دورية أكاديمية
Neuron-associated macrophage proliferation in the sensory ganglia is associated with peripheral nerve injury-induced neuropathic pain involving CX3CR1 signaling.
العنوان: | Neuron-associated macrophage proliferation in the sensory ganglia is associated with peripheral nerve injury-induced neuropathic pain involving CX3CR1 signaling. |
---|---|
المؤلفون: | Guimarães RM; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil.; Graduate Program in Basic and Applied Immunology, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil., Aníbal-Silva CE; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil.; Graduate Program in Basic and Applied Immunology, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil., Davoli-Ferreira M; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil.; Graduate Program in Basic and Applied Immunology, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil.; Department of Physiology and Pharmacology, Snyder Institute for Chronic Diseases, Cumming School of Medicine, University of Calgary, Calgary, Canada., Gomes FIF; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil., Mendes A; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil., Cavallini MCM; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil.; Graduate Program in Basic and Applied Immunology, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil., Fonseca MM; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil.; Department of Anesthesiology, Pain Mechanisms Laboratory, Wake Forest University School of Medicine, Winston-Salem, United States., Damasceno S; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil., Andrade LP; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil.; Graduate Program in Basic and Applied Immunology, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil., Colonna M; Department of Pathology and Immunology, Washington University School of Medicine in Saint Louis, Saint Louis, United States., Rivat C; Univ Montpellier, Montpellier, France; Inserm U-1298, Institut des Neurosciences de Montpellier, Montpellier, France., Cunha FQ; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil., Alves-Filho JC; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil., Cunha TM; Center for Research in Inflammatory Diseases (CRID), Department of Pharmacology, Ribeirão Preto Medical School, University of São Paulo, Ribeirao Preto, Brazil. |
المصدر: | ELife [Elife] 2023 May 31; Vol. 12. Date of Electronic Publication: 2023 May 31. |
نوع المنشور: | Journal Article |
اللغة: | English |
بيانات الدورية: | Publisher: eLife Sciences Publications, Ltd Country of Publication: England NLM ID: 101579614 Publication Model: Electronic Cited Medium: Internet ISSN: 2050-084X (Electronic) Linking ISSN: 2050084X NLM ISO Abbreviation: Elife Subsets: MEDLINE |
أسماء مطبوعة: | Original Publication: Cambridge, UK : eLife Sciences Publications, Ltd., 2012- |
مواضيع طبية MeSH: | Peripheral Nerve Injuries*/complications , Neuralgia*, Mice ; Animals ; Ganglia, Spinal ; Macrophages ; Ganglia, Sensory ; Sensory Receptor Cells ; Cell Proliferation ; Hyperalgesia |
مستخلص: | Resident macrophages are distributed across all tissues and are highly heterogeneous due to adaptation to different tissue-specific environments. The resident macrophages of the sensory ganglia (sensory neuron-associated macrophages, sNAMs) are in close contact with the cell body of primary sensory neurons and might play physiological and pathophysiological roles. After peripheral nerve injury, there is an increase in the population of macrophages in the sensory ganglia, which have been implicated in different conditions, including neuropathic pain development. However, it is still under debate whether macrophage accumulation in the sensory ganglia after peripheral nerve injury is due to the local proliferation of resident macrophages or a result of blood monocyte infiltration. Here, we confirmed that the number of macrophages increased in the sensory ganglia after the spared nerve injury (SNI) model in mice. Using different approaches, we found that the increase in the number of macrophages in the sensory ganglia after SNI is a consequence of the proliferation of resident CX3CR1 + macrophages, which participate in the development of neuropathic pain, but not due to infiltration of peripheral blood monocytes. These proliferating macrophages are the source of pro-inflammatory cytokines such as TNF and IL-1b. In addition, we found that CX3CR1 signaling is involved in the sNAMs proliferation and neuropathic pain development after peripheral nerve injury. In summary, these results indicated that peripheral nerve injury leads to sNAMs proliferation in the sensory ganglia in a CX3CR1-dependent manner accounting for neuropathic pain development. In conclusion, sNAMs proliferation could be modulated to change pathophysiological conditions such as chronic neuropathic pain. Competing Interests: RG, CA, MD, FG, AM, MC, MF, SD, LA, MC, CR, FC, JA, TC No competing interests declared (© 2023, Guimarães, Aníbal-Silva et al.) |
