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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

Putative glutamine synthetase immunoreactivity (GS-IR, green) in the brain of G. insensibilis. Cell nuclei are counterstained with propidium iodide (red label). (a) to (c) Various glial cell morphologies. Note the end feet and the flocculent profiles of the astrocyte-like cell shown in (a). (d and e) GS-IR in brains of MAD gammarids. Glial cell bodies are present at the surface of the metacercariae. Fine processes (arrow) are apposed to the cystic wall in this stack of confocal sections through a metacercaria (e). (f) and (g) Confocal sections at different levels of an invagination of the cyst wall in a metacercaria. The sections are tangential to the cyst; a section at the surface of the metacercaria (f) shows flocculent glial profiles around the opening of the invagination (arrow); a section taken through the cyst wall reveals the GS-IR wall of the invagination (g); (h) Brain of a MAD gammarid with one live and one encapsulated metacercaria. The asterisk indicates a larva encapsulated and presumably moribund. The arrow points to the invagination of the cyst wall presented in pictures (f) an (g) in a second metacercaria. In (c), (f), (g), (h), single confocal sections; in (a), (b), (c insert), (d), (e), stacks of confocal sections. For clarity the propidium iodide counterstain has been omitted in (a) and in the insert of (c). Anterior is up; h, host; p, parasite. Scale bars: (c), (d), (h) 300 µm; (a), (b), (e), 50 µm; (f), (g), 20 µm.
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Figure 3: Putative glutamine synthetase immunoreactivity (GS-IR, green) in the brain of G. insensibilis. Cell nuclei are counterstained with propidium iodide (red label). (a) to (c) Various glial cell morphologies. Note the end feet and the flocculent profiles of the astrocyte-like cell shown in (a). (d and e) GS-IR in brains of MAD gammarids. Glial cell bodies are present at the surface of the metacercariae. Fine processes (arrow) are apposed to the cystic wall in this stack of confocal sections through a metacercaria (e). (f) and (g) Confocal sections at different levels of an invagination of the cyst wall in a metacercaria. The sections are tangential to the cyst; a section at the surface of the metacercaria (f) shows flocculent glial profiles around the opening of the invagination (arrow); a section taken through the cyst wall reveals the GS-IR wall of the invagination (g); (h) Brain of a MAD gammarid with one live and one encapsulated metacercaria. The asterisk indicates a larva encapsulated and presumably moribund. The arrow points to the invagination of the cyst wall presented in pictures (f) an (g) in a second metacercaria. In (c), (f), (g), (h), single confocal sections; in (a), (b), (c insert), (d), (e), stacks of confocal sections. For clarity the propidium iodide counterstain has been omitted in (a) and in the insert of (c). Anterior is up; h, host; p, parasite. Scale bars: (c), (d), (h) 300 µm; (a), (b), (e), 50 µm; (f), (g), 20 µm.

Mentions: Putative glutamine synthetase immunoreactive (GS-IR) cell bodies were distributed throughout the brain at the level of the neuropils in both MAD (with metacercaria and altered demeanor) and normal gammarids. GS-IR cells showed a variety of morphology: "astrocyte"-like, x- shaped, or globular (Fig. 3). Large astrocyte-like cells spanning more than 100 μm extended fine processes terminating in end feet and flocculent material (Fig. 3a). Other GS-IR cells were more compact (Fig. 3b). The most noticeable glial cell bodies formed a sheath at the surface of the neuropils and extended thin processes within the tangle of neurites, thus staining the entire neuropil. The antennal neuropils were generally the most intensely immunoreactive whereas the olfactory lobes were less densely labeled. A pair of prominent identifiable cells was present in every individual laterally on either side of the brain, projecting fine extensions toward the center of the optic lobes (Fig. 3c).


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

Helluy S, Thomas F - Parasit Vectors (2010)

Putative glutamine synthetase immunoreactivity (GS-IR, green) in the brain of G. insensibilis. Cell nuclei are counterstained with propidium iodide (red label). (a) to (c) Various glial cell morphologies. Note the end feet and the flocculent profiles of the astrocyte-like cell shown in (a). (d and e) GS-IR in brains of MAD gammarids. Glial cell bodies are present at the surface of the metacercariae. Fine processes (arrow) are apposed to the cystic wall in this stack of confocal sections through a metacercaria (e). (f) and (g) Confocal sections at different levels of an invagination of the cyst wall in a metacercaria. The sections are tangential to the cyst; a section at the surface of the metacercaria (f) shows flocculent glial profiles around the opening of the invagination (arrow); a section taken through the cyst wall reveals the GS-IR wall of the invagination (g); (h) Brain of a MAD gammarid with one live and one encapsulated metacercaria. The asterisk indicates a larva encapsulated and presumably moribund. The arrow points to the invagination of the cyst wall presented in pictures (f) an (g) in a second metacercaria. In (c), (f), (g), (h), single confocal sections; in (a), (b), (c insert), (d), (e), stacks of confocal sections. For clarity the propidium iodide counterstain has been omitted in (a) and in the insert of (c). Anterior is up; h, host; p, parasite. Scale bars: (c), (d), (h) 300 µm; (a), (b), (e), 50 µm; (f), (g), 20 µm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Putative glutamine synthetase immunoreactivity (GS-IR, green) in the brain of G. insensibilis. Cell nuclei are counterstained with propidium iodide (red label). (a) to (c) Various glial cell morphologies. Note the end feet and the flocculent profiles of the astrocyte-like cell shown in (a). (d and e) GS-IR in brains of MAD gammarids. Glial cell bodies are present at the surface of the metacercariae. Fine processes (arrow) are apposed to the cystic wall in this stack of confocal sections through a metacercaria (e). (f) and (g) Confocal sections at different levels of an invagination of the cyst wall in a metacercaria. The sections are tangential to the cyst; a section at the surface of the metacercaria (f) shows flocculent glial profiles around the opening of the invagination (arrow); a section taken through the cyst wall reveals the GS-IR wall of the invagination (g); (h) Brain of a MAD gammarid with one live and one encapsulated metacercaria. The asterisk indicates a larva encapsulated and presumably moribund. The arrow points to the invagination of the cyst wall presented in pictures (f) an (g) in a second metacercaria. In (c), (f), (g), (h), single confocal sections; in (a), (b), (c insert), (d), (e), stacks of confocal sections. For clarity the propidium iodide counterstain has been omitted in (a) and in the insert of (c). Anterior is up; h, host; p, parasite. Scale bars: (c), (d), (h) 300 µm; (a), (b), (e), 50 µm; (f), (g), 20 µm.
Mentions: Putative glutamine synthetase immunoreactive (GS-IR) cell bodies were distributed throughout the brain at the level of the neuropils in both MAD (with metacercaria and altered demeanor) and normal gammarids. GS-IR cells showed a variety of morphology: "astrocyte"-like, x- shaped, or globular (Fig. 3). Large astrocyte-like cells spanning more than 100 μm extended fine processes terminating in end feet and flocculent material (Fig. 3a). Other GS-IR cells were more compact (Fig. 3b). The most noticeable glial cell bodies formed a sheath at the surface of the neuropils and extended thin processes within the tangle of neurites, thus staining the entire neuropil. The antennal neuropils were generally the most intensely immunoreactive whereas the olfactory lobes were less densely labeled. A pair of prominent identifiable cells was present in every individual laterally on either side of the brain, projecting fine extensions toward the center of the optic lobes (Fig. 3c).

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