Contribution of macrophages to enhanced regenerative capacity of dorsal root ganglia sensory neurons by conditioning injury
Although the central branches of the dorsal root ganglion (DRG) sensory neurons do not spontaneously regenerate, a conditioning peripheral injury can promote their regeneration. A potential role of macrophages in axonal regeneration was proposed, but it has not been critically addressed whether macr...
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Published in | The Journal of neuroscience Vol. 33; no. 38; pp. 15095 - 15108 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Society for Neuroscience
18.09.2013
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Subjects | |
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Abstract | Although the central branches of the dorsal root ganglion (DRG) sensory neurons do not spontaneously regenerate, a conditioning peripheral injury can promote their regeneration. A potential role of macrophages in axonal regeneration was proposed, but it has not been critically addressed whether macrophages play an essential role in the conditioning injury model. After sciatic nerve injury (SNI) in rats, the number of macrophages in DRGs gradually increased by day 7. The increase persisted up to 28 d and was accompanied by upregulation of inflammatory mediators, including oncomodulin. A macrophage deactivator, minocycline, reduced the macrophage number and expressions of the inflammatory mediators. Molecular signatures of conditioning effects were abrogated by minocycline, and enhanced regenerative capacity was substantially attenuated both in vitro and in vivo. Delayed minocycline infusion abrogated the SNI-induced long-lasting heightened neurite outgrowth potential, indicating a role for macrophages in the maintenance of regenerative capacity. Intraganglionic cAMP injection also resulted in an increase in macrophages, and minocycline abolished the cAMP effect on neurite outgrowth. However, conditioned media (CM) from macrophages treated with cAMP did not exhibit neurite growth-promoting activity. In contrast, CM from neuron-macrophage cocultures treated with cAMP promoted neurite outgrowth greatly, highlighting a requirement for neuron-macrophage interactions for the induction of a proregenerative macrophage phenotype. The growth-promoting activity in the CM was profoundly attenuated by an oncomodulin neutralizing antibody. These results suggest that the neuron-macrophage interactions involved in eliciting a proregenerative phenotype in macrophages may be a novel target to induce long-lasting regenerative processes after axonal injuries in the CNS. |
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AbstractList | Although the central branches of the dorsal root ganglion (DRG) sensory neurons do not spontaneously regenerate, a conditioning peripheral injury can promote their regeneration. A potential role of macrophages in axonal regeneration was proposed, but it has not been critically addressed whether macrophages play an essential role in the conditioning injury model. After sciatic nerve injury (SNI) in rats, the number of macrophages in DRGs gradually increased by day 7. The increase persisted up to 28 d and was accompanied by upregulation of inflammatory mediators, including oncomodulin. A macrophage deactivator, minocycline, reduced the macrophage number and expressions of the inflammatory mediators. Molecular signatures of conditioning effects were abrogated by minocycline, and enhanced regenerative capacity was substantially attenuated both
in vitro
and
in vivo
. Delayed minocycline infusion abrogated the SNI-induced long-lasting heightened neurite outgrowth potential, indicating a role for macrophages in the maintenance of regenerative capacity. Intraganglionic cAMP injection also resulted in an increase in macrophages, and minocycline abolished the cAMP effect on neurite outgrowth. However, conditioned media (CM) from macrophages treated with cAMP did not exhibit neurite growth-promoting activity. In contrast, CM from neuron–macrophage cocultures treated with cAMP promoted neurite outgrowth greatly, highlighting a requirement for neuron–macrophage interactions for the induction of a proregenerative macrophage phenotype. The growth-promoting activity in the CM was profoundly attenuated by an oncomodulin neutralizing antibody. These results suggest that the neuron–macrophage interactions involved in eliciting a proregenerative phenotype in macrophages may be a