Conditional Disruption of Beta 1 Integrin in Schwann Cells Impedes Interactions with Axons

Overview

Journal J Cell Biol

Specialty Cell Biology

Date 2002 Jan 5

PMID 11777940

Citations 155

Authors

M Laura Feltri

Diana Graus Porta

Stefano C Previtali

Alessandro Nodari

Barbara Migliavacca

Arianna Cassetti

Amanda Littlewood-Evans

Louis F Reichardt

Albee Messing

Angelo Quattrini

Ulrich Mueller

Lawrence Wrabetz

Affiliations

Soon will be listed here.

Abstract

In dystrophic mice, a model of merosin-deficient congenital muscular dystrophy, laminin-2 mutations produce peripheral nerve dysmyelination and render Schwann cells unable to sort bundles of axons. The laminin receptor and the mechanism through which dysmyelination and impaired sorting occur are unknown. We describe mice in which Schwann cell-specific disruption of beta1 integrin, a component of laminin receptors, causes a severe neuropathy with impaired radial sorting of axons. beta 1-null Schwann cells populate nerves, proliferate, and survive normally, but do not extend or maintain normal processes around axons. Interestingly, some Schwann cells surpass this problem to form normal myelin, possibly due to the presence of other laminin receptors such as dystroglycan and alpha 6 beta 4 integrin. These data suggest that beta 1 integrin links laminin in the basal lamina to the cytoskeleton in order for Schwann cells to ensheath axons, and alteration of this linkage contributes to the peripheral neuropathy of congenital muscular dystrophy.

Citing Articles

Schwann Cell-Specific Ablation of Beclin 1 Impairs Myelination and Leads to Motor and Sensory Neuropathy in Mice.

Gambarotto L, Russo L, Bresolin S, Persano L, DAmore R, Ronchi G Adv Sci (Weinh). 2024; 12(5):e2308965.

PMID: 39680476 PMC: 11792035. DOI: 10.1002/advs.202308965.

Adipo-glial signaling mediates metabolic adaptation in peripheral nerve regeneration.

Sundaram V, Schutza V, Schroter N, Backhaus A, Bilsing A, Joneck L Cell Metab. 2023; 35(12):2136-2152.e9.

PMID: 37989315 PMC: 10722468. DOI: 10.1016/j.cmet.2023.10.017.

Pleiotrophin-Neuregulin1 promote axon regeneration and sorting in conduit repair of critical nerve gap injuries.

Gu X, Rahman F, Bendale G, Tran B, Miyata J, Hernandez A Res Sq. 2023; .

PMID: 37986821 PMC: 10659554. DOI: 10.21203/rs.3.rs-3429258/v1.

Prospects of Using Chitosan-Based Biopolymers in the Treatment of Peripheral Nerve Injuries.

Zhang M, An H, Zhang F, Jiang H, Wan T, Wen Y Int J Mol Sci. 2023; 24(16).

PMID: 37629137 PMC: 10454829. DOI: 10.3390/ijms241612956.

Generation of new transgenic SMARCA4-deficient mouse models results in neuromuscular weakness and paralysis of limbs.

Neyazi S, Altendorf L, Schwetje D, Gobel C, Schoof M, Holdhof D Brain Pathol. 2022; 33(3):e13146.

PMID: 36582072 PMC: 10154361. DOI: 10.1111/bpa.13146.

References

Jessen K, Mirsky R . Schwann cells and their precursors emerge as major regulators of nerve development. Trends Neurosci. 1999; 22(9):402-10. DOI: 10.1016/s0166-2236(98)01391-5. View

Tomaselli K, Doherty P, Emmett C, Damsky C, Walsh F, Reichardt L . Expression of beta 1 integrins in sensory neurons of the dorsal root ganglion and their functions in neurite outgrowth on two laminin isoforms. J Neurosci. 1993; 13(11):4880-8. PMC: 2710121. View

Lefcort F, Venstrom K, McDonald J, Reichardt L . Regulation of expression of fibronectin and its receptor, alpha 5 beta 1, during development and regeneration of peripheral nerve. Development. 1992; 116(3):767-82. PMC: 2710134. DOI: 10.1242/dev.116.3.767. View

Bronner-Fraser M, Artinger M, Muschler J, Horwitz A . Developmentally regulated expression of alpha 6 integrin in avian embryos. Development. 1992; 115(1):197-211. DOI: 10.1242/dev.115.1.197. View

