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10493 2007 9120 Article-Web 1..14 Exp Appl Acarol (2007) 43:265–278 DOI 10.1007/s10493-007-9120-z Serotonin-like immunoreactivity in the central nervous system of two ixodid tick species Natalie A. Hummel · Andrew Y. Li · Colleen M. Witt Received: 14 June 2007 / Accepted: 8 November 2007 / Published online: 27 November 2007 © Springer Science+Business Media B.V. 2007 Abstract Immunocytochemistry was used to describe the distribution of serotonin-like immunoreactive (5HT-IR) neurons and neuronal processes in the central nervous system (CNS), the synganglion, of two ixodid tick species; the winter tick, Dermacentor albipictus and the lone star tick, Amblyomma americanum. 5HT-IR neurons were identiWed in the synganglion of both tick species. D. albipictus had a signiWcantly higher number of 5HT-IR neurons than A. americanum. The labeling pattern and number of 5HT-IR neurons were sig- niWcantly diVerent between sexes in D. albipictus, but were not signiWcantly diVerent between sexes in A. americanum. 5HT-IR neurons that were located in the cortex of the synganglion projected processes into the neuropils, invading neuromeres in the supraesophageal ganglion including the protocerebrum, postero-dorsal, antero-dorsal and cheliceral neuromeres. In the subesophageal ganglion, dense 5HT-IR neuronal processes were found in the olfactory lobes, This article reports the results of research only. Mention of a proprietary product does not constitute an endorsement or a recommendation by the USDA for its use. The U.S. Government’s right to retain a non-exclusive, royalty free license in and to any copyright is acknowledged. N. A. Hummel (&) · A. Y. Li (&) ARS, Knipling-Bushland U.S. Livestock Insects Research Laboratory, USDA, 2700 Fredericksburg Road, Kerrville, TX 78028, USA e-mail: [email protected] A. Y. Li e-mail: [email protected] Present Address: N. A. Hummel Department of Entomology, Louisiana State University, 404 Life Sciences Building, Baton Rouge, LA 70803, USA C. M. Witt Department of Biology, RCMI Advanced Imaging Core, University of Texas at San Antonio, 6900 North Loop 1604, San Antonio, TX 78249, USA 1 C 266 Exp Appl Acarol (2007) 43:265–278 pedal, and opisthosomal neuromeres. Double-labeling with neurobiotin backWlled from the Wrst leg damaged at the Haller’s organ revealed serotoninergic neuronal processes surround- ing the glomeruli in the olfactory lobes. The high number of the 5HT-IR neurons and the extensive neuronal processes present in various regions of the synganglion suggest that serotonin plays a signiWcant role in tick physiology. Keywords 5-Hydroxytryptamine · 5-HT · Acari · Amblyomma americanum · Dermacentor albipictus · Synganglion Introduction Ticks are among the most signiWcant vectors of arthropod-borne diseases that aVect man and animals (Drummond 2004). The most common method used to control ticks on vertebrate hosts is chemical control (George et al. 2002). Acaricides used to control ticks are mostly nerve poisons that target either the ion channels of neurons, neurotransmitter receptors, or enzymes required for the normal function of ticks (Dekeyser 2005). Resistance to major classes of these acaricides has developed in some tick species, and the resistance problem makes tick control more diYcult and also endangers the continued success of the USDA’s Cattle Fever Tick Eradication Program (CFTEP) (George et al. 2002; Li et al. 2003, 2004). One of the major reasons to study the physiology and molecular biology of ticks is to iden- tify new targets or metabolic pathways for developing novel tick control technology. Serotonin (5-hydroxytryptamine, 5-HT) is an important regulatory molecule in the neuro- nal circuit that controls feeding and salivation in many invertebrates. Serotonin-like immuno- reactivity has been identiWed in the central nervous system (CNS) of many species of invertebrates (see review by Nässel 1988) including spiders (Seyfarth et al. 1990a, b), and is a well-documented neurohormone in insects (Lange et al. 1989; Schachtner and Bräunig 1993; Coast et al. 2002; Lange 2004). The serotoninergic neuronal circuit plays a critical role in regulating the feeding of aphids and whiteXies, and a novel insecticide, pymetrozine, has been developed to speciWcally interrupt such a system, therefore achieving the control of these pest species (Harrewijn and Kayser 1997). Dacks et al. (2003) found that feeding by the Xesh Xy Neobellieria bullata (Parker) (Diptera: Sarcophagidae) decreased following seroto- nin microinjection. Fain and Berridge (1979) found that application of serotonin to isolated salivary glands of the blow Xy Calliphora erythrocephala (Diptera: Calliphoridae) stimulates Xuid secretion. Serotonin does not stimulate salivary secretions by tick salivary glands (see review by Bowman and Sauer 2004). The addition of both serotonin and histamine to a blood-meal, however, resulted in a decrease in the resistance amplitude associated with sali- vation and feeding of the Rocky Mountain wood tick, Dermacentor andersoni Stiles (Acari: Ixodidae), indicating that serotonin and histamine together have an anti-feedant eVect (Paine et al. 