1932

Abstract

Schwann cells in the peripheral nervous system (PNS) are essential for the support and myelination of axons, ensuring fast and accurate communication between the central nervous system and the periphery. Schwann cells and related glia accompany innervating axons in virtually all tissues in the body, where they exhibit remarkable plasticity and the ability to modulate pathology in extraordinary, and sometimes surprising, ways. Here, we provide a brief overview of the various glial cell types in the PNS and describe the cornerstone cellular and molecular processes that enable Schwann cells to perform their canonical functions. We then dive into discussing exciting noncanonical functions of Schwann cells and related PNS glia, which include their role in organizing the PNS, in regulating synaptic activity and pain, in modulating immunity, in providing a pool of stem cells for different organs, and, finally, in influencing cancer.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-110920-030610
2022-07-08
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/neuro/45/1/annurev-neuro-110920-030610.html?itemId=/content/journals/10.1146/annurev-neuro-110920-030610&mimeType=html&fmt=ahah

Literature Cited

  1. Abdo H, Calvo-Enrique L, Lopez JM, Song J, Zhang MD et al. 2019. Specialized cutaneous Schwann cells initiate pain sensation. Science 365:695–99
    [Google Scholar]
  2. Adameyko I, Lallemend F, Aquino JB, Pereira JA, Topilko P et al. 2009. Schwann cell precursors from nerve innervation are a cellular origin of melanocytes in skin. Cell 139:366–79
    [Google Scholar]
  3. Aquino JB, Sierra R. 2018. Schwann cell precursors in health and disease. Glia 66:465–76
    [Google Scholar]
  4. Araque A, Parpura V, Sanzgiri RP, Haydon PG. 1999. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci 22:208–15
    [Google Scholar]
  5. Arroyo EJ, Xu YT, Zhou L, Messing A, Peles E et al. 1999. Myelinating Schwann cells determine the inter-nodal localization of Kv1.1, Kv1.2, Kvβ2, and Caspr. J. Neurocytol. 28:333–47
    [Google Scholar]
  6. Arthur-Farraj PJ, Latouche M, Wilton DK, Quintes S, Chabrol E et al. 2012. c-Jun reprograms Schwann cells of injured nerves to generate a repair cell essential for regeneration. Neuron 75:633–47
    [Google Scholar]
  7. Arthur-Farraj PJ, Morgan CC, Adamowicz M, Gomez-Sanchez JA, Fazal SV et al. 2017. Changes in the coding and non-coding transcriptome and DNA methylome that define the Schwann cell repair phenotype after nerve injury. Cell Rep 20:2719–34
    [Google Scholar]
  8. Avraham O, Deng PY, Jones S, Kuruvilla R, Semenkovich CF et al. 2020. Satellite glial cells promote regenerative growth in sensory neurons. Nat. Commun. 11:4891
    [Google Scholar]
  9. Babetto E, Wong KM, Beirowski B. 2020. A glycolytic shift in Schwann cells supports injured axons. Nat. Neurosci. 23:1215–28
    [Google Scholar]
  10. Balice-Gordon RJ, Bone LJ, Scherer SS. 1998. Functional gap junctions in the Schwann cell myelin sheath. J. Cell Biol. 142:1095–104
    [Google Scholar]
  11. Barnett SC, Chang L. 2004. Olfactory ensheathing cells and CNS repair: going solo or in need of a friend?. Trends Neurosci 27:54–60
    [Google Scholar]
  12. Benito C, Davis CM, Gomez-Sanchez JA, Turmaine M, Meijer D et al. 2017. STAT3 controls the long-term survival and phenotype of repair Schwann cells during nerve regeneration. J. Neurosci. 37:4255–69
    [Google Scholar]
  13. Benninger Y, Thurnherr T, Pereira JA, Krause S, Wu X et al. 2007. Essential and distinct roles for cdc42 and rac1 in the regulation of Schwann cell biology during peripheral nervous system development. J. Cell Biol. 177:1051–61
    [Google Scholar]
  14. Bermingham JR Jr., Shearin H, Pennington J, O'Moore J, Jaegle M et al. 2006. The claw paw mutation reveals a role for Lgi4 in peripheral nerve development. Nat. Neurosci. 9:76–84
    [Google Scholar]
  15. Bhat MA, Rios JC, Lu Y, Garcia-Fresco GP, Ching W et al. 2001. Axon-glia interactions and the domain organization of myelinated axons requires neurexin IV/Caspr/Paranodin. Neuron 30:369–83
    [Google Scholar]
  16. Birchmeier C, Nave KA. 2008. Neuregulin-1, a key axonal signal that drives Schwann cell growth and differentiation. Glia 56:1491–97
    [Google Scholar]
  17. Boilly B, Faulkner S, Jobling P, Hondermarck H. 2017. Nerve dependence: from regeneration to cancer. Cancer Cell 31:342–54
    [Google Scholar]
  18. Boucanova F, Pollmeier G, Sandor K, Morado Urbina C, Nijssen J et al. 2021. Disrupted function of lactate transporter MCT1, but not MCT4, in Schwann cells affects the maintenance of motor end-plate innervation. Glia 69:124–36
