Neuropathic pain caused by miswiring and abnormal end organ targeting.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
06 2022
06 2022
Historique:
received:
15
04
2021
accepted:
20
04
2022
pubmed:
26
5
2022
medline:
7
6
2022
entrez:
25
5
2022
Statut:
ppublish
Résumé
Nerve injury leads to chronic pain and exaggerated sensitivity to gentle touch (allodynia) as well as a loss of sensation in the areas in which injured and non-injured nerves come together
Identifiants
pubmed: 35614217
doi: 10.1038/s41586-022-04777-z
pii: 10.1038/s41586-022-04777-z
pmc: PMC9159955
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
137-145Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2022. The Author(s).
Références
Devor, M. in Wall and Melzack’s Textbook of Pain 5th edn (eds McMahon, S. B. & Koltzenburg, M.) 905–927 (Churchill Livingstone, 2006).
Campbell, J. N. & Meyer, R. A. Mechanisms of neuropathic pain. Neuron 52, 77–92 (2006).
pubmed: 17015228
pmcid: 1810425
doi: 10.1016/j.neuron.2006.09.021
Finnerup, N. B., Kuner, R. & Jensen, T. S. Neuropathic pain: from mechanisms to treatment. Physiol. Rev. 101, 259–301 (2021).
pubmed: 32584191
doi: 10.1152/physrev.00045.2019
Campbell, J. N., Raja, S. N., Meyer, R. A. & Mackinnon, S. E. Myelinated afferents signal the hyperalgesia associated with nerve injury. Pain 32, 89–94 (1988).
pubmed: 3340426
doi: 10.1016/0304-3959(88)90027-9
Dhandapani, R. et al. Control of mechanical pain hypersensitivity in mice through ligand-targeted photoablation of TrkB-positive sensory neurons. Nat. Commun. 9, 1640 (2018).
pubmed: 29691410
pmcid: 5915601
doi: 10.1038/s41467-018-04049-3
Tashima, R. et al. Optogenetic activation of non-nociceptive Aβ fibers induces neuropathic pain-like sensory and emotional behaviors after nerve injury in rats. eNeuro 5, https://doi.org/10.1523/eneuro.0450-17.2018 (2018).
Moehring, F., Halder, P., Seal, R. P. & Stucky, C. L. Uncovering the cells and circuits of touch in normal and pathological settings. Neuron 100, 349–360 (2018).
pubmed: 30359601
pmcid: 6708582
doi: 10.1016/j.neuron.2018.10.019
Ji, R.-R. & Strichartz, G. Cell signaling and the genesis of neuropathic pain. Sci. STKE 2004, re14 (2004).
doi: 10.1126/stke.2522004re14
Beggs, S., Trang, T. & Salter, M. W. P2X4R
pubmed: 22837036
pmcid: 5023423
doi: 10.1038/nn.3155
Ji, R. R., Donnelly, C. R. & Nedergaard, M. Astrocytes in chronic pain and itch. Nat. Rev. Neurosci. 20, 667–685 (2019).
pubmed: 31537912
pmcid: 6874831
doi: 10.1038/s41583-019-0218-1
Chen, G., Zhang, Y. Q., Qadri, Y. J., Serhan, C. N. & Ji, R. R. Microglia in pain: detrimental and protective roles in pathogenesis and resolution of pain. Neuron 100, 1292–1311 (2018).
pubmed: 30571942
pmcid: 6312407
doi: 10.1016/j.neuron.2018.11.009
Cheng, L. et al. Identification of spinal circuits involved in touch-evoked dynamic mechanical pain. Nat. Neurosci. 20, 804–814 (2017).
pubmed: 28436981
pmcid: 5470641
doi: 10.1038/nn.4549
Peirs, C. et al. Dorsal horn circuits for persistent mechanical pain. Neuron 87, 797–812 (2015).
pubmed: 26291162
pmcid: 4562334
doi: 10.1016/j.neuron.2015.07.029
Coull, J. A. et al. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 438, 1017–1021 (2005).
pubmed: 16355225
doi: 10.1038/nature04223
Foster, E. et al. Targeted ablation, silencing, and activation establish glycinergic dorsal horn neurons as key components of a spinal gate for pain and itch. Neuron 85, 1289–1304 (2015).
pubmed: 25789756
pmcid: 4372258
doi: 10.1016/j.neuron.2015.02.028
Kuner, R. & Flor, H. Structural plasticity and reorganisation in chronic pain. Nat. Rev. Neurosci. 18, 20–30 (2016).
pubmed: 27974843
doi: 10.1038/nrn.2016.162
Burnett, M. G. & Zager, E. L. Pathophysiology of peripheral nerve injury: a brief review. Neurosurg. Focus 16, E1 (2004).
