Localization of tyrosine hydroxylase-like immunoreactivity in the nervous systems of Biomphalaria glabrata and Biomphalaria alexandrina, intermediate hosts for schistosomiasis

Theodor Bilharz Research Institute

Bibliographic Information

Authors: Vallejo D.; Habib M.R.; Delgado N.; Vaasjo L.O.; Croll R.P.; Miller M.W.

Journal: Journal of Comparative Neurology

Publisher: Wiley-Liss Inc.

Publication Date: 4 April 2014

Volume / Issue: Volume 522 / Issue 11

Pages: 2532–2552

ISSN: 219967

DOI: 10.1002/cne.23548

Scopus: View on Scopus

PubMed: 24477836

Document Type: Article

Access: All Open Access; Green Open Access

Authors and Affiliations

Vallejo D., Institute of Neurobiology, Department of Anatomy and Neurobiology, University of Puerto Rico, San Juan, Puerto Rico 00901, Medical Sciences Campus, United States; Habib M.R., Department of Physiology and Biophysics, Dalhousie University, Halifax, NS, B3H 4R2, Canada, Medical Malacology Laboratory, Theodor Bilharz Research Institute, Giza, Egypt; Delgado N., Institute of Neurobiology, Department of Anatomy and Neurobiology, University of Puerto Rico, San Juan, Puerto Rico 00901, Medical Sciences Campus, United States; Vaasjo L.O., Institute of Neurobiology, Department of Anatomy and Neurobiology, University of Puerto Rico, San Juan, Puerto Rico 00901, Medical Sciences Campus, United States; Croll R.P., Department of Physiology and Biophysics, Dalhousie University, Halifax, NS, B3H 4R2, Canada; Miller M.W., Institute of Neurobiology, Department of Anatomy and Neurobiology, University of Puerto Rico, San Juan, Puerto Rico 00901, Medical Sciences Campus, United States

Abstract

Planorbid snails of the genus Biomphalaria are major intermediate hosts for the digenetic trematode parasite Schistosoma mansoni. Evidence suggests that levels of the neurotransmitter dopamine (DA) are reduced during the course of S. mansoni multiplication and transformation within the snail. This investigation used immunohistochemical methods to localize tyrosine hydroxylase (TH), the rate-limiting enzyme in the biosynthesis of catecholamines, in the nervous system of Biomphalaria. The two species examined, Biomphalaria glabrata and Biomphalaria alexandrina, are the major intermediate hosts for S. mansoni in sub-Saharan Africa, where more than 90% of global cases of human intestinal schistosomiasis occur. TH-like immunoreactive (THli) neurons were distributed throughout the central nervous system (CNS) and labeled fibers were present in all commissures, connectives, and nerves. Some asymmetries were observed, including a large distinctive neuron (LPeD1) in the pedal ganglion described previously in several pulmonates. The majority of TH-like immunoreactive neurons were detected in the peripheral nervous system (PNS), especially in lip and foot regions of the anterior integument. Independent observations supporting the dopaminergic phenotype of THli neurons included 1) block of LPeD1 synaptic signaling by the D2/3 antagonist sulpiride, and 2) the similar localization of aqueous aldehyde (FaGlu)-induced fluorescence. The distribution of THli neurons indicates that, as in other gastropods, dopamine functions as a sensory neurotransmitter and in the regulation of feeding and reproductive behaviors in Biomphalaria. It is hypothesized that infection could stimulate transmitter release from dopaminergic sensory neurons and that dopaminergic signaling could contribute to modifications of both host and parasite behavior. © 2014 Wiley Periodicals, Inc.

Keywords

Dopamine; Pond snail; Pulmonate mollusk; Schistosoma mansoni; Trematode; Animals; Biomphalaria; Catecholamines; Central Nervous System; Coloring Agents; Dopamine Antagonists; Formaldehyde; Ganglia, Invertebrate; Glutaral; Immunohistochemistry; Neurons; Peripheral Nervous System; Species Specificity; Sulpiride; Synaptic Transmission; Tyrosine 3-Monooxygenase; aldehyde; catecholamine; neurotransmitter; tyrosine 3 monooxygenase; coloring agent; dopamine receptor blocking agent; glutaraldehyde; animal cell; animal tissue; article; Biomphalaria alexandrina; Biomphalaria glabrata; brain ganglion; controlled study; dopaminergic system; enzyme localization; enzyme mechanism; fluorescence analysis; immunoreactivity; integument; nonhuman; priority journal; signal transduction; animal; comparative study; cytology; drug effects; enzymology; ganglion; metabolism; nerve cell; parasitology; physiology; species difference

Citation Information

Scopus Citations: 34

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