    [Google Scholar]
  19. Brown AM, Evans RD, Black J, Ransom BR. 2012. Schwann cell glycogen selectively supports myelinated axon function. Ann. Neurol. 72:406–18
    [Google Scholar]
  20. Bunimovich YL, Keskinov AA, Shurin GV, Shurin MR. 2017. Schwann cells: a new player in the tumor microenvironment. Cancer Immunol. Immunother. 66:959–68
    [Google Scholar]
  21. Campana WM. 2007. Schwann cells: activated peripheral glia and their role in neuropathic pain. Brain Behav. Immun. 21:522–27
    [Google Scholar]
  22. Castro R, Taetzsch T, Vaughan SK, Godbe K, Chappell J et al. 2020. Specific labeling of synaptic Schwann cells reveals unique cellular and molecular features. eLife 9:e56935
    [Google Scholar]
  23. Cattin AL, Burden JJ, Van Emmenis L, Mackenzie FE, Hoving JJ et al. 2015. Macrophage-induced blood vessels guide Schwann cell-mediated regeneration of peripheral nerves. Cell 162:1127–39
    [Google Scholar]
  24. Cavaletti G, Marmiroli P. 2010. Chemotherapy-induced peripheral neurotoxicity. Nat. Rev. Neurol. 6:657–66
    [Google Scholar]
  25. Chen CS, Weber J, Holtkamp SJ, Ince LM, de Juan A et al. 2021. Loss of direct adrenergic innervation after peripheral nerve injury causes lymph node expansion through IFN-γ. J. Exp. Med. 218:e20202377
    [Google Scholar]
  26. Ching W, Zanazzi G, Levinson SR, Salzer JL. 1999. Clustering of neuronal sodium channels requires contact with myelinating Schwann cells. J. Neurocytol. 28:295–301
    [Google Scholar]
  27. Clark JK, O'Keefe A, Mastracci TL, Sussel L, Matise MP, Kucenas S. 2014. Mammalian Nkx2.2+ perineurial glia are essential for motor nerve development. Dev. Dyn. 243:1116–29
    [Google Scholar]
  28. Clements MP, Byrne E, Camarillo Guerrero LF, Cattin AL, Zakka L et al. 2017. The wound microenvironment reprograms Schwann cells to invasive mesenchymal-like cells to drive peripheral nerve regeneration. Neuron 96:98–114.e7
    [Google Scholar]
  29. Coleman MP, Hoke A. 2020. Programmed axon degeneration: from mouse to mechanism to medicine. Nat. Rev. Neurosci. 21:183–96
    [Google Scholar]
  30. Colombelli C, Palmisano M, Eshed-Eisenbach Y, Zambroni D, Pavoni E et al. 2015. Perlecan is recruited by dystroglycan to nodes of Ranvier and binds the clustering molecule gliomedin. J. Cell Biol. 208:313–29
    [Google Scholar]
  31. Colombo S, Petit V, Wagner RY, Champeval D, Yajima Iet al 2022. Stabilization of β-catenin promotes melanocyte specification at the expense of the Schwann cell lineage. Development 149:dev194407
    [Google Scholar]
  32. Cram JP, Wu J, Cover RA, Rizvi TA, Chaney KEet al 2022. P2RY14 cAMP signaling regulates Schwann cell precursor self-renewal, proliferation, and nerve tumor initiation in a mouse model of neurofibromatosis. eLife 11:e73511
    [Google Scholar]
  33. Crippa S, Pergolini I, Javed AA, Honselmann KC, Weiss MJ et al. 2020. Implications of perineural invasion on disease recurrence and survival after pancreatectomy for pancreatic head ductal adenocarcinoma. Ann. Surg. In press
    [Google Scholar]
  34. Darabid H, Perez-Gonzalez AP, Robitaille R. 2014. Neuromuscular synaptogenesis: coordinating partners with multiple functions. Nat. Rev. Neurosci. 15:703–18
    [Google Scholar]
  35. De Logu F, Nassini R, Hegron A, Landini L, Jensen DDet al 2022. Schwann cell endosome CGRP signals elicit periorbital mechanical allodynia in mice. Nat. Commun 13:646
    [Google Scholar]
  36. Deborde S, Omelchenko T, Lyubchik A, Zhou Y, He S et al. 2016. Schwann cells induce cancer cell dispersion and invasion. J. Clin. Investig. 126:1538–54
    [Google Scholar]
  37. DeFrancesco-Lisowitz A, Lindborg JA, Niemi JP, Zigmond RE. 2015. The neuroimmunology of degeneration and regeneration in the peripheral nervous system. Neuroscience 302:174–203
    [Google Scholar]
  38. Demir IE, Boldis A, Pfitzinger PL, Teller S, Brunner E et al. 2014. Investigation of Schwann cells at neoplastic cell sites before the onset of cancer invasion. J. Natl. Cancer Inst. 106:dju184
    [Google Scholar]
  39. Dubeykovskaya Z, Si Y, Chen X, Worthley DL, Renz BW et al. 2016. Neural innervation stimulates splenic TFF2 to arrest myeloid cell expansion and cancer. Nat. Commun. 7:10517
    [Google Scholar]
  40. Dyachuk V, Furlan A, Shahidi MK, Giovenco M, Kaukua N et al. 2014. Neurodevelopment. Parasympathetic neurons originate from nerve-associated peripheral glial progenitors. Science 345:82–87
    [Google Scholar]
