Pathological pain and the neuroimmune interface

Peter M. Grace; Mark R. Hutchinson; Steven F. Maier; Linda R. Watkins

doi:10.1038/nri3621

journal article Feb 28, 2014

Pathological pain and the neuroimmune interface

Peter M. Grace Mark R. Hutchinson

Steven F. Maier Linda R. Watkins

Nature Reviews Immunology Vol. 14 No. 4 pp. 217-231 · Springer Science and Business Media LLC

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References

177

[1]

Maier, S. F., Wiertelak, E. P., Martin, D. & Watkins, L. R. Interleukin-1 mediates the behavioral hyperalgesia produced by lithium chloride and endotoxin. Brain Res. 623, 321–324 (1993). 10.1016/0006-8993(93)91446-y

[2]

Ferreira, S. H., Lorenzetti, B. B., Bristow, A. F. & Poole, S. Interleukin-1β as a potent hyperalgesic agent antagonized by a tripeptide analogue. Nature 334, 698–700 (1988). 10.1038/334698a0

[3]

Watkins, L. R. et al. Characterization of cytokine-induced hyperalgesia. Brain Res. 654, 15–26 (1994). 10.1016/0006-8993(94)91566-0

[4]

Bianchi, M., Sacerdote, P., Ricciardi-Castagnoli, P., Mantegazza, P. & Panerai, A. E. Central effects of tumor necrosis factor alpha and interleukin-1 alpha on nociceptive thresholds and spontaneous locomotor activity. Neurosci. Lett. 148, 76–80 (1992). 10.1016/0304-3940(92)90808-k

[5]

Watkins, L. R., Maier, S. F. & Goehler, L. E. Immune activation: the role of pro-inflammatory cytokines in inflammation, illness responses and pathological pain states. Pain 63, 289–302 (1995). 10.1016/0304-3959(95)00186-7

[6]

Garrison, C. J., Dougherty, P. M., Kajander, K. C. & Carlton, S. M. Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res. 565, 1–7 (1991). 10.1016/0006-8993(91)91729-k

[7]

Svensson, M. et al. The response of central glia to peripheral nerve injury. Brain Res. Bull. 30, 499–506 (1993). 10.1016/0361-9230(93)90284-i

[8]

Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat

R L. Watkins, D Martin, P Ulrich et al.

Pain 1997 10.1016/s0304-3959(97)03369-1

[9]

Meller, S. T., Dykstra, C., Grzybycki, D., Murphy, S. & Gebhart, G. F. The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat. Neuropharmacology 33, 1471–1478 (1994). 10.1016/0028-3908(94)90051-5

[10]

Ledeboer, A. et al. Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain 115, 71–83 (2005). 10.1016/j.pain.2005.02.009

[11]

Milligan, E. D. et al. Intrathecal HIV-1 envelope glycoprotein gp120 induces enhanced pain states mediated by spinal cord proinflammatory cytokines. J. Neurosci. 21, 2808–2819 (2001). The first demonstration that spinal microgliosis is sufficient to induce nociceptive hypersensitivity via production and release of pro-inflammatory cytokines. 10.1523/jneurosci.21-08-02808.2001

[12]

Cellular and Molecular Mechanisms of Pain

Allan I. Basbaum, Diana M. Bautista, Grégory Scherrer et al.

Cell 2009 10.1016/j.cell.2009.09.028

[13]

Ossipov, M. H., Dussor, G. O. & Porreca, F. Central modulation of pain. J. Clin. Invest. 120, 3779–3787 (2010). 10.1172/jci43766

[14]

Pizzo, P. A. & Clark, N. M. Alleviating suffering 101-pain relief in the United States. N. Engl. J. Med. 366, 197–199 (2012). 10.1056/nejmp1109084

[15]

Central Sensitization: A Generator of Pain Hypersensitivity by Central Neural Plasticity

Alban Latremoliere, Clifford J. Woolf

The Journal of Pain 2009 10.1016/j.jpain.2009.06.012

[16]

Scholz, J. & Woolf, C. J. The neuropathic pain triad: neurons, immune cells and glia. Nature Neurosci. 10, 1361–1368 (2007). 10.1038/nn1992