References: | Immunity. 2014 Jul 17;41(1):21-35. (PMID: 25035951) J Exp Med. 2014 Jul 28;211(8):1533-49. (PMID: 25002752) Cell. 2019 Sep 5;178(6):1509-1525.e19. (PMID: 31491389) Mol Pain. 2009 Sep 22;5:53. (PMID: 19772627) Methods. 2001 Dec;25(4):402-8. (PMID: 11846609) Nat Commun. 2016 Jun 28;7:12029. (PMID: 27349690) Pain. 2014 Oct;155(10):2161-70. (PMID: 25139590) J Neurosci. 1995 Jul;15(7 Pt 2):5130-8. (PMID: 7623140) Immunity. 2016 Mar 15;44(3):439-449. (PMID: 26982352) J Immunol. 2012 Jan 1;188(1):29-36. (PMID: 22079990) Brain Behav Immun. 2021 Jan;91:556-567. (PMID: 33197543) Nat Neurosci. 2017 Sep;20(9):1213-1216. (PMID: 28714953) J Leukoc Biol. 2019 Sep;106(3):541-551. (PMID: 31150565) Nat Commun. 2020 Sep 29;11(1):4891. (PMID: 32994417) J Neurosci. 2009 Jun 24;29(25):8051-62. (PMID: 19553445) Pflugers Arch. 2017 Jan;469(1):123-134. (PMID: 27957611) Pain Rep. 2021 Mar 09;6(1):e873. (PMID: 33981924) Immunity. 2019 Jun 18;50(6):1482-1497.e7. (PMID: 31201094) Science. 2022 May 13;376(6594):eabd5926. (PMID: 35549409) Nat Immunol. 2013 Oct;14(10):986-95. (PMID: 24048120) Sci Adv. 2020 Aug 26;6(35):eabb2119. (PMID: 32923636) Nat Neurosci. 2010 Jan;13(1):133-40. (PMID: 20023653) Blood. 2011 Nov 24;118(22):e156-67. (PMID: 21951685) Brain Behav Immun. 2014 Aug;40:155-65. (PMID: 24681252) Proc Natl Acad Sci U S A. 2023 Feb 14;120(7):e2215906120. (PMID: 36763532) J Neuroimmunol. 2007 Mar;184(1-2):164-71. (PMID: 17275921) Brain Behav Immun. 2007 Jul;21(5):642-51. (PMID: 17174525) Pain. 2018 Jul;159(7):1308-1316. (PMID: 29554018) J Neurochem. 2008 Jan;104(1):254-63. (PMID: 17944871) Sci Rep. 2020 May 26;10(1):8648. (PMID: 32457369) J Neuroinflammation. 2018 Apr 6;15(1):101. (PMID: 29625610) Lancet Neurol. 2012 Jul;11(7):629-42. (PMID: 22710756) Cell Rep. 2016 Jul 19;16(3):605-14. (PMID: 27373153) J Clin Invest. 2014 May;124(5):2023-36. (PMID: 24743146) J Neuroinflammation. 2018 Mar 15;15(1):81. (PMID: 29544518) Mol Ther. 2005 Aug;12(2):314-20. (PMID: 15925545) Nat Commun. 2020 May 21;11(1):2552. (PMID: 32439942) Exp Neurol. 2020 May;327:113244. (PMID: 32057794) Brain Res. 2011 Aug 8;1405:95-108. (PMID: 21741621) Nat Neurosci. 2020 May;23(5):676-689. (PMID: 32284604) J Immunol. 2020 Jan 15;204(2):271-279. (PMID: 31907269) J Vis Exp. 2013 Oct 06;(80):. (PMID: 24145664) Pain. 2000 Aug;87(2):149-158. (PMID: 10924808) Proc Natl Acad Sci U S A. 2007 Jun 19;104(25):10655-60. (PMID: 17551020) Nat Rev Immunol. 2014 Jun;14(6):392-404. (PMID: 24854589) Nat Commun. 2020 Jan 14;11(1):264. (PMID: 31937758) Elife. 2020 Dec 02;9:. (PMID: 33263277) J Neuroinflammation. 2021 Oct 13;18(1):227. (PMID: 34645458) Cell Rep. 2020 May 19;31(7):107657. (PMID: 32433966) J Neurosci. 2013 Sep 18;33(38):15095-108. (PMID: 24048840) PLoS One. 2010 Oct 27;5(10):e13693. (PMID: 21060874) J Neuropathol Exp Neurol. 2018 Oct 1;77(10):929-941. (PMID: 30169768) J Neurosci. 2017 Jul 5;37(27):6408-6422. (PMID: 28576938) Pain. 2019 Jan;160(1):102-116. (PMID: 30169421) Exp Cell Res. 2003 Apr 1;284(2):196-210. (PMID: 12651153) Mol Pain. 2011 Sep 28;7:74. (PMID: 21951975) J Neurosci. 2019 Aug 28;39(35):6848-6864. (PMID: 31270160) Mol Pain. 2010 Nov 05;6:76. (PMID: 21050491) FEBS Lett. 1997 May 5;407(3):313-9. (PMID: 9175875) J Neurosci. 2017 Oct 25;37(43):10258-10277. (PMID: 28912156) J Leukoc Biol. 2021 Jun;109(6):1063-1070. (PMID: 33020963) Science. 2019 Mar 15;363(6432):. (PMID: 30872492) Nature. 2013 Apr 25;496(7446):445-55. (PMID: 23619691) Eur J Neurosci. 2004 Sep;20(5):1150-60. (PMID: 15341587) Nat Neurosci. 2016 Jan;19(1):94-101. (PMID: 26642091) Nat Neurosci. 2019 Jun;22(6):1021-1035. (PMID: 31061494) Mol Cell Biol. 2000 Jun;20(11):4106-14. (PMID: 10805752) Immunity. 2016 Mar 15;44(3):450-462. (PMID: 26982353) J Clin Invest. 2022 Dec 1;132(23):. (PMID: 36227694) Nat Rev Immunol. 2005 Dec;5(12):953-64. (PMID: 16322748) Nat Rev Drug Discov. 2014 Jul;13(7):533-48. (PMID: 24948120) Nat Immunol. 2016 Jan;17(1):2-8. (PMID: 26681456) |
فهرسة مساهمة: | Keywords: CCR2; CX3CR1; cytokines; immunology; inflammation; macrophages; monocytes; mouse; nerve injury |
تواريخ الأحداث: | Date Created: 20230531 Date Completed: 20230616 Latest Revision: 20230618 |
رمز التحديث: | 20240628 |
مُعرف محوري في PubMed: | PMC10266765 |
DOI: | 10.7554/eLife.78515 |
PMID: | 37254842 |
قاعدة البيانات: | MEDLINE |
تدمد: | 2050-084X |
---|---|
DOI: | 10.7554/eLife.78515 |