Mislocalization of fukutin protein by disease-causing missense mutations can be rescued with treatments directed at folding amelioration

Journal of Biological Chemistry

Volumn 287, Issue 11, 2012, Pages 8398-8406

  Tachikawa, Masaji ^a   Kanagawa, Motoi ^a   Yu, Chih Chieh ^a   Kobayashi, Kazuhiro ^a   Toda, Tatsushi ^a  

^a KOBE UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACES; CELLULAR LOCALIZATION; CURCUMIN; ENDOPLASMIC RETICULUM; GOLGI APPARATUS; LAMININ; LOW TEMPERATURES; MISLOCALIZATION; MISSENSE MUTANTS; MOLECULAR PATHOGENESIS; MOUSE EMBRYONIC STEM CELLS; MUSCULAR DYSTROPHY; MUTANT PROTEINS; MYOBLAST CELLS; NOCODAZOLE; PATHOPHYSIOLOGICAL; POINT MUTATIONS; SUBCELLULAR LOCATION; THERAPEUTIC BENEFITS; WILD TYPES;

CELL CULTURE; CELL MEMBRANES; ESTERIFICATION; GENES; GLYCOSYLATION;

PROTEINS;

ALPHA DYSTROGLYCAN; BREFELDIN A; CURCUMIN; FUKUTIN; LAMININ; MUTANT PROTEIN; N ACETYLGLUCOSAMINYLTRANSFERASE; NOCODAZOLE; PROTEIN O MANNOSE BETA 1,2 N ACETYLGLUCOSAMINYLTRANSFERASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYONIC STEM CELL; ENDOPLASMIC RETICULUM; FUKUTIN DEFICIENT MUSCULAR DYSTROPHY; GLYCOSYLATION; GOLGI COMPLEX; LOW TEMPERATURE; MISSENSE MUTATION; MOLECULAR PATHOLOGY; MOUSE; MUSCULAR DYSTROPHY; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; WILD TYPE;

AMINO ACID SUBSTITUTION; ANIMALS; ANTINEOPLASTIC AGENTS; BREFELDIN A; CELL LINE; DYSTROGLYCANS; GLYCOSYLATION; HUMANS; MICE; MICE, MUTANT STRAINS; MUTATION, MISSENSE; N-ACETYLGLUCOSAMINYLTRANSFERASES; NOCODAZOLE; PROTEIN FOLDING; PROTEIN SYNTHESIS INHIBITORS; PROTEIN TRANSPORT; PROTEINS; WALKER-WARBURG SYNDROME;

EID: 84858061102     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.300905     Document Type: Article

References (43)

