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. 1984 Mar 1;98(3):1072–1081. doi: 10.1083/jcb.98.3.1072

Attachment of vimentin filaments to desmosomal plaques in human meningiomal cells and arachnoidal tissue

PMCID: PMC2113124  PMID: 6365927

Abstract

Desmosomal proteins are co-expressed with intermediate-sized filaments (IF) of the cytokeratin type in epithelial cells, and these IF are firmly attached to the desmosomal plaque. In meningiomal and certain arachnoidal cells, however, vimentin IF are attached to desmosomal plaques. Meningiomas obtained after surgery, arachnoid "membranes", and arachnoid granulations at autopsy, as well as meningiomal cells grown in short-term culture have been examined by single and double immunofluorescence and immunoelectron microscopy using antibodies to desmoplakins, vimentin, cytokeratins, glial filament protein, neurofilament protein, and procollagen. In addition, two-dimensional gel electrophoresis of the cytoskeletal proteins has been performed. Using all of these techniques, vimentin was the only IF protein that was detected in significant amounts. The junctions morphologically resembling desmosomes of epithelial cells have been identified as true desmosomes by antibodies specific for desmoplakins and they provided the membrane attachment sites for the vimentin IF. These findings show that anchorage of IF to the cell surface at desmosomal plaques is not restricted to cytokeratin IF as in epithelial cells and desmin IF as in cardiac myocytes, suggesting that binding to desmosomes and hemidesmosomes is a more common feature of IF organization. The co- expression of desmosomal proteins and IF of the vimentin type only defines a new class of cell ("desmofibrocyte") and may also provide an important histodiagnostic criterion.

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Selected References

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  1. Blose S. H., Chacko S. Rings of intermediate (100 A) filament bundles in the perinuclear region of vascular endothelial cells. Their mobilization by colcemid and mitosis. J Cell Biol. 1976 Aug;70(2 Pt 1):459–466. doi: 10.1083/jcb.70.2.459. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bravo R., Small J. V., Fey S. J., Larsen P. M., Celis J. E. Architecture and polypeptide composition of HeLa cytoskeletons. Modification of cytoarchitectural polypeptides during mitosis. J Mol Biol. 1982 Jan 5;154(1):121–143. doi: 10.1016/0022-2836(82)90421-1. [DOI] [PubMed] [Google Scholar]
  3. Cervós-Navarro J., Vazquez J. J. An electron microscopic study of meningiomas. Acta Neuropathol. 1969;13(4):301–323. doi: 10.1007/BF00686120. [DOI] [PubMed] [Google Scholar]
  4. Cohen S. M., Gorbsky G., Steinberg M. S. Immunochemical characterization of related families of glycoproteins in desmosomes. J Biol Chem. 1983 Feb 25;258(4):2621–2627. [PubMed] [Google Scholar]
  5. Cowin P., Garrod D. R. Antibodies to epithelial desmosomes show wide tissue and species cross-reactivity. Nature. 1983 Mar 10;302(5904):148–150. doi: 10.1038/302148a0. [DOI] [PubMed] [Google Scholar]
  6. Dahl D., Strocchi P., Bignami A. Vimentin in the central nervous system. A study of the mesenchymal-type intermediate filament-protein in Wallerian degeneration and in postnatal rat development by two-dimensional gel electrophoresis. Differentiation. 1982;22(3):185–190. doi: 10.1111/j.1432-0436.1982.tb01248.x. [DOI] [PubMed] [Google Scholar]
  7. Debus E., Flügge G., Weber K., Osborn M. A monoclonal antibody specific for the 200 K polypeptide of the neurofilament triplet. EMBO J. 1982;1(1):41–45. doi: 10.1002/j.1460-2075.1982.tb01121.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dowling L. M., Parry D. A., Sparrow L. G. Structural homology between hard alpha-keratin and the intermediate filament proteins desmin and vimentin. Biosci Rep. 1983 Jan;3(1):73–78. doi: 10.1007/BF01121573. [DOI] [PubMed] [Google Scholar]
