Home LiteratureArticle Details
PMID: 15883201 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Tight junctions in Schwann cells of peripheral myelinated axons: a lesson from claudin-19-deficient mice.

The Journal of cell biology ·Vol. 169 ·No. 3 ·2005-05-09 ·Pages 527-38

Miyamoto T, Morita K, Takemoto D, Takeuchi K, Kitano Y, Miyakawa T, Nakayama K, Okamura Y, Sasaki H, Miyachi Y, Furuse M, Tsukita S

Abstract

Tight junction (TJ)-like structures have been reported in Schwann cells, but their molecular composition and physiological function remain elusive. We found that claudin-19, a novel member of the claudin family (TJ adhesion molecules in epithelia), constituted these structures. Claudin-19-deficient mice were generated, and they exhibited behavioral abnormalities that could be attributed to peripheral nervous system deficits. Electrophysiological analyses showed that the claudin-19 deficiency affected the nerve conduction of peripheral myelinated fibers. Interestingly, the overall morphology of Schwann cells lacking claudin-19 expression appeared to be normal not only in the internodal region but also at the node of Ranvier, except that TJs completely disappeared, at least from the outer/inner mesaxons. These findings have indicated that, similar to epithelial cells, Schwann cells also bear claudin-based TJs, and they have also suggested that these TJs are not involved in the polarized morphogenesis but are involved in the electrophysiological "sealing" function of Schwann cells.

