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Salivary glands in ixodid ticks: control and mechanism of secretion

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Abstract

The salivary glands are vital to the biological success of ixodid ticks and the major route for pathogen transmission. Important functions include the absorption of water vapor from unsaturated air by free-living ticks, excretion of excess fluid for blood meal concentration, and the secretion of bioactive protein and lipid compounds during tick feeding. Fluid secretion is controlled by nerves. Dopamine is the neurotransmitter at the neuroeffector junction regulating secretion via adenylate cyclase and an increase in cellular cAMP. Dopamine also affects the release of arachidonic acid which is subsequently converted to prostaglandins. Prostaglandin E2 (PGE2) is secreted at extremely high levels into tick saliva for export to the host where it impacts the host physiology. Additionally, PGE2 has an autocrine or paracrine role within the salivary gland itself where it interacts with a PGE2 receptor to induce secretion (exocytosis) of bioactive saliva proteins via a phosphoinositide signalling pathway and an increase in cellular Ca2+. Regulation of fluid secretion has been extensively studied, but little is known about the mechanism of fluid secretion. Continuing advances in tick salivary gland physiology will be made as key regulatory and secretory gland proteins are purified and/or their genes cloned and sequenced.

Introduction

Ticks are ectoparasitic, obligate blood-feeding acarines comprised of two major families, the Argasidae and Ixodidae. A third minor family, Nutalliellidae, consists of only one species. Argasid ticks feed rapidly, and consume relatively small meals of blood in contrast to the longer-feeding, more voracious ixodid ticks. The Ixodidae are major vectors of pathogens which cause diseases such as Rocky Mountain spotted fever, Lyme disease, monocytic and granulocytic erhlichiosis in humans and theileriosis and babesiosis in cattle. The prolonged period of attachment and the ability of ixodid ticks to transmit a wide range of pathogens have sparked great interest in studying ixodid salivary gland physiology and salivary gland secretions during tick feeding. Further interest relates to an apparent secretion from a single acinus type (type I) in the salivary glands of free-living ticks that assists in absorbing water from unsaturated air.

Section snippets

Ixodid tick salivary gland secretions

Ixodid ticks are unique amongst ectoparasites in their relatively long-term association with the vertebrate host. Female lone star ticks Amblyomma americanum, for example, attach and feed slowly for 7– 14 days before a 24–48 h period of rapid feeding when they fully engorge and disengage from the host. The female increases from about 4 to 600 mg during this period of attachment. Despite the substantial increase in weight, the quantity of blood imbibed is grossly underestimated if only the

Control of salivary gland fluid secretion

Salivary gland fluid secretion is controlled by nerves, with no evidence of control by hormones (Sauer et al., 1995). Nerves from the tick's central nervous system (synganglion) impinge directly upon the salivary glands (Binnington and Kemp, 1980, Fawcett et al., 1986, Kaufman and Harris, 1983, Megaw, 1977). The nerve(s) run posteriorly along, and are closely associated with, the ducts and terminate in synapses on cells near the lumen of the acini (Fawcett et al., 1986). Three kinds of

Physiology of the salivary glands in unfed ixodid ticks

Ticks often survive months and even years between bloodmeals. A major factor in the tick's ability to survive for prolonged periods without feeding is a remarkable ability to preserve water balance, assisted by an ability to absorb water from unsaturated air (Rudolph and Knulle, 1974, McMullen et al., 1976, Needham et al., 1990, Needham and Teel, 1991, Sigal et al., 1999). The mouth was established as the site of water vapor uptake in ticks (Rudolph and Knulle, 1974) and the salivary glands

Conclusions

The functional diversity of secretory products that facilitate prolonged tick attachment and feeding and the capacity to serve as a conduit for pathogens have prompted detailed studies of the ixodid tick salivary gland. Anatomically, the glands exhibit an extraordinary increase in mass and structural reorganization without an increase in cell number during tick feeding. Plasma membranes and mitochondria in type III and to a lesser extent type II acini proliferate, permitting the salivary glands

Acknowledgements

We thank R.W. Barker and S.K. Wikel for reviewing the manuscript and providing valuable comments. The manuscript was approved for publication by the Oklahoma Agricultural Experiment Station. This work was supported by the Oklahoma Center for the Advancement of Science and Technology (OCAST), grant numbers HR-98-056 and HR-98-057.

References (102)

  • D.C Jaworski et al.

    A secreted calreticulin in ixodid tick saliva

    Journal of Insect Physiology

    (1995)
  • J Karczewski et al.

    Disagregin is a fibrinogen receptor antagonist lacking the Arg–Gly–Asp sequence from the tick, Ornithodoros moubata

    Journal of Biological Chemistry

    (1994)
  • W.R Kaufman

    The influence of adrenergic agonists and their antagonists on isolated salivary glands of ixodid ticks

    European Journal of Pharmacology

    (1977)
  • W.J Lamoreaux et al.

    Fluid secretion by isolated tick salivary glands depends on an intact cytoskeleton

    International Journal for Parasitology

    (1994)
  • S.D Mane et al.

    Cyclic AMP-dependent protein kinase from the salivary glands of the tick, Amblyomma americanum — partial purification and properties

    Insect Biochemistry

    (1985)
  • H Mao et al.

    DNA binding properties of the ecdysteroid receptor in the salivary gland of the female ixodid tick, Amblyomma hebraeum

    Inscet Biochemistry and Molecular Biology

    (1998)
  • H Mao et al.

    Some properties of the ecdysteroid receptor in the salivary gland of the ixodid tick, Amblyomma hebraeum

    General and Comparative Endocrinology

    (1995)
  • H.L McMullen et al.

