York, pp 373–375

    Google Scholar 

  • Hebb CO (1972) Biosynthesis of acetylcholine in nervous tissue. Physiol Rev 52:918–957

    Google Scholar 

  • Hess A (1972) Histochemical localization of cholinesterase in the brain of the cockroach (Periplaneta americana). Brain Res 46:287–295

    Google Scholar 

  • Hildebrand JG, Townsel JG, Kravitz EA (1974) Distribution of acetylcholine, choline, choline acetyltransferase and acetylcholinesterase in regions and single identified axons of the lobster nervous system. J Neurochem 23:951–963

    Google Scholar 

  • Ivanov VP (1983) Central nervous system. In: Balashov YuS (ed) An atlas of tick ultrastructure. Entomological Society of America, pp 175–190

  • Jones BR, Smith BF, LeFlore WB (1979) The ultrastructural localiation of acetylcholinesterase activity in the scolex of the cysticerus of Hydatigera taeniaeformis. Cytobios 26:7–24

    Google Scholar 

  • Jurchenko O, Kultas K, Vulfius C (1973) Cholinesterase activity in ganglia of Gastropoda, Lymnaea stagnalis and Planorbarius corneus. II. Histochemical investigation. Comp Biochem Physiol 45A:61–68

    Google Scholar 

  • Kral K, Schneider L (1981) Fine structural localisation of acetylcholinesterase activity in the compound eye of the honeybee (Apis mellifica L.). Cell Tissue Res 221:351–359

    Google Scholar 

  • Landolt AM, Sandri C (1966) Cholinergische Synapsen im Oberschlundganglion der Waldameise (Formica lugubris Zett.). Z Zellforsch 69:246–259

    Google Scholar 

  • Lane NJ (1974) The organization of insect nervous systems. In: Treherne JE (ed) insect neurobiology. North-Holland, Amsterdam, pp 1–71

    Google Scholar 

  • Lazar M, Vigny M (1980) Modulation of the distribution of acetylcholinesterase molecular forms in a murine neuroblastoma x sympathetic ganglion cell hybrid cell line. J Neurochem 35:1067–1079

    Google Scholar 

  • Lee A-H, Metcalf RL, Booth GM (1973) House cricket acetylcholinesterase: histochemical localization and in situ inhibition by 0,0-dimethyl S-aryl phosphorothiolates. Ann Enlomol Soc Am 66:333–343

    Google Scholar 

  • Lewis PR (1977) Metal precipitation methods for hydrolytic enzymes. In: Lewis PR, Knight DP (eds) Staining methods for sectioned material. North-Holland, Amsterdam, pp 137–223

    Google Scholar 

  • Lewis PR, Shute CCD (1966) The distribution of cholinesterase in cholinergic neurons demonstrated with the electron microscope. J Cell Sci 1:381–390

    Google Scholar 

  • Lewis PR, Shute CCD (1969) An electron microscopy study of cholinesterase distribution in the rat adrenal medulla. J Microsc 89:181–193

    Google Scholar 

  • Maynard EA (1971) Microscopic localization of cholinesterases in the nervous systems of the lobsters, Panulirus argus and Homarus americanus. Tissue Cell 3:215–250

    Google Scholar 

  • McCaman RE, Dewhurst SA (1970) Choline acetyltransferase in individual neurons of Aplysia californica. J Neurochem 17:1421–1426

    Google Scholar 

  • McLaren DJ (1972) Ultrastructural and cytochemical studies on the sensory organelles and nervous system of Dipetalonema vitae (Nematoda: Filaroidea). Parasitology 65:507–528

    Google Scholar 

  • Mesulam M-M (1982) Principles of horseradish peroxidase neurohistochemistry and their applications for tracing neural pathways — xonal transport, enzyme histochemistry and light microscopic analysis, appendix VII. In: Mesulam M-M (ed) Tracing neural connections with horseradish peroxidase. John Wiley & Sons, Chichester, pp 134–135

    Google Scholar 

  • Nadol JB, Brzin M, DeLorenzo AID (1970) Fine structural localization of acetylcholinesterase in sensory and motor neurons of the muscle receptor organ in Homarus. J Comp Neurol 140:399–420

    Google Scholar 

  • Newman G, Kerkut GA, Walker RJ (1968) The structure of the brain of Helix aspersa. Electron microscope localizaton of cholinesterase and amines. Symp Zool Soc Lond 22:1–17

    Google Scholar 

  • Nolan J, Schnitzerling HJ (1975) Characterization of acetylcholinesterases of acaricide-resistant and susceptible strains of the cattle tick Boophilus microplus (Can.) I. Extraction of the critical component and comparison with enzyme from other sources. Pest Biochem Physiol 5:178–188

    Google Scholar 

  • Nolan J, Schnitzerling HJ (1976) Characterization of acetylcholinesterases of acaricide-resistant and susceptible strains of the cattle tick Boophilus microplus (Can.) II. The substrate specificity and catalytic efficiency of the critical enzyme component. Pest Biochem Physiol 6:142–147

    Google Scholar 

  • Obenchain FD (1974) Structure and anatomical relationships of the synganglion in the American dog tick, Dermacentor variabilis (Acari: Ixodidae). J Morphol 142:205–224

