Dual color photoactivation localization microscopy of cardiomyopathy- associated desmin mutants

Journal of Biological Chemistry

Volumn 287, Issue 19, 2012, Pages 16047-16057

  Brodehl, Andreas ^a   Hedde, Per Niklas ^b   Dieding, Mareike ^c   Fatima, Azra ^d   Walhorn, Volker ^c   Gayda, Susan ^b   Šarić, Tomo ^d   Klauke, Bärbel ^a   Gummert, Jan ^a   Anselmetti, Dario ^c   Heilemann, Mike ^e   Nienhaus, Gerd Ulrich ^b,f   Milting, Hendrik ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c BIELEFELD UNIVERSITY   (Germany)

^d UNIVERSITY OF COLOGNE   (Germany)

^e UNIVERSITY OF WÜRZBURG   (Germany)

^f University of Illinois at Urbana Champaign   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR LEVELS; DUAL COLOR; FILAMENT FORMATION; FILAMENT STRUCTURE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FLUORESCENT PROTEIN; GENE CODING; HIGH RESOLUTION DATA; IN-VITRO; IN-VIVO; INTERMEDIATE FILAMENTS; LIVING CELL; MOLECULAR UNDERSTANDING; PHOTOACTIVATABLE; PHOTOACTIVATION; RIGHT VENTRICULAR; SHORT DISTANCES; STRUCTURAL EFFECT; STRUCTURAL PATTERN;

ATOMIC FORCE MICROSCOPY; DEFECTS; ENERGY TRANSFER; FLUORESCENCE; GENES;

PROTEINS;

DESMIN;

ARTICLE; CARDIOMYOPATHY; CONTROLLED STUDY; DES GENE; DUAL COLOR PHOTOACTIVATION LOCALIZATION MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENE; GENE MUTATION; GENETIC HETEROGENEITY; HETEROZYGOSITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MICROSCOPY; PHOTOACTIVATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

ANIMALS; CARDIOMYOPATHIES; CELL LINE; CELL LINE, TUMOR; DESMIN; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMANS; IMMUNOBLOTTING; INTERMEDIATE FILAMENTS; LUMINESCENT MEASUREMENTS; LUMINESCENT PROTEINS; MICROSCOPY; MICROSCOPY, ATOMIC FORCE; MICROSCOPY, FLUORESCENCE; MUTANT PROTEINS; MUTATION; PROTEIN BINDING; TRANSFECTION;

EID: 84860868750     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.313841     Document Type: Article

References (47)