    Possible role in uptake of water vapour by ixodid tick salivary glands

    Journal of Insect Physiology

    (1976)
  • J.L McSwain et al.

    Cyclic AMP mediated phosphorylation of endogenous proteins in salivary glands of the lone star tick, Amblyomma americanum (L.)

    Insect Biochemistry

    (1985)
  • J.L McSwain et al.

    Amblyomma americanum (L.): protein kinase C-independent fluid secretion by isolated salivary glands

    Experimental Parasitology

    (1992)
  • J.L McSwain et al.

    Brain factor induced formation of inositol phosphates in tick salivary glands

    Insect Biochemistry

    (1989)
  • M.W.J Megaw et al.

    Structure and function of the salivary glands of the tick, Boophilus microplus Canestrini (Acarina:Ixodidae)

    International Journal of Insect Morphology and Embryology

    (1979)
  • G.R Needham et al.

    Control of fluid secretion by isolated salivary glands of the lone star tick

    Journal of Insect Physiology

    (1975)
  • G.C Paesen et al.

    Tick histamine-binding proteins: isolation, cloning and three-dimensional structure

    Molecular Cell

    (1999)
  • G.C Paesen et al.

    A tick homolgue of the human Ki nuclear autoantigen

    Biochimica et Biophysica Acta

    (1996)
  • M.J Palmer et al.

    Molecular cloning of cAMP-dependent protein kinase catalytic subunit isoforms from the lone star tick, Amblyomma americanum (L.)

    Insect Biochemistry and Molecular Biology

    (1999)
  • Y Qian et al.

    A specific prostaglandin E2 receptor and its role in modulating salivary secretion in the female tick, Amblyomma americanum (L.)

    Insect Biochemistry and Molecular Biology

    (1997)
  • Y Qian et al.

    Prostaglandin E2 in the salivary glands of the female tick Amblyomma americanum (L.): calcium mobilization and exocytosis

    Insect Biochemistry and Molecular Biology

    (1998)
  • A.E Qureshi et al.

    Protein phosphatase 1 and 2A in tick salivary glands as assessed by responses to okadaic acid

    Insect Biochemistry and Molecular Biology

    (1994)
  • S Raina et al.

    Molecular cloning and characterization of an aquaporin cDNA from salivary, lacrimal, and respiratory tissues

    Journal of Biological Chemistry

    (1995)
  • J.M.C Ribeiro et al.

    Amblyomma americanum: characterization of salivary prostaglandins E2 and F by RP-HPLC/bioassay and gas chromatography–mass spectrometry

    Experimental Parasitology

    (1992)
  • J.M.C Ribeiro et al.

    Ixodes scapularis: salivary kininase activity is a metallo-dipeptidyl carboxypeptidase

    Experimental Parasitology

    (1998)
  • C.W Roddy et al.

    The role of inositol 1,4,5-trisphosphate in mobilizing calcium from intracellular stores in the salivary glands of Amblyomma americanum (L.)

    Insect Biochemistry

    (1990)
  • S.P Schmidt et al.

    Dopamine sensitive adenylate cyclase in the salivary glands of the lone star tick

    Comparative Biochemistry and Physiology

    (1982)
  • M.M Shipley et al.

    Distribution of arachidonic acid among phospholipid subclasses of lone star tick salivary glands

    Insect Biochemistry and Molecular Biology

    (1994)
  • T Toda et al.

    Three different genes in S. cerevisiae encode the catalytic subunits of the cAMP-dependent protein kinase

    Cell

    (1987)
  • M.D Uhler et al.

    Evidence for a second isoform of the catalytic subunit of cAMP-dependent protein kinase

    Journal of Biological Chemistry

    (1986)
  • X Wang et al.

    Variabilin, a novel RGD-containing antagonist of glycoprotein Iib–IIIa and platelet aggregation inhibitor from the hard tick Dermacentor variabilis

    Journal of Biological Chemistry

    (1996)
  • S Wiemann et al.

    Isoform Cβ2, an unusual form of the bovine catalytic subunit of cAMP-dependent protein kinase

    Journal of Biological Chemistry

    (1991)
  • S.J Beebe et al.

    Molecular cloning of tissue-specific protein kinase (Cγ) from human testis — representing a third isoform for the catalytic subunit of cAMP-dependent protein kinase

    Molecular Endocrinology

    (1990)
  • K.C Binnington et al.

    Role of tick salivary glands in feeding and disease transmission

    Advances in Parasitology

    (1980)
  • A.S Bowman et al.

    Tick saliva: recent advances and implications for vector competence

    Medical and Veterinary Entomology

    (1997)
  • A.S Bowman et al.

    Regulation of free arachidonic acid levels in isolated salivary glands from the lone star tick: a role for dopamine

    Archives of Insect Biochemistry and Physiology

    (1995)
  • L.B Coons et al.

    The Acari-ticks

  • L.B Coons et al.

    Evidence that developmental changes in type III acini in the tick Amblyomma hebraeum (Acari:Ixodidae) are initiated by a hemolymph-borne factor

    Experimental and Applied Acarology

    (1988)
  • L.B Coons et al.

    Developmental changes in the salivary glands of male and female Dermacentor variabilis (Say) during feeding

  • L.B Coons et al.

    Evidence of a myoepithelial cell in tick salivary glands

    International Journal for Parasitology

    (1994)
  • L.B Coons et al.

    Fine structure of the salivary glands of unfed male Dermacentor variabilis (Say) (Ixodoidea: Ixodidae)

    The Journal of Parasitology

    (1973)
  • A.L Crampton et al.

    Expressed sequence tags and new genes from the cattle tick, Boophilus microplus

    Experimental and Applied Acarology

    (1998)
  • D.W Fawcett et al.

    The cell biology of the ixodid tick salivary gland

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