1. Fukuyama, Y., Osawa, M., and Suzuki, H. (1981) Congenital progressive muscular dystrophy of the Fukuyama type: clinical, genetic and pathological considerations. Brain Dev. 3, 1-29 (Pubitemid 11125887)
2. Toda, T., Segawa, M., Nomura, Y., Nonaka, I., Masuda, K., Ishihara, T., Sakai, M., Tomita, I., Origuchi, Y., Ohno, K., Misugi, N., Sasaki, Y., Takada, K., Kawai, M., Otani, K., Murakami, T., Saito, K., Fukuyama, Y., Shimizu, T., Kanazawa, I., and Nakamura, Y. (1993) Localization of a gene for Fukuyama- type congenital muscular dystrophy to chromosome 9q31-33. Nat. Genet. 5, 283-286 (Pubitemid 23330394)
3. Kobayashi, K., Nakahori, Y., Miyake, M., Matsumura, K., Kondo-Iida, E., Nomura, Y., Segawa, M., Yoshioka, M., Saito, K., Osawa, M., Hamano, K., Sakakihara, Y., Nonaka, I., Nakagome, Y., Kanazawa, I., Nakamura, Y., Tokunaga, K., and Toda, T. (1998) An ancient retrotransposal insertion causes Fukuyama-type congenital muscular dystrophy. Nature 394, 388-392 (Pubitemid 28373837)
4. Kondo-Iida, E., Kobayashi, K., Watanabe, M., Sasaki, J., Kumagai, T., Koide, H., Saito, K., Osawa, M., Nakamura, Y., and Toda, T. (1999) Novel mutations and genotype-phenotype relationships in 107 families with Fukuyama- type congenital muscular dystrophy (FCMD). Hum. Mol. Genet. 8, 2303-2309 (Pubitemid 29525346)
5. Kobayashi, K., Sasaki, J., Kondo-Iida, E., Fukuda, Y., Kinoshita, M., Sunada, Y., Nakamura, Y., and Toda, T. (2001) Structural organization, complete genomic sequences and mutational analyses of the Fukuyama-type congenital muscular dystrophy gene, fukutin. FEBS Lett. 489, 192-196 (Pubitemid 32126407)
6. Murakami, T., Hayashi, Y. K., Noguchi, S., Ogawa, M., Nonaka, I., Tanabe, Y., Ogino, M., Takada, F., Eriguchi, M., Kotooka, N., Campbell, K. P., Osawa, M., and Nishino, I. (2006) Fukutin gene mutations cause dilated cardiomyopathy with minimal muscle weakness. Ann. Neurol. 60, 597-602 (Pubitemid 44871802)
7. Silan, F., Yoshioka, M., Kobayashi, K., Simsek, E., Tunc, M., Alper, M., Cam, M., Guven, A., Fukuda, Y., Kinoshita, M., Kocabay, K., and Toda, T. (2003)Anew mutation of the fukutin gene in a non-Japanese patient. Ann. Neurol. 53, 392-396 (Pubitemid 36258644)
8. de Bernabé, D. B., van Bokhoven, H., van Beusekom, E., Van den Akker, W., Kant, S., Dobyns, W. B., Cormand, B., Currier, S., Hamel, B., Talim, B., Topaloglu, H., and Brunner, H. G. (2003) A homozygous nonsense mutation in the fukutin gene causes a Walker-Warburg syndrome phenotype. J. Med. Genet. 40, 845-848 (Pubitemid 37485497)
9. Godfrey, C., Escolar, D., Brockington, M., Clement, E. M., Mein, R., Jimenez- Mallebrera, C., Torelli, S., Feng, L., Brown, S. C., Sewry, C. A., Rutherford, M., Shapira, Y., Abbs, S., and Muntoni, F. (2006) Fukutin gene mutations in steroid-responsive limb girdle muscular dystrophy. Ann. Neurol. 60, 603-610 (Pubitemid 44871803)
10. Godfrey, C., Clement, E., Mein, R., Brockington, M., Smith, J., Talim, B., Straub, V., Robb, S., Quinlivan, R., Feng, L., Jimenez-Mallebrera, C., Mercuri, E., Manzur, A. Y., Kinali, M., Torelli, S., Brown, S. C., Sewry, C. A., Bushby, K., Topaloglu, H., North, K., Abbs, S., and Muntoni, F. (2007) Refining genotype phenotype correlations in muscular dystrophies with defective glycosylation of dystroglycan. Brain 130, 2725-2735 (Pubitemid 47511718)