1. Goldfarb, L. G., Park, K. Y., Cervenáková, 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 (Pubitemid 28357917)
2. Goldfarb, L. G., and Dalakas, M. C. (2009) Tragedy in a heartbeat. Malfunctioning desmin causes skeletal and cardiac muscle disease. J. Clin. Invest. 119, 1806-1813
3. Muñoz-Mármol, A. M., Strasser, G., Isamat, M., Coulombe, P. A., Yang, Y., Roca, X., Vela, E., Mate, J. L., Coll, J., Fernández- 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. U.S.A. 95, 11312-11317 (Pubitemid 28450125)
4. Hong, D., Wang, Z., Zhang, W., Xi, J., Lu, J., Luan, X., and Yuan, Y. (2011) A series of Chinese patients with desminopathy associated with six novel and one reported mutations in the desmin gene. Neuropathol Appl. Neurobiol. 37, 257-270
5. Bär, H., Strelkov, S. V., Sjöberg, G., Aebi, U., and Herrmann, H. (2004) The biology of desmin filaments. How do mutations affect their structure, assembly, and organisation? J. Struct. Biol. 148, 137-152 (Pubitemid 39346004)
6. van Tintelen, J. P., Van Gelder, I. C., Asimaki, A., Suurmeijer, A. J., Wiesfeld, A. C., Jongbloed, J. D., van den Wijngaard, A., Kuks, J. B., van Spaendonck-Zwarts, K. Y., Notermans, N., Boven, L., van den Heuvel, F., Veenstra-Knol, H. E., Saffitz, J. E., Hofstra, R. M., and van den Berg, M. P. (2009) Severe cardiac phenotype with right ventricular predominance in a large cohort of patients with a single missense mutation in the DES gene. Heart Rhythm 6, 1574-1583
7. Otten, E., Asimaki, A., Maass, A., van Langen, I. M., van der Wal, A., de Jonge, N., van den Berg, M. P., Saffitz, J. E., Wilde, A. A., Jongbloed, J. D., and van Tintelen, J. P. (2010) Desmin mutations as a cause of right ventricular heart failure affect the intercalated disks. Heart Rhythm 7, 1058-1064
8. Klauke, B., Kossmann, S., Gaertner, A., Brand, K., Stork, I., Brodehl, A., Dieding, M., Walhorn, V., Anselmetti, D., Gerdes, D., Bohms, B., Schulz, U., Zu Knyphausen, E., Vorgerd, M., Gummert, J., and Milting, H. (2010) De novo desmin-mutation N116S is associated with arrhythmogenic right ventricular cardiomyopathy. Hum. Mol. Genet 19, 4595-4607
9. Vernengo, L., Chourbagi, O., Panuncio, A., Lilienbaum, A., Batonnet-Pichon, S., Bruston, F., Rodrigues-Lima, F., Mesa, R., Pizzarossa, C., Demay, L., Richard, P., Vicart, P., and Rodriguez, M. M. (2010) Desmin myopathy with severe cardiomyopathy in a Uruguayan family due to a codon deletion in a new location within the desmin 1A rod domain. Neuromuscul. Disord. 20, 178-187
10. 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, 735-742
11. Capetanaki, Y., Bloch, R. J., Kouloumenta, A., Mavroidis, M., and Psarras, S. (2007) Muscle intermediate filaments and their links to membranes and membranous organelles. Exp. Cell Res. 313, 2063-2076 (Pubitemid 46842980)
12. Herrmann, H., and Aebi, U. (2004) Intermediate filaments. Molecular structure, assembly mechanism, and integration into functionally distinct intracellular Scaffolds. Annu. Rev. Biochem. 73, 749-789 (Pubitemid 39050385)
13. Nicolet, S., Herrmann, H., Aebi, U., and Strelkov, S. V. (2010) Atomic structure of vimentin coil 2. J. Struct. Biol. 170, 369-376
14. Chernyatina, A. A., Nicolet, S., and Strelkov, S. V. (2011) 7th European Conference on Intermediate Filaments in Health and Disease, Mykonos, Greece, June 16-19, 2011 (Capetanaki, Y., and Mavroidis, M., eds) European Society for Intermediate Filament Biology
15. Herrmann, H., Strelkov, S. V., Burkhard, P., and Aebi, U. (2009) Intermediate filaments. Primary determinants of cell architecture and plasticity. J. Clin. Invest. 119, 1772-1783
16. Bar, H., Fischer, D., Goudeau, B., Kley, R. A., Clemen, C. S., Vicart, P., Herrmann, H., Vorgerd, M., and Schroder, R. (2005) Pathogenic effects of a novel heterozygous R350P desmin mutation on the assembly of desmin intermediate filaments in vivo and in vitro. Hum. Mol. Genet 14, 1251-1260 (Pubitemid 40744485)