novel target to induce long-lasting regenerative processes after axonal injuries in the CNS. Although the central branches of the dorsal root ganglion (DRG) sensory neurons do not spontaneously regenerate, a conditioning peripheral injury can promote their regeneration. A potential role of macrophages in axonal regeneration was proposed, but it has not been critically addressed whether macrophages play an essential role in the conditioning injury model. After sciatic nerve injury (SNI) in rats, the number of macrophages in DRGs gradually increased by day 7. The increase persisted up to 28 d and was accompanied by upregulation of inflammatory mediators, including oncomodulin. A macrophage deactivator, minocycline, reduced the macrophage number and expressions of the inflammatory mediators. Molecular signatures of conditioning effects were abrogated by minocycline, and enhanced regenerative capacity was substantially attenuated both in vitro and in vivo. Delayed minocycline infusion abrogated the SNI-induced long-lasting heightened neurite outgrowth potential, indicating a role for macrophages in the maintenance of regenerative capacity. Intraganglionic cAMP injection also resulted in an increase in macrophages, and minocycline abolished the cAMP effect on neurite outgrowth. However, conditioned media (CM) from macrophages treated with cAMP did not exhibit neurite growth-promoting activity. In contrast, CM from neuron-macrophage cocultures treated with cAMP promoted neurite outgrowth greatly, highlighting a requirement for neuron-macrophage interactions for the induction of a proregenerative macrophage phenotype. The growth-promoting activity in the CM was profoundly attenuated by an oncomodulin neutralizing antibody. These results suggest that the neuron-macrophage interactions involved in eliciting a proregenerative phenotype in macrophages may be a novel target to induce long-lasting regenerative processes after axonal injuries in the CNS. |
Author | Jeong, Soo Ryeong Kang, Young Mi Kim, Jinha Shin, Haeyoung Hwang, Dong Hoon Choi, Jun Young Kwon, Min Jung Kim, Byung Gon |
Author_xml | – sequence: 1 givenname: Min Jung surname: Kwon fullname: Kwon, Min Jung organization: Brain Disease Research Center, Institute for Medical Sciences and Department of Neurology, Ajou University School of Medicine, Suwon, 443-721, Republic of Korea and Neuroscience Graduate Program, Department of Biomedical Sciences, Ajou University Graduate School of Medicine, Suwon, 443-721, Republic of Korea – sequence: 2 givenname: Jinha surname: Kim fullname: Kim, Jinha – sequence: 3 givenname: Haeyoung surname: Shin fullname: Shin, Haeyoung – sequence: 4 givenname: Soo Ryeong surname: Jeong fullname: Jeong, Soo Ryeong – sequence: 5 givenname: Young Mi surname: Kang fullname: Kang, Young Mi – sequence: 6 givenname: Jun Young surname: Choi fullname: Choi, Jun Young – sequence: 7 givenname: Dong Hoon surname: Hwang fullname: Hwang, Dong Hoon – sequence: 8 givenname: Byung Gon surname: Kim fullname: Kim, Byung Gon |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24048840$$D View this record in MEDLINE/PubMed |
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Snippet | Although the central branches of the dorsal root ganglion (DRG) sensory neurons do not spontaneously regenerate, a conditioning peripheral injury can promote... |
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SubjectTerms | Analysis of Variance Animals Axons - physiology Calcium-Binding Proteins - metabolism Cell Separation Cells, Cultured Cholera Toxin - metabolism Coculture Techniques Cyclic AMP - pharmacology Cytokines - metabolism Disease Models, Animal Dose-Response Relationship, Drug Enzyme-Linked Immunosorbent Assay Female Flow Cytometry Ganglia, Spinal - pathology GAP-43 Protein - genetics GAP-43 Protein - metabolism Gene Expression Regulation - drug effects Gene Expression Regulation - physiology Glial Fibrillary Acidic Protein Macrophages - drug effects Macrophages - physiology Microfilament Proteins - metabolism Minocycline - pharmacology Nerve Growth Factors - genetics Nerve Growth Factors - metabolism Nerve Regeneration - physiology Rats Rats, Sprague-Dawley Sciatic Neuropathy - pathology Sciatic Neuropathy - physiopathology Sensory Receptor Cells - drug effects Sensory Receptor Cells - physiology |
Title | Contribution of macrophages to enhanced regenerative capacity of dorsal root ganglia sensory neurons by conditioning injury |
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