Skip to main content
SpringerLink
Log in

Current Views on Perineurial Cells: Unique Origin, Structure, Functions

  • Reviews
  • Published:
Journal of Evolutionary Biochemistry and Physiology Aims and scope Submit manuscript

Abstract

This review aims to consolidate current views on the cells of one of the peripheral nerve sheath layers, perineurium. The relevance of the subject matter owes the lack of basic knowledge about the involvement of these cells in the restoration of damaged nerve conductors, as well as the need to unravel the molecular mechanisms that stimulate the regeneration of damaged nerves. The review summarizes recent data on the morphofunctional features of the perineurium, phylogenetic and ontogenetic origins of perineurial cells, and molecular features of the regulation of the blood–nerve barrier. It accentuates the uniqueness of the ontogenetic origin of the perineurium, characterizes immunohistochemical markers of perineurial cells, describes the features of the perineurium in the dorsal root ganglia and spinal nerve roots.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.

Similar content being viewed by others

REFERENCES

  1. Bersnev VP, Hamzaev RI, Boroda JuI (2009) Results of using an epineural suture of the sciatic nerve. Vestnik hirurgii im. I.I. Grekova 168 (1): 61–63 (In Russ).

    CAS  Google Scholar 

  2. Shchanitsyn IN, Ivanov AN, Bazhanov SP, Ninel VG, Puchin’jan DM, Norkin IA (2017) Stimulation of peripheral nerve regeneration: current status, problems and perspectives. Uspekhi fiziologicheskih nauk 48(3): 92–112 (In Russ).

    Google Scholar 

  3. Shchudlo NA, Borisova IV, Shchudlo MM (2013) Morphometric assessment of the effectiveness of post–traumatic regeneration of peripheral nerves using single and repeated courses of electrostimulation. Neuroscience and Behavioral Physiology 43(9): 1097–1101. https://doi.org/10.1007/s11055-013-9855-4

    Article  CAS  Google Scholar 

  4. Litvinenko IV, Odinak MM, Zhivolupov SA, Bulatov AR, Rashidov NA, Bardakov SN (2018) Clinical and instrumental characteristics of traumatic lesions of peripheral nerves of limbs. Vestnik Rossiyskoi Voyenno-meditsinskoi akademii 3 (63): 50–56 (In Russ).

    Google Scholar 

  5. Nisht AYu, Chirskii VS, Fomin NF (2019) Morphological foundations of restoration of motor innervation in injuries of peripheral nerves. Journal of Anatomy and Histopathology 8 (4): 66–73 https://doi.org/10.18499/2225-7357-2019-8-4-66-73

    Article  Google Scholar 

  6. Pannese E (1981) The satellite cells of the sensory ganglia. Adv Anat Embryol Cell Biol 65: 1–111. https://doi.org/10.1007/978-3-642-67750-2

    Article  CAS  PubMed  Google Scholar 

  7. Nozdrachev AD, Chumasov EI (1999) Peripheral Nervous System. Nauka, SPb (In Russ).

    Google Scholar 

  8. Chelyshev YuA, Saitkulov KI (2000 Development, phenotypic characteristics and communication of Schwann cells). Uspekhi fiziologicheskih nauk 31 (3): 54–69 (In Russ).

  9. Zochodne DW (2008) Neurobiology of peripheral nerve regeneration. Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, Sao Paulo: Cambridge University Press.

    Book  Google Scholar 

  10. Reina MA, Arriazu R, Collier CB, Sala-Blanch X, Izquierdo L, de Andrés J (2013) Electron microscopy of human peripheral nerves of clinical relevance to the practice of nerve blocks. A structural and ultrastructural review based on original experimental and laboratory data. Rev Esp Anestesiol Reanim 60(10): 552–562. https://doi.org/10.1016/j.redar.2013.06.006

    Article  CAS  PubMed  Google Scholar 

  11. Petrova ES (2019) Current views on Schwann cells: development, plasticity, functions. J Evol Biochem Phys 55: 433–447. https://doi.org/10.1134/S0022093019060012

    Article  Google Scholar 

  12. Chumasov EI, Kolos EA, Petrova ES, Korzhevskii DE (2020) Immunohistochemistry of the Peripheral Nervous System. SpecLit, SPb.

    Google Scholar 

  13. Bhatheja K, Field J (2006) Schwann cells: origins and role in axonal maintenance and regeneration. Int J Biochem Cell Biol 38: 1995–1999. https://doi.org/10.1016/j.biocel.2006.05.007

    Article  CAS  PubMed  Google Scholar 

  14. Salzer JL (2015) Schwann cell myelination. Cold Spring Harb. Perspect Biol 7 (8): a020529. https://doi.org/10.1101/cshperspect.a020529

    Article  Google Scholar 

  15. Shanthaveerappa TR, Bourne GH (1966) Perineural epithelium: a new concept of its role in the integrity of the peripheral nervous system. Science 154(3755): 1464–1467.

    Article  CAS  Google Scholar 

  16. Kundalić B, Ugrenović S, Jovanović I, Stefanović N, Petrović V, Kundalić J, Stojanović V, Živković V, Antić V (2014) Morphometric analysis of connective tissue sheaths of sural nerve in diabetic and nondiabetic patients. Biomed Res Int 2014: 870930. https://doi.org/10.1155/2014/870930

    Article  PubMed  PubMed Central  Google Scholar 

  17. Pinã-Oviedo S, Ortiz-Hidalgo C (2008) The normal and neoplastic perineurium. A review. Adv Anat Pathol 15:147–164. https://doi.org/10.1097/PAP.0b013e31816f8519

    Article  PubMed  Google Scholar 

  18. Berthold C-H, Fraher JP, King RHM, Rydmark M (2005) Microscopic anatomy of the peripheral nervous system. In: Dyck PJ, Thomas PK (Eds) Peripheral Neuropathy. Elsevier Health Sciences. pp 35–91.