  41. Dzhashiashvili Y, Zhang Y, Galinska J, Lam I, Grumet M, Salzer JL. 2007. Nodes of Ranvier and axon initial segments are ankyrin G-dependent domains that assemble by distinct mechanisms. J. Cell Biol. 177:857–70
    [Google Scholar]
  42. Edgar JM, McLaughlin M, Werner HB, McCulloch MC, Barrie JA et al. 2009. Early ultrastructural defects of axons and axon-glia junctions in mice lacking expression of Cnp1. Glia 57:1815–24
    [Google Scholar]
  43. Einheber S, Zanazzi G, Ching W, Scherer S, Milner TA et al. 1997. The axonal membrane protein Caspr, a homologue of neurexin IV, is a component of the septate-like paranodal junctions that assemble during myelination. J. Cell Biol. 139:1495–506
    [Google Scholar]
  44. Eshed Y, Feinberg K, Poliak S, Sabanay H, Sarig-Nadir O et al. 2005. Gliomedin mediates Schwann cell-axon interaction and the molecular assembly of the nodes of Ranvier. Neuron 47:215–29
    [Google Scholar]
  45. Espinosa-Medina I, Outin E, Picard CA, Chettouh Z, Dymecki S et al. 2014. Parasympathetic ganglia derive from Schwann cell precursors. Science 345:87–90
    [Google Scholar]
  46. Faivre-Sarrailh C. 2020. Molecular organization and function of vertebrate septate-like junctions. Biochim. Biophys. Acta Biomembr. 1862:183211
    [Google Scholar]
  47. Fehmi J, Scherer SS, Willison HJ, Rinaldi S. 2018. Nodes, paranodes and neuropathies. J. Neurol. Neurosurg. Psychiatry 89:61–71
    [Google Scholar]
  48. Feltri ML, Poitelon Y, Previtali SC. 2016. How Schwann cells sort axons: new concepts. Neuroscientist 22:252–65
    [Google Scholar]
  49. Filbin MT. 2003. Myelin-associated inhibitors of axonal regeneration in the adult mammalian CNS. Nat. Rev. Neurosci. 4:703–13
    [Google Scholar]
  50. Finzsch M, Schreiner S, Kichko T, Reeh P, Tamm ER et al. 2010. Sox10 is required for Schwann cell identity and progression beyond the immature Schwann cell stage. J. Cell Biol. 189:701–12
    [Google Scholar]
  51. Forese MG, Pellegatta M, Canevazzi P, Gullotta GS, Podini P et al. 2020. Prostaglandin D2 synthase modulates macrophage activity and accumulation in injured peripheral nerves. Glia 68:95–110
    [Google Scholar]
  52. Funfschilling U, Supplie LM, Mahad D, Boretius S, Saab AS et al. 2012. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485:517–21
    [Google Scholar]
  53. Furlan A, Adameyko I. 2018. Schwann cell precursor: a neural crest cell in disguise?. Dev. Biol. 444:Suppl. 1S25–35
    [Google Scholar]
  54. Furlan A, Dyachuk V, Kastriti ME, Calvo-Enrique L, Abdo H et al. 2017. Multipotent peripheral glial cells generate neuroendocrine cells of the adrenal medulla. Science 357:eaal3753
    [Google Scholar]
  55. Gasparini G, Pellegatta M, Crippa S, Lena MS, Belfiori G et al. 2019. Nerves and pancreatic cancer: new insights into a dangerous relationship. Cancers 11:893
    [Google Scholar]
  56. George D, Ahrens P, Lambert S 2018. Satellite glial cells represent a population of developmentally arrested Schwann cells. Glia 66:1496–506
    [Google Scholar]
  57. Gerber D, Pereira JA, Gerber J, Tan G, Dimitrieva S et al. 2021. Transcriptional profiling of mouse peripheral nerves to the single-cell level to build a sciatic nerve ATlas (SNAT). eLife 10:e58591
    [Google Scholar]
  58. Ghidinelli M, Poitelon Y, Shin YK, Ameroso D, Williamson C et al. 2017. Laminin 211 inhibits protein kinase A in Schwann cells to modulate neuregulin 1 type III-driven myelination. PLOS Biol 15:e2001408
    [Google Scholar]
  59. Gillespie CS, Sherman DL, Fleetwood-Walker SM, Cottrell DF, Tait S et al. 2000. Peripheral demyelination and neuropathic pain behavior in periaxin-deficient mice. Neuron 26:523–31
    [Google Scholar]
  60. Goebbels S, Oltrogge JH, Kemper R, Heilmann I, Bormuth I et al. 2010. Elevated phosphatidylinositol 3,4,5-trisphosphate in glia triggers cell-autonomous membrane wrapping and myelination. J. Neurosci. 30:8953–64
    [Google Scholar]
  61. Gomez-Sanchez JA, Carty L, Iruarrizaga-Lejarreta M, Palomo-Irigoyen M, Varela-Rey M et al. 2015. Schwann cell autophagy, myelinophagy, initiates myelin clearance from injured nerves. J. Cell Biol. 210:153–68
    [Google Scholar]
  62. Grace PM, Hutchinson MR, Maier SF, Watkins LR. 2014. Pathological pain and the neuroimmune interface. Nat. Rev. Immunol. 14:217–31
    [Google Scholar]
  63. Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C et al. 1998. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280:1610–13
    [Google Scholar]
  64. Groh J, Klein I, Hollmann C, Wettmarshausen J, Klein D, Martini R. 2015. CSF-1-activated macrophages are target-directed and essential mediators of Schwann cell dedifferentiation and dysfunction in Cx32-deficient mice. Glia 63:977–86
