Cholinergic Signaling Regulates Macrophage Migration During Acute and Chronic Inflammation via Α7 Nicotinic Acetylcholine Receptor

Authors' Affiliations

Kasey Keever, Department of Biomedical Sciences, Quillen College of Medicine, East Tennessee State University, Johnson City, TN Kui Cui, Department of Biomedical Sciences, Quillen College of Medicine, East Tennessee State University, Johnson City, TN Nicole Ceausu, Department of Biomedical Sciences, Quillen College of Medicine, East Tennessee State University, Johnson City, TN Meghan Addorioso, Center for Biomedical Science and Center for Bioelectronic Medicine, The Feinstein Institute for Medical Research, Northwell Health, Manhasset, NY, USA David L. Williams, Department Of Surgery, Center for Excellence in Inflammation, Infectious Disease and Immunity, East Tennessee State University, Johnson City, TN Valentin A. Pavlov, Center for Biomedical Science and Center for Bioelectronic Medicine, The Feinstein Institute for Medical Research, Northwell Health, Manhasset, NY, US; Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Hempstead, NY 11550, USA Valentin Yakubenko, Department of Biomedical Sciences, Center for Excellence in Inflammation, Immunity and Infectious Disease, East Tennessee State University, Johnson City, TN

Location

Culp Room 303

Start Date

4-6-2022 10:00 AM

End Date

4-6-2022 11:00 AM

Faculty Sponsor’s Department

Biomedical Sciences

Name of Project's Faculty Sponsor

Valentin Yakubenko

Additional Sponsors

Antonio Rusinol, Tammy Ozment-Skelton, Chuanfu Li, Robert Schoborg, Valentin Yakubenko

Classification of First Author

Graduate Student-Doctoral

Competition Type

Non-Competitive

Type

Oral Presentation

Project's Category

Immune System

Abstract or Artist's Statement

The a7 nicotinic acetylcholine receptor (a7nAChR) expressed on macrophages, a critical link between the neural and immune systems, provides a defense mechanism during inflammatory diseases. Release of acetylcholine in target tissues activates a7nAChR, a necessary element of the cholinergic anti-inflammatory pathway, inhibiting pro-inflammatory signaling pathways via NF-kB. However, other potential aspects of a7nAChR function are not well understood.

The purpose of our project is to evaluate the role of a7nAChR activation in macrophage migration and accumulation at the site of inflammation. We first evaluated the survival of WT and a7nAChR-/- mice during LPS-induced endotoxemia. We found that a7nAChR-/- mice have significantly decreased survival compared to WT.

We next examined differences in monocyte migration by tracking adoptively transferred, fluorescently labeled a7nAChR-/- and WT monocytes in the model of LPS-induced endotoxemia using flow cytometry and imaging flow cytometry. We found that a7nAChR-/- monocytes have significantly reduced migration to the lung, liver, and spleen during endotoxemia, in both a7nAChR-/- and WT recipient mice.

Based on this result, we investigated if adoptive transfer of WT or a7nAChR-/- monocytes would decrease or improve survival in LPS-induced endotoxemia. Adoptively transferred, unlabeled WT monocytes improved survival in a7nAChR-/- recipient mice, though this effect did not reach significance. Survival was unaffected by adoptive transfer of a7nAChR-/- monocytes. Notably, this data coincides with the protective role of both macrophages and a7nAChR during sepsis that has been demonstrated in multiple recent publications.

To reveal a potential mechanism, we tested the effect of a7nAChR-deficiency on the expression of adhesive and chemokine receptors at the macrophage surface. We selected 10 receptors to evaluate via qRT-PCR and flow cytometry. Our qRT-PCR experiments demonstrated a significantly reduced expression in CCR5, CCR2, integrin αMß2, and integrin αXß2 in a7nAChR-/- peritoneal macrophages, when compared to WT. The reduction in expression of CCR2 and αXß2 was corroborated by our flow cytometry results. Interestingly, the decrease in CCR5 and αMß2 was lower, but still detectable, and this discrepancy can be attributed to post transcriptional regulation of these receptors.