    Chapter  Google Scholar 

  19. Ubogu EE (2020) Biology of the human blood-nerve barrier in health and disease. Exp Neurol 328: 113272. https://doi.org/10.1016/j.expneurol.2020.113272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Barros CS, Franco SJ, Müller U (2011) Extracellular matrix: functions in the nervous system. Cold Spring Harb Perspect Biol 3(1):a005108. https://doi.org/10.1101/cshperspect.a005108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Bove GM, Light AR (1995) Calcitonin Gene-Related peptide and peripherin immunoreactivity in nerve sheaths. Somatosensory and Motor Research 12 (1): 49–57. https://doi.org/10.3109/08990229509063141

    Article  CAS  PubMed  Google Scholar 

  22. Reina MA, Boezaart AP, Tubbs RS, Zasimovich Y, Fernández-Domínguez M, Fernández P, Sala-Blanch X (2019) Another (internal) epineurium: beyond the anatomical barriers of nerves. Clin Anat 33(2):199–206. https://doi.org/10.1002/ca.23442

    Article  PubMed  Google Scholar 

  23. Sala-Blanch X, Reina MA, Ribalta T, Prats-Galino A (2013) Sciatic nerve structure and nomenclature: epineurium to paraneurium: is this a new paradigm? Reg Anesth Pain Med 38 (5):463–465. https://doi.org/10.1097/AAP.0b013e3182a1b6c5

    Article  PubMed  Google Scholar 

  24. Zatolokina MA (2016) Morphogenesis of Changes in the Paraneural Connective Tissue Structures of Peripheral Nerves in an Evolutionary Aspect. KGMU, Kursk (In Russ).

    Google Scholar 

  25. Murthy NK, Spinner RJ (2020) Letter to the editor: the paraneurium (circumneurium) and its clinical implications with benign and malignant nerve lesions. Clin Anat 34(8):1133-1134. https://doi.org/10.1002/ca.23639

    Article  PubMed  Google Scholar 

  26. Reina MA, Boezaart A, Nin OC, Zasimovich Y, Sala-Blanch X (2020) Yet another perineural layer: so what? Reg Anesth Pain Med 45(6):483–484. https://doi.org/10.1136/rapm-2019-100765

    Article  PubMed  Google Scholar 

  27. Krnjevic K (1954) The connective tissue of the frog sciatic nerve. Q J Exp Physiol Cogn Med Sci 39(1): 55–72. https://doi.org/10.1113/expphysiol.1954.sp001048

    Article  CAS  PubMed  Google Scholar 

  28. Marani E, Lakke EAJF (2012) Peripheral Nervous System. In: Mai JK, Paxinos G (eds) The human nervous system. Elsevier, Amsterdam, pp 82–140.

    Chapter  Google Scholar 

  29. Kucenas S (2015) Perineurial glia. Cold Spring Harb Perspect Biol 7(6): a020511. https://doi.org/10.1101/cshperspect.a020511

    Article  PubMed  PubMed Central  Google Scholar 

  30. Shanthaveerappa TR, Bourne GH (1963) Demonstration of perineural epithelium in whale and shark peripheral nerves. Nature197: 702–703. https://doi.org/10.1038/197702a0

    Article  CAS  PubMed  Google Scholar 

  31. Kucenas S, Takada N, Park HC, Woodruff E, Broadie K, Appel B (2008) CNS-derived glia ensheath peripheral nerves and mediate motor root development. Nat Neurosci 11:143–151. https://doi.org/10.1038/nn2025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Binari LA, Lewis GM, Kucenas S (2013) Perineurial glia require Notch signaling during motor nerve development but not regeneration. J Neurosci 33(10):4241–4252. https://doi.org/10.1523/JNEUROSCI.4893-12.2013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Du Plessis DG, Mouton YM, Muller CJ, Geiger DHJ (1996) An ultrastructural study of the development of the chicken perineurial sheath. Anat 189 (Pt 3): 631–641.

    Google Scholar 

  34. Server A, Reina MA, Boezaart AP, Prats-Galino A, Esteves Coelho M, Sala-Blanch X (2018) Microanatomical nerve architecture of 6 mammalian species: Is trans-species translational anatomic extrapolation valid? Reg Anesth Pain Med 43(5):496–501. https://doi.org/10.1097/AAP.0000000000000772

    Article  PubMed  Google Scholar 

  35. Chumasov EI (1975) On the structure of the perineurium of the peripheral nervous system. Arch of Anatomy, Histology and Embryology 68 (4): 29–34 (In Russ).

    CAS  Google Scholar 

  36. Takebe K, Nio-Kobayashi Y, Takanashi-Iwanaga H, Iwanaga T (2006) Histochemical demonstration of a monocarboxylate transporter in the mouse perineurium with special reference to GLUT1. Biomedical Res 29 (6): 297–306. https://doi.org/10.2220/biomedres.29.297

    Article  Google Scholar 

  37. Topp KS, Boyd BS (2012) Peripheral nerve: from the microscopic functional unit of the axon to thebiomechanically loaded macroscopic structure. J Hand Ther 25(2):142–151; quiz 152. https://doi.org/10.1016/j.jht.2011.09.002

    Article  PubMed  Google Scholar 

  38. Dolzhikov AA, Dolzhikova IN (2018) Perineurium of peripheral nerves: fundamental and applied issues of its morphology and functions. Aktual’nye problemy gumanitarnykh i estestvennykh nauk 9: 54–62 (In Russ).

