Microglia in invertebrate ganglia.

Sonetti, Dario; Ottaviani, Enzo; Bianchi, Francesca; Rodriguez, Madeline; Stefano, Michelle L.; Scharrer, Berta; Stefano, George B.

doi:10.1073/pnas.91.19.9180

Cited by 66 publications

(37 citation statements)

References 24 publications

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“…Indeed, the authors could identify a fragment of the estrogen receptor-beta gene with 100% sequence identity to the human counterpart (856). The egress from the excised ganglia as an assay of microglial activity was also described for the snail Planorbarius corneus and the insect Leucophaea maderae (847). Traumatic injury triggers proliferative response in microglial cells from Planorbarius corneus (712); activation of microglia was associated with expression of inducible NOS (iNOS) (711).…”

Section: Evolutionary Origins Of Microgliamentioning

confidence: 99%

Physiology of Microglia

Kettenmann

Hanisch

Нода

et al. 2011

Physiological Reviews

3,134

2,981

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Microglial cells are the resident macrophages in the central nervous system. These cells of mesodermal/mesenchymal origin migrate into all regions of the central nervous system, disseminate through the brain parenchyma, and acquire a specific ramified morphological phenotype termed “resting microglia.” Recent studies indicate that even in the normal brain, microglia have highly motile processes by which they scan their territorial domains. By a large number of signaling pathways they can communicate with macroglial cells and neurons and with cells of the immune system. Likewise, microglial cells express receptors classically described for brain-specific communication such as neurotransmitter receptors and those first discovered as immune cell-specific such as for cytokines. Microglial cells are considered the most susceptible sensors of brain pathology. Upon any detection of signs for brain lesions or nervous system dysfunction, microglial cells undergo a complex, multistage activation process that converts them into the “activated microglial cell.” This cell form has the capacity to release a large number of substances that can act detrimental or beneficial for the surrounding cells. Activated microglial cells can migrate to the site of injury, proliferate, and phagocytose cells and cellular compartments.

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Section: Evolutionary Origins Of Microgliamentioning

confidence: 99%

Physiology of Microglia

Kettenmann

Hanisch

Нода

et al. 2011

Physiological Reviews

3,134

2,981

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“…Other ganglia (five per treatment) were placed in a ring of Vaseline on a slide, and a coverslip was added to each slide. After 24 h of incubation at 20°C, the ganglia were examined for microglial egress number and conformation (see below) as described previously (7,12,13).Pharmacological additions to the incubation media plus microglia or ganglia were added first to the artificial seawater before final adjustments, following the addition of the cell-free hemolymph. Examination of cell numbers in the incubation media on the slide preparations was…”

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confidence: 99%

Cannabinoid Receptors Are Coupled to Nitric Oxide Release in Invertebrate Immunocytes, Microglia, and Human Monocytes

Stefano

Liu

Goligorsky

1996

Journal of Biological Chemistry

175

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The present study demonstrates that stereoselective binding sites for anandamide, a naturally occurring cannabinoid substance, can be found in invertebrate immunocytes and microglia. The anandamide-binding site is monophasic and of high affinity, exhibiting a K d of 34.3 nM with a B max of 441 fmol/mg protein. These sites are highly selective, as demonstrated by the inability of other types of signaling molecules to displace [ 3 H]anandamide. Furthermore, this binding site is coupled to nitric oxide release in the invertebrate tissues examined as well as in human monocytes. Interestingly, the cannabinoid-stimulated release of nitric oxide initiates cell rounding. Thus, these cannabinoid actions resemble those of opiate alkaloids. In this regard, we demonstrate that these signaling systems use the same effector system, i.e. nitric oxide release, but separate receptors. Last, the presence of a cannabinoid receptor in selected evolutionary diverse organisms indicates that this signaling system has been conserved for more than 500 million years. ␦-9-Tetrahydrocannabinol (THC)1 is the active ingredient of marijuana (1). In 1988 a receptor for this substance was identified in the rat brain (2) and subsequently cloned (3). An arachidonic acid derivative, anandamide (N-arachidonoyl-ethanolamine), was later identified as the endogenous ligand for this receptor (4). Extracellular anandamide is rapidly and selectively taken up in neurons, where its degradation to ethanolamine and arachidonate takes place (5). Thus, in a relatively short period of time, a great deal of information has been obtained on cannabinoid receptors and their ligands in mammals.In this regard, it was of interest to determine if cannabinoidbinding sites are found in invertebrates. The present report demonstrates the existance of such a cannabinoid system for the first time.[ 3 H]Anandamide-binding sites are found in Mytilus edulis immunocytes and pedal ganglia microglia membrane homogenates. Furthermore, these high affinity sites appear to be coupled to NO release. Thus, both cannabinoids and opiates share the same effector system by engaging distinct receptors (6, 7). MATERIALS AND METHODSM. edulis, a marine bivalve mollusk, were harvested from Long Island Sound at Montauk and maintained in the laboratory for 3 weeks prior to dissection (9). Invertebrate immunocytes and microglia were collected and processed as described elsewhere in detail (7,10,11).Analysis of Anandamide Binding-Immunocytes ( 10 7 ) were homogenized in 50 volume of 0.32 M sucrose, pH 7.4, at 4°C by the use of a Brinkmann Instruments Polytron (30 s, setting 5). The crude homogenate was centrifuged at 900 ϫ g for 10 min at 4°C, and the supernatant was preserved on ice. The whitish crude pellet was resuspended after homogenization (15 s, setting 5) in 30 volume of 0.32 M sucrose/Tris-HCl buffer, pH 7.4, and centrifuged at 900 ϫ g for 10 min. The extraction procedure was repeated one more time, and the combined supernatants were centrifuged at 900 ϫ g for 10 min. The resulting supern...

