Recruitment of Beneficial M2 Macrophages to Injured Spinal Cord Is Orchestrated by Remote Brain Choroid Plexus
Monocyte-derived macrophages are essential for recovery after spinal cord injury, but their homing mechanism is poorly understood. Here, we show that although of common origin, the homing of proinflammatory (M1) and the “alternatively activated” anti-inflammatory (M2) macrophages to traumatized spin...
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| Published in | Immunity (Cambridge, Mass.) Vol. 38; no. 3; pp. 555 - 569 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
21.03.2013
Elsevier Limited |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Monocyte-derived macrophages are essential for recovery after spinal cord injury, but their homing mechanism is poorly understood. Here, we show that although of common origin, the homing of proinflammatory (M1) and the “alternatively activated” anti-inflammatory (M2) macrophages to traumatized spinal cord (SC) was distinctly regulated, neither being through breached blood-brain barrier. The M1 macrophages (Ly6chiCX3CR1lo) derived from monocytes homed in a CCL2 chemokine-dependent manner through the adjacent SC leptomeninges. The resolving M2 macrophages (Ly6cloCX3CR1hi) derived from monocytes trafficked through a remote blood-cerebrospinal-fluid (CSF) barrier, the brain-ventricular choroid plexus (CP), via VCAM-1-VLA-4 adhesion molecules and epithelial CD73 enzyme for extravasation and epithelial transmigration. Blockage of these determinants, or mechanical CSF flow obstruction, inhibited M2 macrophage recruitment and impaired motor-function recovery. The CP, along with the CSF and the central canal, provided an anti-inflammatory supporting milieu, potentially priming the trafficking monocytes. Overall, our finding demonstrates that the route of monocyte entry to central nervous system provides an instructional environment to shape their function.
[Display omitted]
► Breached BBB is not a preferred entry route for monocytes infiltrating injured SC ► M2 macrophage homing to injured SC is orchestrated by the brain choroid plexus ► The choroid plexus and CSF provide trafficking monocytes with an M2-biased milieu ► M1 macrophages home to injured SC via leptomeninges, in a CCL2-dependent manner |
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| AbstractList | Monocyte-derived macrophages are essential for recovery after spinal cord injury, but their homing mechanism is poorly understood. Here, we show that although of common origin, the homing of proinflammatory (M1) and the "alternatively activated" anti-inflammatory (M2) macrophages to traumatized spinal cord (SC) was distinctly regulated, neither being through breached blood-brain barrier. The M1 macrophages (Ly6c(hi)CX3CR1(lo)) derived from monocytes homed in a CCL2 chemokine-dependent manner through the adjacent SC leptomeninges. The resolving M2 macrophages (Ly6c(lo)CX3CR1(hi)) derived from monocytes trafficked through a remote blood-cerebrospinal-fluid (CSF) barrier, the brain-ventricular choroid plexus (CP), via VCAM-1-VLA-4 adhesion molecules and epithelial CD73 enzyme for extravasation and epithelial transmigration. Blockage of these determinants, or mechanical CSF flow obstruction, inhibited M2 macrophage recruitment and impaired motor-function recovery. The CP, along with the CSF and the central canal, provided an anti-inflammatory supporting milieu, potentially priming the trafficking monocytes. Overall, our finding demonstrates that the route of monocyte entry to central nervous system provides an instructional environment to shape their function.Monocyte-derived macrophages are essential for recovery after spinal cord injury, but their homing mechanism is poorly understood. Here, we show that although of common origin, the homing of proinflammatory (M1) and the "alternatively activated" anti-inflammatory (M2) macrophages to traumatized spinal cord (SC) was distinctly regulated, neither being through breached blood-brain barrier. The M1 macrophages (Ly6c(hi)CX3CR1(lo)) derived from monocytes homed in a CCL2 chemokine-dependent manner through the adjacent SC leptomeninges. The resolving M2 macrophages (Ly6c(lo)CX3CR1(hi)) derived from monocytes trafficked through a remote blood-cerebrospinal-fluid (CSF) barrier, the brain-ventricular choroid plexus (CP), via VCAM-1-VLA-4 adhesion molecules and epithelial CD73 enzyme for extravasation and epithelial transmigration. Blockage of these determinants, or mechanical CSF flow obstruction, inhibited M2 macrophage recruitment and impaired motor-function recovery. The CP, along with the CSF and the central canal, provided an anti-inflammatory supporting milieu, potentially priming the trafficking monocytes. Overall, our finding demonstrates that the route of monocyte entry to central nervous system provides an instructional environment to shape their function. Monocyte-derived macrophages are essential for recovery after spinal cord injury, but their homing mechanism is poorly understood. Here, we show that although of common origin, the homing of proinflammatory (M1) and the "alternatively activated" anti-inflammatory (M2) macrophages to traumatized spinal cord (SC) was distinctly