pubmed: 15174821
doi: 10.3171/foc.2004.16.5.2
Griffin, J. W., Pan, B., Polley, M. A., Hoffman, P. N. & Farah, M. H. Measuring nerve regeneration in the mouse. Exp. Neurol. 223, 60–71 (2010).
pubmed: 20080088
doi: 10.1016/j.expneurol.2009.12.033
Jessen, K. R., Mirsky, R. & Lloyd, A. C. Schwann cells: development and role in nerve repair. Cold Spring Harb. Perspect. Biol. 7, a020487 (2015).
pubmed: 25957303
pmcid: 4484967
doi: 10.1101/cshperspect.a020487
Bolívar, S., Navarro, X. & Udina, E. Schwann cell role in selectivity of nerve regeneration. Cells 9, 2131 (2020).
pmcid: 7563640
doi: 10.3390/cells9092131
Taylor, K. S., Anastakis, D. J. & Davis, K. D. Chronic pain and sensorimotor deficits following peripheral nerve injury. Pain 151, 582–591 (2010).
pubmed: 20655145
doi: 10.1016/j.pain.2010.06.032
Peleshok, J. C. & Ribeiro-da-Silva, A. Delayed reinnervation by nonpeptidergic nociceptive afferents of the glabrous skin of the rat hindpaw in a neuropathic pain model. J. Comp. Neurol. 519, 49–63 (2011).
pubmed: 21120927
doi: 10.1002/cne.22500
Kerr, J. N. & Denk, W. Imaging in vivo: watching the brain in action. Nat. Rev. Neurosci. 9, 195–205 (2008).
pubmed: 18270513
doi: 10.1038/nrn2338
Basbaum, A. I., Bautista, D. M., Scherrer, G. & Julius, D. Cellular and molecular mechanisms of pain. Cell 139, 267–284 (2009).
pubmed: 19837031
pmcid: 2852643
doi: 10.1016/j.cell.2009.09.028
Agarwal, N., Offermanns, S. & Kuner, R. Conditional gene deletion in primary nociceptive neurons of trigeminal ganglia and dorsal root ganglia. Genesis 38, 122–129 (2004).
pubmed: 15048809
doi: 10.1002/gene.20010
Decosterd, I. & Woolf, C. J. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87, 149–158 (2000).
pubmed: 10924808
doi: 10.1016/S0304-3959(00)00276-1
Djouhri, L., Fang, X., Koutsikou, S. & Lawson, S. N. Partial nerve injury induces electrophysiological changes in conducting (uninjured) nociceptive and nonnociceptive DRG neurons: possible relationships to aspects of peripheral neuropathic pain and paresthesias. Pain 153, 1824–1836 (2012).
pubmed: 22721911
pmcid: 3425771
doi: 10.1016/j.pain.2012.04.019
Song, Y. et al. The mechanosensitive ion channel piezo inhibits axon regeneration. Neuron 102, 373–389 (2019).
pubmed: 30819546
pmcid: 6487666
doi: 10.1016/j.neuron.2019.01.050
Zigmond, R. E. & Echevarria, F. D. Macrophage biology in the peripheral nervous system after injury. Prog. Neurobiol. 173, 102–121 (2019).
pubmed: 30579784
doi: 10.1016/j.pneurobio.2018.12.001
Monk, K. R., Feltri, M. L. & Taveggia, C. New insights on Schwann cell development. Glia 63, 1376–1393 (2015).
pubmed: 25921593
pmcid: 4470834
doi: 10.1002/glia.22852
Weinstein, B. M. Vessels and nerves: marching to the same tune. Cell 120, 299–302 (2005).
pubmed: 15707889
doi: 10.1016/j.cell.2005.01.010
Abraira, V. E. & Ginty, D. D. The sensory neurons of touch. Neuron 79, 618–639 (2013).
pubmed: 23972592
doi: 10.1016/j.neuron.2013.07.051
Fleming, M. S. & Luo, W. The anatomy, function, and development of mammalian Aβ low-threshold mechanoreceptors. Front. Biol. 8, 408–420 (2013).
doi: 10.1007/s11515-013-1271-1
Neubarth, N. L. et al. Meissner corpuscles and their spatially intermingled afferents underlie gentle touch perception. Science 368, eabb2751 (2020).
pubmed: 32554568
pmcid: 7354383
doi: 10.1126/science.abb2751
Dogiel, A. S. Die Nervenendigunden in Meissnerschen tasktköperen. Monthly Int. J. Anat. Physiol. 9, 76–85 (1892).
