Injured sensory neuron-derived CSF1 induces microglial proliferation and DAP12-dependent pain

Nature Neuroscience

Volumn 19, Issue 1, 2015, Pages 94-101

  Guan, Zhonghui ^a   Kuhn, Julia A ^b   Wang, Xidao ^b   Colquitt, Bradley ^b   Solorzano, Carlos ^b   Vaman, Smitha ^b   Guan, Andrew K ^b   Evans Reinsch, Zoe ^b,e   Braz, Joao ^b   Devor, Marshall ^c   Abboud Werner, Sherry L ^d   Lanier, Lewis L ^a   Lomvardas, Stavros ^b,f   Basbaum, Allan I ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^d UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; CSF1R PROTEIN, MOUSE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR RECEPTOR; SIGNAL TRANSDUCING ADAPTOR PROTEIN; TYROBP PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CELL PROLIFERATION; CELL SELF-RENEWAL; CONTROLLED STUDY; HYPERSENSITIVITY; MECHANICAL HYPERSENSITIVITY; MICROGLIA; MOTONEURON; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SPINAL CORD VENTRAL HORN; UPREGULATION; ANIMAL; GENE EXPRESSION REGULATION; MALE; METABOLISM; NEURALGIA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL PROLIFERATION; GENE EXPRESSION REGULATION; MACROPHAGE COLONY-STIMULATING FACTOR; MALE; MICE; MICROGLIA; MOTOR NEURONS; NEURALGIA; PERIPHERAL NERVE INJURIES; RECEPTORS, GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; SENSORY RECEPTOR CELLS; UP-REGULATION;

EID: 84953838191     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.4189     Document Type: Article

References (55)