regulated, neither being through breached blood-brain barrier. The M1 macrophages (Ly6chiCX3CR1lo) derived from monocytes homed in a CCL2 chemokine-dependent manner through the adjacent SC leptomeninges. The resolving M2 macrophages (Ly6cloCX3CR1hi) derived from monocytes trafficked through a remote blood-cerebrospinal-fluid (CSF) barrier, the brain-ventricular choroid plexus (CP), via VCAM-1-VLA-4 adhesion molecules and epithelial CD73 enzyme for extravasation and epithelial transmigration. Blockage of these determinants, or mechanical CSF flow obstruction, inhibited M2 macrophage recruitment and impaired motor-function recovery. The CP, along with the CSF and the central canal, provided an anti-inflammatory supporting milieu, potentially priming the trafficking monocytes. Overall, our finding demonstrates that the route of monocyte entry to central nervous system provides an instructional environment to shape their function. Monocyte-derived macrophages are essential for recovery after spinal cord injury, but their homing mechanism is poorly understood. Here, we show that although of common origin, the homing of proinflammatory (M1) and the “alternatively activated” anti-inflammatory (M2) macrophages to traumatized spinal cord (SC) was distinctly regulated, neither being through breached blood-brain barrier. The M1 macrophages (Ly6chiCX3CR1lo) derived from monocytes homed in a CCL2 chemokine-dependent manner through the adjacent SC leptomeninges. The resolving M2 macrophages (Ly6cloCX3CR1hi) derived from monocytes trafficked through a remote blood-cerebrospinal-fluid (CSF) barrier, the brain-ventricular choroid plexus (CP), via VCAM-1-VLA-4 adhesion molecules and epithelial CD73 enzyme for extravasation and epithelial transmigration. Blockage of these determinants, or mechanical CSF flow obstruction, inhibited M2 macrophage recruitment and impaired motor-function recovery. The CP, along with the CSF and the central canal, provided an anti-inflammatory supporting milieu, potentially priming the trafficking monocytes. Overall, our finding demonstrates that the route of monocyte entry to central nervous system provides an instructional environment to shape their function. [Display omitted] ► Breached BBB is not a preferred entry route for monocytes infiltrating injured SC ► M2 macrophage homing to injured SC is orchestrated by the brain choroid plexus ► The choroid plexus and CSF provide trafficking monocytes with an M2-biased milieu ► M1 macrophages home to injured SC via leptomeninges, in a CCL2-dependent manner Monocyte-derived macrophages are essential for recovery after spinal cord injury, but their homing mechanism is poorly understood. Here, we show that although of common origin, the homing of proinflammatory (M1) and the "alternatively activated" anti-inflammatory (M2) macrophages to traumatized spinal cord (SC) was distinctly regulated, neither being through breached blood-brain barrier. The M1 macrophages (Ly6c(hi)CX3CR1(lo)) derived from monocytes homed in a CCL2 chemokine-dependent manner through the adjacent SC leptomeninges. The resolving M2 macrophages (Ly6c(lo)CX3CR1(hi)) derived from monocytes trafficked through a remote blood-cerebrospinal-fluid (CSF) barrier, the brain-ventricular choroid plexus (CP), via VCAM-1-VLA-4 adhesion molecules and epithelial CD73 enzyme for extravasation and epithelial transmigration. Blockage of these determinants, or mechanical CSF flow obstruction, inhibited M2 macrophage recruitment and impaired motor-function recovery. The CP, along with the CSF and the central canal, provided an anti-inflammatory supporting milieu, potentially priming the trafficking monocytes. Overall, our finding demonstrates that the route of monocyte entry to central nervous system provides an instructional environment to shape their function. Monocyte-derived macrophages are essential for recovery after spinal cord injury, but their homing mechanism is poorly understood. Here, we show that although of common origin, the homing of proinflammatory (M1) and the “alternatively activated” anti-inflammatory (M2) macrophages to traumatized spinal cord (SC) was distinctly regulated, neither being through breached blood-brain barrier. The M1 macrophages (Ly6c hi CX3CR1 lo ) derived from monocytes homed in a CCL2 chemokine-dependent manner through the adjacent SC leptomeninges. The resolving M2 macrophages (Ly6c lo CX3CR1 hi ) derived from monocytes trafficked through a remote blood-cerebrospinal-fluid (CSF) barrier, the brain-ventricular choroid plexus (CP), via VCAM-1-VLA-4 adhesion molecules and epithelial CD73 enzyme for extravasation and epithelial transmigration. Blockage of these determinants, or mechanical CSF flow obstruction, inhibited M2 macrophage recruitment and impaired motor-function recovery. The CP, along with the CSF and the central canal, provided an anti-inflammatory supporting milieu, potentially priming the trafficking monocytes. Overall, our finding demonstrates that the route of monocyte entry to central nervous system provides an instructional environment to shape their function. |
| Author | Rosenzweig, Neta Kim, Ki-Wook Yovel, Gili Bendel, Peter Lira, Sergio A. Kalchenko, Vyacheslav Klein, Eugenia Shechter, Ravid Jung, Steffen Ruckh, Julia Miller, Omer London, Anat Schwartz, Michal |
