Biallelic Mutations in MYPN, Encoding Myopalladin, Are Associated with Childhood-Onset, Slowly Progressive Nemaline Myopathy

American Journal of Human Genetics

Volumn 100, Issue 1, 2017, Pages 169-178

  Miyatake, Satoko ^a,b   Mitsuhashi, Satomi ^c,d,e   Hayashi, Yukiko K ^c,f   Purevjav, Enkhsaikhan ^g   Nishikawa, Atsuko ^c,h   Koshimizu, Eriko ^a   Suzuki, Mikiya ⁱ   Yatabe, Kana ⁱ   Tanaka, Yuzo ⁱ   Ogata, Katsuhisa ⁱ   Kuru, Satoshi ^j   Shiina, Masaaki ^a   Tsurusaki, Yoshinori ^a   Nakashima, Mitsuko ^a   Mizuguchi, Takeshi ^a   Miyake, Noriko ^a   Saitsu, Hirotomo ^a,k   Ogata, Kazuhiro ^a   Kawai, Mitsuru ⁱ   Towbin, Jeffrey ^g   Nonaka, Ikuya ^c   Nishino, Ichizo ^c   Matsumoto, Naomichi ^a   more..

^a YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b YOKOHAMA CITY UNIVERSITY HOSPITAL   (Japan)

^c NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^d NATIONAL INSTITUTE OF MENTAL HEALTH   (Japan)

^e TOKAI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^f TOKYO MEDICAL UNIVERSITY   (Japan)

^g UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

^h UNIVERSITY OF YAMANASHI   (Japan)

ⁱ Higashisaitama National Hospital   (Japan)

^j SUZUKA NATIONAL HOSPITAL   (Japan)

^k HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

more..

Author keywords

congenital myopathy; intranuclear rod myopathy; MYPN; nemaline myopathy; whole exome sequencing

Indexed keywords

CELL PROTEIN; MUTANT PROTEIN; MYPN PROTEIN; UNCLASSIFIED DRUG; MUSCLE PROTEIN; MYPN PROTEIN, HUMAN;

ADULT; ARTICLE; CASE REPORT; CLINICAL FEATURE; FEMALE; GENETIC HETEROGENEITY; GENETIC SCREENING; HEART DISEASE; HUMAN; LOSS OF FUNCTION MUTATION; MALE; MUSCLE DISEASE; MUSCLE WEAKNESS; NEMALINE MYOPATHY; ONSET AGE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RESPIRATORY FUNCTION DISORDER; SARCOMERE; WALKING DIFFICULTY; WHOLE EXOME SEQUENCING; ALLELE; ANIMAL; CHILD; DISEASE COURSE; GENE TARGETING; GENETICS; METABOLISM; MIDDLE AGED; MOUSE; MUTATION; PATHOLOGY; PEDIGREE; PRESCHOOL CHILD; SKELETAL MUSCLE; ULTRASTRUCTURE;

ADULT; AGE OF ONSET; ALLELES; ANIMALS; CHILD; CHILD, PRESCHOOL; DISEASE PROGRESSION; FEMALE; GENE KNOCK-IN TECHNIQUES; HUMANS; MALE; MICE; MIDDLE AGED; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUTATION; MYOPATHIES, NEMALINE; PEDIGREE;

EID: 85009796995     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2016.11.017     Document Type: Article

References (37)