Cauna, N. Nerve supply and nerve endings in Meissner’s corpuscles. Am. J. Anat. 99, 315–350 (1956).
pubmed: 13372495
doi: 10.1002/aja.1000990206
Johansson, O., Fantini, F. & Hu, H. Neuronal structural proteins, transmitters, transmitter enzymes and neuropeptides in human Meissner’s corpuscles: a reappraisal using immunohistochemistry. Arch. Dermatol. Res. 291, 419–424 (1999).
pubmed: 10482012
doi: 10.1007/s004030050432
Paré, M., Elde, R., Mazurkiewicz, J. E., Smith, A. M. & Rice, F. L. The Meissner corpuscle revised: a multiafferented mechanoreceptor with nociceptor immunochemical properties. J. Neurosci. 21, 7236–7246 (2001).
pubmed: 11549734
pmcid: 6763005
doi: 10.1523/JNEUROSCI.21-18-07236.2001
Ishida-Yamamoto, A., Senba, E. & Tohyama, M. Calcitonin gene-related peptide- and substance P-immunoreactive nerve fibers in Meissner’s corpuscles of rats: an immunohistochemical analysis. Brain Res. 453, 362–366 (1988).
doi: 10.1016/0006-8993(88)90179-5
Seal, R. P. et al. Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. Nature 462, 651–655 (2009).
pubmed: 19915548
pmcid: 2810205
doi: 10.1038/nature08505
Delfini, M.-C. et al. TAFA4, a chemokine-like protein, modulates injury-induced mechanical and chemical pain hypersensitivity in mice. Cell Rep. 5, 378–388 (2013).
pubmed: 24139797
doi: 10.1016/j.celrep.2013.09.013
Abrahamsen, B. et al. The cell and molecular basis of mechanical, cold, and inflammatory pain. Science 321, 702–705 (2008).
pubmed: 18669863
doi: 10.1126/science.1156916
Rivers, W. H. R. & Head, H. A human experiment in nerve division. Brain 31, 323–450 (1908).
doi: 10.1093/brain/31.3.323
Compston, A. A human experiment in nerve division by W. H. R. Rivers MD FRS, Fellow of St John’s College, Cambridge and Henry Head MD FRS, Physician to the London Hospital, Brain 1908: 31; 323–450. Brain 132, 2903–2905 (2009).
pubmed: 19877308
doi: 10.1093/brain/awp288
Woolf, C. J., Shortland, P. & Coggeshall, R. E. Peripheral nerve injury triggers central sprouting of myelinated afferents. Nature 355, 75–78 (1992).
pubmed: 1370574
doi: 10.1038/355075a0
Bogen, O., Alessandri-Haber, N., Chu, C., Gear, R. W. & Levine, J. D. Generation of a pain memory in the primary afferent nociceptor triggered by PKCε activation of CPEB. J. Neurosci. 32, 2018–2026 (2012).
pubmed: 22323716
pmcid: 3305286
doi: 10.1523/JNEUROSCI.5138-11.2012
Calvo, M., Dawes, J. M. & Bennett, D. L. The role of the immune system in the generation of neuropathic pain. Lancet Neurol. 11, 629–642 (2012).
pubmed: 22710756
doi: 10.1016/S1474-4422(12)70134-5
Usoskin, D. et al. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat. Neurosci. 18, 145–153 (2015).
doi: 10.1038/nn.3881
Abdo, H. et al. Specialized cutaneous Schwann cells initiate pain sensation. Science 365, 695–699 (2019).
pubmed: 31416963
doi: 10.1126/science.aax6452
Rinwa, P. et al. Demise of nociceptive Schwann cells causes nerve retraction and pain hyperalgesia. Pain 162, 1816–1827 (2021).
doi: 10.1097/j.pain.0000000000002169
Maksimovic, S. et al. Epidermal Merkel cells are mechanosensory cells that tune mammalian touch receptors. Nature 509, 617–621 (2014).
pubmed: 24717432
pmcid: 4097312
doi: 10.1038/nature13250
Woo, S. H. et al. Piezo2 is required for Merkel-cell mechanotransduction. Nature 509, 622–626 (2014).
pubmed: 24717433
pmcid: 4039622
doi: 10.1038/nature13251
Arcourt, A. et al. Touch receptor-derived sensory information alleviates acute pain signaling and fine-tunes nociceptive reflex coordination. Neuron 93, 179–193 (2017).
pubmed: 27989460
doi: 10.1016/j.neuron.2016.11.027
Melzack, R. & Wall, P. D. Pain mechanisms: a new theory. Science 150, 971–979 (1965).
pubmed: 5320816
doi: 10.1126/science.150.3699.971
Prescott, S. A., Ma, Q. & De Koninck, Y. Normal and abnormal coding of somatosensory stimuli causing pain. Nat. Neurosci. 17, 183–191 (2014).