  9. Drochmans P., Freudenstein C., Wanson J. C., Laurent L., Keenan T. W., Stadler J., Leloup R., Franke W. W. Structure and biochemical composition of desmosomes and tonofilaments isolated from calf muzzle epidermis. J Cell Biol. 1978 Nov;79(2 Pt 1):427–443. doi: 10.1083/jcb.79.2.427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Eriksson A., Thornell L. E. Intermediate (skeletin) filaments in heart Purkinje fibers. A correlative morphological and biochemical identification with evidence of a cytoskeletal function. J Cell Biol. 1979 Feb;80(2):231–247. doi: 10.1083/jcb.80.2.231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. FARQUHAR M. G., PALADE G. E. Junctional complexes in various epithelia. J Cell Biol. 1963 May;17:375–412. doi: 10.1083/jcb.17.2.375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fischer H., Schwechheimer K. Interaction of simian virus 40 with human glioma cells. Hum Neurobiol. 1983;2(2):59–64. [PubMed] [Google Scholar]
  13. Frank E. H., Burge B. W., Liwnicz B. H., Lotspeich L. J., White J. C., Wechsler S. L., Mayfield F. H., Keller J. T. Cytokeratin provides a specific marker for human arachnoid cells grown in vitro. Exp Cell Res. 1983 Jul;146(2):371–376. doi: 10.1016/0014-4827(83)90138-6. [DOI] [PubMed] [Google Scholar]
  14. Franke W. W., Lüder M. R., Kartenbeck J., Zerban H., Keenan T. W. Involvement of vesicle coat material in casein secretion and surface regeneration. J Cell Biol. 1976 Apr;69(1):173–195. doi: 10.1083/jcb.69.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Franke W. W., Moll R., Mueller H., Schmid E., Kuhn C., Krepler R., Artlieb U., Denk H. Immunocytochemical identification of epithelium-derived human tumors with antibodies to desmosomal plaque proteins. Proc Natl Acad Sci U S A. 1983 Jan;80(2):543–547. doi: 10.1073/pnas.80.2.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Franke W. W., Moll R., Schiller D. L., Schmid E., Kartenbeck J., Mueller H. Desmoplakins of epithelial and myocardial desmosomes are immunologically and biochemically related. Differentiation. 1982;23(2):115–127. doi: 10.1111/j.1432-0436.1982.tb01274.x. [DOI] [PubMed] [Google Scholar]
  17. Franke W. W., Schmid E., Breitkreutz D., Lüder M., Boukamp P., Fusenig N. E., Osborn M., Weber K. Simultaneous expression of two different types of intermediate sized filaments in mouse keratinocytes proliferating in vitro. Differentiation. 1979;14(1-2):35–50. doi: 10.1111/j.1432-0436.1979.tb01010.x. [DOI] [PubMed] [Google Scholar]
  18. Franke W. W., Schmid E., Freudenstein C., Appelhans B., Osborn M., Weber K., Keenan T. W. Intermediate-sized filaments of the prekeratin type in myoepithelial cells. J Cell Biol. 1980 Mar;84(3):633–654. doi: 10.1083/jcb.84.3.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Franke W. W., Schmid E., Grund C., Müller H., Engelbrecht I., Moll R., Stadler J., Jarasch E. D. Antibodies to high molecular weight polypeptides of desmosomes: specific localization of a class of junctional proteins in cells and tissue. Differentiation. 1981;20(3):217–241. doi: 10.1111/j.1432-0436.1981.tb01178.x. [DOI] [PubMed] [Google Scholar]
  20. Franke W. W., Schmid E., Osborn M., Weber K. Different intermediate-sized filaments distinguished by immunofluorescence microscopy. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5034–5038. doi: 10.1073/pnas.75.10.5034. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Franke W. W., Schmid E., Schiller D. L., Winter S., Jarasch E. D., Moll R., Denk H., Jackson B. W., Illmensee K. Differentiation-related patterns of expression of proteins of intermediate-size filaments in tissues and cultured cells. Cold Spring Harb Symp Quant Biol. 1982;46(Pt 1):431–453. doi: 10.1101/sqb.1982.046.01.041. [DOI] [PubMed] [Google Scholar]