MeSH Terms
Animals Axons/metabolism,pathology,ultrastructure Cell Membrane/metabolism,pathology,ultrastructure Claudins Female Male Membrane Proteins/genetics,metabolism Mice Mice, Inbred C57BL Mice, Knockout Myelin Sheath/metabolism,pathology,ultrastructure Nerve Fibers, Myelinated/metabolism,pathology,ultrastructure Neural Conduction/genetics Peripheral Nerves/abnormalities,metabolism,ultrastructure Ranvier's Nodes/metabolism,pathology,ultrastructure Schwann Cells/metabolism,pathology,ultrastructure Tight Junctions/metabolism,pathology,ultrastructure
Chemicals
Claudins Cldn19 protein, mouse Membrane Proteins
Authors & Affiliations
12 authors, click to expand affiliations / ORCID
Miyamoto Tatsuo
Department of Cell Biology, Graduate School of Medicine, Kyoto University, Japan.
Morita Kazumasa
Takemoto Daisuke
Takeuchi Kosei
Kitano Yuka
Miyakawa Tsuyoshi
Nakayama Kiyomi
Okamura Yasushi
Sasaki Hiroyuki
Miyachi Yoshiki
Furuse Mikio
Tsukita Shoichiro
References (60)
60 references, click to expand
  1. 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. 1997 Dec 15;139(6):1495-506 PMID: 9396755
  2. Paranodin, a glycoprotein of neuronal paranodal membranes.
    Neuron. 1997 Aug;19(2):319-31 PMID: 9292722
  3. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin.
    J Cell Biol. 1998 Jun 29;141(7):1539-50 PMID: 9647647
  4. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration.
    J Cell Biol. 1998 Jul 13;142(1):117-27 PMID: 9660867
  5. Neurexin IV, caspr and paranodin--novel members of the neurexin family: encounters of axons and glia.
    Trends Neurosci. 1998 Oct;21(10):444-9 PMID: 9786343
  6. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts.
    J Cell Biol. 1998 Oct 19;143(2):391-401 PMID: 9786950
  7. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands.
    Proc Natl Acad Sci U S A. 1999 Jan 19;96(2):511-6 PMID: 9892664
  8. Characterization of progressive motor deficits in mice transgenic for the human Huntington's disease mutation.
    J Neurosci. 1999 Apr 15;19(8):3248-57 PMID: 10191337
  9. Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis.
    J Cell Biol. 1999 May 3;145(3):579-88 PMID: 10225958
  10. Occludin and claudins in tight-junction strands: leading or supporting players?
    Trends Cell Biol. 1999 Jul;9(7):268-73 PMID: 10370242
  11. Paracellin-1, a renal tight junction protein required for paracellular Mg2+ resorption.
    Science. 1999 Jul 2;285(5424):103-6 PMID: 10390358
  12. Endothelial claudin: claudin-5/TMVCF constitutes tight junction strands in endothelial cells.
    J Cell Biol. 1999 Oct 4;147(1):185-94 PMID: 10508865
  13. Charcot-Marie-Tooth disease (hereditary motor sensory neuropathies) and hereditary sensory and autonomic neuropathies.
    Neurologist. 2004 Nov;10(6):327-37 PMID: 15518599
  14. A radial component of central myelin sheaths.
    J Biophys Biochem Cytol. 1961 Dec;11:733-5 PMID: 14485724
  15. Junctional complexes in various epithelia.
    J Cell Biol. 1963 May;17:375-412 PMID: 13944428
  16. FURTHER OBSERVATIONS ON THE STRUCTURE OF MYELIN SHEATHS IN THE CENTRAL NERVOUS SYSTEM.
    J Cell Biol. 1964 Feb;20:281-96 PMID: 14126873
  17. The molecular physiology of tight junction pores.
    Physiology (Bethesda). 2004 Dec;19:331-8 PMID: 15546850
  18. CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice.
    Cell. 1999 Dec 10;99(6):649-59 PMID: 10612400
  19. On the molecular architecture of myelinated fibers.
    Histochem Cell Biol. 2000 Jan;113(1):1-18 PMID: 10664064
  20. Molecular domains of myelinated axons.
    Curr Opin Neurobiol. 2000 Oct;10(5):558-65 PMID: 11084317
  21. Multifunctional strands in tight junctions.
    Nat Rev Mol Cell Biol. 2001 Apr;2(4):285-93 PMID: 11283726
  22. Freeze-fracture properties of central myelin in the bullfrog.
    Neuroscience. 1976 Dec;1(6):459-67 PMID: 11370238
  23. Organizing principles of the axoglial apparatus.
    Neuron. 2001 May;30(2):335-44 PMID: 11394997
  24. Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor.
    J Neurosci. 2001 Jul 15;21(14):5239-50 PMID: 11438599
  25. Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments.
    J Am Soc Nephrol. 2002 Apr;13(4):875-86 PMID: 11912246
  26. Cellular junctions of myelinated nerves (Review).
    Mol Membr Biol. 2002 Apr-Jun;19(2):95-101 PMID: 12126235
  27. Distinct claudins and associated PDZ proteins form different autotypic tight junctions in myelinating Schwann cells.
    J Cell Biol. 2002 Oct 28;159(2):361-72 PMID: 12403818
  28. Adaptation of core mechanisms to generate cell polarity.
    Nature. 2003 Apr 17;422(6933):766-74 PMID: 12700771
  29. Composition and function of PDZ protein complexes during cell polarization.
    Am J Physiol Renal Physiol. 2003 Sep;285(3):F377-87 PMID: 12890661
  30. The claudin-like megatrachea is essential in septate junctions for the epithelial barrier function in Drosophila.
