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Parasitic manipulation and neuroinflammation: Evidence from the system Microphallus papillorobustus (Trematoda) - Gammarus (Crustacea).

Helluy S, Thomas F - Parasit Vectors (2010)

Bottom Line: Immunocytochemical experiments followed by confocal microscopy were performed to study the distribution of glutamine synthetase, a glial cell marker, and nitric oxide synthase in the brain of gammarids.Astrocyte-like glia and their processes were abundant at the surface of the parasites while levels of nitric oxide synthase were elevated at the host-parasite interface in the brain of gammarids harboring mature cerebral larvae and demonstrating altered behavior.Taken together these results lend support to the neuroinflammation hypothesis whereby a chronic CNS specific immune response induced by the parasite plays a role in the disruption of neuromodulation, neuronal integrity, and behavior in infected hosts.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences, Wellesley College, Wellesley, MA 02481, USA. shelluy@wellesley.edu.

ABSTRACT

Background: Neuropathological consequences of neuroinflammatory processes have been implicated in a wide range of diseases affecting the central nervous system (CNS). Glial cells, the resident immune cells of the CNS, respond to tissue injury by releasing proinflammatory cytokines and free radicals such as nitric oxide. We explored the possibility that neuroimmune responses are involved in parasitic manipulation of host behavior in a trematode-crustacean association. The cerebral larva of the flatworm Microphallus papillorobustus alters responses to environmental stimuli - and thus reflex pathways - in the crustacean Gammarus insensibilis, in a way that enhances predation of the crustacean by birds, definitive hosts of the parasite.

Results: Immunocytochemical experiments followed by confocal microscopy were performed to study the distribution of glutamine synthetase, a glial cell marker, and nitric oxide synthase in the brain of gammarids. Astrocyte-like glia and their processes were abundant at the surface of the parasites while levels of nitric oxide synthase were elevated at the host-parasite interface in the brain of gammarids harboring mature cerebral larvae and demonstrating altered behavior.

Conclusion: Taken together these results lend support to the neuroinflammation hypothesis whereby a chronic CNS specific immune response induced by the parasite plays a role in the disruption of neuromodulation, neuronal integrity, and behavior in infected hosts.

No MeSH data available.


Related in: MedlinePlus

Larvae of Microphallus papillorobustus in whole mount brains of G. insensibilis. (a) The arrow indicates a mature metacercaria encysted in the protocerebrum, while the arrowhead points to a young larva partially melanized in the deutocerebrum of a gammarid with altered behavior (MAD). Red lipidic granules are seen at the surface of the brain. (b) A dead metacercaria is encapsulated and melanized in the protocerebrum of a normal gammarid. Anterior is up in these whole mounts viewed with a stereomicroscope. The brains are approximately 1 mm wide.
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Figure 1: Larvae of Microphallus papillorobustus in whole mount brains of G. insensibilis. (a) The arrow indicates a mature metacercaria encysted in the protocerebrum, while the arrowhead points to a young larva partially melanized in the deutocerebrum of a gammarid with altered behavior (MAD). Red lipidic granules are seen at the surface of the brain. (b) A dead metacercaria is encapsulated and melanized in the protocerebrum of a normal gammarid. Anterior is up in these whole mounts viewed with a stereomicroscope. The brains are approximately 1 mm wide.

Mentions: A simple behavioral test, knocking on the side of the glass aquarium, was used to ascribe each gammarid to one of two categories: "altered behavior" if the animal swam to the surface toward the overhead light, or "normal behavior" if the animal did not swim to the surface following disturbance. For each brain of the September sample, the following characteristics were noted: behavioral status, presence of metacercariae of M. papillorobustus in the brain, presence of metacercariae belonging to various species in the body (M. papillorobustus, Maritrema subdolum, and other microphallids), and presence of nematodes including Gammarinema gammari (Table 1). All the gammarids with abnormal behavior were infected with at least one fully-developed cerebral metacercaria of M. papillorobustus but harbored up to 13 cysts (length of cysts: 280 to 330 μm; thickness of cyst wall: 15 to 25 μm). A large proportion of normal gammarids (38%) was also infected with cerebral metacercariae, young ones with thin cyst walls, but also larvae encapsulated and melanized (Fig. 1), and larvae apparently mature. Signs of melanization were observed in 13% of the brains (n = 115) but were not seen in the abdomen.