17. Sharma, S., Mücke, N., Katus, H. A., Herrmann, H., and Bär, H. (2009) Disease mutations in the "head" domain of the extra-sarcomeric protein desmin distinctly alter its assembly and network-forming properties. J. Mol. Med. 87, 1207-1219
18. Claycomb, W. C., Lanson, N. A., Jr., Stallworth, B. S., Egeland, D. B., Delcarpio, J. B., Bahinski, A., and Izzo, N. J., Jr. (1998) HL-1 cells. A cardiac muscle cell line that contracts and retains phenotypic characteristics of the adult cardiomyocyte. Proc. Natl. Acad. Sci. U.S.A. 95, 2979-2984 (Pubitemid 28135840)
19. Yu, J., Vodyanik, M. A., Smuga-Otto, K., Antosiewicz-Bourget, J., Frane, J. L., Tian, S., Nie, J., Jonsdottir, G. A., Ruotti, V., Stewart, R., Slukvin, I. I., and Thomson, J. A. (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 1917-1920
20. Mummery, C., Ward-van Oostwaard, D., Doevendans, P., Spijker, R., van den Brink, S., Hassink, R., van der Heyden, M., Opthof, T., Pera, M., de la Riviere, A. B., Passier, R., and Tertoolen, L. (2003) Differentiation of human embryonic stem cells to cardiomyocytes. Role of coculture with visceral endoderm-like cells. Circulation 107, 2733-2740
21. Gupta, M. K., Illich, D. J., Gaarz, A., Matzkies, M., Nguemo, F., Pfannkuche, K., Liang, H., Classen, S., Reppel, M., Schultze, J. L., Hescheler, J., and Sarić, T. (2010) Global transcriptional profiles of beating clusters derived from human induced pluripotent stem cells and embryonic stem cells are highly similar. BMC Dev. Biol. 10, 98
22. Kreplak, L., Bär, H., Leterrier, J. F., Herrmann, H., and Aebi, U. (2005) Exploring the mechanical behavior of single intermediate filaments. J. Mol. Biol. 354, 569-577 (Pubitemid 41628276)
23. Hedde, P. N., Fuchs, J., Oswald, F., Wiedenmann, J., and Nienhaus, G. U. (2009) Online image analysis software for photoactivation localization microscopy. Nat. Methods 6, 689-690
24. Fuchs, J., Böhme, S., Oswald, F., Hedde, P. N., Krause, M., Wiedenmann, J., and Nienhaus, G. U. (2010) A photoactivatable marker protein for pulse-chase imaging with superresolution. Nat. Methods 7, 627-630
25. Shroff, H., Galbraith, C. G., Galbraith, J. A., White, H., Gillette, J., Olenych, S., Davidson, M. W., and Betzig, E. (2007) Dual-color superresolution imaging of genetically expressed probes within individual adhesion complexes. Proc. Natl. Acad. Sci. U.S.A. 104, 20308-20313
26. Clegg, R. M. (1992) Fluorescence resonance energy transfer and nucleic acids. Methods Enzymol. 211, 353-388
27. Hachet-Haas, M., Converset, N., Marchal, O., Matthes, H., Gioria, S., Galzi, J. L., and Lecat, S. (2006) FRET and colocalization analyzer. A method to validate measurements of sensitized emission FRET acquired by confocal microscopy and available as an ImageJ Plug-in. Microsc. Res. Tech. 69, 941-956 (Pubitemid 44888237)
28. Levin, J., Bulst, S., Thirion, C., Schmidt, F., Bötzel, K., Krause, S., Pertl, C., Kretzschmar, H., Walter, M. C., Giese, A., and Lochmüller, H. (2010) Divergent molecular effects of desmin mutations on protein assembly in myofibrillar myopathy. J. Neuropathol. Exp. Neurol. 69, 415-424
29. Dalakas, M. C., Dagvadorj, A., Goudeau, B., Park, K. Y., Takeda, K., Simon-Casteras, M., Vasconcelos, O., Sambuughin, N., Shatunov, A., Nagle, J. W., Sivakumar, K., Vicart, P., and Goldfarb, L. G. (2003) Progressive skeletal myopathy, a phenotypic variant of desmin myopathy associated with desmin mutations. Neuromuscul. Disord. 13, 252-258 (Pubitemid 36279430)
30. Hedberg, K. K., and Chen, L. B. (1986) Absence of intermediate filaments in a human adrenal cortex carcinoma-derived cell line. Exp. Cell Res. 163, 509-517 (Pubitemid 16077149)
31. Nienhaus, K., Nienhaus, G. U., Wiedenmann, J., and Nar, H. (2005) Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP. Proc. Natl. Acad. Sci. U.S.A. 102, 9156-9159 (Pubitemid 40923533)