    [Google Scholar]
  65. Grove M, Brophy PJ. 2014. FAK is required for Schwann cell spreading on immature basal lamina to coordinate the radial sorting of peripheral axons with myelination. J. Neurosci. 34:13422–34
    [Google Scholar]
  66. Gysler SM, Drapkin R. 2021. Tumor innervation: peripheral nerves take control of the tumor microenvironment. J. Clin. Investig. 131:e147276
    [Google Scholar]
  67. Hanani M, Spray DC. 2020. Emerging importance of satellite glia in nervous system function and dysfunction. Nat. Rev. Neurosci. 21:485–98
    [Google Scholar]
  68. Hayakawa Y, Sakitani K, Konishi M, Asfaha S, Niikura R et al. 2017. Nerve growth factor promotes gastric tumorigenesis through aberrant cholinergic signaling. Cancer Cell 31:21–34
    [Google Scholar]
  69. He Y, Kim JY, Dupree J, Tewari A, Melendez-Vasquez C et al. 2010. Yy1 as a molecular link between neuregulin and transcriptional modulation of peripheral myelination. Nat. Neurosci. 13:1472–80
    [Google Scholar]
  70. Hu X, Hicks CW, He W, Wong P, Macklin WB et al. 2006. Bace1 modulates myelination in the central and peripheral nervous system. Nat. Neurosci. 9:1520–25
    [Google Scholar]
  71. Huang S, Ziegler CGK, Austin J, Mannoun N, Vukovic M et al. 2021. Lymph nodes are innervated by a unique population of sensory neurons with immunomodulatory potential. Cell 184:441–59.e25
    [Google Scholar]
  72. Huxley AF, Stampfli R. 1949. Evidence for saltatory conduction in peripheral myelinated nerve fibres. J. Physiol. 108:315–39
    [Google Scholar]
  73. Ishii A, Furusho M, Bansal R. 2021. Mek/ERK1/2-MAPK and PI3K/Akt/mTOR signaling plays both independent and cooperative roles in Schwann cell differentiation, myelination and dysmyelination. Glia 69:2429–46
    [Google Scholar]
  74. Jaegle M, Mandemakers W, Broos L, Zwart R, Karis A et al. 1996. The POU factor Oct-6 and Schwann cell differentiation. Science 273:507–10
    [Google Scholar]
  75. Jagalur NB, Ghazvini M, Mandemakers W, Driegen S, Maas A et al. 2011. Functional dissection of the Oct6 Schwann cell enhancer reveals an essential role for dimeric Sox10 binding. J. Neurosci. 31:8585–94
    [Google Scholar]
  76. Jahromi BS, Robitaille R, Charlton MP. 1992. Transmitter release increases intracellular calcium in peri-synaptic Schwann cells in situ. Neuron 8:1069–77
    [Google Scholar]
  77. Jang SY, Shin YK, Park SY, Park JY, Lee HJ et al. 2016. Autophagic myelin destruction by Schwann cells during Wallerian degeneration and segmental demyelination. Glia 64:730–42
    [Google Scholar]
  78. Jessen KR, Arthur-Farraj P. 2019. Repair Schwann cell update: adaptive reprogramming, EMT, and stemness in regenerating nerves. Glia 67:421–37
    [Google Scholar]
  79. Jessen KR, Mirsky R, Lloyd AC. 2015. Schwann cells: development and role in nerve repair. Cold Spring Harb. Perspect. Biol. 7:a020487
    [Google Scholar]
  80. Jha MK, Lee Y, Russell KA, Yang F, Dastgheyb RM et al. 2020. Monocarboxylate transporter 1 in Schwann cells contributes to maintenance of sensory nerve myelination during aging. Glia 68:161–77
    [Google Scholar]
  81. Joseph NM, Mukouyama YS, Mosher JT, Jaegle M, Crone SA et al. 2004. Neural crest stem cells undergo multilineage differentiation in developing peripheral nerves to generate endoneurial fibroblasts in addition to Schwann cells. Development 131:5599–612
    [Google Scholar]
  82. Kao SC, Wu H, Xie J, Chang CP, Ranish JA et al. 2009. Calcineurin/NFAT signaling is required for neuregulin-regulated Schwann cell differentiation. Science 323:651–54
    [Google Scholar]
  83. Kaukua N, Shahidi MK, Konstantinidou C, Dyachuk V, Kaucka M et al. 2014. Glial origin of mesenchymal stem cells in a tooth model system. Nature 513:551–54
    [Google Scholar]
  84. Keswani SC, Leitz GJ, Hoke A. 2004. Erythropoietin is neuroprotective in models of HIV sensory neuropathy. Neurosci. Lett. 371:102–5
    [Google Scholar]
  85. Kristensson K, Olsson Y. 1971. The perineurium as a diffusion barrier to protein tracers. Differences between mature and immature animals. Acta Neuropathol 17:127–38
    [Google Scholar]
  86. La Marca R, Cerri F, Horiuchi K, Bachi A, Feltri ML et al. 2011. TACE (ADAM17) inhibits Schwann cell myelination. Nat. Neurosci. 14:857–65
    [Google Scholar]
  87. Laura M, Pipis M, Rossor AM, Reilly MM. 2019. Charcot-Marie-Tooth disease and related disorders: an evolving landscape. Curr. Opin. Neurol. 32:641–50
    [Google Scholar]