1. 1 Nance, J.R., Dowling, J.J., Gibbs, E.M., Bönnemann, C.G., Congenital myopathies: an update. Curr. Neurol. Neurosci. Rep. 12 (2012), 165–174.
2. 2 Romero, N.B., Sandaradura, S.A., Clarke, N.F., Recent advances in nemaline myopathy. Curr. Opin. Neurol. 26 (2013), 519–526.
3. 3 Nowak, K.J., Wattanasirichaigoon, D., Goebel, H.H., Wilce, M., Pelin, K., Donner, K., Jacob, R.L., Hübner, C., Oexle, K., Anderson, J.R., et al. Mutations in the skeletal muscle alpha-actin gene in patients with actin myopathy and nemaline myopathy. Nat. Genet. 23 (1999), 208–212.
4. 4 Pelin, K., Hilpelä, P., Donner, K., Sewry, C., Akkari, P.A., Wilton, S.D., Wattanasirichaigoon, D., Bang, M.L., Centner, T., Hanefeld, F., et al. Mutations in the nebulin gene associated with autosomal recessive nemaline myopathy. Proc. Natl. Acad. Sci. USA 96 (1999), 2305–2310.
5. 5 Laing, N.G., Wilton, S.D., Akkari, P.A., Dorosz, S., Boundy, K., Kneebone, C., Blumbergs, P., White, S., Watkins, H., Love, D.R., et al. A mutation in the alpha tropomyosin gene TPM3 associated with autosomal dominant nemaline myopathy NEM1. Nat. Genet., 10, 1995, 249.
6. 6 Donner, K., Ollikainen, M., Ridanpää, M., Christen, H.J., Goebel, H.H., de Visser, M., Pelin, K., Wallgren-Pettersson, C., Mutations in the beta-tropomyosin (TPM2) gene—a rare cause of nemaline myopathy. Neuromuscul. Disord. 12 (2002), 151–158.
7. 7 Johnston, J.J., Kelley, R.I., Crawford, T.O., Morton, D.H., Agarwala, R., Koch, T., Schäffer, A.A., Francomano, C.A., Biesecker, L.G., A novel nemaline myopathy in the Amish caused by a mutation in troponin T1. Am. J. Hum. Genet. 67 (2000), 814–821.
8. 8 Agrawal, P.B., Greenleaf, R.S., Tomczak, K.K., Lehtokari, V.L., Wallgren-Pettersson, C., Wallefeld, W., Laing, N.G., Darras, B.T., Maciver, S.K., Dormitzer, P.R., Beggs, A.H., Nemaline myopathy with minicores caused by mutation of the CFL2 gene encoding the skeletal muscle actin-binding protein, cofilin-2. Am. J. Hum. Genet. 80 (2007), 162–167.
9. 9 Yuen, M., Sandaradura, S.A., Dowling, J.J., Kostyukova, A.S., Moroz, N., Quinlan, K.G., Lehtokari, V.L., Ravenscroft, G., Todd, E.J., Ceyhan-Birsoy, O., et al. Leiomodin-3 dysfunction results in thin filament disorganization and nemaline myopathy. J. Clin. Invest. 124 (2014), 4693–4708.
10. 10 Sambuughin, N., Yau, K.S., Olivé, M., Duff, R.M., Bayarsaikhan, M., Lu, S., Gonzalez-Mera, L., Sivadorai, P., Nowak, K.J., Ravenscroft, G., et al. Dominant mutations in KBTBD13, a member of the BTB/Kelch family, cause nemaline myopathy with cores. Am. J. Hum. Genet. 87 (2010), 842–847.
11. 11 Ravenscroft, G., Miyatake, S., Lehtokari, V.L., Todd, E.J., Vornanen, P., Yau, K.S., Hayashi, Y.K., Miyake, N., Tsurusaki, Y., Doi, H., et al. Mutations in KLHL40 are a frequent cause of severe autosomal-recessive nemaline myopathy. Am. J. Hum. Genet. 93 (2013), 6–18.
12. 12 Gupta, V.A., Ravenscroft, G., Shaheen, R., Todd, E.J., Swanson, L.C., Shiina, M., Ogata, K., Hsu, C., Clarke, N.F., Darras, B.T., et al. Identification of KLHL41 Mutations Implicates BTB-Kelch-Mediated Ubiquitination as an Alternate Pathway to Myofibrillar Disruption in Nemaline Myopathy. Am. J. Hum. Genet. 93 (2013), 1108–1117.
