Ectopic expression of desmin in the epidermis of transgenic mice permits development of a normal epidermis

Differentiation

Volumn 70, Issue 1, 2002, Pages 56-68

  Kirfel, Jutta ^a   Peters, Bettina ^a,d   Grund, Christine ^b   Reifenberg, Kurt ^c   Magin, Thomas M ^a  

^a UNIVERSITY OF BONN   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c JOHANNES GUTENBERG UNIVERSITY   (Germany)

^d Memorec Biotec GmbH   (Germany)

Author keywords

Desmin; Epidermolysis bullosa simplex (EBS); Intermediate filament (IF); Keratin

Indexed keywords

DESMIN; INTERMEDIATE FILAMENT PROTEIN; KERATIN; CYTOKERATIN 14; KRT1 14 PROTEIN, MOUSE; KRT1-14 PROTEIN, MOUSE; KRT14 PROTEIN, HUMAN;

ANIMAL TISSUE; ARTICLE; BASAL CELL; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; CYTOARCHITECTURE; CYTOSKELETON; HETEROZYGOTE; INTERMEDIATE FILAMENT; KERATINOCYTE; MATING SYSTEM; MOUSE; NEWBORN; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SKIN EPITHELIUM; TRANSGENIC MOUSE; ANIMAL; DISEASE MODEL; EPIDERMIS; EPIDERMOLYSIS BULLOSA SIMPLEX; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNOHISTOCHEMISTRY; METABOLISM; PHENOTYPE; ULTRASTRUCTURE;

ANIMALIA; MUS MUSCULUS;

ANIMALS; DESMIN; DISEASE MODELS, ANIMAL; EPIDERMIS; EPIDERMOLYSIS BULLOSA SIMPLEX; HUMANS; IMMUNOHISTOCHEMISTRY; KERATIN-14; KERATINOCYTES; KERATINS; MICE; MICE, TRANSGENIC; PHENOTYPE;

EID: 0036514095     PISSN: 03014681     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-0436.2002.700106.x     Document Type: Article

References (64)