[17]

Araque, A. & Navarrete, M. Glial cells in neuronal network function. Phil. Trans. R. Soc. B 365, 2375–2381 (2010). 10.1098/rstb.2009.0313

[18]

Hanisch, U. K. Functional diversity of microglia - how heterogeneous are they to begin with? Front. Cell Neurosci. 7, 65 (2013). 10.3389/fncel.2013.00065

[19]

Resting Microglial Cells Are Highly Dynamic Surveillants of Brain Parenchyma in Vivo

Axel Nimmerjahn, Frank Kirchhoff, Fritjof Helmchen

Science 2005 10.1126/science.1110647

[20]

Kettenmann, H., Hanisch, U. K., Noda, M. & Verkhratsky, A. Physiology of microglia. Physiol. Rev. 91, 461–553 (2011). 10.1152/physrev.00011.2010

[21]

Sofroniew, M. V. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 32, 638–647 (2009). 10.1016/j.tins.2009.08.002

[22]

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). 10.1523/jneurosci.2308-08.2008

[23]

Grace, P. M., Rolan, P. E. & Hutchinson, M. R. Peripheral immune contributions to the maintenance of central glial activation underlying neuropathic pain. Brain Behav. Immun. 25, 1322–1332 (2011). 10.1016/j.bbi.2011.04.003

[24]

Zhang, J. et al. Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain. J. Neurosci. 27, 12396–12406 (2007). 10.1523/jneurosci.3016-07.2007

[25]

T-Cell Infiltration and Signaling in the Adult Dorsal Spinal Cord Is a Major Contributor to Neuropathic Pain-Like Hypersensitivity

Michael Costigan, Andrew Moss, Alban Latremoliere et al.

The Journal of Neuroscience 2009 10.1523/jneurosci.4569-09.2009

[26]

Leger, T., Grist, J., D'Acquisto, F., Clark, A. K. & Malcangio, M. Glatiramer acetate attenuates neuropathic allodynia through modulation of adaptive immune cells. J. Neuroimmunol. 234, 19–26 (2011). 10.1016/j.jneuroim.2011.01.005

[27]

Meng, X. et al. Spinal interleukin-17 promotes thermal hyperalgesia and NMDA NR1 phosphorylation in an inflammatory pain rat model. Pain 154, 294–305 (2013). 10.1016/j.pain.2012.10.022

[28]

Tsuda, M. et al. IFNγ receptor signaling mediates spinal microglia activation driving neuropathic pain. Proc. Natl Acad. Sci. USA 106, 8032–8037 (2009). 10.1073/pnas.0810420106

[29]

Austin, P. J., Kim, C. F., Perera, C. J. & Moalem-Taylor, G. Regulatory T cells attenuate neuropathic pain following peripheral nerve injury and experimental autoimmune neuritis. Pain 153, 1916–1931 (2012). 10.1016/j.pain.2012.06.005

[30]

Taoka, Y. et al. Role of neutrophils in spinal cord injury in the rat. Neuroscience 79, 1177–1182 (1997). 10.1016/s0306-4522(97)00011-0

[31]

Sweitzer, S. M., Hickey, W. F., Rutkowski, M. D., Pahl, J. L. & DeLeo, J. A. Focal peripheral nerve injury induces leukocyte trafficking into the central nervous system: potential relationship to neuropathic pain. Pain 100, 163–170 (2002). 10.1016/s0304-3959(02)00257-9

[32]

Kwok, Y. H. et al. TLR 2 and 4 responsiveness from isolated peripheral blood mononuclear cells from rats and humans as potential chronic pain biomarkers. PLoS ONE 8, e77799 (2013). 10.1371/journal.pone.0077799

[33]

Grace, P. M. et al. Harnessing pain heterogeneity and RNA transcriptome to identify blood-based pain biomarkers: a novel correlational study design and bioinformatics approach in a graded chronic constriction injury model. J. Neurochem. 122, 976–994 (2012). 10.1111/j.1471-4159.2012.07833.x

[34]