Syroid D, Maycox P, Burrola P, Liu N, Wen D, Lee K . Cell death in the Schwann cell lineage and its regulation by neuregulin. Proc Natl Acad Sci U S A. 1996; 93(17):9229-34. PMC: 38624. DOI: 10.1073/pnas.93.17.9229. View

Bradley W, Jenkison M . Abnormalities of peripheral nerves in murine muscular dystrophy. J Neurol Sci. 1973; 18(2):227-47. DOI: 10.1016/0022-510x(73)90009-9. View

Zorick , Syroid , ARROYO , SCHERER , LEMKE . The Transcription Factors SCIP and Krox-20 Mark Distinct Stages and Cell Fates in Schwann Cell Differentiation. Mol Cell Neurosci. 1996; 8(2/3):129-45. DOI: 10.1006/mcne.1996.0052. View

Previtali S, Feltri M, Archelos J, Quattrini A, Wrabetz L, Hartung H . Role of integrins in the peripheral nervous system. Prog Neurobiol. 2001; 64(1):35-49. DOI: 10.1016/s0301-0082(00)00045-9. View

MICHELSON A, RUSSELL E, Harman P . Dystrophia Muscularis: A HEREDITARY PRIMARY MYOPATHY IN THE HOUSE MOUSE. Proc Natl Acad Sci U S A. 1955; 41(12):1079-84. PMC: 528200. DOI: 10.1073/pnas.41.12.1079. View

10.

Stephens L, Sonne J, Fitzgerald M, Damsky C . Targeted deletion of beta 1 integrins in F9 embryonal carcinoma cells affects morphological differentiation but not tissue-specific gene expression. J Cell Biol. 1993; 123(6 Pt 1):1607-20. PMC: 2290911. DOI: 10.1083/jcb.123.6.1607. View

11.

Podratz J, Rodriguez E, Windebank A . Role of the extracellular matrix in myelination of peripheral nerve. Glia. 2001; 35(1):35-40. DOI: 10.1002/glia.1068. View

12.

Schoenwaelder S, Burridge K . Bidirectional signaling between the cytoskeleton and integrins. Curr Opin Cell Biol. 1999; 11(2):274-86. DOI: 10.1016/s0955-0674(99)80037-4. View

13.

Fassler R, Meyer M . Consequences of lack of beta 1 integrin gene expression in mice. Genes Dev. 1995; 9(15):1896-908. DOI: 10.1101/gad.9.15.1896. View

14.

Terashima T, Yasuda H, Terada M, Kogawa S, Maeda K, Haneda M . Expression of Rho-family GTPases (Rac, cdc42, RhoA) and their association with p-21 activated kinase in adult rat peripheral nerve. J Neurochem. 2001; 77(4):986-93. DOI: 10.1046/j.1471-4159.2001.00336.x. View

15.

Wrabetz L, Feltri M, Quattrini A, Imperiale D, Previtali S, DAntonio M . P(0) glycoprotein overexpression causes congenital hypomyelination of peripheral nerves. J Cell Biol. 2000; 148(5):1021-34. PMC: 2174542. DOI: 10.1083/jcb.148.5.1021. View

16.

Feltri M, DAntonio M, Quattrini A, Numerato R, Arona M, Previtali S . A novel P0 glycoprotein transgene activates expression of lacZ in myelin-forming Schwann cells. Eur J Neurosci. 1999; 11(5):1577-86. DOI: 10.1046/j.1460-9568.1999.00568.x. View

17.

Perkins C, Bray G, Aguayo A . Ongoing block of Schwann cell differentiation and deployment in dystrophic mouse spinal roots. Brain Res. 1981; 227(2):213-20. DOI: 10.1016/0165-3806(81)90109-7. View

18.

Blaess S, Senften M, Littlewood-Evans A, Damsky C, Huang Z, Orban P . Beta1-class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron. 2001; 31(3):367-79. DOI: 10.1016/s0896-6273(01)00374-9. View

19.

Anderson D . Cellular and molecular biology of neural crest cell lineage determination. Trends Genet. 1997; 13(7):276-80. DOI: 10.1016/s0168-9525(97)01187-6. View

20.

Zhang X, Topaloglu H, Cruaud C, Tesson F, Weissenbach J, Tome F . Mutations in the laminin alpha 2-chain gene (LAMA2) cause merosin-deficient congenital muscular dystrophy. Nat Genet. 1995; 11(2):216-8. DOI: 10.1038/ng1095-216. View