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“…For example, one of the activities linked to invertebrate glia is functionally associated with the blood-brain barrier integrity of insects, as well as maintenance and repair of invertebrate nerve cells [61]. In earlier reports, invertebrate immuno-competent glial cells have been demonstrated to possess similar properties as previously described for mammalian microglia including a shared set of chemical messengers such as interleukins and opioid peptides [61][62][63][64]. These morphological and biochemical similarities suggest an evolutionarily driven functional convergence of immuno-competent glial cells [62][63][64].…”

Section: Evolutionary Origin Of Microglial/neuronal Couplingmentioning

confidence: 61%

“…In earlier reports, invertebrate immuno-competent glial cells have been demonstrated to possess similar properties as previously described for mammalian microglia including a shared set of chemical messengers such as interleukins and opioid peptides [61][62][63][64]. These morphological and biochemical similarities suggest an evolutionarily driven functional convergence of immuno-competent glial cells [62][63][64]. In this regard, our group and others have demonstrated compelling anatomical and biochemical linkages between invertebrate immunocytes/microglia and mammalian monocytic/microglial/macrophage lineages that include functional utilization of a shared set of chemical messengers [27,43,44,51,[65][66][67].…”

Section: Evolutionary Origin Of Microglial/neuronal Couplingmentioning

confidence: 86%

“…As documented by video time lapse microscopy [62,74], this phenomenon is visualized by stationary microglia becoming amoeboid, macrophage-like, and mobile following traumatic stimuli in invertebrate ganglia [62][63][64]75]. By functional criteria, noted earlier, activated or polarized macrophages represent a potent immune cell type with the potential to secrete numerous neuroactive signal molecules that permit free penetration of the vertebrate the blood-brain barrier.…”

Section: Additional Functional Commonalitiesmentioning

confidence: 99%

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Evolutionary Perspective on Microglial/Neuronal Coupling with Special Relevance to Psychiatric Illnesses

Stefano¹,

Kream²

2015

J Psychiatry

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Journal of Psychiatry AbstractMicroglia have selectively evolved as a morphologically and chemically distinct class of immuno-competent CNS resident cells with potent bidirectional signaling capabilities linked to induction of a macrophage-like phenotype following metabolic, microbiological, or viral insults. It has been empirically determined that a conserved set of shared chemical messengers connects a communication network mediating reciprocal exchange of regulatory information between immune, central nervous, and neuroendocrine systems. From an evolutionary perspective, the pluripotent neuro-protective capabilities of invertebrate microglia have been extended and amplified in classes of mammalian microglia. The state-dependent plasticity of microglia has provoked considerable empirical investigation into their functional/regulatory roles in mediating innate immune surveillance and neural protection within the CNS. Upon pathophysiological dysregulation, aberrant microglial activities may provide significant contributory factors in the etiology and persistence of major neurological, degenerative, and psychiatric disorders. Within this context, invertebrate microglia appear to represent highly appropriate model systems to investigate underlying cellular and molecular mechanisms involved in higher order neuroimmune regulation of multiple CNS activities by mammalian microglia.

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Microglia in invertebrate ganglia.

Cited by 66 publications

References 24 publications

Physiology of Microglia

Physiology of Microglia

Cannabinoid Receptors Are Coupled to Nitric Oxide Release in Invertebrate Immunocytes, Microglia, and Human Monocytes

Evolutionary Perspective on Microglial/Neuronal Coupling with Special Relevance to Psychiatric Illnesses

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