  22. Franke W. W., Schmid E., Weber K., Osborn M. HeLa cells contain intermediate-sized filaments of the prekeratin type. Exp Cell Res. 1979 Jan;118(1):95–109. doi: 10.1016/0014-4827(79)90587-1. [DOI] [PubMed] [Google Scholar]
  23. Franke W. W., Schmid E., Winter S., Osborn M., Weber K. Widespread occurrence of intermediate-sized filaments of the vimentin-type in cultured cells from diverse vertebrates. Exp Cell Res. 1979 Oct 1;123(1):25–46. doi: 10.1016/0014-4827(79)90418-x. [DOI] [PubMed] [Google Scholar]
  24. GUSEK W. [Submicroscopic studies as a contribution to the structure and oncology of meningioma]. Beitr Pathol Anat. 1962 Dec;127:274–326. [PubMed] [Google Scholar]
  25. Gabbiani G., Rungger-Brändle E., de Chastonay C., Franke W. W. Vimentin-containing smooth muscle cells in aortic intimal thickening after endothelial injury. Lab Invest. 1982 Sep;47(3):265–269. [PubMed] [Google Scholar]
  26. Gabbiani G., Schmid E., Winter S., Chaponnier C., de Ckhastonay C., Vandekerckhove J., Weber K., Franke W. W. Vascular smooth muscle cells differ from other smooth muscle cells: predominance of vimentin filaments and a specific alpha-type actin. Proc Natl Acad Sci U S A. 1981 Jan;78(1):298–302. doi: 10.1073/pnas.78.1.298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Geiger B., Schmid E., Franke W. W. Spatial distribution of proteins specific for desmosomes and adhaerens junctions in epithelial cells demonstrated by double immunofluorescence microscopy. Differentiation. 1983;23(3):189–205. doi: 10.1111/j.1432-0436.1982.tb01283.x. [DOI] [PubMed] [Google Scholar]
  28. Geiger B., Tokuyasu K. T., Dutton A. H., Singer S. J. Vinculin, an intracellular protein localized at specialized sites where microfilament bundles terminate at cell membranes. Proc Natl Acad Sci U S A. 1980 Jul;77(7):4127–4131. doi: 10.1073/pnas.77.7.4127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Geisler N., Weber K. Comparison of the proteins of two immunologically distinct intermediate-sized filaments by amino acid sequence analysis: desmin and vimentin. Proc Natl Acad Sci U S A. 1981 Jul;78(7):4120–4123. doi: 10.1073/pnas.78.7.4120. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Geisler N., Weber K. The amino acid sequence of chicken muscle desmin provides a common structural model for intermediate filament proteins. EMBO J. 1982;1(12):1649–1656. doi: 10.1002/j.1460-2075.1982.tb01368.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Gigi O., Geiger B., Eshhar Z., Moll R., Schmid E., Winter S., Schiller D. L., Franke W. W. Detection of a cytokeratin determinant common to diverse epithelial cells by a broadly cross-reacting monoclonal antibody. EMBO J. 1982;1(11):1429–1437. doi: 10.1002/j.1460-2075.1982.tb01334.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Goldman R. D. The role of three cytoplasmic fibers in BHK-21 cell motility. I. Microtubules and the effects of colchicine. J Cell Biol. 1971 Dec;51(3):752–762. doi: 10.1083/jcb.51.3.752. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Gorbsky G., Steinberg M. S. Isolation of the intercellular glycoproteins of desmosomes. J Cell Biol. 1981 Jul;90(1):243–248. doi: 10.1083/jcb.90.1.243. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Gordon W. E., 3rd, Bushnell A., Burridge K. Characterization of the intermediate (10 nm) filaments of cultured cells using an autoimmune rabbit antiserum. Cell. 1978 Feb;13(2):249–261. doi: 10.1016/0092-8674(78)90194-0. [DOI] [PubMed] [Google Scholar]
  35. Hanukoglu I., Fuchs E. The cDNA sequence of a Type II cytoskeletal keratin reveals constant and variable structural domains among keratins. Cell. 1983 Jul;33(3):915–924. doi: 10.1016/0092-8674(83)90034-x. [DOI] [PubMed] [Google Scholar]
  36. Hanukoglu I., Fuchs E. The cDNA sequence of a human epidermal keratin: divergence of sequence but conservation of structure among intermediate filament proteins. Cell. 1982 Nov;31(1):243–252. doi: 10.1016/0092-8674(82)90424-x. [DOI] [PubMed] [Google Scholar]