11. Cotarelo, R. P., Valero, M. C., Prados, B., Peña, A., Rodríguez, L., Fano, O., Marco, J. J., Martínez-Frías, M. L., and Cruces, J. (2008) Two new patients bearing mutations in the fukutin gene confirm the relevance of this gene in Walker-Warburg syndrome. Clin. Genet. 73, 139-145
12. Manzini, M. C., Gleason, D., Chang, B. S., Hill, R. S., Barry, B. J., Partlow, J. N., Poduri, A., Currier, S., Galvin-Parton, P., Shapiro, L. R., Schmidt, K., Davis, J. G., Basel-Vanagaite, L., Seidahmed, M. Z., Salih, M. A., Dobyns, W. B., and Walsh, C. A. (2008) Ethnically diverse causes of Walker-Warburg syndrome (WWS): FCMD mutations are a more common cause of WWS outside of the Middle East. Hum. Mutat. 29, E231-E241
13. Vuillaumier-Barrot, S., Quijano-Roy, S., Bouchet-Seraphin, C., Maugenre, S., Peudenier, S., Van den Bergh, P., Marcorelles, P., Avila-Smirnow, D., Chelbi, M., Romero, N. B., Carlier, R. Y., Estournet, B., Guicheney, P., and Seta, N. (2009) Four Caucasian patients with mutations in the fukutin gene and variable clinical phenotype. Neuromuscul. Disord. 19, 182-188
14. Michele, D. E., Barresi, R., Kanagawa, M., Saito, F., Cohn, R. D., Satz, J. S., Dollar, J., Nishino, I., Kelley, R. I., Somer, H., Straub, V., Mathews, K. D., Moore, S. A., and Campbell, K. P. (2002) Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418, 417-422 (Pubitemid 34826841)
15. Matsumoto, H., Noguchi, S., Sugie, K., Ogawa, M., Murayama, K., Hayashi, Y. K., and Nishino, I. (2004) Subcellular localization of fukutin and fukutin-related protein in muscle cells. J. Biochem. 135, 709-712 (Pubitemid 38899718)
16. Xiong, H., Kobayashi, K., Tachikawa, M., Manya, H., Takeda, S., Chiyonobu, T., Fujikake, N., Wang, F., Nishimoto, A., Morris, G. E., Nagai, Y., Kanagawa, M., Endo, T., and Toda, T. (2006) Molecular interaction between fukutin and POMGnT1 in the glycosylation pathway of α-dystroglycan. Biochem. Biophys. Res. Commun. 350, 935-941 (Pubitemid 44584182)
17. Aravind, L., and Koonin, E. V. (1999) The fukutin protein family: predicted enzymes modifying cell surface molecules. Curr. Biol. 9, R836-837
18. Yoshida, A., Kobayashi, K., Manya, H., Taniguchi, K., Kano, H., Mizuno, M., Inazu, T., Mitsuhashi, H., Takahashi, S., Takeuchi, M., Herrmann, R., Straub, V., Talim, B., Voit, T., Topaloglu, H., Toda, T., and Endo, T. (2001) Muscular dystrophy and neuronal migration disorder caused by mutations in a glycosyltransferase, POMGnT1. Dev. Cell 1, 717-724 (Pubitemid 33586123)
19. Beltrán-Valero de Bernabé, D., Currier, S., Steinbrecher, A., Celli, J., van Beusekom, E., van der Zwaag, B., Kayserili, H., Merlini, L., Chitayat, D., Dobyns, W. B., Cormand, B., Lehesjoki, A. E., Cruces, J., Voit, T., Walsh, C. A., van Bokhoven, H., and Brunner, H. G. (2002) Mutations in the O-mannosyltransferase gene POMT1 give rise to the severe neuronal migration disorder Walker-Warburg syndrome. Am. J. Hum. Genet. 71, 1033-1043 (Pubitemid 35305223)
20. van Reeuwijk, J., Janssen, M., van den Elzen, C., Beltran-Valero de Bernabé, D., Sabatelli, P., Merlini, L., Boon, M., Scheffer, H., Brockington, M., Muntoni, F., Huynen, M. A., Verrips, A., Walsh, C. A., Barth, P. G., Brunner, H. G., and van Bokhoven, H. (2005) POMT2 mutations cause α-dystroglycan hypoglycosylation and Walker-Warburg syndrome. J. Med. Genet. 42, 907-912 (Pubitemid 41811312)