Kwok, Y. H., Hutchinson, M. R., Gentgall, M. G. & Rolan, P. E. Increased responsiveness of peripheral blood mononuclear cells to in vitro TLR 2, 4 and 7 ligand stimulation in chronic pain patients. PLoS ONE 7, e44232 (2012). 10.1371/journal.pone.0044232

[35]

Hutchinson, M. R., La Vincente, S. F. & Somogyi, A. A. In vitro opioid induced proliferation of peripheral blood immune cells correlates with in vivo cold pressor pain tolerance in humans: a biological marker of pain tolerance. Pain 110, 751–755 (2004). 10.1016/j.pain.2004.05.017

[36]

Tian, L., Rauvala, H. & Gahmberg, C. G. Neuronal regulation of immune responses in the central nervous system. Trends Immunol. 30, 91–99 (2009). 10.1016/j.it.2008.11.002

[37]

Hoarau, J. J. et al. Activation and control of CNS innate immune responses in health and diseases: a balancing act finely tuned by neuroimmune regulators (NIReg). CNS Neurol. Disord. Drug Targets 10, 25–43 (2011). 10.2174/187152711794488601

[38]

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). 10.1038/nature01868

[39]

Coull, J. A. et al. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438, 1017–1021 (2005). The first report to identify a mechanism for glial-mediated enhancement of pain signalling. 10.1038/nature04223

[40]

Tsuda, M. et al. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 424, 778–783 (2003). 10.1038/nature01786

[41]

Glia and pain: Is chronic pain a gliopathy?

Ru-Rong Ji, Temugin Berta, Maiken Nedergaard

Pain 2013 10.1016/j.pain.2013.06.022

[42]

Milligan, E. D. & Watkins, L. R. Pathological and protective roles of glia in chronic pain. Nature Rev. Neurosci. 10, 23–36 (2009). 10.1038/nrn2533

[43]

Kim, D. et al. A critical role of toll-like receptor 2 in nerve injury-induced spinal cord glial cell activation and pain hypersensitivity. J. Biol. Chem. 282, 14975–14983 (2007). 10.1074/jbc.m607277200

[44]

Wen, Y. R. et al. Nerve conduction blockade in the sciatic nerve prevents but does not reverse the activation of p38 mitogen-activated protein kinase in spinal microglia in the rat spared nerve injury model. Anesthesiology 107, 312–321 (2007). 10.1097/01.anes.0000270759.11086.e7

[45]

Suter, M. R., Berta, T., Gao, Y. J., Decosterd, I. & Ji, R. R. Large A-fiber activity is required for microglial proliferation and p38 MAPK activation in the spinal cord: different effects of resiniferatoxin and bupivacaine on spinal microglial changes after spared nerve injury. Mol. Pain 5, 53 (2009). 10.1186/1744-8069-5-53

[46]

Kawasaki, Y. et al. Distinct roles of matrix metalloproteases in the early- and late-phase development of neuropathic pain. Nature Med. 14, 331–336 (2008). 10.1038/nm1723

[47]

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). 10.1523/jneurosci.5169-09.2010

[48]

Abbadie, C. et al. Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2. Proc. Natl Acad. Sci. USA 100, 7947–7952 (2003). 10.1073/pnas.1331358100

[49]

Van Steenwinckel, J. et al. CCL2 released from neuronal synaptic vesicles in the spinal cord is a major mediator of local inflammation and pain after peripheral nerve injury. J. Neurosci. 31, 5865–5875 (2011). 10.1523/jneurosci.5986-10.2011

[50]

Dansereau, M. A. et al. Spinal CCL2 pronociceptive action is no longer effective in CCR2 receptor antagonist-treated rats. J. Neurochem. 106, 757–769 (2008). 10.1111/j.1471-4159.2008.05429.x

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Published: Feb 28, 2014
Vol/Issue: 14(4)
Pages: 217-231
License: View

Authors

Department of Psychology and

L

Linda R. Watkins

Department of Psychology and

Cite This Article

Peter M. Grace, Mark R. Hutchinson, Steven F. Maier, et al. (2014). Pathological pain and the neuroimmune interface. Nature Reviews Immunology, 14(4), 217-231. https://doi.org/10.1038/nri3621

Pathological pain and the neuroimmune interface

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