1. Basbaum A.I., Bautista D.M., Scherrer G., & Julius D. Cellular and molecular mechanisms of pain. Cell. 139, 267-284 (2009).
2. von Hehn C.A., Baron R., & Woolf C.J. Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron. 73, 638-652 (2012).
3. Backonja M., & Woolf C.J. Future directions in neuropathic pain therapy: closing the translational loop. Oncologist 15 (suppl. 2), 24-29 (2010).
4. Sieweke M.H., & Allen J.E. Beyond stem cells: self-renewal of differentiated macrophages. Science. 342, 1242974 (2013).
5. Salter M.W., & Beggs S. Sublime microglia: expanding roles for the guardians of the CNS. Cell. 158, 15-24 (2014).
6. Beggs S., Trang T., & Salter M.W. P2X4R+ microglia drive neuropathic pain. Nat. Neurosci. 15, 1068-1073 (2012).
7. Ji R.R., Berta T., & Nedergaard M. Glia and pain: is chronic pain a gliopathy? Pain 154 (suppl. 1), S10-S28 (2013).
8. Clark A.K., & Malcangio M. Fractalkine/CX3CR1 signaling during neuropathic pain. Front. Cell. Neurosci. 8, 121 (2014).
9. Grace P.M., Hutchinson M.R., Maier S.F., & Watkins L.R. Pathological pain and the neuroimmune interface. Nat. Rev. Immunol. 14, 217-231 (2014).
10. Colburn R.W., Rickman A.J., & DeLeo J.A. The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Exp. Neurol. 157, 289-304 (1999).
11. Zhuang Z.Y., et al. Role of the CX3CR1/p38 MAPK pathway in spinal microglia for the development of neuropathic pain following nerve injury-induced cleavage of fractalkine. Brain Behav. Immun. 21, 642-651 (2007).
12. Old E.A., & Malcangio M. Chemokine mediated neuron-glia communication and aberrant signaling in neuropathic pain states. Curr. Opin. Pharmacol. 12, 67-73 (2012).
13. Biber K., et al. Neuronal CCL21 up-regulates microglia P2X4 expression and initiates neuropathic pain development. EMBO J. 30, 1864-1873 (2011).
14. Jung H., et al. Visualization of chemokine receptor activation in transgenic mice reveals peripheral activation of CCR2 receptors in states of neuropathic pain. J. Neurosci. 29, 8051-8062 (2009).
15. Calvo M., et al. Neuregulin-ErbB signaling promotes microglial proliferation and chemotaxis contributing to microgliosis and pain after peripheral nerve injury. J. Neurosci. 30, 5437-5450 (2010).
16. Tsuda M., et al. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature. 424, 778-783 (2003).
17. Ulmann L., et al. Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J. Neurosci. 28, 11263-11268 (2008).
18. Echeverry S., Shi X.Q., & Zhang J. Characterization of cell proliferation in rat spinal cord following peripheral nerve injury and the relationship with neuropathic pain. Pain. 135, 37-47 (2008).
19. Priller J., et al. Targeting gene-modified hematopoietic cells to the central nervous system: use of green fluorescent protein uncovers microglial engraftment. Nat. Med. 7, 1356-1361 (2001).
20. Ajami B., Bennett J.L., Krieger C., Tetzlaff W., & Rossi F.M. Local self-renewal can sustain CNS microglia maintenance and function throughout adult life. Nat. Neurosci. 10, 1538-1543 (2007).
21. LaCroix-Fralish M.L., Austin J.S., Zheng F.Y., Levitin D.J., & Mogil J.S. Patterns of pain: meta-Analysis of microarray studies of pain. Pain. 152, 1888-1898 (2011).
22. Perkins J.R., et al. A comparison of RNA-seq and exon arrays for whole genome transcription profiling of the L5 spinal nerve transection model of neuropathic pain in the rat. Mol. Pain. 10, 7 (2014).
23. Suzumura A., Sawada M., Yamamoto H., & Marunouchi T. Effects of colony stimulating factors on isolated microglia in vitro. J. Neuroimmunol. 30, 111-120 (1990).
24. Ginhoux F., et al. Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science. 330, 841-845 (2010).
25. Schulz C., et al. A lineage of myeloid cells independent of Myb and hematopoietic stem cells. Science. 336, 86-90 (2012).
26. Wang Y., et al. IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat. Immunol. 13, 753-760 (2012).
27. Tsujino H., et al. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol. Cell. Neurosci. 15, 170-182 (2000).
28. Hökfelt T., Brumovsky P., Shi T., Pedrazzini T., & Villar M. NPY and pain as seen from the histochemical side. Peptides. 28, 365-372 (2007).
29. Burnett S.H., et al. Conditional macrophage ablation in transgenic mice expressing a Fas-based suicide gene. J. Leukoc. Biol. 75, 612-623 (2004).
30. Harris S.E., et al. Meox2Cre-mediated disruption of CSF-1 leads to osteopetrosis and osteocyte defects. Bone. 50, 42-53 (2012).
31. Zurborg S., et al. Generation and characterization of an Advillin-Cre driver mouse line. Mol. Pain. 7, 66 (2011).
32. Shields S.D., Eckert W.A. III & Basbaum A.I. Spared nerve injury model of neuropathic pain in the mouse: a behavioral and anatomic analysis. J. Pain. 4, 465-470 (2003).
33. Coull J.A., et al. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature. 438, 1017-1021 (2005).
34. Hickman S.E., et al. The microglial sensome revealed by direct RNA sequencing. Nat. Neurosci. 16, 1896-1905 (2013).
35. Kobayashi M., Konishi H., Takai T., & Kiyama H. A DAP12-dependent signal promotes pro-inflammatory polarization in microglia following nerve injury and exacerbates degeneration of injured neurons. Glia. 63, 1073-1082 (2015).
36. Bakker A.B., et al. DAP12-deficient mice fail to develop autoimmunity due to impaired antigen priming. Immunity. 13, 345-353 (2000).
37. Devor M., & Raber P. Heritability of symptoms in an experimental model of neuropathic pain. Pain. 42, 51-67 (1990).
38. Bédard A., Tremblay P., Chernomoretz A., & Vallières L. Identification of genes preferentially expressed by microglia and upregulated during cuprizone-induced inflammation. Glia. 55, 777-789 (2007).
39. Otero K., et al. Macrophage colony-stimulating factor induces the proliferation and survival of macrophages via a pathway involving DAP12 and beta-catenin. Nat. Immunol. 10, 734-743 (2009).
40. Raivich G., et al. Regulation of MCSF receptors on microglia in the normal and injured mouse central nervous system: a quantitative immunofluorescence study using confocal laser microscopy. J. Comp. Neurol. 395, 342-358 (1998).
41. Yamamoto S., Nakajima K., & Kohsaka S. Macrophage-colony stimulating factor as an inducer of microglial proliferation in axotomized rat facial nucleus. J. Neurochem. 115, 1057-1067 (2010).
42. Dubois N.C., Hofmann D., Kaloulis K., Bishop J.M., & Trumpp A. Nestin-Cre transgenic mouse line Nes-Cre1 mediates highly efficient Cre/loxP mediated recombination in the nervous system, kidney, and somite-derived tissues. Genesis. 44, 355-360 (2006).
43. Yoshida H., et al. The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature. 345, 442-444 (1990).
44. Raivich G., Moreno-Flores M.T., Möller J.C., & Kreutzberg G.W. Inhibition of posttraumatic microglial proliferation in a genetic model of macrophage colony-stimulating factor deficiency in the mouse. Eur. J. Neurosci. 6, 1615-1618 (1994).
45. Elmore M.R., et al. Colony-stimulating factor 1 receptor signaling is necessary for microglia viability, unmasking a microglia progenitor cell in the adult brain. Neuron. 82, 380-397 (2014).
46. Biber K., & Boddeke E. Neuronal CC chemokines: the distinct roles of CCL21 and CCL2 in neuropathic pain. Front. Cell. Neurosci. 8, 210 (2014).
47. Ransohoff R.M., & Cardona A.E. The myeloid cells of the central nervous system parenchyma. Nature. 468, 253-262 (2010).
48. Masuda T., et al. IRF8 is a critical transcription factor for transforming microglia into a reactive phenotype. Cell Reports. 1, 334-340 (2012).
49. Masuda T., et al. Transcription factor IRF5 drives P2X4R+-reactive microglia gating neuropathic pain. Nat. Commun. 5, 3771 (2014).
50. Coull J.A., et al. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature. 424, 938-942 (2003).
51. Sim J.A., et al. Altered hippocampal synaptic potentiation in P2X4 knock-out mice. J. Neurosci. 26, 9006-9009 (2006).
52. Cavanaugh D.J., et al. Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc. Natl. Acad. Sci. USA. 106, 9075-9080 (2009).
53. Bráz J.M., et al. Forebrain GABAergic neuron precursors integrate into adult spinal cord and reduce injury-induced neuropathic pain. Neuron. 74, 663-675 (2012).
54. Wang X., et al. Excitatory superficial dorsal horn interneurons are functionally heterogeneous and required for the full behavioral expression of pain and itch. Neuron. 78, 312-324 (2013).
55. Solorzano C., et al. Primary afferent and spinal cord expression of gastrin-releasing peptide: message, protein, and antibody concerns. J. Neurosci. 35, 648-657 (2015).