The Sexual Dimorphism of the Neuroimmune Response in the Brains of <i>Taenia crassiceps</i>-Infected Mice

Background: Helminth infections are associated with cognitive deficits, especially in school-age children. Deworming treatment in heavily infected children improves their short- and long-term memory recall. In mice, intraperitoneal helminth infection with <i>Taenia crassiceps</i> (<i&...

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Main Authors: Karen Elizabeth Nava-Castro, Diana Lizeth Ruiz-Antonio, María del Sol Ríos-Avila, Claudia Angélica Garay-Canales, Lenin Pavón, Romel Hernandez-Bello, Víctor Hugo Del Río-Araiza, Manuel Iván Girón-Pérez, Jorge Morales-Montor
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Language:English
Published: MDPI AG 2024-11-01
Series:Brain Sciences
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Online Access:https://www.mdpi.com/2076-3425/14/11/1127
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author Karen Elizabeth Nava-Castro
Diana Lizeth Ruiz-Antonio
María del Sol Ríos-Avila
Claudia Angélica Garay-Canales
Lenin Pavón
Romel Hernandez-Bello
Víctor Hugo Del Río-Araiza
Manuel Iván Girón-Pérez
Jorge Morales-Montor
author_facet Karen Elizabeth Nava-Castro
Diana Lizeth Ruiz-Antonio
María del Sol Ríos-Avila
Claudia Angélica Garay-Canales
Lenin Pavón
Romel Hernandez-Bello
Víctor Hugo Del Río-Araiza
Manuel Iván Girón-Pérez
Jorge Morales-Montor
author_sort Karen Elizabeth Nava-Castro
collection DOAJ
description Background: Helminth infections are associated with cognitive deficits, especially in school-age children. Deworming treatment in heavily infected children improves their short- and long-term memory recall. In mice, intraperitoneal helminth infection with <i>Taenia crassiceps</i> (<i>T. crassiceps</i>) shows sexual dimorphism in terms of the parasite load, immune response, hormone levels, and behavioral changes. We have previously shown poorer short-term memory performance and changes in the concentrations of cytokines and neurotransmitters in the hippocampus, which were replicated in this study. The molecular changes in other brain structures, such as those related to reproduction, are unknown. Methods: Male and female Balb/cAnN mice were chronically infected with <i>T. crassiceps</i> larvae. We determined the peritoneal parasite load and established the presence of cytokines and neurotransmitters in the hippocampus, olfactory bulb, and hypothalamus. Results: The parasite load was higher in female than male infected mice, as expected. In the hippocampus, the neurotransmitters norepinephrine and serotonin increased in males but decreased in females. In contrast, in the olfactory bulb and hypothalamus, the neurotransmitters assessed showed no statistical differences. The cytokine profiles were different in each brain structure. The TNF-α levels in the olfactory bulb and the IL-4 levels in the hippocampus of infected mice were dimorphic; IFN-γ was augmented in both male and female infected animals, although the increase was higher in infected males. Conclusions: The brain responds to peripheral infection with cytokine levels that vary from structure to structure. This could be a partial explanation for the dimorphic behavioral alterations associated with infection, it also demonstrates the synergic interaction between the immune, the endocrine, and the nervous systems.