  37. Hynes R. O., Destree A. T. 10 nm filaments in normal and transformed cells. Cell. 1978 Jan;13(1):151–163. doi: 10.1016/0092-8674(78)90146-0. [DOI] [PubMed] [Google Scholar]
  38. Kartenbeck J., Franke W. W., Moser J. G., Stoffels U. Specific attachment of desmin filaments to desmosomal plaques in cardiac myocytes. EMBO J. 1983;2(5):735–742. doi: 10.1002/j.1460-2075.1983.tb01493.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kartenbeck J., Schmid E., Franke W. W., Geiger B. Different modes of internalization of proteins associated with adhaerens junctions and desmosomes: experimental separation of lateral contacts induces endocytosis of desmosomal plaque material. EMBO J. 1982;1(6):725–732. doi: 10.1002/j.1460-2075.1982.tb01237.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Kelly D. E. Fine structure of desmosomes. , hemidesmosomes, and an adepidermal globular layer in developing newt epidermis. J Cell Biol. 1966 Jan;28(1):51–72. doi: 10.1083/jcb.28.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  42. Moll R., Franke W. W., Schiller D. L., Geiger B., Krepler R. The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell. 1982 Nov;31(1):11–24. doi: 10.1016/0092-8674(82)90400-7. [DOI] [PubMed] [Google Scholar]
  43. Moll R., Franke W. W., Volc-Platzer B., Krepler R. Different keratin polypeptides in epidermis and other epithelia of human skin: a specific cytokeratin of molecular weight 46,000 in epithelia of the pilosebaceous tract and basal cell epitheliomas. J Cell Biol. 1982 Oct;95(1):285–295. doi: 10.1083/jcb.95.1.285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Moll R., Krepler R., Franke W. W. Complex cytokeratin polypeptide patterns observed in certain human carcinomas. Differentiation. 1983;23(3):256–269. doi: 10.1111/j.1432-0436.1982.tb01291.x. [DOI] [PubMed] [Google Scholar]
  45. Mueller H., Franke W. W. Biochemical and immunological characterization of desmoplakins I and II, the major polypeptides of the desmosomal plaque. J Mol Biol. 1983 Feb 5;163(4):647–671. doi: 10.1016/0022-2836(83)90116-x. [DOI] [PubMed] [Google Scholar]
  46. NAPOLITANO L., KYLE R., FISHER E. R. ULTRASTRUCTURE OF MENINGIOMAS AND THE DERIVATION AND NATURE OF THEIR CELLULAR COMPONENTS. Cancer. 1964 Feb;17:233–241. doi: 10.1002/1097-0142(196402)17:2<233::aid-cncr2820170213>3.0.co;2-n. [DOI] [PubMed] [Google Scholar]
  47. O'Farrell P. Z., Goodman H. M., O'Farrell P. H. High resolution two-dimensional electrophoresis of basic as well as acidic proteins. Cell. 1977 Dec;12(4):1133–1141. doi: 10.1016/0092-8674(77)90176-3. [DOI] [PubMed] [Google Scholar]
  48. Osborn M., Altmannsberger M., Shaw G., Schauer A., Weber K. Various sympathetic derived human tumors differ in neurofilament expression. Use in diagnosis of neuroblastoma, ganglioneuroblastoma and pheochromocytoma. Virchows Arch B Cell Pathol Incl Mol Pathol. 1982 Aug;40(2):141–156. doi: 10.1007/BF02932859. [DOI] [PubMed] [Google Scholar]
  49. Overton J. The fat of desmosomes in trypsinized tissue. J Exp Zool. 1968 Jun;168(2):203–214. doi: 10.1002/jez.1401680208. [DOI] [PubMed] [Google Scholar]
  50. Pruss R. M., Mirsky R., Raff M. C., Thorpe R., Dowding A. J., Anderton B. H. All classes of intermediate filaments share a common antigenic determinant defined by a monoclonal antibody. Cell. 1981 Dec;27(3 Pt 2):419–428. doi: 10.1016/0092-8674(81)90383-4. [DOI] [PubMed] [Google Scholar]
  51. RAIMONDI A. J., MULLAN S., EVANS J. P. Human brain tumors: an electron-microscopic study. J Neurosurg. 1962 Sep;19:731–753. doi: 10.3171/jns.1962.19.9.0731. [DOI] [PubMed] [Google Scholar]