| AuthorAffiliation | 4 Department of Veterinary Resources, The Weizmann Institute of Science, Rehovot 76100, Israel 3 The Irving and Cherna Moskowitz Center for Nano and Bio Nano Imaging, The Weizmann Institute of Science, Rehovot 76100, Israel 2 Department of Immunology, The Weizmann Institute of Science, Rehovot 76100, Israel 1 Department of Neurobiology, The Weizmann Institute of Science, Rehovot 76100, Israel 6 Immunology Institute, Mount Sinai School of Medicine, New York, NY 10029-6574, USA 5 Department of Chemical Research Support, The Weizmann Institute of Science, Rehovot 76100, Israel |
| AuthorAffiliation_xml | – name: 1 Department of Neurobiology, The Weizmann Institute of Science, Rehovot 76100, Israel – name: 2 Department of Immunology, The Weizmann Institute of Science, Rehovot 76100, Israel – name: 4 Department of Veterinary Resources, The Weizmann Institute of Science, Rehovot 76100, Israel – name: 6 Immunology Institute, Mount Sinai School of Medicine, New York, NY 10029-6574, USA – name: 5 Department of Chemical Research Support, The Weizmann Institute of Science, Rehovot 76100, Israel – name: 3 The Irving and Cherna Moskowitz Center for Nano and Bio Nano Imaging, The Weizmann Institute of Science, Rehovot 76100, Israel |
| Author_xml | – sequence: 1 givenname: Ravid surname: Shechter fullname: Shechter, Ravid email: ravid.shechter@weizmann.ac.il organization: Department of Neurobiology, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 2 givenname: Omer surname: Miller fullname: Miller, Omer organization: Department of Neurobiology, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 3 givenname: Gili surname: Yovel fullname: Yovel, Gili organization: Department of Neurobiology, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 4 givenname: Neta surname: Rosenzweig fullname: Rosenzweig, Neta organization: Department of Neurobiology, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 5 givenname: Anat surname: London fullname: London, Anat organization: Department of Neurobiology, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 6 givenname: Julia surname: Ruckh fullname: Ruckh, Julia organization: Department of Neurobiology, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 7 givenname: Ki-Wook surname: Kim fullname: Kim, Ki-Wook organization: Department of Immunology, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 8 givenname: Eugenia surname: Klein fullname: Klein, Eugenia organization: The Irving and Cherna Moskowitz Center for Nano and Bio Nano Imaging, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 9 givenname: Vyacheslav surname: Kalchenko fullname: Kalchenko, Vyacheslav organization: Department of Veterinary Resources, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 10 givenname: Peter surname: Bendel fullname: Bendel, Peter organization: Department of Chemical Research Support, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 11 givenname: Sergio A. surname: Lira fullname: Lira, Sergio A. organization: Immunology Institute, Mount Sinai School of Medicine, New York, NY 10029-6574, USA – sequence: 12 givenname: Steffen surname: Jung fullname: Jung, Steffen organization: Department of Immunology, The Weizmann Institute of Science, Rehovot 76100, Israel – sequence: 13 givenname: Michal surname: Schwartz fullname: Schwartz, Michal email: michal.schwartz@weizmann.ac.il organization: Department of Neurobiology, The Weizmann Institute of Science, Rehovot 76100, Israel |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23477737$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | 5'-Nucleotidase - antagonists & inhibitors 5'-Nucleotidase - genetics 5'-Nucleotidase - immunology Adenosine Diphosphate - analogs & derivatives Adenosine Diphosphate - pharmacology Animals Antigens, Ly - immunology Antigens, Ly - metabolism Blood-Brain Barrier - immunology Blood-Brain Barrier - metabolism Cell Movement - genetics Cell Movement - immunology Choroid Plexus - immunology Choroid Plexus - metabolism CX3C Chemokine Receptor 1 Cytokines Enzyme Inhibitors - pharmacology Flow Cytometry Gene Expression - immunology Green Fluorescent Proteins - genetics Green Fluorescent Proteins - metabolism Integrin alpha4beta1 - genetics Integrin alpha4beta1 - immunology Leukocyte Common Antigens - immunology Leukocyte Common Antigens - metabolism Macrophages - drug effects Macrophages - immunology Macrophages - metabolism Meninges - immunology Meninges - metabolism Mice Mice, Inbred C57BL Mice, Knockout Microscopy, Confocal Monocytes - drug effects Monocytes - immunology Monocytes - metabolism Receptors, Chemokine - genetics Receptors, Chemokine - immunology Recruitment Reverse Transcriptase Polymerase Chain Reaction Rodents Spinal Cord - immunology Spinal Cord - metabolism Spinal Cord Injuries - cerebrospinal fluid Spinal Cord Injuries - genetics Spinal Cord Injuries - immunology Statistical analysis Vascular Cell Adhesion Molecule-1 - genetics Vascular Cell Adhesion Molecule-1 - immunology |
| Title | Recruitment of Beneficial M2 Macrophages to Injured Spinal Cord Is Orchestrated by Remote Brain Choroid Plexus |
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