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spelling doaj-art-11207b10527b4bbc8a4e7f9c7f7d69662025-08-20T02:28:11ZengMDPI AGBrain Sciences2076-34252024-11-011411112710.3390/brainsci14111127The Sexual Dimorphism of the Neuroimmune Response in the Brains of <i>Taenia crassiceps</i>-Infected MiceKaren Elizabeth Nava-Castro0Diana Lizeth Ruiz-Antonio1María del Sol Ríos-Avila2Claudia Angélica Garay-Canales3Lenin Pavón4Romel Hernandez-Bello5Víctor Hugo Del Río-Araiza6Manuel Iván Girón-Pérez7Jorge Morales-Montor8Grupo de Biología y Química Atmosféricas, Departamento de Ciencias Ambientales, Instituto de Ciencias de la Atmósfera y Cambio Climático, Universidad Nacional Autónoma de México, Ciudad de México 04510, Coyoacán, MexicoDepartamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Ciudad de México 04510, Coyoacán, MexicoGrupo de Biología y Química Atmosféricas, Departamento de Ciencias Ambientales, Instituto de Ciencias de la Atmósfera y Cambio Climático, Universidad Nacional Autónoma de México, Ciudad de México 04510, Coyoacán, MexicoDepartamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Ciudad de México 04510, Coyoacán, MexicoLaboratorio de Psicoinmunología de la Dirección de Investigaciones en Neurociencias, Instituto Nacional de Psiquiatría “Ramón de la Fuente Muñiz”, Ciudad de México 14370, Tlalpan, MexicoDepartamento de Microbiología, Facultad de Medicina, Universidad Autónoma de Nuevo León, Monterrey 64260, Nuevo León, MexicoDepartamento de Parasitología, Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, Ciudad de México 04510, Coyoacán, MexicoLaboratorio de Inmunotoxicología, Secretaría de Investigación y Posgrado, Universidad Autónoma de Nayarit, Tepic 63184, Nayarit, MexicoDepartamento de Inmunología, Instituto de Investigaciones Biomédicas, Universidad Nacional Autónoma de México, Ciudad de México 04510, Coyoacán, MexicoBackground: Helminth infections are associated with cognitive deficits, especially in school-age children. Deworming treatment in heavily infected children improves their short- and long-term memory recall. In mice, intraperitoneal helminth infection with <i>Taenia crassiceps</i> (<i>T. crassiceps</i>) shows sexual dimorphism in terms of the parasite load, immune response, hormone levels, and behavioral changes. We have previously shown poorer short-term memory performance and changes in the concentrations of cytokines and neurotransmitters in the hippocampus, which were replicated in this study. The molecular changes in other brain structures, such as those related to reproduction, are unknown. Methods: Male and female Balb/cAnN mice were chronically infected with <i>T. crassiceps</i> larvae. We determined the peritoneal parasite load and established the presence of cytokines and neurotransmitters in the hippocampus, olfactory bulb, and hypothalamus. Results: The parasite load was higher in female than male infected mice, as expected. In the hippocampus, the neurotransmitters norepinephrine and serotonin increased in males but decreased in females. In contrast, in the olfactory bulb and hypothalamus, the neurotransmitters assessed showed no statistical differences. The cytokine profiles were different in each brain structure. The TNF-α levels in the olfactory bulb and the IL-4 levels in the hippocampus of infected mice were dimorphic; IFN-γ was augmented in both male and female infected animals, although the increase was higher in infected males. Conclusions: The brain responds to peripheral infection with cytokine levels that vary from structure to structure. This could be a partial explanation for the dimorphic behavioral alterations associated with infection, it also demonstrates the synergic interaction between the immune, the endocrine, and the nervous systems.https://www.mdpi.com/2076-3425/14/11/1127sexual dimorphismneuroinflammationneurotransmitterscytokinescysticercosis<i>Taenia crassiceps</i>
spellingShingle Karen Elizabeth Nava-Castro
Diana Lizeth Ruiz-Antonio
María del Sol Ríos-Avila
Claudia Angélica Garay-Canales
Lenin Pavón
Romel Hernandez-Bello
Víctor Hugo Del Río-Araiza
Manuel Iván Girón-Pérez
Jorge Morales-Montor
The Sexual Dimorphism of the Neuroimmune Response in the Brains of <i>Taenia crassiceps</i>-Infected Mice
Brain Sciences
sexual dimorphism
neuroinflammation
neurotransmitters
cytokines
cysticercosis
<i>Taenia crassiceps</i>
title The Sexual Dimorphism of the Neuroimmune Response in the Brains of <i>Taenia crassiceps</i>-Infected Mice
title_full The Sexual Dimorphism of the Neuroimmune Response in the Brains of <i>Taenia crassiceps</i>-Infected Mice
title_fullStr The Sexual Dimorphism of the Neuroimmune Response in the Brains of <i>Taenia crassiceps</i>-Infected Mice
title_full_unstemmed The Sexual Dimorphism of the Neuroimmune Response in the Brains of <i>Taenia crassiceps</i>-Infected Mice
title_short The Sexual Dimorphism of the Neuroimmune Response in the Brains of <i>Taenia crassiceps</i>-Infected Mice
title_sort sexual dimorphism of the neuroimmune response in the brains of i taenia crassiceps i infected mice
topic sexual dimorphism
neuroinflammation
neurotransmitters
cytokines
cysticercosis
<i>Taenia crassiceps</i>
url https://www.mdpi.com/2076-3425/14/11/1127
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