13. 13 Ryan, M.M., Schnell, C., Strickland, C.D., Shield, L.K., Morgan, G., Iannaccone, S.T., Laing, N.G., Beggs, A.H., North, K.N., Nemaline myopathy: a clinical study of 143 cases. Ann. Neurol. 50 (2001), 312–320.
14. 14 Laing, N.G., Dye, D.E., Wallgren-Pettersson, C., Richard, G., Monnier, N., Lillis, S., Winder, T.L., Lochmüller, H., Graziano, C., Mitrani-Rosenbaum, S., et al. Mutations and polymorphisms of the skeletal muscle alpha-actin gene (ACTA1). Hum. Mutat. 30 (2009), 1267–1277.
15. 15 Mitsuhashi, S., Hatakeyama, H., Karahashi, M., Koumura, T., Nonaka, I., Hayashi, Y.K., Noguchi, S., Sher, R.B., Nakagawa, Y., Manfredi, G., et al. Muscle choline kinase beta defect causes mitochondrial dysfunction and increased mitophagy. Hum. Mol. Genet. 20 (2011), 3841–3851.
16. 16 Saitsu, H., Nishimura, T., Muramatsu, K., Kodera, H., Kumada, S., Sugai, K., Kasai-Yoshida, E., Sawaura, N., Nishida, H., Hoshino, A., et al. De novo mutations in the autophagy gene WDR45 cause static encephalopathy of childhood with neurodegeneration in adulthood. Nat. Genet. 45 (2013), 445–449 e1.
17. 17 Wang, K., Li, M., Hakonarson, H., ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res., 38, 2010, e164.
18. 18 Bang, M.L., Mudry, R.E., McElhinny, A.S., Trombitás, K., Geach, A.J., Yamasaki, R., Sorimachi, H., Granzier, H., Gregorio, C.C., Labeit, S., Myopalladin, a novel 145-kilodalton sarcomeric protein with multiple roles in Z-disc and I-band protein assemblies. J. Cell Biol. 153 (2001), 413–427.
19. 19 Purevjav, E., Arimura, T., Augustin, S., Huby, A.C., Takagi, K., Nunoda, S., Kearney, D.L., Taylor, M.D., Terasaki, F., Bos, J.M., et al. Molecular basis for clinical heterogeneity in inherited cardiomyopathies due to myopalladin mutations. Hum. Mol. Genet. 21 (2012), 2039–2053.
20. 20 Zou, Y., Evans, S., Chen, J., Kuo, H.C., Harvey, R.P., Chien, K.R., CARP, a cardiac ankyrin repeat protein, is downstream in the Nkx2-5 homeobox gene pathway. Development 124 (1997), 793–804.
21. 21 Li, H., Durbin, R., Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25 (2009), 1754–1760.
22. 22 Higasa, K., Miyake, N., Yoshimura, J., Okamura, K., Niihori, T., Saitsu, H., Doi, K., Shimizu, M., Nakabayashi, K., Aoki, Y., et al. Human genetic variation database, a reference database of genetic variations in the Japanese population. J. Hum. Genet. 61 (2016), 547–553.
23. 23 Nozawa, R.S., Nagao, K., Igami, K.T., Shibata, S., Shirai, N., Nozaki, N., Sado, T., Kimura, H., Obuse, C., Human inactive X chromosome is compacted through a PRC2-independent SMCHD1-HBiX1 pathway. Nat. Struct. Mol. Biol. 20 (2013), 566–573.
24. 24 Ugai, H., Murata, T., Nagamura, Y., Ugawa, Y., Suzuki, E., Nakata, H., Kujime, Y., Inamoto, S., Hirose, M., Inabe, K., et al. A database of recombinant viruses and recombinant viral vectors available from the RIKEN DNA bank. J. Gene Med. 7 (2005), 1148–1157.