1. Bader, B.L., Jahn, L. and Franke, W.W. (1988) Low level expression of cytokeratins 8, 18 and 19 in vascular smooth muscle cells of human umbilical cord and in cultured cells derived therefrom, with an analysis of the chromosomal locus containing the cytokeratin 19 gene. Eur J Cell Biol 47:300-319.
2. Berteretche, M.V., Dunia, I., Devilliers, G., van-der, K.A., Pieper, F., Bloemendal, H., Benedetti, E.L. and Forest, N. (1993) Abnormal incisor-tooth differentiation in transgenic mice expressing the muscle-specific desmin gene. Eur J Cell Biol 62:183-193.
3. Blessing, M., Nanney, L.B., King, L.E., Jones, C.M. and Hogan, B.L. (1993a) Transgenic mice as a model to study the role of TGF-beta-related molecules in hair follicles. Genes Dev 7:204-215.
4. Blessing, M., Ruther, U. and Franke, W.W. (1993b) Ectopic synthesis of epidermal cytokeratins in pancreatic islet cells of transgenic mice interferes with cytoskeletal order and insulin production. J Cell Biol 120:743-755.
5. Bova, M.P., Yaron, O., Huang, Q., Ding, L., Haley, D.A., Stewart, P.L. and Horwitz, J. (1999) Mutation R120G in alphaB-crystallin, which is linked to a desmin-related myopathy, results in an irregular structure and defective chaperone-like function. Proc Natl Acad Sci USA 96:6137-6142.
6. Brenner, M., Johnson, A.B., Boespflug-Tanguy, O., Rodriguez, D., Goldman, J.E. and Messing, A. (2001) Mutations in GFAP, encoding glial fibrillary acidic protein, are associated with Alexander disease. Nat Genet 27:117-120.
7. Cao, T., Longley, M., Wang, X. and Roop, D. (2001) An Inducible Mouse Model for Epidermolysis Bullosa Simplex. Implications for gene therapy. J Cell Biol 152:651-656.
8. Capetanaki, Y. and Milner, D.J. (1998) Desmin cytoskeleton in muscle integrity and function. Subcell Biochem 31:463-495.
9. Casanova, M.L., Bravo, A., Ramirez, A., Morreale, d.E., Were, F., Merlino, G., Vidal, M. and Jorcano, J.L. (1999) Exocrine pancreatic disorders in transsgenic mice expressing human keratin 8. J Clin Invest 103:1587-1595.
10. Dalakas, M.C., Park, K.Y., Semino-Mora, C., Lee, H.S., Sivakumar, K. and Goldfarb, L.G. (2000) Desmin myopathy, a skeletal myopathy with cardiomyopathy caused by mutations in the desmin gene. N Engl J Med 342:770-780.
11. Fine, J.D., McGrath, J. and Eady, R.A. (2000) Inherited epidermolysis bullosa comes into the new millenium: a revised classification system based on current knowledge of pathogenetic mechanisms and the clinical, laboratory, and epidemiologic findings of large, well-defined patient cohorts. J Am Acad Dermatol 43:135-137.
12. Fuchs, E. and Cleveland, D.W. (1998) A structural scaffolding of intermediate filaments in health and disease. Science 279:514-519.
13. Fuchs, E. and Green, H. (1980) Changes in keratin gene expression during terminal differentiation of the keratinocyte. Cell 19:1033-1042.
14. Fuchs, E. and Weber, K. (1994) Intermediate filaments: structure, dynamics, function, and disease. Annu Rev Biochem 63:345-382.
15. Fuchs, E. and Yang, Y. (1999) Crossroads on cytoskeletal high-ways. Cell 98:547-550.
16. Geerts, A., Eliasson, C., Niki, T., Wielant, A., Vaeyens, F. and Pekny, M. (2001) Formation of normal desmin intermediate filaments in mouse hepatic stellate cells requires vimentin. Hepatology 33:177-188.
17. Geerts, D., Fontao, L., Nievers, M.G., Schaapveld, R.Q., Purkis, P.E., Wheeler, G.N., Lane, E.B., Leigh, I.M. and Sonnenberg, A. (1999) Binding of integrin alpha6beta4 to plectin prevents plectin association with F-actin but does not interfere with intermediate filament binding. J Cell Biol 147:417-434.
18. Goldfarb, L.G., Park, K.Y., Cervenakova, L., Gorokhova, S., Lee, H.S., Vasconcelos, O., Nagle, J.W., Semino-Mora, C., Sivakumar, K. and Dalakas, M.C. (1998) Missense mutations in desmin associated with familial cardiac and skeletal myopathy. Nat Genet 19:402-403.
19. Guo, L., Degenstein, L., Dowling, J., Yu, Q.C., Wollmann, R., Perman, B. and Fuchs, E. (1995) Gene targeting of BPAG1: abnormalities in mechanical strength and cell migration in stratified epithelia and neurologic degeneration. Cell 81:233-243.
20. Hatzfeld, M. and Franke, W.W. (1985) Pair formation and promiscuity of cytokeratins: formation in vitro of heterotypic complexes and intermediate-sized filaments by homologous and heterologous recombinations of purified polypeptides. J Cell Biol 101:1826-1841.
21. Hatzfeld, M., Haffner, C., Schulze, K. and Vinzens, U. (2000) The function of plakophilin 1 in desmosome assembly and actin filament organization. J Cell Biol 149:209-222.
22. Herrmann, H. and Aebi, U. (2000) Intermediate filaments and their associates: multi-talented structural elements specifying cytoarchitecture and cytodynamics. Curr Opin Cell Biol 12:79-90.