  52. Schiller D. L., Franke W. W., Geiger B. A subfamily of relatively large and basic cytokeratin polypeptides as defined by peptide mapping is represented by one or several polypeptides in epithelial cells. EMBO J. 1982;1(6):761–769. doi: 10.1002/j.1460-2075.1982.tb01243.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Schmid E., Franke W. W., Grund C., Schiller D. L., Kolb H., Paweletz N. An epithelial cell line with elongated myoid morphology derived from bovine mammary gland. Expression of cytokeratins and desmosomal plaque proteins in unusual arrays. Exp Cell Res. 1983 Jul;146(2):309–328. doi: 10.1016/0014-4827(83)90133-7. [DOI] [PubMed] [Google Scholar]
  54. Schmid E., Osborn M., Rungger-Brändle E., Gabbiani G., Weber K., Franke W. W. Distribution of vimentin and desmin filaments in smooth muscle tissue of mammalian and avian aorta. Exp Cell Res. 1982 Feb;137(2):329–340. doi: 10.1016/0014-4827(82)90034-9. [DOI] [PubMed] [Google Scholar]
  55. Sharp G., Osborn M., Weber K. Occurrence of two different intermediate filament proteins in the same filament in situ within a human glioma cell line. An immunoelectron microscopical study. Exp Cell Res. 1982 Oct;141(2):385–395. doi: 10.1016/0014-4827(82)90227-0. [DOI] [PubMed] [Google Scholar]
  56. Shaw G., Weber K. The distribution of the neurofilament triplet proteins within individual neurones. Exp Cell Res. 1981 Nov;136(1):119–125. doi: 10.1016/0014-4827(81)90043-4. [DOI] [PubMed] [Google Scholar]
  57. Skerrow C. J., Matoltsy A. G. Chemical characterization of isolated epidermal desmosomes. J Cell Biol. 1974 Nov;63(2 Pt 1):524–530. doi: 10.1083/jcb.63.2.524. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Staehelin L. A. Structure and function of intercellular junctions. Int Rev Cytol. 1974;39:191–283. doi: 10.1016/s0074-7696(08)60940-7. [DOI] [PubMed] [Google Scholar]
  59. Steinert P. M., Idler W. W., Goldman R. D. Intermediate filaments of baby hamster kidney (BHK-21) cells and bovine epidermal keratinocytes have similar ultrastructures and subunit domain structures. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4534–4538. doi: 10.1073/pnas.77.8.4534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Steinert P. M., Rice R. H., Roop D. R., Trus B. L., Steven A. C. Complete amino acid sequence of a mouse epidermal keratin subunit and implications for the structure of intermediate filaments. Nature. 1983 Apr 28;302(5911):794–800. doi: 10.1038/302794a0. [DOI] [PubMed] [Google Scholar]
  61. Summerhayes I. C., Cheng Y. S., Sun T. T., Chen L. B. Expression of keratin and vimentin intermediate filaments in rabbit bladder epithelial cells at different stages of benzo[a]pyrene-induced neoplastic progression. J Cell Biol. 1981 Jul;90(1):63–69. doi: 10.1083/jcb.90.1.63. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Tani E., Ikeda K., Yamagata S., Nishiura M., Higashi N. Specialized junctional complexes in human meningioma. Acta Neuropathol. 1974;28(4):305–315. doi: 10.1007/BF00685285. [DOI] [PubMed] [Google Scholar]
  63. Tokuyasu K. T., Dutton A. H., Geiger B., Singer S. J. Ultrastructure of chicken cardiac muscle as studied by double immunolabeling in electron microscopy. Proc Natl Acad Sci U S A. 1981 Dec;78(12):7619–7623. doi: 10.1073/pnas.78.12.7619. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Tokuyasu K. T., Dutton A. H., Singer S. J. Immunoelectron microscopic studies of desmin (skeletin) localization and intermediate filament organization in chicken cardiac muscle. J Cell Biol. 1983 Jun;96(6):1736–1742. doi: 10.1083/jcb.96.6.1736. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Virtanen I., Lehto V. P., Lehtonen E., Vartio T., Stenman S., Kurki P., Wager O., Small J. V., Dahl D., Badley R. A. Expression of intermediate filaments in cultured cells. J Cell Sci. 1981 Aug;50:45–63. doi: 10.1242/jcs.50.1.45. [DOI] [PubMed] [Google Scholar]
  66. Weber K., Geisler N. The structural relation between intermediate filament proteins in living cells and the alpha-keratins of sheep wool. EMBO J. 1982;1(10):1155–1160. doi: 10.1002/j.1460-2075.1982.tb00006.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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