    Google Scholar 

  39. Dixon JS, Jen PY, Gosling JA (1998) Immunohistochemical characteristics of human paraganglion cells and sensory corpuscles associated with the urinary bladder. A developmental study in the male fetus, neonate and infant. J Anat 192 (3): 407–415. https://doi.org/10.1046/j.1469-7580.1998.19230407.x

    Article  PubMed  PubMed Central  Google Scholar 

  40. Vega JA, Del Valle ME, Haro JJ, Naves FJ, Calzada B, Uribelarrea R (1994) The inner-core, outer-core and capsule cells of the human Pacinian corpuscles: an immunohistochemical study. Eur J Morphol 32(1):11–18.

    CAS  PubMed  Google Scholar 

  41. Banin VV, Bykov VL (ed) (2009) Terminologia histological. International Terms in Human Cytology and Histology with an Official List of Russian Equivalents. GEOTAR-Media, M. (In Russ).

    Google Scholar 

  42. Matejčík V, Haviarová Z, Kuruc R, Šteňo A, Šteňo J (2019) The composition and structure of peripheral nerves. In: Intraspinal Variations of Nerve Roots. Springer, Cham, pp 3–13.

    Chapter  Google Scholar 

  43. Suter TACS, Jaworski A (2019) Cell migration and axon guidance at the border between central and peripheral nervous system. Science 365(6456):eaaw8231. https://doi.org/10.1126/science.aaw8231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Andres KH (1967) On the fine structure of the arachnoidea and dura mater of mammals. Z Zellforsch Mikrosk Anat 79(2): 272–295.

    Article  CAS  Google Scholar 

  45. McCabe JS, Low FN (1969) The subarachnoid angle: an area of transition in peripheral nerve. Anat Rec 164 (1):15–33. https://doi.org/10.1002/ar.1091640102

    Article  CAS  PubMed  Google Scholar 

  46. Haller FR, Low FN (1971) The fine structure of the peripheral nerve root sheath in the subarachnoid space in the rat and other laboratory animals. Am J Anat 131(1):1–19. https://doi.org/10.1002/aja.1001310102

    Article  CAS  PubMed  Google Scholar 

  47. Umovist MN, Tchaikovsky YB (1987) Modern concepts of the structure and function of the nerve sheaths. Archive of anatomy, histology and embryology 1: 98–96 (In Russ).

    Google Scholar 

  48. Bechter K, Schmitz B (2014) Cerebrospinal fluid outflow along lumbar nerves and possible relevance for pain research: case report and review. Croat Med J 55(4): 399–404. https://doi.org/10.3325/cmj.2014.55.399

    Article  PubMed  PubMed Central  Google Scholar 

  49. Mizisin AP, Weerasuriya A (2011) Homeostatic regulation of the endoneurial microenvironment during development, aging and in response to trauma, disease and toxic insult. Acta Neuropathol 121 (3): 291–312. https://doi.org/10.1007/s00401-010-0783-x

    Article  CAS  PubMed  Google Scholar 

  50. Pettersson CA (1993) Sheaths of the spinal nerve roots. Permeability and structural characteristics of dorsal and ventral spinal nerve roots of the rat. Acta Neuropathol 85(2): 129–137. https://doi.org/10.1007/BF00227759

    Article  CAS  PubMed  Google Scholar 

  51. Zakharov A, Papaiconomou C, Djenic J, Midha R, Johnston M (2003) Lymphatic cerebrospinal fluid absorption pathways in neonatal sheep revealed by subarachnoid injection of Microfil. Neuropathol Appl Neurobiol 29(6):563–573. https://doi.org/10.1046/j.0305-1846.2003.00508.x

    Article  CAS  PubMed  Google Scholar 

  52. Frater JL, Hall GS, Procop GW (2001) Histologic features of zygomycosis: emphasis on perineural invasion and fungal morphology. Arch Pathol Lab Med 125 (3): 375–378. https://doi.org/10.1043/0003-9985(2001)125<0375:HFOZ>2.0.CO;2

    Article  CAS  PubMed  Google Scholar 

  53. Dando SJ, Mackay-Sim A, Norton R, Currie BJ, St John JA, Ekberg JA, Batzloff M, Ulett GC, Beacham IR (2014) Pathogens penetrating the central nervous system: infection pathways and the cellular and molecular mechanisms of invasion. Clin Microbiol Rev 27(4): 691–726. https://doi.org/10.1128/CMR.00118-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Schmitt M, Neubauer A, Greiner J, Xu X, Barth TF, Bechter K (2011) Spreading of acute myeloid leukemia cells by trafficking along the peripheral outflow pathway of cerebrospinal fluid. Anticancer Res 31(6):2343–2345.