pubmed: 24473266
pmcid: 4079041
doi: 10.1038/nn.3629
Duan, B., Cheng, L. & Ma, Q. Spinal circuits transmitting mechanical pain and itch. Neurosci. Bull. 34, 186–193 (2018).
pubmed: 28484964
doi: 10.1007/s12264-017-0136-z
Liu, Y. et al. Touch and tactile neuropathic pain sensitivity are set by corticospinal projections. Nature 561, 547–550 (2018).
pubmed: 30209395
pmcid: 6163083
doi: 10.1038/s41586-018-0515-2
Hippenmeyer, S. et al. A developmental switch in the response of DRG neurons to ETS transcription factor signaling. PLoS Biol. 3, e159 (2005).
pubmed: 15836427
pmcid: 1084331
doi: 10.1371/journal.pbio.0030159
Gangadharan, V. et al. Peripheral calcium-permeable AMPA receptors regulate chronic inflammatory pain in mice. J. Clin. Invest. 121, 1608–1623 (2011).
pubmed: 21383497
pmcid: 3069784
doi: 10.1172/JCI44911
Buch, T. et al. A Cre-inducible diphtheria toxin receptor mediates cell lineage ablation after toxin administration. Nat. Methods 2, 419–426 (2005).
pubmed: 15908920
doi: 10.1038/nmeth762
Theer, P. & Denk, W. On the fundamental imaging-depth limit in two-photon microscopy. J. Opt. Soc. Am. A 23, 3139–3149 (2006).
doi: 10.1364/JOSAA.23.003139
Lowe, D. G. Distinctive image features from scale-invariant keypoints. Int. J. Comput. Vis. 60, 91–110 (2004).
doi: 10.1023/B:VISI.0000029664.99615.94
Bay, H., Tuytelaars, T. & Van Gool, L. SURF: Speeded Up Robust Features. In Proc. 9th European Conference on Computer Vision (eds Leonardis, A., Bischof, H. & Pinz, A.) 404–417 (Springer, 2006).
Wahba, G. Spline Models for Observational Data (Society for Industrial and Applied Mathematics, 1990).
Picelli, S. et al. Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 9, 171–181 (2014).
pubmed: 24385147
doi: 10.1038/nprot.2014.006
Hennig, B. P. et al. Large-scale low-cost NGS library preparation using a robust Tn5 purification and tagmentation protocol. G3 8, 79–89 (2018).
doi: 10.1534/g3.117.300257
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
doi: 10.1093/bioinformatics/bts635
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
doi: 10.1186/s13059-014-0550-8
Bauer, S & Gagneur, J. Mgsa: Model-based gene set analysis. R version 1.42.0 https://github.com/sba1/mgsa-bioc (2021).
Jew, B. et al. Accurate estimation of cell composition in bulk expression through robust integration of single-cell information. Nat. Commun. 11, 1971 (2020).
pubmed: 32332754
pmcid: 7181686
doi: 10.1038/s41467-020-15816-6
Hua, Y., Laserstein, P. & Helmstaedter, M. Large-volume en-bloc staining for electron microscopy-based connectomics. Nat. Commun. 6, 7923 (2015).
pubmed: 26235643
doi: 10.1038/ncomms8923
Denk., W. & Horstmann, H. Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol. 2, e329 (2004).
pubmed: 15514700
pmcid: 524270
doi: 10.1371/journal.pbio.0020329
Karimi, A., Odenthal, J., Drawitsch, F., Boergens, K. M. & Helmstaedter, M. Cell-type specific innervation of cortical pyramidal cells at their apical dendrites. eLife 9, e46876 (2020).
pubmed: 32108571
pmcid: 7297530
doi: 10.7554/eLife.46876
Motta, A. et al. Dense connectomic reconstruction in layer 4 of the somatosensory cortex. Science 366, eaay3134 (2019).
pubmed: 31649140
doi: 10.1126/science.aay3134
Boergens, K. et al. webKnossos: efficient online 3D data annotation for connectomics. Nat. Methods 14, 691–694 (2017).
pubmed: 28604722
doi: 10.1038/nmeth.4331
Selvaraj, D. et al. A functional role for VEGFR1 expressed in peripheral sensory neurons in cancer pain. Cancer Cell 27, 780–796 (2015).
pubmed: 26058077
pmcid: 4469373
doi: 10.1016/j.ccell.2015.04.017
Schweizerhof, M. et al. Hematopoietic colony-stimulating factors mediate tumor-nerve interactions and bone cancer pain. Nat. Med. 15, 802–807 (2009).
pubmed: 19525966
doi: 10.1038/nm.1976