    Google Scholar 

  • Polz-Tejera G, Hunt SP, Schmidt J (1980) Nicotinic receptors in sensory ganglia. Brain Res 195:223–230

    Google Scholar 

  • Pound JM (1981) Hormonal relationships in reproduction of feale Ornithodoros parkeri (Cooley). Ph.D. thesis, University of Georgia

  • Roulston WJ, Schuntner CA, Schnitzerling HJ (1966) Metabolism of coumaphos in larvae of the cattle tick Boophilus microplus. Aust J Biol Sci 21:97–109

    Google Scholar 

  • Sanes J, Hildebrand JG (1976a) Structure and development of antennae in a moth, Manduca sexta. Dev Biol 51:282–299

    Google Scholar 

  • Sanes J, Hildebrand JG (1976b) Origin and development of sensory neurons in an insect antenna. Dev Biol 51:300–319

    Google Scholar 

  • Sanes J, Hildebrand JG (1976c) Acetylcholine and its metabolizing enzymes in developing antennae of the moth, Manduca sexta. Dev Biol 52:105–120

    Google Scholar 

  • Schafer R (1973) Acetylcholine: Fast axoplasmic transport in insect chemoreceptor fibers. Science 180:315–317

    Google Scholar 

  • Schnitzerling HJ, Nolan J, Davey PA (1982) A comparative study of the reactivity of acetylcholinesterases of the cattle tick Boophilus microplus and the cattle erythrocytes with organophosphorus and carbamate inhibitors. Pest Biochem Physiol 18:216–225

    Google Scholar 

  • Schuntner CA, Smallman BN (1972) Cholinergic systems in organophosphorus-resistant and -susceptible larvae of the cattle tick Boophilus microplus. Pest Biochem Physiol 2:78–84

    Google Scholar 

  • Silver A (1974) The Biology of Cholinesterases. North-Holland, Amsterdam

    Google Scholar 

  • Smallman BN, Riddles PW (1977) Choline acetyltransferase in organophosphorus-resistant and -susceptible strains of the cattle tick, Boophilus microplus. Pest Biochem Physiol 7:355–359

    Google Scholar 

  • Smallman BN, Schuntner CA (1972) Authentication of the cholinergic system in the cattle tick, Boophilus microplus. Insect Biochem 2:67–77

    Google Scholar 

  • Smith DS, Treherne JE (1965) The electron microscopic localization of cholinesterase activity in the central nervous system of an insect, Periplaneta americana. L. J Cell Biol 26:445–459

    Google Scholar 

  • Stephens LB, Greenberg MJ (1973) The localization of acetylcholinesterase and butyrylcholinesterase in the heart, cardiac ganglion and the lateral and dorsal nerves of Limulus polyphemus. J Histochem Cytochem 21:923–931

    Google Scholar 

  • Stone BF (1968) Brain cholinesterase activity and its inheritance in cattle tick (Boophilus microplus) strains resistant and susceptible to organophosphorus acaricides. Aust J Biol Sci 21:321–330

    Google Scholar 

  • Stone BF, Nolan J, Schuntner CA (1976) Biochemical genetics of resistance to organophosphorus acaricides in three strains of the cattle tick, Boophilus microplus. Aust J Biol Sci 29:265–279

    Google Scholar 

  • Tatchell RJ (1971) Electrophoretic studies on the proteins of the haemolymph, saliva, and eggs of the cattle tick, Boophilus microplus. Insect Biochem 1:47–55

    Google Scholar 

  • Taylor PB, Rieger F, Shelanski M, Greene LA (1981) Cellular localization of the multiple molecular forms of acetylcholinesterase in cultured neuronal cells. J Biol Chem 256:3827–3830

    Google Scholar 

  • Teravainen H (1969) Ultrastructural distribution of cholinesterase activity in the ventral nerve cord of the earthworm Lumbricus terrestris. Histochemie 18:177–190

    Google Scholar 

  • Treherne JE (1974) The environment and function of insect nerve cells. In: Treherne JE (ed) Insect neurobiology. North-Holland, Amsterdam, pp 187–244

    Google Scholar 

  • Villegas GM, Villegas J (1974) Acetylcholinesterase localization in the giant nerve fiber of the squid. J Ultrastruct Res 46:149–163

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biological Sciences, Old Dominion University, Norfolk, Virginia, USA

    Keith A. Carson Ph.D., Daniel S. Sonenshine & DeMar Taylor

  2. Department of Anatomy and Cell Biology, Eastern Virginia Medical School, Norfolk, Virginia, USA

    Keith A. Carson Ph.D.

  3. Neurobiology Program, Trailer L, University of North Carolina, Chapel Hill, North Carolina, USA

    Linda M. Boland

Authors
  1. Keith A. Carson Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel S. Sonenshine
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Linda M. Boland
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. DeMar Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carson, K.A., Sonenshine, D.S., Boland, L.M. et al. Ultrastructural localization of acetylcholinesterase in the synganglion of the tick, Dermacentor variabilis (Say). Cell Tissue Res. 249, 615–623 (1987). https://doi.org/10.1007/BF00217333

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00217333

Key words

Search

Navigation