    PubMed  Google Scholar 

  55. Brown IS (2016) Pathology of perineural spread. J Neurol Surg B Skull Base 77(2): 124–130. https://doi.org/10.1055/s-0036-1571837

    Article  PubMed  PubMed Central  Google Scholar 

  56. Reale E, Luciano L, Spitznas M (1976) Freeze-fracture aspects of the perineurium of spinal ganglia. J Neurocytol 5: 385–394. https://doi.org/10.1007/BF01181646

    Article  CAS  PubMed  Google Scholar 

  57. Arvidson B (1979) A study of the perineurial diffusion barrier of a peripheral ganglion. Acta Neuropathol 46(1–2):139–144. https://doi.org/10.1007/BF00684815

    Article  CAS  PubMed  Google Scholar 

  58. Weerasuriya A, Mizisin AP (2011) The blood-nerve barrier: structure and functional significance. Methods Mol Biol 686: 149–173. https://doi.org/10.1007/978-1-60761-938-3_6

    Article  CAS  PubMed  Google Scholar 

  59. Masliukov PM, Emanuilov AI, Madalieva LV, Moiseev KY, Bulibin AV, Korzina MB, Porseva VV, Korobkin AA, Smirnova VP (2014) Development of nNOS-positive neurons in the rat sensory and sympathetic ganglia. Neuroscience 256: 271–281. https://doi.org/10.1016/j.neuroscience.2013.10.013

    Article  CAS  PubMed  Google Scholar 

  60. Nikolaev SI, Gallyamov AR, Mamin GV, Chelyshev YuA (2014) Poly(ε-caprolactone) nerve conduit and local delivery of VEGF and FGF2 genes stimulate neuroregeneration. Bulletin of Experimental Biology and Medicine 157 (1): 155–158. https://doi.org/10.1007/s10517-014-2513-1

    Article  CAS  PubMed  Google Scholar 

  61. Emanuylov AI, Maslyukov PM, Nozdrachev AD (2019) Sympathetic innervation of the heart in early postnatal ontogenesis. Russian Journal of Physiology 105 (9): 1133–1141(In Russ). https://doi.org/10.1134/S086981391909005X

    Article  Google Scholar 

  62. Pummi KP, Heape AM, Grenman RA, Peltonen JT, Peltonen SA (2004) Tight junction proteins ZO-1, occludin, and claudins in developing and adult human perineurium. J Histochem Cytochem 52 (8): 1037–1046. https://doi.org/10.1369/jhc.3A6217.2004

    Article  CAS  PubMed  Google Scholar 

  63. Tsukita S, Tanaka H, Tamura A (2019) The claudins: from tight junctions to biological systems.Trends Biochem Sci 44(2):141–152. https://doi.org/10.1016/j.tibs.2018.09.008

    Article  CAS  PubMed  Google Scholar 

  64. Alanne MH, Pummi K, Heape AM, Grenman R, Peltonen J, Peltonen S (2009) Tight junction proteins in human Schwann cell autotypic junctions. J Histochem Cytochem 57 (6): 523–529. https://doi.org/10.1369/jhc.2009.951681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Hirakawa H, Okajima S, Nagaoka T, Takamatsu T, Oyamada M (2003) Loss and recovery of the blood-nerve barrier in the rat sciatic nerve after crush injury are associated with expression of intercellular junctional proteins. Exp Cell Res 284 (2): 196–210. https://doi.org/10.1016/s0014-4827(02)00035-6

    Article  CAS  PubMed  Google Scholar 

  66. Lux TJ, Hu X, Ben-Kraiem A, Blum R, Chen JT, Rittner HL (2020) Regional differences in tight junction protein expression in the blood-DRG barrier and their alterations after nerve traumatic injury in rats. Int J Mol Sci: 21(1): E270. https://doi.org/10.3390/ijms21010270

    Article  CAS  Google Scholar 

  67. Sauer RS, Krug SM, Hackel D, Staat C, Konasin N, Yang S, Niedermirtl B, Bosten J, Günther R, Dabrowski S, Doppler K, Sommer C, Blasig IE, Brack A, Rittner HL (2014) Safety, efficacy, and molecular mechanism of claudin-1-specific peptides to enhance blood-nerve-barrier permeability. J Control Release 185: 88–98. https://doi.org/10.1016/j.jconrel.2014.04.029

    Article  CAS  PubMed  Google Scholar 

  68. Miyamoto T, Morita K, Takemoto D, Takeuchi K, Kitano Y, Miyakawa T, Nakayama K, Okamura Y, Sasaki H, Miyachi Y, Furuse M, Tsukita S (2005) Tight junctions in Schwann cells of peripheral myelinated axons: a lesson from claudin-19-deficient mice. J Cell Biol 169(3): 527–538. https://doi.org/10.1083/jcb.200501154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Reinhold AK, Schwabe J, Lux TJ, Salvador E, Rittner HL (2018) Quantitative and microstructural changes of the blood-nerve barrier in peripheral neuropathy. Front Neurosci 12: 936. https://doi.org/10.3389/fnins.2018.00936. eCollection 2018

    Article  PubMed  PubMed Central  Google Scholar 

  70. Ando-Akatsuka Y, Saitou M, Hirase T, Kishi M, Sakakibara A, Itoh M, Yonemura S, Furuse M, Tsukita S (1996) Interspecies diversity of the occludin sequence: cDNA cloning of human, mouse, dog, and rat-kangaroo homologues. Journal of Cell Biology 133 (1): 43–47. https://doi.org/10.1083/jcb.133.1.43

    Article  CAS  PubMed  Google Scholar 

  71. Mazzeo A, Rodolico C, Monici MC, Migliorato A, Aguennouz M, Vita G (1997) Perineurium talin immunoreactivity decreases in diabetic neuropathy. J Neurol Sci 146 (1): 7–11. https://doi.org/10.1016/s0022-510x(96)00285-7