  88. Le Douarin NM, Teillet MA. 1974. Experimental analysis of the migration and differentiation of neuroblasts of the autonomic nervous system and of neurectodermal mesenchymal derivatives, using a biological cell marking technique. Dev. Biol. 41:162–84
    [Google Scholar]
  89. Lisak RP, Skundric D, Bealmear B, Ragheb S. 1997. The role of cytokines in Schwann cell damage, protection, and repair. J. Infect. Dis. 176:Suppl. 2S173–79
    [Google Scholar]
  90. Love FM, Thompson WJ. 1999. Glial cells promote muscle reinnervation by responding to activity-dependent postsynaptic signals. J. Neurosci. 19:10390–96
    [Google Scholar]
  91. Lyons DA, Pogoda HM, Voas MG, Woods IG, Diamond B et al. 2005. erbb3 and erbb2 are essential for Schwann cell migration and myelination in zebrafish. Curr. Biol. 15:513–24
    [Google Scholar]
  92. Ma KH, Hung HA, Svaren J. 2016. Epigenomic regulation of Schwann cell reprogramming in peripheral nerve injury. J. Neurosci. 36:9135–47
    [Google Scholar]
  93. Magnon C, Hall SJ, Lin J, Xue X, Gerber L et al. 2013. Autonomic nerve development contributes to prostate cancer progression. Science 341:1236361
    [Google Scholar]
  94. Malong L, Napoli I, White IJ, Stierli S, Bossio A, Lloyd AC. 2019. Macrophages enforce the blood nerve barrier. bioRxiv 493494. https://doi.org/10.1101/493494
    [Crossref]
  95. Martini R, Fischer S, Lopez-Vales R, David S 2008. Interactions between Schwann cells and macrophages in injury and inherited demyelinating disease. Glia 56:1566–77
    [Google Scholar]
  96. Martini R, Willison H. 2016. Neuroinflammation in the peripheral nerve: cause, modulator, or bystander in peripheral neuropathies?. Glia 64:475–86
    [Google Scholar]
  97. Martyn GV, Shurin GV, Keskinov AA, Bunimovich YL, Shurin MR. 2019. Schwann cells shape the neuro-immune environs and control cancer progression. Cancer Immunol. Immunother. 68:1819–29
    [Google Scholar]
  98. Meyer zu Horste G, Heidenreich H, Mausberg AK, Lehmann HC, ten Asbroek AL et al. 2010. Mouse Schwann cells activate MHC class I and II restricted T-cell responses, but require external peptide processing for MHC class II presentation. Neurobiol. Dis. 37:483–90
    [Google Scholar]
  99. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B et al. 2004. Axonal neuregulin-1 regulates myelin sheath thickness. Science 304:700–3
    [Google Scholar]
  100. Mizukami H, Osonoi S. 2020. Pathogenesis and molecular treatment strategies of diabetic neuropathy collateral glucose-utilizing pathways in diabetic polyneuropathy. Int. J. Mol. Sci. 22:94
    [Google Scholar]
  101. Monk KR, Naylor SG, Glenn TD, Mercurio S, Perlin JR et al. 2009. A G protein-coupled receptor is essential for Schwann cells to initiate myelination. Science 325:1402–5
    [Google Scholar]
  102. Morris JH, Hudson AR, Weddell G. 1972. A study of degeneration and regeneration in the divided rat sciatic nerve based on electron microscopy. II. The development of the “regenerating unit.. Z. Zellforsch. Mikrosk. Anat. 124:103–30
    [Google Scholar]
  103. Murata K, Dalakas MC. 2000. Expression of the co-stimulatory molecule BB-1, the ligands CTLA-4 and CD28 and their mRNAs in chronic inflammatory demyelinating polyneuropathy. Brain 123:Pt. 81660–66
    [Google Scholar]
  104. Murinson BB, Archer DR, Li Y, Griffin JW. 2005a. Degeneration of myelinated efferent fibers prompts mitosis in Remak Schwann cells of uninjured C-fiber afferents. J. Neurosci. 25:1179–87
    [Google Scholar]
  105. Murinson BB, Hoffman PN, Banihashemi MR, Meyer RA, Griffin JW. 2005b. C-fiber (Remak) bundles contain both isolectin B4-binding and calcitonin gene-related peptide-positive axons. J. Comp. Neurol. 484:392–402
    [Google Scholar]
  106. Napoli I, Noon LA, Ribeiro S, Kerai AP, Parrinello S et al. 2012. A central role for the ERK-signaling pathway in controlling Schwann cell plasticity and peripheral nerve regeneration in vivo. Neuron 73:729–42
    [Google Scholar]
  107. Nave KA, Werner HB. 2021. Ensheathment and myelination of axons: evolution of glial functions. Annu. Rev. Neurosci. 44:197–219
    [Google Scholar]
  108. Newbern JM, Li X, Shoemaker SE, Zhou J, Zhong J et al. 2011. Specific functions for ERK/MAPK signaling during PNS development. Neuron 69:91–105
    [Google Scholar]
  109. Nodari A, Zambroni D, Quattrini A, Court FA, D'Urso A et al. 2007. β1 integrin activates Rac1 in Schwann cells to generate radial lamellae during axonal sorting and myelination. J. Cell Biol. 177:1063–75
    [Google Scholar]
  110. Ohara PT, Vit JP, Bhargava A, Jasmin L. 2008. Evidence for a role of connexin 43 in trigeminal pain using RNA interference in vivo. J. Neurophysiol. 100:3064–73