The role of these receptors was further investigated in an in vitro 3D migration assay. Macrophages deficient in a7nAChR showed significantly decreased migration within a fibrin matrix (integrin αMß2 dependent) along a RANTES gradient (CCR5-mediated). The reduction in the migration of a7nAChR-/- macrophages toward MCP-1 (CCR2-mediated) did not reach significance, although still measurable. This experiment confirmed the chemokine-independent contribution of αMß2 to mesenchymal macrophage migration. These protective effects of αMß2 and CCR5 during sepsis were reported previously and are related to the regulation of monocyte recruitment and efflux at the site of inflammation.

In summary, we discovered a new link between the parasympathetic nervous system and immune response based on a7nAChR-regulated macrophage migration during inflammation. The signaling pathway downstream of a7nAChR that modulates αMß2 and CCR5 expression is yet to be identified and is the objective of our ongoing investigation.

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Apr 6th, 10:00 AM Apr 6th, 11:00 AM

Cholinergic Signaling Regulates Macrophage Migration During Acute and Chronic Inflammation via Α7 Nicotinic Acetylcholine Receptor

Culp Room 303

The a7 nicotinic acetylcholine receptor (a7nAChR) expressed on macrophages, a critical link between the neural and immune systems, provides a defense mechanism during inflammatory diseases. Release of acetylcholine in target tissues activates a7nAChR, a necessary element of the cholinergic anti-inflammatory pathway, inhibiting pro-inflammatory signaling pathways via NF-kB. However, other potential aspects of a7nAChR function are not well understood.

The purpose of our project is to evaluate the role of a7nAChR activation in macrophage migration and accumulation at the site of inflammation. We first evaluated the survival of WT and a7nAChR-/- mice during LPS-induced endotoxemia. We found that a7nAChR-/- mice have significantly decreased survival compared to WT.

We next examined differences in monocyte migration by tracking adoptively transferred, fluorescently labeled a7nAChR-/- and WT monocytes in the model of LPS-induced endotoxemia using flow cytometry and imaging flow cytometry. We found that a7nAChR-/- monocytes have significantly reduced migration to the lung, liver, and spleen during endotoxemia, in both a7nAChR-/- and WT recipient mice.

Based on this result, we investigated if adoptive transfer of WT or a7nAChR-/- monocytes would decrease or improve survival in LPS-induced endotoxemia. Adoptively transferred, unlabeled WT monocytes improved survival in a7nAChR-/- recipient mice, though this effect did not reach significance. Survival was unaffected by adoptive transfer of a7nAChR-/- monocytes. Notably, this data coincides with the protective role of both macrophages and a7nAChR during sepsis that has been demonstrated in multiple recent publications.

To reveal a potential mechanism, we tested the effect of a7nAChR-deficiency on the expression of adhesive and chemokine receptors at the macrophage surface. We selected 10 receptors to evaluate via qRT-PCR and flow cytometry. Our qRT-PCR experiments demonstrated a significantly reduced expression in CCR5, CCR2, integrin αMß2, and integrin αXß2 in a7nAChR-/- peritoneal macrophages, when compared to WT. The reduction in expression of CCR2 and αXß2 was corroborated by our flow cytometry results. Interestingly, the decrease in CCR5 and αMß2 was lower, but still detectable, and this discrepancy can be attributed to post transcriptional regulation of these receptors.

The role of these receptors was further investigated in an in vitro 3D migration assay. Macrophages deficient in a7nAChR showed significantly decreased migration within a fibrin matrix (integrin αMß2 dependent) along a RANTES gradient (CCR5-mediated). The reduction in the migration of a7nAChR-/- macrophages toward MCP-1 (CCR2-mediated) did not reach significance, although still measurable. This experiment confirmed the chemokine-independent contribution of αMß2 to mesenchymal macrophage migration. These protective effects of αMß2 and CCR5 during sepsis were reported previously and are related to the regulation of monocyte recruitment and efflux at the site of inflammation.

In summary, we discovered a new link between the parasympathetic nervous system and immune response based on a7nAChR-regulated macrophage migration during inflammation. The signaling pathway downstream of a7nAChR that modulates αMß2 and CCR5 expression is yet to be identified and is the objective of our ongoing investigation.