    Article  CAS  PubMed  Google Scholar 

  72. Jaakkola S, Savunen O, Halme T, Uitto J, Peltonen J (1993) Basement membranes during development of human nerve: Schwann cells and perineurial cells display marked changes in their expression profiles for laminin subunits and beta 1 and beta 4 integrins. J Neurocytol 22(3): 215–230. https://doi.org/10.1007/BF01246360

    Article  CAS  PubMed  Google Scholar 

  73. Nagaoka T, Oyamada M, Okajima S, Takamatsu T (1999) Differential expression of gap junction proteins connexin 26, 32, and 43 in normal and crush-injured rat sciatic nerves. Close relationship between connexin43 and occludin in the perineurium. J Histochem Cytochem 47(7): 937–948. https://doi.org/10.1177/002215549904700711

    Article  CAS  PubMed  Google Scholar 

  74. Stark B, Carlstedt T, Cullheim S, Risling M (2000) Developmental and lesion-induced changes in the distribution of the glucose transporter Glut-1 in the central and peripheral nervous system. Exp Brain Res 131(1):74–84. https://doi.org/10.1007/s002219900300

    Article  CAS  PubMed  Google Scholar 

  75. Muona P, Sollberg S, Peltonen J, Uitto J (1992) Glucose transporters of rat peripheral nerve. Differential expression of GLUT1 gene by Schwann cells and perineural cells in vivo and in vitro. Diabetes 41: 1587–1596. https://doi.org/10.2337/diab.41.12.1587

    Article  CAS  PubMed  Google Scholar 

  76. Muona P, Jaakkola S, Salonen V, Peltonen J (1993) Expression of glucose transporter 1 in adult and developing human peripheral nerve. Diabetologia 36: 133–140. https://doi.org/10.1007/BF00400694

    Article  CAS  PubMed  Google Scholar 

  77. Tserentsoodol N, Shin BC, Koyama H, Suzuki T, Takata K (1999) Immunolocalization of tight junction proteins, occludin and ZO-1, and glucose transporter GLUT1 in the cells of the blood-nerve barrier. Arch Histol Cytol 62(5):459–469. https://doi.org/10.1679/aohc.62.459.

    Article  CAS  PubMed  Google Scholar 

  78. Takebe K, Nio-Kobayashi J, Takahashi-Iwanaga H, Iwanaga T (2008) Histochemical demonstration of a monocarboxylate transporter in the mouse perineurium with special reference to GLUT1. Biomed Res 29(6): 297–306. https://doi.org/10.2220/biomedres.29.297

    Article  CAS  PubMed  Google Scholar 

  79. Achtstätter T, Fouquet B, Rungger-Brändle E, Franke WW (1989) Cytokeratin filaments and desmosomes in the epithelioid cells of the perineurialand arachnoidal sheaths of some vertebrate species. Differentiation. 40(2):129–149. https://doi.org/10.1111/j.1432-0436.1989.tb00822.x

    Article  PubMed  Google Scholar 

  80. Kovalenko VL, Shevtsov VI, Shchudlo MM, Shchudlo NA (2000) Reactive properties of epi- and perineurium: experimental and morphological basis for nerve suture technique. Bulletin of Experimental Biology and Medicine 130(2): 793–797. https://doi.org/10.1007/BF02766098

    Article  CAS  PubMed  Google Scholar 

  81. Thomas PK, Bhagat S (1978) The effect of extraction of the intrafascicular contents of peripheral nerve trunks on perineurial structure. Acta Neuropathol (Berl) 43: 135–141. https://doi.org/10.1007/BF00685008

  82. 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(9): 1116–1129. https://doi.org/10.1002/dvdy.24158

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Anderson WA, Willenberg AR, Bosak AJ, Willenberg BJ, Lambert S (2018) Use of a capillary alginate gel (CapgelTM) to study the three-dimensional development of sensory nerves reveals the formation of a rudimentary perineurium. J Neurosci Methods 305: 46–53. https://doi.org/10.1016/j.jneumeth.2018.05.003

    Article  CAS  PubMed  Google Scholar 

  84. Fontenas L, Kucenas S (2021) Spinal cord precursors utilize neural crest cell mechanisms to generate hybrid peripheral myelinating glia. Elife 10: e64267. https://doi.org/10.7554/eLife.64267.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Peltonen S, Alanne M, Peltonen J (2013) Barriers of the peripheral nerve. Tissue Barriers 1:e24956. https://doi.org/10.4161/tisb.24956

    Article  PubMed  PubMed Central  Google Scholar 

  86. Sima A, Sourander P (1973) The effect of perinatal undernutrition on perineurial diffusion barrier to exogenous protein. An experimental study on rat sciatic nerve. Acta Neuropathol 24 (3): 263–272. https://doi.org/10.1007/BF00687596

    Article  CAS  PubMed  Google Scholar 

  87. Sima A, Sourander P (1974) The permeability of perineurium to peroxidase after early undernutrition. An ultrastructural study on rat sciatic nerve. Acta Neuropathol 28(1):15–23. https://doi.org/10.1007/BF00687514

    Article  CAS  PubMed  Google Scholar 

  88. Le Douarin NM (1986) Cell line segregation during peripheral nervous system ontogeny. Science 231: 1515–1522

    Article  CAS  Google Scholar 

  89. Le Douarin NM, Dupin E (2012) The neural crest in vertebrate evolution. Curr Opin Genet Dev 22(4): 381–389. https://doi.org/10.1016/j.gde.2012.06.001