    [Google Scholar]
  111. Orita S, Henry K, Mantuano E, Yamauchi K, De Corato A et al. 2013. Schwann cell LRP1 regulates Remak bundle ultrastructure and axonal interactions to prevent neuropathic pain. J. Neurosci. 33:5590–602
    [Google Scholar]
  112. Ozkaynak E, Abello G, Jaegle M, van Berge L, Hamer D et al. 2010. Adam22 is a major neuronal receptor for Lgi4-mediated Schwann cell signaling. J. Neurosci. 30:3857–64
    [Google Scholar]
  113. Paavola KJ, Sidik H, Zuchero JB, Eckart M, Talbot WS. 2014. Type IV collagen is an activating ligand for the adhesion G protein-coupled receptor GPR126. Sci. Signal. 7:ra76
    [Google Scholar]
  114. Parfejevs V, Antunes AT, Sommer L. 2018. Injury and stress responses of adult neural crest-derived cells. Dev. Biol. 444:Suppl. 1S356–65
    [Google Scholar]
  115. Parkinson DB, Bhaskaran A, Arthur-Farraj P, Noon LA, Woodhoo A et al. 2008. c-Jun is a negative regulator of myelination. J. Cell Biol. 181:625–37
    [Google Scholar]
  116. Parmantier E, Lynn B, Lawson D, Turmaine M, Namini SS et al. 1999. Schwann cell-derived Desert hedgehog controls the development of peripheral nerve sheaths. Neuron 23:713–24
    [Google Scholar]
  117. Parrinello S, Napoli I, Ribeiro S, Wingfield Digby P, Fedorova M et al. 2010. EphB signaling directs peripheral nerve regeneration through Sox2-dependent Schwann cell sorting. Cell 143:145–55
    [Google Scholar]
  118. Pascual G, Dominguez D, Elosua-Bayes M, Beckedorff F, Laudanna Cet al 2021. Dietary palmitic acid promotes a prometastatic memory via Schwann cells. Nature 599:48590
    [Google Scholar]
  119. Pawlowski A, Weddell G. 1967. Induction of tumours in denervated skin. Nature 213:1234–37
    [Google Scholar]
  120. Pellegatta M, De Arcangelis A, D'Urso A, Nodari A, Zambroni D et al. 2013. α6β1 and α7β1 integrins are required in Schwann cells to sort axons. J. Neurosci. 33:17995–8007
    [Google Scholar]
  121. Pellegatta M, Taveggia C. 2019. The complex work of proteases and secretases in Wallerian degeneration: beyond neuregulin-1. Front. . Cell Neurosci 13:93
    [Google Scholar]
  122. Pereira JA, Benninger Y, Baumann R, Goncalves AF, Ozcelik M et al. 2009. Integrin-linked kinase is required for radial sorting of axons and Schwann cell remyelination in the peripheral nervous system. J. Cell Biol. 185:147–61
    [Google Scholar]
  123. Peters A, Muir AR. 1959. The relationship between axons and Schwann cells during development of peripheral nerves in the rat. Q. J. Exp. Physiol. Cogn. Med. Sci. 44:117–30
    [Google Scholar]
  124. Petersen SC, Luo R, Liebscher I, Giera S, Jeong SJ et al. 2015. The adhesion GPCR GPR126 has distinct, domain-dependent functions in Schwann cell development mediated by interaction with laminin-211. Neuron 85:755–69
    [Google Scholar]
  125. Poitelon Y, Lopez-Anido C, Catignas K, Berti C, Palmisano M et al. 2016. YAP and TAZ control peripheral myelination and the expression of laminin receptors in Schwann cells. Nat. Neurosci. 19:879–87
    [Google Scholar]
  126. Progatzky F, Shapiro M, Hui Chng S, Garcia-Cassani B, Classon CH et al. 2021. Regulation of intestinal immunity and tissue repair by enteric glia. Nature 599:125–30
    [Google Scholar]
  127. Radomska KJ, Topilko P. 2017. Boundary cap cells in development and disease. Curr. Opin. Neurobiol. 47:209–15
    [Google Scholar]
  128. Rasband MN, Peles E. 2021. Mechanisms of node of Ranvier assembly. Nat. Rev. Neurosci. 22:7–20
    [Google Scholar]
  129. Reddy LV, Koirala S, Sugiura Y, Herrera AA, Ko CP. 2003. Glial cells maintain synaptic structure and function and promote development of the neuromuscular junction in vivo. Neuron 40:563–80
    [Google Scholar]
  130. Reed CB, Feltri ML, Wilson ER. 2021. Peripheral glia diversity. J. Anat. In press
    [Google Scholar]
  131. Reed CB, Frick LR, Weaver A, Sidoli M, Schlant E et al. 2020. Deletion of calcineurin in Schwann cells does not affect developmental myelination, but reduces autophagy and delays myelin clearance after peripheral nerve injury. J. Neurosci. 40:6165–76
    [Google Scholar]
  132. Reist NE, Smith SJ. 1992. Neurally evoked calcium transients in terminal Schwann cells at the neuromuscular junction. PNAS 89:7625–29
    [Google Scholar]
  133. Renz BW, Tanaka T, Sunagawa M, Takahashi R, Jiang Z et al. 2018. Cholinergic signaling via muscarinic receptors directly and indirectly suppresses pancreatic tumorigenesis and cancer stemness. Cancer Discov 8:1458–73
    [Google Scholar]
