Infection with intestinal helminth (Hymenolepis diminuta) impacts exploratory behavior and cognitive processes in rats by changing the central level of neurotransmitters.


Journal

PLoS pathogens
ISSN: 1553-7374
Titre abrégé: PLoS Pathog
Pays: United States
ID NLM: 101238921

Informations de publication

Date de publication:
03 2022
Historique:
received: 15 10 2021
accepted: 02 02 2022
revised: 24 03 2022
pubmed: 15 3 2022
medline: 23 4 2022
entrez: 14 3 2022
Statut: epublish

Résumé

Parasites may significantly affect the functioning of the host organism including immune response and gut-brain-axis ultimately leading to alteration of the host behavior. The impact of intestinal worms on the host central nervous system (CNS) remains unexplored. The aim of this study was to evaluate the effect of intestinal infection by the tapeworm Hymenolepis diminuta on behavior and functions of the CNS in rats. The 3 months old animals were infected, and the effects on anxiety, exploration, sensorimotor skills and learning processes were assessed at 18 months in Open Field (OF), Novel Object Recognition (NOR) and the Water Maze (WM) tests. After completing the behavioral studies, both infected and non-infected rats were sacrificed, and the collected tissues were subjected to biochemical analysis. The levels of neurotransmitters, their metabolites and amino acids in selected structures of the CNS were determined by HPLC. In addition, the gene expression profile of the pro- and anti-inflammatory cytokines (TNF-α, IL-1β, IL-6 and IL-10) was evaluated by Real-Time PCR to determine the immune response within the CNS to the tapeworm infection. The parasites caused significant changes in exploratory behavior, most notably, a reduction of velocity and total distance moved in the OF test; the infected rats exhibited decreased frequency in the central zone, which may indicate a higher level of anxiety. Additionally, parasite infestation improved spatial memory, assessed in the WM test, and recognition of new objects. These changes are related to the identified reduction in noradrenaline level in the CNS structures and less pronounced changes in striatal serotonergic neurotransmission. H. diminuta infestation was also found to cause a significant reduction of hippocampal expression of IL-6. Our results provide new data for further research on brain function during parasitic infections especially in relation to helminths and diseases in which noradrenergic system may play an important role.

Identifiants

pubmed: 35286352
doi: 10.1371/journal.ppat.1010330
pii: PPATHOGENS-D-21-02092
pmc: PMC8947016
doi:

Substances chimiques

Interleukin-6 0
Neurotransmitter Agents 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1010330

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Kamilla Blecharz-Klin (K)

Department of Experimental and Clinical Pharmacology, Medical University of Warsaw, Centre for Preclinical Research and Technology CePT, Warsaw, Poland.

Magdalena Świerczyńska (M)

Department of Experimental and Clinical Pharmacology, Medical University of Warsaw, Centre for Preclinical Research and Technology CePT, Warsaw, Poland.

Agnieszka Piechal (A)

Department of Experimental and Clinical Pharmacology, Medical University of Warsaw, Centre for Preclinical Research and Technology CePT, Warsaw, Poland.

Adriana Wawer (A)

Department of Experimental and Clinical Pharmacology, Medical University of Warsaw, Centre for Preclinical Research and Technology CePT, Warsaw, Poland.

Ilona Joniec-Maciejak (I)

Department of Experimental and Clinical Pharmacology, Medical University of Warsaw, Centre for Preclinical Research and Technology CePT, Warsaw, Poland.

Justyna Pyrzanowska (J)

Department of Experimental and Clinical Pharmacology, Medical University of Warsaw, Centre for Preclinical Research and Technology CePT, Warsaw, Poland.

Ewa Wojnar (E)

Department of Experimental and Clinical Pharmacology, Medical University of Warsaw, Centre for Preclinical Research and Technology CePT, Warsaw, Poland.

Anna Zawistowska-Deniziak (A)

W. Stefański Institute of Parasitology, Polish Academy of Sciences, Warsaw, Poland.

Anna Sulima-Celińska (A)

Department of General Biology and Parasitology, Medical University of Warsaw, Warsaw, Poland.

Daniel Młocicki (D)

W. Stefański Institute of Parasitology, Polish Academy of Sciences, Warsaw, Poland.
Department of General Biology and Parasitology, Medical University of Warsaw, Warsaw, Poland.

Dagmara Mirowska-Guzel (D)

Department of Experimental and Clinical Pharmacology, Medical University of Warsaw, Centre for Preclinical Research and Technology CePT, Warsaw, Poland.

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Classifications MeSH