    Article  CAS  PubMed  Google Scholar 

  90. Etchevers HC, Dupin E, Le Douarin NM (2019) The diverse neural crest: from embryology to human pathology. Development 146(5): dev169821. https://doi.org/10.1242/dev.169821

    Article  CAS  PubMed  Google Scholar 

  91. Petersen J, Adameyko I (2017) Nerve-associated neural crest: peripheral glial cells generate multiple fates in the body. Curr Opin Genet Dev 45: 10–14. https://doi.org/10.1016/j.gde.2017.02.006

    Article  CAS  PubMed  Google Scholar 

  92. Joseph NM, Mukouyama YS, Mosher JT, Jaegle M, Crone SA, Dormand E-L, Lee K-F, Meijer D, Anderson DJ, Morrison SJ (2004) Neural crest stem cells undergo multilineage differentiation in developing peripheral nerves to generate endoneurial fibroblasts in addition to Schwann cells. Development 131(22): 5599–5612. https://doi.org/10.1242/dev.01429

    Article  CAS  PubMed  Google Scholar 

  93. Dupin E, Sommer L (2012) Neural crest progenitors and stem cells: from early development to adulthood. Developmental Biology 366: 83–95. https://doi.org/10.1016/j.ydbio.2012.02.035

    Article  CAS  PubMed  Google Scholar 

  94. Le Douarin NM, Dupin E (2018) The “beginnings” of the neural crest. Dev Biol 444 (1): S3–S13. https://doi.org/10.1016/j.ydbio.2018.07.019

    Article  CAS  PubMed  Google Scholar 

  95. Graham A (2003) The neural crest. Curr Biol 13(10): R381–384. https://doi.org/10.1016/s0960-9822(03)00315-4

    Article  CAS  PubMed  Google Scholar 

  96. Graham A, Begbie J, McGonnell I (2004) Significance of the cranial neural crest. Dev Dyn 229(1): 5–13. https://doi.org/10.1002/dvdy.10442

    Article  PubMed  Google Scholar 

  97. Chumasov EI (1976) Morphology of perineurium in organotypic culture of sensitive ganglia. In: Tissue Biology. Tartu. 79–82.

    Google Scholar 

  98. Chumasov EI, Konovalov GV (1977) The Morphology of the Nervous Tissue in Culture. Nervous Tissue Culture. Medicina, M, 63–127 (In Russ).

    Google Scholar 

  99. Bunge MB,Wood PM, Tynan LB, Bates ML, Sanes JR (1989) Perineurium originates from fibroblasts: Demonstration in vitro with a retroviral marker. Science 243: 229–231. https://doi.org/10.1126/science.2492115

    Article  PubMed  Google Scholar 

  100. Kazamel M, Boes CJ (2017) Renaut Corpuscles or Peripheral Nerve Infarcts? A Historical Overview. Can J Neurol Sci 44(2): 184–189. https://doi.org/10.1017/cjn.2016.406.

    Article  PubMed  Google Scholar 

  101. Petrova ES (2012) The use of stem cells to stimulate the regeneration of the damaged nerve. Tsitologiya 54 (7): 525–540.

    CAS  Google Scholar 

  102. Petrova ES (2015) Injured nerve regeneration using cell-based therapies: current challenges. Acta Naturae 7(3): 38–47. https://doi.org/10.32607/20758251-2015-7-3-38-47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Petrova ES (2018) Differentiation potential of mesenchymal stem cells and stimulation of nerve regeneration. Russian Journal of Developmental Biology 49 (4): 193–205. https://doi.org/10.1134/S1062360418040033

    Article  Google Scholar 

  104. Huang CW, Huang WC, Qiu X, Fernandes Ferreira da Silva F, Wang A, Patel S, Nesti LJ, Poo MM, Li S (2017) The differentiation stage of transplanted stem cells modulates nerve regeneration. Sci Rep 7(1):17401. https://doi.org/10.1038/s41598-017-17043-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Du J, Zhen G, Chen H, Zhang S, Qing L, Yang X, Lee G, Mao HQ, Jia X (2018) Optimal electrical stimulation boosts stem cell therapy in nerve regeneration. Biomaterials 181: 347–359. https://doi.org/10.1016/j.biomaterials.2018.07.015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Xia B, Chen G, Zou Y, Yang L, Pan J, Lv Y (2019) Low-intensity pulsed ultrasound combination with induced pluripotent stem cells-derived neural crest stem cells and growth differentiation factor 5 promotes sciatic nerve regeneration and functional recovery. J Tissue Eng Regen Med 13(4): 625–636. https://doi.org/10.1002/term.2823

    Article  CAS  PubMed  Google Scholar 

  107. Petrova E, Isaeva E, Kolos E, Korzhevskii D (2018) Allogeneic bone marrow mesenchymal stem cells in the epineurium and perineurium of the recipient rat. Biological Communications 63 (2): 123–132. https://doi.org/10.21638/spbu03.2018.205

    Article  Google Scholar 

  108. Petrova ES, Kolos EA, Korzhevskii DE (2021) Changes in the thickness of rat nerve sheaths after single subperineural administration of rat bone marrow mesenchymal stem cells. Bull Exp Biol Med 171: 547–552. https://doi.org/10.1007/s10517-021-05267-4

    Article  CAS  PubMed  Google Scholar 

  109. Kucenas S, Wang WD, Knapik EW, Appel B (2009) A selective glial barrier at motor axon exit points prevents oligodendrocyte migration from the spinal cord. J Neurosci 29: 15187–15194. https://doi.org/10.1523/JNEUROSCI.4193-09.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Lunn ER, Scourfield J, Keynes RJ, Stern CD (1987) The neural tube origin of ventral root sheath cells in the chick embryo. Development 101: 247–254.