    Dev Cell. 2003 Oct;5(4):611-20 PMID: 14536062
  31. Polarized domains of myelinated axons.
    Neuron. 2003 Oct 9;40(2):297-318 PMID: 14556710
  32. Apicobasal polarization: epithelial form and function.
    Curr Opin Cell Biol. 2003 Dec;15(6):747-52 PMID: 14644201
  33. Dominant intermediate Charcot-Marie-Tooth type C maps to chromosome 1p34-p35.
    Am J Hum Genet. 2003 Dec;73(6):1423-30 PMID: 14606043
  34. The local differentiation of myelinated axons at nodes of Ranvier.
    Nat Rev Neurosci. 2003 Dec;4(12):968-80 PMID: 14682359
  35. Tetraspanin protein CD9 is a novel paranodal component regulating paranodal junctional formation.
    J Neurosci. 2004 Jan 7;24(1):96-102 PMID: 14715942
  36. Sinuous is a Drosophila claudin required for septate junction organization and epithelial tube size control.
    J Cell Biol. 2004 Jan 19;164(2):313-23 PMID: 14734539
  37. The tight junction: a multifunctional complex.
    Am J Physiol Cell Physiol. 2004 Jun;286(6):C1213-28 PMID: 15151915
  38. Barriers built on claudins.
    J Cell Sci. 2004 May 15;117(Pt 12):2435-47 PMID: 15159449
  39. Setting up a selective barrier at the apical junction complex.
    Curr Opin Cell Biol. 2004 Apr;16(2):140-5 PMID: 15196556
  40. Charcot-Marie-Tooth disease: an update.
    Curr Opin Neurol. 2004 Oct;17(5):579-85 PMID: 15367862
  41. Junctions in the central nervous system of the cat. I. Membrane fusion in central myelin.
    Cell Tissue Res. 1974 May 8;148(4):565-76 PMID: 4836649
  42. Possible role of zonula occludens of the myelin sheath in demyelinating conditions.
    Nature. 1974 Oct 25;251(5477):725-7 PMID: 4610402
  43. Structure and function of intercellular junctions.
    Int Rev Cytol. 1974;39:191-283 PMID: 4611943
  44. Zonulae occludentes of the myelin lamellae in the nerve fibre layer of the retina and in the optic nerve of the rabbit: a demonstration by the freeze-fracture method.
    J Neurocytol. 1975 Apr;4(2):131-40 PMID: 1123652
  45. Intramembranous particle distribution at the node of Ranvier and adjacent axolemma in myelinated axons of the frog brain.
    J Neurocytol. 1976 Dec;5(6):731-45 PMID: 1087339
  46. Membrane morphology of the vertebrate nervous system. A study with freeze-etch technique.
    Prog Brain Res. 1977;46:1-384 PMID: 854571
  47. The development of a zonula occludens in peripheral myelin of the chick embryo. A freeze-fracture study.
    Cell Tissue Res. 1978 May 29;189(2):187-201 PMID: 657237
  48. An experimental analysis of interlamellar tight junctions in amphibian and mammalian C.N.S. myelin.
    J Neurocytol. 1978 Aug;7(4):489-503 PMID: 690675
  49. The movement of membranous organelles in axons. Electron microscopic identification of anterogradely and retrogradely transported organelles.
    J Cell Biol. 1980 Mar;84(3):513-30 PMID: 6153657
  50. Interlamellar tight junctions of central myelin. I. Developmental mechanisms during myelogenesis.
    Cell Tissue Res. 1980;213(1):81-94 PMID: 7459997
  51. Comparative analysis of junctions in the myelin sheath of central and peripheral axons of fish, amphibians and mammals: a freeze-fracture study using complementary replicas.
    J Neurocytol. 1980 Feb;9(1):15-38 PMID: 7205331
  52. Tight junction contact events and temporary gap junctions in the sciatic nerve fibres of the chicken during Wallerian degeneration and subsequent regeneration.
    J Neurocytol. 1982 Oct;11(5):839-58 PMID: 7143029
  53. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction.
    Anal Biochem. 1987 Apr;162(1):156-9 PMID: 2440339
  54. Occludin: a novel integral membrane protein localizing at tight junctions.
    J Cell Biol. 1993 Dec;123(6 Pt 2):1777-88 PMID: 8276896
  55. A Drosophila homologue of membrane-skeleton protein 4.1 is associated with septate junctions and is encoded by the coracle gene.
    Development. 1994 Mar;120(3):545-57 PMID: 8162854
  56. Novel E-cadherin-mediated adhesion in peripheral nerve: Schwann cell architecture is stabilized by autotypic adherens junctions.
    J Cell Biol. 1995 Apr;129(1):189-202 PMID: 7698985
  57. Tight junctions and the molecular basis for regulation of paracellular permeability.
    Am J Physiol. 1995 Oct;269(4 Pt 1):G467-75 PMID: 7485497
  58. A Drosophila neurexin is required for septate junction and blood-nerve barrier formation and function.
    Cell. 1996 Dec 13;87(6):1059-68 PMID: 8978610
  59. Identification of a novel contactin-associated transmembrane receptor with multiple domains implicated in protein-protein interactions.
    EMBO J. 1997 Mar 3;16(5):978-88 PMID: 9118959
  60. Tight junctions.
    J Cell Sci. 1998 Mar;111 ( Pt 5):541-7 PMID: 9454728
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
2005-05-09
Pages
527-38
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2171943
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]