  134. Robitaille R. 1995. Purinergic receptors and their activation by endogenous purines at perisynaptic glial cells of the frog neuromuscular junction. J. Neurosci. 15:7121–31
    [Google Scholar]
  135. Rosenbluth J, Nave KA, Mierzwa A, Schiff R. 2006. Subtle myelin defects in PLP-null mice. Glia 54:172–82
    [Google Scholar]
  136. Saab AS, Tzvetavona ID, Trevisiol A, Baltan S, Dibaj P et al. 2016. Oligodendroglial NMDA receptors regulate glucose import and axonal energy metabolism. Neuron 91:119–32
    [Google Scholar]
  137. Saito F, Moore SA, Barresi R, Henry MD, Messing A et al. 2003. Unique role of dystroglycan in peripheral nerve myelination, nodal structure, and sodium channel stabilization. Neuron 38:747–58
    [Google Scholar]
  138. Salzer JL. 2015. Schwann cell myelination. Cold Spring Harb. Perspect. Biol. 7:a020529
    [Google Scholar]
  139. Schnaar RL, Lopez PH. 2009. Myelin-associated glycoprotein and its axonal receptors. J. Neurosci. Res. 87:3267–76
    [Google Scholar]
  140. Schwaller F, Begay V, Garcia-Garcia G, Taberner FJ, Moshourab R et al. 2021. USH2A is a Meissner's corpuscle protein necessary for normal vibration sensing in mice and humans. Nat. Neurosci. 24:74–81
    [Google Scholar]
  141. Seguella L, Gulbransen BD. 2021. Enteric glial biology, intercellular signalling and roles in gastrointestinal disease. Nat. Rev. Gastroenterol. Hepatol. 18:571–87
    [Google Scholar]
  142. Sherman DL, Krols M, Wu LM, Grove M, Nave KA et al. 2012. Arrest of myelination and reduced axon growth when Schwann cells lack mTOR. J. Neurosci. 32:1817–25
    [Google Scholar]
  143. Siqueira Mietto B, Kroner A, Girolami EI, Santos-Nogueira E, Zhang J, David S 2015. Role of IL-10 in resolution of inflammation and functional recovery after peripheral nerve injury. J. Neurosci. 35:16431–42
    [Google Scholar]
  144. Smith CJ, Morris AD, Welsh TG, Kucenas S. 2014. Contact-mediated inhibition between oligodendrocyte progenitor cells and motor exit point glia establishes the spinal cord transition zone. PLOS Biol 12:e1001961
    [Google Scholar]
  145. Snaidero N, Velte C, Myllykoski M, Raasakka A, Ignatev A et al. 2017. Antagonistic functions of MBP and CNP establish cytosolic channels in CNS myelin. Cell Rep 18:314–23
    [Google Scholar]
  146. Spierings E, de Boer T, Wieles B, Adams LB, Marani E, Ottenhoff TH. 2001. Mycobacterium leprae-specific, HLA class II-restricted killing of human Schwann cells by CD4+ Th1 cells: a novel immunopathogenic mechanism of nerve damage in leprosy. J. Immunol. 166:5883–88
    [Google Scholar]
  147. Srinivasan R, Sun G, Keles S, Jones EA, Jang SW et al. 2012. Genome-wide analysis of EGR2/SOX10 binding in myelinating peripheral nerve. Nucleic Acids Res 40:6449–60
    [Google Scholar]
  148. Stassart RM, Fledrich R, Velanac V, Brinkmann BG, Schwab MH et al. 2013. A role for Schwann cell-derived neuregulin-1 in remyelination. Nat. Neurosci. 16:48–54
    [Google Scholar]
  149. Stierli S, Imperatore V, Lloyd AC. 2019. Schwann cell plasticity-roles in tissue homeostasis, regeneration, and disease. Glia 67:2203–15
    [Google Scholar]
  150. Suadicani SO, Cherkas PS, Zuckerman J, Smith DN, Spray DC, Hanani M. 2010. Bidirectional calcium signaling between satellite glial cells and neurons in cultured mouse trigeminal ganglia. Neuron Glia Biol 6:43–51
    [Google Scholar]
  151. Tait S, Gunn-Moore F, Collinson JM, Huang J, Lubetzki C et al. 2000. An oligodendrocyte cell adhesion molecule at the site of assembly of the paranodal axo-glial junction. J. Cell Biol. 150:657–66
    [Google Scholar]
  152. Tasdemir-Yilmaz OE, Druckenbrod NR, Olukoya OO, Dong W, Yung AR et al. 2021. Diversity of developing peripheral glia revealed by single-cell RNA sequencing. Dev. Cell 56:2516–35.e8
    [Google Scholar]
  153. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J et al. 2005. Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47:681–94
    [Google Scholar]
  154. Todd KJ, Darabid H, Robitaille R. 2010. Perisynaptic glia discriminate patterns of motor nerve activity and influence plasticity at the neuromuscular junction. J. Neurosci. 30:11870–82
    [Google Scholar]
  155. Topilko P, Schneider-Maunoury S, Levi G, Baron-Van Evercooren A, Chennoufi AB et al. 1994. Krox-20 controls myelination in the peripheral nervous system. Nature 371:796–99
    [Google Scholar]
  156. Traka M, Goutebroze L, Denisenko N, Bessa M, Nifli A et al. 2003. Association of TAG-1 with Caspr2 is essential for the molecular organization of juxtaparanodal regions of myelinated fibers. J. Cell Biol. 162:1161–72
    [Google Scholar]