    Article  CAS  Google Scholar 

  111. Boyd BS, Gray AT, Dilley A, Wanek L, Topp KS (2012) The pattern of tibial nerve excursion with active ankle dorsiflexion is different in older people with diabetes mellitus. Clin Biomech (Bristol, Avon) 27 (9): 967–971. https://doi.org/10.1016/j.clinbiomech.2012.06.013

  112. Ross MH, Reith EJ (1989) Perineurium: Evidence for contractile elements. Science 165: 604–606. https://doi.org/10.1126/science.165.3893.604

    Article  Google Scholar 

  113. De Jonge RR, Vreijling JP, Meintjes A, Kwa MS, van Kampen AH, van Schaik IN, Baas F (2003) Transcriptional profile of the human peripheral nervous system by serial analysis of gene expression. Genomics 82(2): 97–108. https://doi.org/10.1016/s0888-7543(03)00124-1

    Article  PubMed  Google Scholar 

  114. De Jonge RR, van Schaik IN, Vreijling JP, Troost D, Baas F (2004) Expression of complement components in the peripheral nervous system. Hum Mol Genet 13(3): 295–302. https://doi.org/10.1093/hmg/ddh029

    Article  CAS  PubMed  Google Scholar 

  115. Pogorelov YV (2001) Histohematological barriers. Guide to Histology, vol. I. SpecLit, SPb, pp 465–494 (In Russ).

    Google Scholar 

  116. Burkel WE (1967) The histological fine structure of perineurium. Anat Rec 158(2):177–189. https://doi.org/10.1002/ar.1091580207

    Article  CAS  PubMed  Google Scholar 

  117. Hall SM, Williams PL (1971) The distribution of electron-dense tracers in peripheral nerve fibres. J Cell Sci 8(2):541–555.

    Article  CAS  Google Scholar 

  118. Klemm H (1970) The perineurium: a diffusion barrier for peroxidase in epineurial and endoneurial application. Z Zellforsch Mikrosk Anat 108(3): 431–445.

    Article  CAS  Google Scholar 

  119. Olsson Y, Reese TS (1971) Permeability of vasa nervorum and perineurium in mouse sciatic nerve studied by fluorescence and electron microscopy. J Neuropathol Exp Neurol 30(1):105–119. https://doi.org/10.1097/00005072-197101000-00011

    Article  CAS  PubMed  Google Scholar 

  120. Palladino SP, Helton ES, Jain P, Dong C, Crowley MR, Crossman DK, Ubogu EE (2017) The Human Blood-Nerve Barrier Transcriptome. Sci Rep 7(1): 17477. https://doi.org/10.1038/s41598-017-17475-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Ouyang X, Dong C, Ubogu EE (2019) In situ molecular characterization of endoneurial microvessels that form the blood-nerve barrier in normal human adult peripheral nerves. J Peripher Nerv Syst 24(2):195–206. https://doi.org/10.1111/jns.12326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Dong C, Ubogu EE (2018) GDNF enhances human blood-nerve barrier function in vitro via MAPK signaling pathways. Tissue Barriers 6(4):1–22. https://doi.org/10.1080/21688370.2018.1546537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Moreau N, Mauborgne A, Couraud PO, Romero IA, Weksler BB, Villanueva L. Pohl M, Boucher Y (2017) Could an endoneurial endothelial crosstalk between Wnt/β-catenin and Sonic Hedgehog pathways underlie the early disruption of the infra-orbital blood-nerve barrier following chronic constriction injury? Mol Pain 13:1744806917727625. https://doi.org/10.1177/1744806917727625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Moreau N, Mauborgne A, Bourgoin S, Couraud PO, Romero IA, Weksler BB, Villanueva L, Pohl M, Boucher Y (2016) Early alterations of Hedgehog signaling pathway in vascular endothelial cells after peripheral nerve injury elicit blood-nerve barrier disruption, nerve inflammation, and neuropathic pain development. Pain 157(4): 827–839. https://doi.org/10.1097/j.pain.0000000000000444

    Article  CAS  PubMed  Google Scholar 

  125. Bykov VL (2007) Cytology and General Histology. Sotis, Sankt-Peterburg (In Russ).

    Google Scholar 

  126. Oldfors A, Johansson BR (1979) Barriers and transport properties of the perineurium. An ultrastructural study with 125I-labeled albuminin and horseradish peroxidase in normal and protein-deprived rats. Acta Neuropathol 47(2):139–143. https://doi.org/10.1007/BF00717037

    Article  CAS  PubMed  Google Scholar 

  127. Oldfors A (1981)Permeability of the perineurium of small nerve fascicles: an ultrastructural study using ferritin in rats. Neuropathol Appl Neurobiol 7(3):183–194. https://doi.org/10.1111/j.1365-2990.1981.tb00088.x

    Article  CAS  PubMed  Google Scholar 

  128. Parmantier E, Lynn B, Lawson D, Turmaine M, Namini SS, Chakrabarti L, McMahon AP, Jessen KR, Mirsky R (1999) Schwann cell-derived Desert hedgehog controls the development of peripheral nerve sheaths. Neuron 23(4): 713–724. https://doi.org/10.1016/s0896-6273(01)80030-1.

