DOI: 10.1002/jnr.1138. Ezrin, radixin, and moesin are components of Schwann cell microvilli

Ezrin, radixin, and moesin are components of Schwann cell microvilli

10.1002/jnr.1138

Crossref journal-article

Wiley

Journal of Neuroscience Research (311)

Abstract

AbstractEzrin, radixin, and moesin (ERM proteins), as well as the neurofibromatosis 2 (NF2) tumor suppressor merlin/schwannomin, all belong to the protein 4.1 family, yet only merlin is a tumor suppressor in Schwann cells. To gain insight into the possible functions of ERM proteins in Schwann cells, we examined their localization in peripheral nerve, because we have previously shown that merlin is found in paranodes and in Schmidt‐Lanterman incisures. All three ERM proteins were highly expressed in the microvilli of myelinating Schwann cells that surround the nodal axolemma as well as in incisures and cytoplasmic puncta in the vicinity of the node. In all of these locations, ERM proteins were colocalized with actin filaments. In contrast, ERM proteins did not surround nodes in the CNS. The colocalization of ERM proteins with actin indicates that they have functions different from those of merlin in myelinating Schwann cells. J. Neurosci. Res. 65:150–164, 2001. © 2001 Wiley‐Liss, Inc.

Bibliography

Scherer, S. S., Xu, T., Crino, P., Arroyo, E. J., & Gutmann, D. H. (2001). Ezrin, radixin, and moesin are components of Schwann cell microvilli. Journal of Neuroscience Research, 65(2), 150â164. Portico.

Authors 5

Steven S. Scherer (first)
Theodore Xu (additional)
Peter Crino (additional)
Edgardo J. Arroyo (additional)
David H. Gutmann (additional)