  157. Trimarco A, Forese MG, Alfieri V, Lucente A, Brambilla P et al. 2014. Prostaglandin D2 synthase/GPR44: a signaling axis in PNS myelination. Nat. Neurosci. 17:1682–92
    [Google Scholar]
  158. Tzekova N, Heinen A, Kury P. 2014. Molecules involved in the crosstalk between immune- and peripheral nerve Schwann cells. J. Clin. Immunol. 34:Suppl. 1S86–104
    [Google Scholar]
  159. Vabnick I, Novakovic SD, Levinson SR, Schachner M, Shrager P. 1996. The clustering of axonal sodium channels during development of the peripheral nervous system. J. Neurosci. 16:4914–22
    [Google Scholar]
  160. Van Raamsdonk CD, Deo M. 2013. Links between Schwann cells and melanocytes in development and disease. Pigment Cell Melanoma Res 26:634–45
    [Google Scholar]
  161. Van Rhijn I, Van den Berg LH, Bosboom WM, Otten HG, Logtenberg T. 2000. Expression of accessory molecules for T-cell activation in peripheral nerve of patients with CIDP and vasculitic neuropathy. Brain 123:Pt. 102020–29
    [Google Scholar]
  162. Veiga-Fernandes H, Pachnis V. 2017. Neuroimmune regulation during intestinal development and homeostasis. Nat. Immunol. 18:116–22
    [Google Scholar]
  163. Verheijen MH, Camargo N, Verdier V, Nadra K, de Preux Charles AS et al. 2009. SCAP is required for timely and proper myelin membrane synthesis. PNAS 106:21383–88
    [Google Scholar]
  164. Wagner R, Myers RR. 1996. Endoneurial injection of TNF-α produces neuropathic pain behaviors. Neuroreport 7:2897–901
    [Google Scholar]
  165. Wanner IB, Mahoney J, Jessen KR, Wood PM, Bates M, Bunge MB. 2006. Invariant mantling of growth cones by Schwann cell precursors characterize growing peripheral nerve fronts. Glia 54:424–38
    [Google Scholar]
  166. Wegner M. 2000. Transcriptional control in myelinating glia: the basic recipe. Glia 29:118–23
    [Google Scholar]
  167. Weinberg HJ, Spencer PS. 1978. The fate of Schwann cells isolated from axonal contact. J. Neurocytol. 7:555–69
    [Google Scholar]
  168. Willem M, Garratt AN, Novak B, Citron M, Kaufmann S et al. 2006. Control of peripheral nerve myelination by the β-secretase BACE1. Science 314:664–66
    [Google Scholar]
  169. Woodhoo A, Alonso MB, Droggiti A, Turmaine M, D'Antonio M et al. 2009. Notch controls embryonic Schwann cell differentiation, postnatal myelination and adult plasticity. Nat. Neurosci. 12:839–47
    [Google Scholar]
  170. Woodhoo ASL. 2018. Development of the Schwann cell lineage: from the neural crest to the myelinated nerve. Glia 56:1481–90
    [Google Scholar]
  171. Wu G, Ringkamp M, Murinson BB, Pogatzki EM, Hartke TV et al. 2002. Degeneration of myelinated efferent fibers induces spontaneous activity in uninjured C-fiber afferents. J. Neurosci. 22:7746–53
    [Google Scholar]
  172. Wu LM, Wang J, Conidi A, Zhao C, Wang H et al. 2016. Zeb2 recruits HDAC-NuRD to inhibit Notch and controls Schwann cell differentiation and remyelination. Nat. Neurosci. 19:1060–72
    [Google Scholar]
  173. Ydens E, Lornet G, Smits V, Goethals S, Timmerman V, Janssens S. 2013. The neuroinflammatory role of Schwann cells in disease. Neurobiol. Dis. 55:95–103
    [Google Scholar]
  174. Yim AKY, Wang PL, Bermingham JR Jr., Hackett A, Strickland Aet al 2022. Disentangling glial diversity in peripheral nerves at single-nuclei resolution. Nat. Neurosci 25:23851
    [Google Scholar]
  175. Yin X, Crawford TO, Griffin JW, Tu P, Lee VM et al. 1998. Myelin-associated glycoprotein is a myelin signal that modulates the caliber of myelinated axons. J. Neurosci. 18:1953–62
    [Google Scholar]
  176. Zahalka AH, Arnal-Estape A, Maryanovich M, Nakahara F, Cruz CD et al. 2017. Adrenergic nerves activate an angio-metabolic switch in prostate cancer. Science 358:321–26
    [Google Scholar]
  177. Zalc B, Colman DR. 2000. Origins of vertebrate success. Science 288:271–72
    [Google Scholar]
  178. Zhang X, Chen Y, Wang C, Huang LY. 2007. Neuronal somatic ATP release triggers neuron-satellite glial cell communication in dorsal root ganglia. PNAS 104:9864–69
    [Google Scholar]
  179. Zhao CM, Hayakawa Y, Kodama Y, Muthupalani S, Westphalen CB et al. 2014. Denervation suppresses gastric tumorigenesis. Sci. Transl. Med. 6:250ra115
    [Google Scholar]
  180. Zotter B, Dagan O, Brady J, Baloui H, Samanta J, Salzer JL. 2022. Gli1 regulates the postnatal acquisition of peripheral nerve architecture. J. Neurosci. 42:183–201
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-110920-030610
Loading
/content/journals/10.1146/annurev-neuro-110920-030610
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error