    Article  CAS  PubMed  Google Scholar 

  129. Jung J, Frump D, Su J, Wang W, Mozaffar T, Gupta R (2015) Desert hedgehog is a mediator of demyelination in compression neuropathies. Exp Neurol 271: 84–94. https://doi.org/10.1016/j.expneurol.2015.04.014

    Article  CAS  PubMed  Google Scholar 

  130. Fontenas L, Kucenas S (2017) Livin’ on the edge: glia shape nervous system transition zones. Curr Opin Neurobiol 47:44–51. https://doi.org/10.1016/j.conb.2017.09.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  131. Chen ZL, Yu WM, Strickland S (2007) Peripheral regeneration. Annu ReNeurosci 30: 209–233. https://doi.org/10.1146/annurev.neuro.30.051606.094337

    Article  CAS  Google Scholar 

  132. Monk KR, Feltri ML, Taveggia C (2015) New insights on Schwann cell development. Glia 63: 1376–1393. https://doi.org/10.1002/glia.22852

    Article  PubMed  PubMed Central  Google Scholar 

  133. Ohara S, Takahashi H, Ikuta F (1986) Ultrastructural alterations of perineurial cells in the early stage of Wallerian degeneration. Lab Invest 54(2): 213–221.

    CAS  PubMed  Google Scholar 

  134. Spencer PS, Weinberg HJ, Raine CS, Prineas JW (1975) The perineurial window—a new model of focal demyelination and remyelination. Brain Res 96: 323–329. https://doi.org/10.1016/0006-8993(75)90742-8

    Article  CAS  PubMed  Google Scholar 

  135. Radek A, Thomas PK, King RH (1986) Perineurial differentiation in interchange grafts of rat peripheral nerve and spinal root. J Anat 147: 207–217.

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Lewis GM, Kucenas S (2014) Perineurial glia are essential for motor axon regrowth following nerve injury. J Neurosci 34(38):12762–12777. https://doi.org/10.1523/JNEUROSCI.1906-14.2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Ohta M, Okajima S, Hirakawa H, Tokunaga D, Fujiwara H, Oda R, Kobashi H, Hirata M, Kubo T (2005) Expression of tight and gap junctional proteins in the perineurial window model of the rat sciatic nerve. Int J Neurosci 115(10):1469–1481. https://doi.org/10.1080/00207450591001871

    Article  CAS  PubMed  Google Scholar 

  138. Toyoda T, Ochiai K, Ohashi K, Tomioka Y, Kimura T, Umemura T (2005) Multiple perineuriomas in chicken (Gallus gallus domesticus). Vet Pathol 42(2):176–183. https://doi.org/10.1354/vp.42-2-176

    Article  CAS  PubMed  Google Scholar 

  139. Pummi KP, Aho HJ, Laato MK, Peltonen JT, Peltonen SA (2006) Tight junction proteins and perineurial cells in neurofibromas. J Histochem Cytochem 54(1): 53–61. https://doi.org/10.1369/jhc.5A6671.2005

    Article  CAS  PubMed  Google Scholar 

  140. Shelekhova KV, Danilova AB, Michal M, Kazakov DV (2008) Hybrid neurofibroma-perineurioma: an additional example of an extradigital tumor. Ann Diagn Pathol 12(3): 233–234. https://doi.org/10.1016/j.anndiagpath.2008.02.012

    Article  PubMed  Google Scholar 

  141. Gibson JD (1979) The origin of the neural macrophage: a quantitative ultrastructural study of cell population changes during Wallerian degeneration. J Anat 129(1):1–19.

    CAS  PubMed  PubMed Central  Google Scholar 

  142. Hirata K, Kawabuchi M (2002) Myelin phagocytosis by macrophages and nonmacrophages during Walleriandegeneration. Microsc Res Tech 57: 541–547. https://doi.org/10.1002/jemt.10108

    Article  PubMed  Google Scholar 

  143. De la Motte DJ, Hall SM, Allt G (1975) A study of the perineurium in peripheral nerve pathology. Acta Neuropathol 33(3): 257–270. https://doi.org/10.1007/BF00688398

    Article  Google Scholar 

Download references

Funding

This work was supported by the State budget funding within a governmental assignment to the Institute of Experimental Medicine.

Author information

Authors and Affiliations

  1. Institute of Experimental Medicine, St. Petersburg, Russia

    E. S. Petrova & E. A. Kolos

Authors
  1. E. S. Petrova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. E. A. Kolos
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

E.S.P.—basic idea, writing a part of the review, E.A.K.—writing a part of the review.

Corresponding author

Correspondence to E. S. Petrova.

Ethics declarations

CONFLICT OF INTEREST

The authors inform that they have no conflict of interest associated with the publication of this article.

Additional information

Translated by A. Polyanovsky

Russian Text © The Author(s), 2022, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2022, Vol. 58, No. 1, pp. 3–23https://doi.org/10.31857/S0044452922010053.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Petrova, E.S., Kolos, E.A. Current Views on Perineurial Cells: Unique Origin, Structure, Functions. J Evol Biochem Phys 58, 1–23 (2022). https://doi.org/10.1134/S002209302201001X

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S002209302201001X

Keywords:

Search

Navigation