References 59 Referenced 68

10.1006/excr.1994.1021
10.1006/excr.1995.1218
10.1007/s004180050001
10.1023/A:1007009613484
{'key': 'e_1_2_6_6_1', 'first-page': '107', 'article-title': 'Molecular architecture of the specialized axonal membrane at the node of Ranvier', 'volume': '52', 'author': 'Bennett V', 'year': '1997', 'journal-title': 'Soc Gen Physiol'} / Soc Gen Physiol / Molecular architecture of the specialized axonal membrane at the node of Ranvier by Bennett V (1997)
10.1242/jcs.105.4.1025 / J Cell Sci / Ezrin is concentrated in the apical microvilli of a wide variety of epithelial cell whereas moesin is found primarily in endothelial cells by Berryman M (1993)
10.1002/glia.440010302
10.1083/jcb.108.3.921
10.1016/S0896-6273(00)80248-2
10.1074/jbc.274.4.2315
10.1083/jcb.139.6.1495
10.1083/jcb.129.1.189
10.1242/dev.120.5.1287 / Development / β4 Integrin expression in myelinating Schwann cells is ab‐axonally polarized, developmentally regulated, and axonally dependent by Feltri ML (1994)
10.1073/pnas.90.22.10846
10.1073/pnas.96.13.7300
10.1101/gad.14.13.1617
10.1212/WNL.49.1.267
10.1242/jcs.112.8.1149 / J Cell Sci / Immunofluorescence detection of ezrin/radixin/moesin (ERM) proteins with their carboxyl‐terminal threonine phosphorylated in cultured cells and tissues: application of a novel fixation protocol using trichloroacetic acid (TCA) as a fixative by Hayashi K (1999)
10.1083/jcb.129.4.1007
10.1093/acprof:oso/9780195082937.003.0003
10.1006/bbrc.1998.9009
10.1007/BF01187068
10.1097/00001756-199607290-00003
10.1002/1096-9861(20001023)426:3<468::AID-CNE9>3.0.CO;2-I
10.1002/(SICI)1098-1136(199811)24:3<313::AID-GLIA5>3.0.CO;2-2
10.1007/BF01268092
10.1073/pnas.79.19.6089
10.1523/JNEUROSCI.07-11-03474.1987
10.1007/BF01194978
10.1083/jcb.140.3.647
10.1523/JNEUROSCI.15-05-03761.1995
10.1523/JNEUROSCI.16-08-02421.1996 / J Neurosci / Inwardly rectifying K+ channels that may participate in K+ buffering are localized in microvilli of Schwann cells by Mi HY (1996)
10.1002/(SICI)1098-1136(199904)26:2<166::AID-GLIA7>3.0.CO;2-Q
10.1074/jbc.270.52.31377
10.1002/(SICI)1097-4695(199812)37:4<487::AID-NEU1>3.0.CO;2-B
10.1016/S0896-6273(01)80030-1
10.1083/jcb.111.6.2651
10.1016/S0959-4388(00)00122-7
{'key': 'e_1_2_6_40_1', 'first-page': '494', 'volume-title': 'The fine structure of the nervous system', 'author': 'Peters A', 'year': '1991'} / The fine structure of the nervous system by Peters A (1991)
10.1007/BF01148309
{'key': 'e_1_2_6_42_1', 'first-page': '769', 'volume-title': 'Degeneration and regeneration of the nervous system', 'author': 'Ramon y Cajal S', 'year': '1928'} / Degeneration and regeneration of the nervous system by Ramon y Cajal S (1928)
10.1242/jcs.110.18.2249 / J Cell Sci / Neurofibromatosis 2 tumor suppressor protein colocalizes with ezrin and CD44 and associates with actin‐containing cytoskeleton by Sainio M (1997)
10.1002/(SICI)1097-4547(19961201)46:5<595::AID-JNR8>3.0.CO;2-E
10.1523/JNEUROSCI.15-12-08281.1995
10.1038/ng0498-354
{'key': 'e_1_2_6_47_1', 'first-page': '4889', 'article-title': 'CD44 expression is aberrant in benign Schwann cell tumors possessing mutations in the neurofibromatosis type 2, but not type 1, gene', 'volume': '57', 'author': 'Sherman L', 'year': '1997', 'journal-title': 'Cancer Res'} / Cancer Res / CD44 expression is aberrant in benign Schwann cell tumors possessing mutations in the neurofibromatosis type 2, but not type 1, gene by Sherman L (1997)
10.1038/sj.onc.1201418
10.1083/jcb.150.5.1071
{'key': 'e_1_2_6_50_1', 'first-page': '1649', 'article-title': 'Universal absence of merlin, but not other ERM family members, in schwannomas', 'volume': '151', 'author': 'Stemmer‐Rachamimov AO', 'year': '1997', 'journal-title': 'Am J Pathol'} / Am J Pathol / Universal absence of merlin, but not other ERM family members, in schwannomas by Stemmer‐Rachamimov AO (1997)
10.1002/(SICI)1097-4695(199712)33:7<914::AID-NEU4>3.0.CO;2-B
10.1083/jcb.125.6.1371
10.1007/BF00296358
10.1007/BF01188423
10.1016/S0955-0674(97)80154-8
10.1002/(SICI)1097-4547(19971015)50:2<321::AID-JNR20>3.0.CO;2-9
{'key': 'e_1_2_6_57_1', 'first-page': '241', 'article-title': 'Wallerian degeneration in ICAM‐1‐deficient mice', 'volume': '152', 'author': 'Vougioukas VI', 'year': '1998', 'journal-title': 'Am J Pathol'} / Am J Pathol / Wallerian degeneration in ICAM‐1‐deficient mice by Vougioukas VI (1998)
10.1242/jcs.107.9.2523 / J Cell Sci / Analysis of a cortical cytoskeletal structure: a role for erzin‐radixin‐moesin (ERM proteins) in the marginal band of chicken erythrocytes by Winckler B (1994)
10.1002/(SICI)1097-4547(19980201)51:3<403::AID-JNR13>3.0.CO;2-7
{'key': 'e_1_2_6_60_1', 'first-page': '148A', 'article-title': 'Buffered picric‐acid formaldehyde: a new rapid fixative for electron‐microscopy', 'volume': '35', 'author': 'Zamboni L', 'year': '1967', 'journal-title': 'J Cell Biol'} / J Cell Biol / Buffered picric‐acid formaldehyde: a new rapid fixative for electron‐microscopy by Zamboni L (1967)

Dates

Type	When
Created	20 years, 10 months ago (Oct. 28, 2004, 7:31 a.m.)
Deposited	1 year, 9 months ago (Nov. 19, 2023, 5:01 a.m.)
Indexed	11 months, 3 weeks ago (Sept. 13, 2024, 12:43 p.m.)
Issued	24 years, 2 months ago (June 28, 2001)
Published	24 years, 2 months ago (June 28, 2001)
Published Online	24 years, 2 months ago (June 28, 2001)
Published Print	24 years, 1 month ago (July 15, 2001)

Funders 0

None

BibTeX

@article{Scherer_2001, title={Ezrin, radixin, and moesin are components of Schwann cell microvilli}, volume={65}, ISSN={1097-4547}, url={http://dx.doi.org/10.1002/jnr.1138}, DOI={10.1002/jnr.1138}, number={2}, journal={Journal of Neuroscience Research}, publisher={Wiley}, author={Scherer, Steven S. and Xu, Theodore and Crino, Peter and Arroyo, Edgardo J. and Gutmann, David H.}, year={2001}, month=jun, pages={150–164} }

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