23. Herrmann, H., Haner, M., Brettel, M., Ku, N.O. and Aebi, U. (1999) Characterization of distinct early assembly units of different intermediate filament proteins. J Mol Biol 286:1403-1420.
24. Herrmann, H. and Harris, J.R. (1998) Intermediate filaments. Subcellular biochemistry. Plenum Press, New York.
25. Hesse, M., Magin, T.M. and Weber, K. (2001) Genes for intermediate filament proteins and the draft sequence of the human genome: novel keratin genes and a surprisingly high number of pseudogenes related to keratin genes 8 and 18. J Cell Sci 114:2569-2575.
26. Hieda, Y., Nishizawa, Y., Uematsu, J. and Owaribe, K. (1992) Identification of a new hemidesmosomal protein, HD1: a major, high molecular mass component of isolated hemidesmosomes. J Cell Biol 116:1497-1506.
27. Hijikata, T., Murakami, T., Imamura, M., Fujimaki, N. and Ishikawa, H. (1999) Plectin is a linker of intermediate filaments to Z-discs in skeletal muscle fibers. J Cell Sci 112:867-876.
28. Hutton, E., Paladini, R.D., Yu, Q.C., Yen, M., Coulombe, P.A. and Fuchs, E. (1998) Functional differences between keratins of stratified and simple epithelia. J Cell Biol 143:487-499.
29. Kartenbeck, J., Franke, W.W., Moser, J.G. and Stoffels, U. (1983) Specific attachment of desmin filaments to desmosomal plaques in cardiac myocytes. EMBO J 2(5):735-742.
30. Kartenbeck, J., Schwechheimer, K., Moll, R. and Franke, W.W. (1984) Attachment of vimentin filaments to desmosomal plaques in human meningiomal cells and arachnoidal tissue. J Cell Biol 98:1072-1081.
31. Kay, L., Li, Z., Mericskay, M., Olivares, J., Tranqui, L., Fontaine, E., Tiivel, T., Sikk, P., Kaambre, T., Samuel, J.L., Rappaport, L., Usson, Y., Leverve, X., Paulin, D. and Saks, V.A. (1997) Study of regulation of mitochondrial respiration in vivo. An analysis of influence of ADP diffusion and possible role of cytoskeleton. Biochim Biophys Acta 1322:41-59.
32. Kopito, R.R. (2000) Aggresomes, inclusion bodies and protein aggregation. Trends Cell Biology 10:524-530.
33. Kouklis, P.D., Hutton, E. and Fuchs, E. (1994) Making a connection: direct binding between keratin intermediate filaments and desmosomal proteins. J Cell Biol 127:1049-1060.
34. Lloyd, C., Yu, Q.C., Cheng, J., Turksen, K., Degenstein, L., Hutton, E. and Fuchs, E. (1995) The basal keratin network of stratified squamous epithelia: defining K15 function in the absence of K14. J Cell Biol 129:1329-1344.
35. Magin, T.M., Kaiser, H.W., Leitgeb, S., Grund, C., Leigh, I.M., Morley, S.M. and Lane, E.B. (2000) Supplementation of a mutant keratin by stable expression of desmin in cultured human EBS keratinocytes. J Cell Sci 113:4231-4239.
36. Magin, T.M., Schroder, R., Leitgeb, S., Wanninger, F., Zatloukal, K., Grund, C. and Melton, D.W. (1998) Lessons from keratin 18 knockout mice: formation of novel keratin filaments, secondary loss of keratin 7 and accumulation of liver-specific keratin 8-positive aggregates. J Cell Biol 140:1441-1451.
37. McGowan, K. and Coulombe, P.A. (1998) The wound repair-associated keratins 6, 16, and 17. Insights into the role of intermediate filaments in specifying keratinocyte cytoarchitecture. Subcell Biochem 31:173-204.
38. McLean, W.H. and Lane, E.B. (1995) Intermediate filaments in disease. Curr Opin Cell Biol 7:118-125.
39. Meng, J.J., Bornslaeger, E.A., Green, K.J., Steinert, P.M. and Ip, W. (1997) Two-hybrid analysis reveals fundamental differences in direct interactions between desmoplakin and cell type-specific intermediate filaments. J Biol Chem 272:21495-21503.
40. Messing, A., Head, M.W., Galles, K., Galbreath, E.J., Goldman, J.E. and Brenner, M. (1998) Fatal encephalopathy with astrocyte inclusions in GFAP transgenic mice. Am J Pathol 152:391-398.
41. Milner, D.J., Mavroidis, M., Weisleder, N. and Capetanaki, Y. (2000) Desmin cytoskeleton linked to muscle mitochondrial distribution and respiratory function. J Cell Biol 150:1283-1298.
42. Milner, D.J., Taffet, G.E., Wang, X., Pham, T., Tamura, T., Hartley, C., Gerdes, A.M. and Capetanaki, Y. (1999) The absence of desmin leads to cardiomyocyte hypertrophy and cardiac dilation with compromised systolic function. J Mol Cell Cardiol 31:2063-2076.
43. Milner, D.J., Weitzer, G., Tran, D., Bradley, A. and Capetanaki, Y. (1996) Disruption of muscle architecture and myocardial degeneration in mice lacking desmin. J Cell Biol 134:1255-1270.
44. Munoz-Marmol, A.M., Strasser, G., Isamat, M., Coulombe, P.A., Yang, Y., Roca, X., Vela, E., Mate, J.L., Coll, J., Fernandez-Figueras, M.T., Navas-Palacios, J.J., Ariza, A. and Fuchs, E. (1998) A dysfunctional desmin mutation in a patient with severe generalized myopathy. Proc Natl Acad Sci USA 95:11312-11317.