32. Wiedenmann, J., Ivanchenko, S., Oswald, F., Schmitt, F., Röcker, C., Salih, A., Spindler, K. D., and Nienhaus, G. U. (2004) EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion. Proc. Natl. Acad. Sci. U.S.A. 101, 15905-15910 (Pubitemid 39507900)
33. Nienhaus, G. U., Nienhaus, K., Hölzle, A., Ivanchenko, S., Renzi, F., Oswald, F., Wolff, M., Schmitt, F., Röcker, C., Vallone, B., Weidemann, W., Heilker, R., Nar, H., and Wiedenmann, J. (2006) Photoconvertible fluorescent protein EosFP. Biophysical properties and cell biology applications. Photochem. Photobiol. 82, 351-358
34. Adam, V., Lelimousin, M., Boehme, S., Desfonds, G., Nienhaus, K., Field, M. J., Wiedenmann, J., McSweeney, S., Nienhaus, G. U., and Bourgeois, D. (2008) Structural characterization of IrisFP, an optical highlighter undergoing multiple photo-induced transformations. Proc. Natl. Acad. Sci. U.S.A. 105, 18343-18348
35. Wiedenmann, J., Gayda, S., Adam, V., Oswald, F., Nienhaus, K., Bourgeois, D., and Nienhaus, G. U. (2011) From EosFP to mIrisFP. Structure-based development of advanced photoactivatable marker proteins of the GFP-family. J. Biophotonics 4, 377-390
36. Andresen, M., Stiel, A. C., Fölling, J., Wenzel, D., Schönle, A., Egner, A., Eggeling, C., Hell, S. W., and Jakobs, S. (2008) Photoswitchable fluorescent proteins enable monochromatic multilabel imaging and dual color fluorescence nanoscopy. Nat. Biotechnol. 26, 1035-1040
37. van Spaendonck-Zwarts, K., van Hessem, L., Jongbloed, J. D., de Walle, H. E., Capetanaki, Y., van der Kooi, A. J., van Langen, I. M., van den Berg, M. P., and van Tintelen, J. P. (2010) Clin. Genet. 89, 354-366
38. Hedde, P. N., and Nienhaus, G. U. (2010) Optical imaging of nanoscale cellular structures. Biophys. Rev. 2, 147-158
39. Raats, J. M., Pieper, F. R., Vree Egberts, W. T., Verrijp, K. N., Ramaekers, F. C., and Bloemendal, H. (1990) Assembly of amino-terminally deleted desmin in vimentin-free cells. J. Cell Biol. 111, 1971-1985
40. Kitamura, S., Ando, S., Shibata, M., Tanabe, K., Sato, C., and Inagaki, M. (1989) Protein kinase C phosphorylation of desmin at four serine residues within the non-α-helical head domain. J. Biol. Chem. 264, 5674-5678 (Pubitemid 19098028)
41. Pica, E. C., Kathirvel, P., Pramono, Z. A., Lai, P. S., and Yee, W. C. (2008) Characterization of a novel S13F desmin mutation associated with desmin myopathy and heart block in a Chinese family. Neuromuscul. Disord. 18, 178-182 (Pubitemid 351289088)
42. Chourbagi, O., Bruston, F., Carinci, M., Xue, Z., Vicart, P., Paulin, D., and Agbulut, O. (2011) Desmin mutations in the terminal consensus motif prevent synemin-desmin heteropolymer filament assembly. Exp. Cell Res. 317, 886-897
43. Bär, H., Mücke, N., Kostareva, A., Sjöberg, G., Aebi, U., and Herrmann, H. (2005) Severe muscle disease-causing desmin mutations interfere with in vitro filament assembly at distinct stages. Proc. Natl. Acad. Sci. U.S.A. 102, 15099-15104 (Pubitemid 41513341)
44. Bär, H., Goudeau, B., Wälde, S., Casteras-Simon, M., Mücke, N., Shatunov, A., Goldberg, Y. P., Clarke, C., Holton, J. L., Eymard, B., Katus, H. A., Fardeau, M., Goldfarb, L., Vicart, P., and Herrmann, H. (2007) Conspicuous involvement of desmin tail mutations in diverse cardiac and skeletal myopathies. Hum. Mutat. 28, 374-386 (Pubitemid 46542924)
45. Ando, S., Nakao, K., Gohara, R., Takasaki, Y., Suehiro, K., and Oishi, Y. (2004) Morphological analysis of glutaraldehyde-fixed vimentin intermediate filaments and assembly-intermediates by atomic force microscopy. Biochim. Biophys. Acta 1702, 53-65 (Pubitemid 39265469)
46. Bär, H., Schopferer, M., Sharma, S., Hochstein, B., Mücke, N., Herrmann, H., and Willenbacher, N. (2010) Mutations in desmin's carboxy-terminal "tail" domain severely modify filament and network mechanics. J. Mol. Biol. 397, 1188-1198
47. Helfand, B. T., Chang, L., and Goldman, R. D. (2003) The dynamic and motile properties of intermediate filaments. Annu. Rev. Cell Dev. Biol. 19, 445-467 (Pubitemid 37487356)