21. Brockington, M., Blake, D. J., Prandini, P., Brown, S. C., Torelli, S., Benson, M. A., Ponting, C. P., Estournet, B., Romero, N. B., Mercuri, E., Voit, T., Sewry, C. A., Guicheney, P., and Muntoni, F. (2001) Mutations in the fukutin-related protein gene (FKRP) cause a form of congenital muscular dystrophy with secondary laminin α2 deficiency and abnormal glycosylation of α-dystroglycan. Am. J. Hum. Genet. 69, 1198-1209 (Pubitemid 33124201)
22. Brockington, M., Yuva, Y., Prandini, P., Brown, S. C., Torelli, S., Benson, M. A., Herrmann, R., Anderson, L. V., Bashir, R., Burgunder, J. M., Fallet, S., Romero, N., Fardeau, M., Straub, V., Storey, G., Pollitt, C., Richard, I.,Sewry, C. A., Bushby, K., Voit, T., Blake, D. J., and Muntoni, F. (2001) Mutations in the fukutin-related protein gene (FKRP) identify limb girdle muscular dystrophy 2I as a milder allelic variant of congenital muscular dystrophy MDC1C. Hum. Mol. Genet. 10, 2851-2859 (Pubitemid 34030916)
23. Longman, C., Brockington, M., Torelli, S., Jimenez-Mallebrera, C., Kennedy, C., Khalil, N., Feng, L., Saran, R. K., Voit, T., Merlini, L., Sewry, C. A., Brown, S. C., and Muntoni, F. (2003) Mutations in the human LARGE gene cause MDC1D, a novel form of congenital muscular dystrophy with severe mental retardation and abnormal glycosylation of α-dystroglycan. Hum. Mol. Genet. 12, 2853-2861 (Pubitemid 37407122)
24. Manya, H., Chiba, A., Yoshida, A., Wang, X., Chiba, Y., Jigami, Y., Margolis, R. U., and Endo, T. (2004) Demonstration of mammalian protein O-mannosyltransferase activity: co-expression of POMT1 and POMT2 required for enzymatic activity. Proc. Natl. Acad. Sci. U.S.A. 101, 500-505 (Pubitemid 38084665)
25. Inamori, K., Yoshida-Moriguchi, T., Hara, Y., Anderson, M. E., Yu, L., and Campbell, K. P. (2012) Dystroglycan function requires xylosyl- and glucuronyltransferase activities of LARGE. Science 335, 93-96
26. Yoshida-Moriguchi, T., Yu, L., Stalnaker, S. H., Davis, S., Kunz, S., Madson, M., Oldstone, M. B., Schachter, H., Wells, L., and Campbell, K. P. (2010) O-mannosyl phosphorylation of α-dystroglycan is required for laminin binding. Science 327, 88-92
27. Matsumoto, H., Hayashi, Y. K., Kim, D. S., Ogawa, M., Murakami, T., Noguchi, S., Nonaka, I., Nakazawa, T., Matsuo, T., Futagami, S., Campbell, K. P., and Nishino, I. (2005) Congenital muscular dystrophy with glycosylation defects of α-dystroglycan in Japan. Neuromuscul. Disord. 15, 342-348
28. Yoshioka, M., Higuchi, Y., Fujii, T., Aiba, H., and Toda, T. (2008) Seizuregenotype relationship in Fukuyama-type congenital muscular dystrophy. Brain Dev. 30, 59-67 (Pubitemid 350296751)
29. Kanagawa, M., Nishimoto, A., Chiyonobu, T., Takeda, S., Miyagoe-Suzuki, Y., Wang, F., Fujikake, N., Taniguchi, M., Lu, Z., Tachikawa, M., Nagai, Y., Tashiro, F., Miyazaki, J., Tajima, Y., Takeda, S., Endo, T., Kobayashi, K., Campbell, K. P., and Toda, T. (2009) Residual laminin binding activity and enhanced dystroglycan glycosylation by LARGE in novel model mice to dystroglycanopathy. Hum. Mol. Genet. 18, 621-631
30. Takeda, S., Kondo, M., Sasaki, J., Kurahashi, H., Kano, H., Arai, K., Misaki, K., Fukui, T., Kobayashi, K., Tachikawa, M., Imamura, M., Nakamura, Y., Shimizu, T., Murakami, T., Sunada, Y., Fujikado, T., Matsumura, K., Terashima, T., and Toda, T. (2003) Fukutin is required for maintenance of muscle integrity, cortical histiogenesis, and normal eye development. Hum. Mol. Genet. 12, 1449-1459 (Pubitemid 36758457)