45. Perng, M.D., Cairns, L., van Den, I.J., Prescott, A., Hutcheson, A.M. and Quinlan, R.A. (1999a) Intermediate filament interactions can be altered by HSP27 and alphaB-crystallin. J Cell Sci 112:2099-2112.
46. Perng, M.D., Muchowski, P.J., van Den, I.J., Wu, G.J., Hutcheson, A.M., Clark, J.I. and Quinlan, R.A. (1999b) The cardiomyopathy and lens cataract mutation in alphaB-crystallin alters its protein structure, chaperone activity, and interaction with intermediate filaments in vitro. J Biol Chem 274:33235-33243.
47. Peters, B., Kirfel, J., Bussow, H., Vidal, M. and Magin, T.M. (2001) Complete cytolysis and neonatal lethality in keratin 5 knockout mice reveal its fundamental role in skin integrity and in epidermolysis bullosa simplex. Mol Biol Cell 12:1775-1789.
48. Pieper, F.R., Raats, J.M., Schaart, G., Dunia, I., van-der, K.A., Benedetti, E.L., Ramaekers, F.C. and Bloemendal, H. (1995) Disruption of vimentin intermediate filaments in transgenic mice by expression of a dominant negative mutant desmin subunit. Eur J Cell Biol 68:355-368.
49. Quinlan, R.A. and Franke, W.W. (1982) Heteropolymer filaments of vimentin and desmin in vascular smooth muscle tissue and cultured baby hamster kidney cells demonstrated by chemical crosslinking. Proc Natl Acad Sci USA 79:3452-3456.
50. Ramirez, A., Bravo, A., Jorcano, J.L. and Vidal, M. (1994) Sequences 5′ of the bovine keratin 5 gene direct tissue-and cell-type-specific expression of a lacZ gene in the adult and during development. Differentiation 58:53-64.
51. Reipert, S., Steinbock, F., Fischer, I., Bittner, R.E., Zeold, A. and Wiche, G. (1999) Association of mitochondria with plectin and desmin intermediate filaments in striated muscle. Exp Cell Res 252:479-491.
52. Roop, D.R., Huitfeldt, H., Kilkenny, A. and Yuspa, S.H. (1987) Regulated expression of differentiation-associated keratins in cultured epidermal cells detected by monospecific antibodies to unique peptides of mouse epidermal keratins. Differentiation 35:143-150.
53. Ruhrberg, C. and Watt, F.M. (1997) The plakin family: versatile organizers of cytoskeletal architecture. Curr Opin Genet Dev 7:392-397.
54. Schluter, C., Duchrow, M., Wohlenberg, C., Becker, M.H., Key, G., Flad, H.D. and Gerdes, J. (1993) The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J Cell Biol 123:513-522.
55. Schroder, R., Warlo, I., Herrmann, H., van der Ven, P.F., Klasen, C., Blumcke, I., Mundegar, R.R., Furst, D.O., Goebel, H.H. and Magin, T.M. (1999) Immunogold EM reveals a close association of plectin and the desmin cytoskeleton in human skeletal muscle. Eur J Cell Biol 78:288-295.
56. Schweitzer, S.C., Klymkowsky, M.W., Bellin, R.M., Robson, R.M., Capetanaki, Y. and Evans, R.M. (2001) Paranemin and the organization of desmin filament networks. J Cell Sci 114:1079-1089.
57. Smith, E.A. and Fuchs, E. (1998) Defining the interactions between intermediate filaments and desmosomes. J Cell Biol 141:1229-1241.
58. Sonnenberg, A., Calafat, J., Janssen, H., Daams, H., van der Raaij-Helmer, LM, Falcioni, R., Kennel, S.J., Aplin, J.D., Baker, J., Loizidou, M. and Garrod, D. (1991) Integrin alpha 6/beta 4 complex is located in hemidesmosomes, suggesting a major role in epidermal cell-basement membrane adhesion. J Cell Biol 113:907-917.
59. Stappenbeck, T.S. and Green, K.J. (1992) The desmoplakin carboxyl terminus coaligns with and specifically disrupts intermediate filament networks when expressed in cultured cells. J Cell Biol 116:1197-1209.
60. Steinbock, F.A., Nikolic, B., Coulombe, P.A., Fuchs, E., Traub, P. and Wiche, G. (2000) Dose-dependent linkage, assembly inhibition and disassembly of vimentin and cytokeratin 5/14 filaments through plectin's intermediate filament-binding domain. J Cell Sci 113:483-491.
61. Thornell, L., Carlsson, L., Li, Z., Mericskay, M. and Paulin, D. (1997) Null mutation in the desmin gene gives rise to a cardiomyopathy. J Mol Cell Cardiol 29:2107-2124.
62. Wiche, G. (1998) Role of plectin in cytoskeleton organization and dynamics. J Cell Sci 111:2477-2486.
63. Wojcik, S.M., Longley, M.A. and Roop, D.R. (2001) Discovery of a novel murine keratin 6 (K6) isoform explains the absence of hair and nail defects in mice deficient for K6a and K6b. J Cell Biol 154:619-630.
64. Yu, K.R., Hijikata, T., Lin, Z.X., Sweeney, H.L., Englander, S.W. and Holtzer, H. (1994) Truncated desmin in PtK2 cells induces desmin-vimentin- cytokeratin coprecipitation, involution of intermediate filament networks, and nuclear fragmentation: a model for many degenerative diseases. Proc Natl Acad Sci USA 91:2497-2501.