Parasitic manipulation and neuroinflammation: Evidence from the system Microphallus papillorobustus (Trematoda) - Gammarus (Crustacea).

Helluy S, Thomas F - Parasit Vectors (2010)

Larvae of Microphallus papillorobustus in whole mount brains of G. insensibilis. (a) The arrow indicates a mature metacercaria encysted in the protocerebrum, while the arrowhead points to a young larva partially melanized in the deutocerebrum of a gammarid with altered behavior (MAD). Red lipidic granules are seen at the surface of the brain. (b) A dead metacercaria is encapsulated and melanized in the protocerebrum of a normal gammarid. Anterior is up in these whole mounts viewed with a stereomicroscope. The brains are approximately 1 mm wide.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2874546&req=5

Figure 1: Larvae of Microphallus papillorobustus in whole mount brains of G. insensibilis. (a) The arrow indicates a mature metacercaria encysted in the protocerebrum, while the arrowhead points to a young larva partially melanized in the deutocerebrum of a gammarid with altered behavior (MAD). Red lipidic granules are seen at the surface of the brain. (b) A dead metacercaria is encapsulated and melanized in the protocerebrum of a normal gammarid. Anterior is up in these whole mounts viewed with a stereomicroscope. The brains are approximately 1 mm wide.
Mentions: A simple behavioral test, knocking on the side of the glass aquarium, was used to ascribe each gammarid to one of two categories: "altered behavior" if the animal swam to the surface toward the overhead light, or "normal behavior" if the animal did not swim to the surface following disturbance. For each brain of the September sample, the following characteristics were noted: behavioral status, presence of metacercariae of M. papillorobustus in the brain, presence of metacercariae belonging to various species in the body (M. papillorobustus, Maritrema subdolum, and other microphallids), and presence of nematodes including Gammarinema gammari (Table 1). All the gammarids with abnormal behavior were infected with at least one fully-developed cerebral metacercaria of M. papillorobustus but harbored up to 13 cysts (length of cysts: 280 to 330 μm; thickness of cyst wall: 15 to 25 μm). A large proportion of normal gammarids (38%) was also infected with cerebral metacercariae, young ones with thin cyst walls, but also larvae encapsulated and melanized (Fig. 1), and larvae apparently mature. Signs of melanization were observed in 13% of the brains (n = 115) but were not seen in the abdomen.

Bottom Line: Immunocytochemical experiments followed by confocal microscopy were performed to study the distribution of glutamine synthetase, a glial cell marker, and nitric oxide synthase in the brain of gammarids.Astrocyte-like glia and their processes were abundant at the surface of the parasites while levels of nitric oxide synthase were elevated at the host-parasite interface in the brain of gammarids harboring mature cerebral larvae and demonstrating altered behavior.Taken together these results lend support to the neuroinflammation hypothesis whereby a chronic CNS specific immune response induced by the parasite plays a role in the disruption of neuromodulation, neuronal integrity, and behavior in infected hosts.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences, Wellesley College, Wellesley, MA 02481, USA. shelluy@wellesley.edu.

ABSTRACT

Background: Neuropathological consequences of neuroinflammatory processes have been implicated in a wide range of diseases affecting the central nervous system (CNS). Glial cells, the resident immune cells of the CNS, respond to tissue injury by releasing proinflammatory cytokines and free radicals such as nitric oxide. We explored the possibility that neuroimmune responses are involved in parasitic manipulation of host behavior in a trematode-crustacean association. The cerebral larva of the flatworm Microphallus papillorobustus alters responses to environmental stimuli - and thus reflex pathways - in the crustacean Gammarus insensibilis, in a way that enhances predation of the crustacean by birds, definitive hosts of the parasite.

Results: Immunocytochemical experiments followed by confocal microscopy were performed to study the distribution of glutamine synthetase, a glial cell marker, and nitric oxide synthase in the brain of gammarids. Astrocyte-like glia and their processes were abundant at the surface of the parasites while levels of nitric oxide synthase were elevated at the host-parasite interface in the brain of gammarids harboring mature cerebral larvae and demonstrating altered behavior.

Conclusion: Taken together these results lend support to the neuroinflammation hypothesis whereby a chronic CNS specific immune response induced by the parasite plays a role in the disruption of neuromodulation, neuronal integrity, and behavior in infected hosts.

No MeSH data available.


Related in: MedlinePlus