31. Denning, G. M., Anderson, M. P., Amara, J. F., Marshall, J., Smith, A. E., and Welsh, M. J. (1992) Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358, 761-764
32. Cheng, S. H., Fang, S. L., Zabner, J., Marshall, J., Piraino, S., Schiavi, S. C., Jefferson, D. M., Welsh, M. J., and Smith, A. E. (1995) Functional activation of the cystic fibrosis trafficking mutant ΔF508-CFTR by overexpression. Am. J. Physiol. 268, L615-624
33. Egan, M. E., Pearson, M., Weiner, S. A., Rajendran, V., Rubin, D., Glöckner- Pagel, J., Canny, S., Du, K., Lukacs, G. L., and Caplan, M. J. (2004) Curcumin, a major constituent of turmeric, corrects cystic fibrosis defects. Science 304, 600-602 (Pubitemid 38541921)
34. Manya, H., Sakai, K., Kobayashi, K., Taniguchi, K., Kawakita, M., Toda, T., and Endo, T. (2003) Loss-of-function of an N-acetylglucosaminyltransferase, POMGnT1, in muscle-eye-brain disease. Biochem. Biophys. Res. Commun. 306, 93-97 (Pubitemid 36629409)
35. Akasaka-Manya, K., Manya, H., and Endo, T. (2004) Mutations of the POMT1 gene found in patients with Walker-Warburg syndrome lead to a defect of proteinO-mannosylation. Biochem. Biophys. Res. Commun. 325, 75-79 (Pubitemid 39441162)
36. Brockington, M., Torelli, S., Prandini, P., Boito, C., Dolatshad, N. F., Longman, C., Brown, S. C., and Muntoni, F. (2005) Localization and functional analysis of the LARGE family of glycosyltransferases: significance for muscular dystrophy. Hum. Mol. Genet. 14, 657-665 (Pubitemid 40309591)
37. Keramaris-Vrantsis, E., Lu, P. J., Doran, T., Zillmer, A., Ashar, J., Esapa, C. T., Benson, M. A., Blake, D. J., Rosenfeld, J., and Lu, Q. L. (2007) Fukutin- related protein localizes to the Golgi apparatus and mutations lead to mislocalization in muscle in vivo. Muscle Nerve 36, 455-465 (Pubitemid 47512069)
38. Kawahara, G., Guyon, J. R., Nakamura, Y., and Kunkel, L. M. (2010) Zebrafish models for human FKRP muscular dystrophies. Hum. Mol. Genet. 19, 623-633
39. Dolatshad, N. F., Brockington, M., Torelli, S., Skordis, L., Wever, U., Wells, D. J., Muntoni, F., and Brown, S. C. (2005) Mutated fukutin-related protein (FKRP) localizes as wild type in differentiated muscle cells. Exp. Cell Res. 309, 370-378 (Pubitemid 41317360)
40. Bao, X., Kobayashi, M., Hatakeyama, S., Angata, K., Gullberg, D., Nakayama, J., Fukuda, M. N., and Fukuda, M. (2009) Tumor suppressor function of laminin-binding α-dystroglycan requires a distinctß3-N- acetylglucosaminyltransferase. Proc. Natl. Acad. Sci. U.S.A. 106, 12109-12114
41. Hafner-Bratkovic, I., Gaspersic, J., Smid, L. M., Bresjanac, M., and Jerala, R. (2008) Curcumin binds to the α-helical intermediate and to the amyloid form of prion protein: a new mechanism for the inhibition of PrP(Sc) accumulation. J. Neurochem. 104, 1553-1564 (Pubitemid 351316769)
42. Ono, K., and Yamada, M. (2006) Antioxidant compounds have potent anti-fibrillogenic and fibril-destabilizing effects for α-synuclein fibrils in vitro. J. Neurochem. 97, 105-115
43. Pey, A. L., Ying, M., Cremades, N., Velazquez-Campoy, A., Scherer, T., Thöny, B., Sancho, J., and Martinez, A. (2008) Identification of pharmacological chaperones as potential therapeutic agents to treat phenylketonuria. J. Clin. Invest. 118, 2858-2867