1983). Yet, addition of serotonin or histamine in isolation had no signiWcant eVect on the change in the resistance amplitude associated with feeding or salivation. McSwain et al. (1989) identiWed an unknown “brain factor” that induces inositol phosphate production in the salivary glands of the lone star tick Amblyomma americanum L. (Acari: Ixodidae). Inositol triphosphate (IP3) is a second messenger which may be produced following ligand binding to a G-protein coupled receptor in the cellular membrane. The identiWcation of a G-protein coupled serotonin receptor in the southern cattle tick, Rhipicephalus microplus (Canestrini) (Acari: Ixodidae) (Chen et al. 2004), along with evidence of neurosecretory activity (Binnington and Tatchell 1973) and immunocytochemical studies (Zhu and Oliver 1991, 2001) suggest that neurotransmitters and/or neuromodulators are produced in the tick synganglion. 1 C Exp Appl Acarol (2007) 43:265–278 267 Furthermore, these data suggest that serotonin may be produced in neurosecretory cells in the tick CNS. To our knowledge, the distribution of serotonin-like immunoreactivity has not been described in the tick CNS. The synganglion is the highly condensed CNS of the tick and contains neurosecretory centers that produce neurohormones (Sonenshine 1991). In ticks, all of the ganglia have been condensed to the point that they are associated directly with the “true brain” which is located in the dorsal aspect of the synganglion. The entire brain is divided into two primary tissue types: the cortex, which contains the somata (neurons), and the neuropils, which con- tain the neuronal projections of these somata. A neurilemma surrounds the CNS. The tick synganglion is divided into two regions by the esophagus which enters ventrally and exits dorsally. The region dorsal and anterior to the esophagus is the supraesophageal ganglion and the region ventral and posterior to the esophagus is the subesophageal ganglion. The objective of this study was to detect the presence of neurons and neuronal processes containing serotonin in the tick CNS, the synganglion, and compare the distribution and density of serotonin-like immunoreactive (5HT-IR) neurons and neuronal processes in both sexes of unfed winter ticks Dermacentor albipictus (Packard) (Acari: Ixodidae) and Ambly- omma americanum. D. albipictus is a one-host tick which completes its entire life-cycle on a single vertebrate host while A. americanum is a three-host tick that parasitizes many small and large vertebrates including deer and humans (Drummond 2004). In order to determine if serotoninergic neuronal processes were associated with the glomeruli in the olfactory lobe, we used a double-labeling technique involving neurobiotin backWlls from the Haller’s organ in the Wrst leg to identify the association between the olfactory glomeruli and 5HT-IR neuronal processes in the tick synganglion. This study provides a description of 5HT-IR structures in the brain of two important tick species and may provide a founda- tion from which we can develop hypotheses and test the possible function of serotonin as a regulatory molecule in tick physiology. Materials and methods Experimental animals The unfed adult A. americanum ticks were from a colony maintained at United States Department of Agriculture (USDA), Agricultural Research Service (ARS), Knipling-Bush- land U.S. Livestock Insects Research Laboratory (KBUSLIRL) in Kerrville, Texas. One- to three-month old, unfed adults were used in this study. All unfed adult ticks were main- tained at 27 § 2°C, 14:10 L:D cycle and a RH of 85% in an incubator with a saturated salt solution. The unfed adult D. albipictus ticks were obtained by infesting larvae under a mus- lin sleeve on the back of a stanchioned Hereford heifer calf at the KBUSLIRL. Larvae were allowed to develop to the metanymphal stage, after which they were forcibly removed from the host (Li et al. 2005) and maintained under the same conditions as for A. americanum until they molted to the adult stage. All unfed D. albipictus adult ticks used in this study were dissected within 24 h after molting. Neurobiotin and general anatomy An unfed adult female A. americanum was placed dorsal side up on a strip of utility wax (Heraeus Kulzer, Armonk, NY, USA) on a glass slide. Ticks were fed 1% Neurobiotin (Vector Laboratories, Inc., Burlingame, CA, USA) in 0.1 M KCl through a #2 capillary tube 1 C 268 Exp Appl Acarol (2007) 43:265–278 (Drummond ScientiWc Co., Broomall, PA, USA) placed over the hypostome. Neurobiotin is an intracellular neuronal tracer molecule that has been used widely for labeling neurons through either intracellular injection or backWll from the end of a nerve. The capillary tubes were removed after 1.5 h, and the slides placed on ice to anesthetize ticks before dissection in cold 4% paraformaldehyde followed by Wxation in 4% paraformaldehyde in 0.1 M PBS (pH 7.4) at 4°C overnight. They were then washed multiple times in Millonig’s Phosphate V Bu er (MPB; 0.164 M NaH2PO4·H2O:0.63 M NaOH (4:1); pH 7.0) followed by dehydra- tion in a graded ethanol series, acetone, and rehydration in a graded ethanol series.
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