25. 25 Fukuda, H., Terashima, M., Koshikawa, M., Kanegae, Y., Saito, I., Possible mechanism of adenovirus generation from a cloned viral genome tagged with nucleotides at its ends. Microbiol. Immunol. 50 (2006), 643–654.
26. 26 Duboscq-Bidot, L., Xu, P., Charron, P., Neyroud, N., Dilanian, G., Millaire, A., Bors, V., Komajda, M., Villard, E., Mutations in the Z-band protein myopalladin gene and idiopathic dilated cardiomyopathy. Cardiovasc. Res. 77 (2008), 118–125.
27. 27 Nunn, L.M., Lopes, L.R., Syrris, P., Murphy, C., Plagnol, V., Firman, E., Dalageorgou, C., Zorio, E., Domingo, D., Murday, V., et al. Diagnostic yield of molecular autopsy in patients with sudden arrhythmic death syndrome using targeted exome sequencing. Europace 18 (2016), 888–896.
28. 28 Hertz, C.L., Christiansen, S.L., Larsen, M.K., Dahl, M., Ferrero-Miliani, L., Weeke, P.E., Pedersen, O., Hansen, T., Grarup, N., Ottesen, G.L., et al. Genetic investigations of sudden unexpected deaths in infancy using next-generation sequencing of 100 genes associated with cardiac diseases. Eur. J. Hum. Genet. 24 (2016), 817–822.
29. 29 Meyer, T., Ruppert, V., Ackermann, S., Richter, A., Perrot, A., Sperling, S.R., Posch, M.G., Maisch, B., Pankuweit, S., German Competence Network Heart Failure. Novel mutations in the sarcomeric protein myopalladin in patients with dilated cardiomyopathy. Eur. J. Hum. Genet. 21 (2013), 294–300.
30. 30 Chami, N., Tadros, R., Lemarbre, F., Lo, K.S., Beaudoin, M., Robb, L., Labuda, D., Tardif, J.C., Racine, N., Talajic, M., Lettre, G., Nonsense mutations in BAG3 are associated with early-onset dilated cardiomyopathy in French Canadians. Can. J. Cardiol. 30 (2014), 1655–1661.
31. 31 Zhao, Y., Feng, Y., Zhang, Y.M., Ding, X.X., Song, Y.Z., Zhang, A.M., Liu, L., Zhang, H., Ding, J.H., Xia, X.S., Targeted next-generation sequencing of candidate genes reveals novel mutations in patients with dilated cardiomyopathy. Int. J. Mol. Med. 36 (2015), 1479–1486.
32. 32 Huby, A.C., Mendsaikhan, U., Takagi, K., Martherus, R., Wansapura, J., Gong, N., Osinska, H., James, J.F., Kramer, K., Saito, K., et al. Disturbance in Z-disk mechanosensitive proteins induced by a persistent mutant myopalladin causes familial restrictive cardiomyopathy. J. Am. Coll. Cardiol. 64 (2014), 2765–2776.
33. 33 Wallgren-Pettersson, C., Laing, N.G., Report of the 70th ENMC International Workshop: nemaline myopathy, 11-13 June 1999, Naarden, The Netherlands. Neuromuscul. Disord. 10 (2000), 299–306.
34. 34 Parast, M.M., Otey, C.A., Characterization of palladin, a novel protein localized to stress fibers and cell adhesions. J. Cell Biol. 150 (2000), 643–656.
35. 35 Nguyen, N.U., Wang, H.V., Dual roles of palladin protein in in vitro myogenesis: inhibition of early induction but promotion of myotube maturation. PLoS ONE, 10, 2015, e0124762.
36. 36 Winter, J.M., Joureau, B., Lee, E.J., Kiss, B., Yuen, M., Gupta, V.A., Pappas, C.T., Gregorio, C.C., Stienen, G.J., Edvardson, S., et al. Mutation-specific effects on thin filament length in thin filament myopathy. Ann. Neurol. 79 (2016), 959–969.
37. 37 Marttila, M., Lemola, E., Wallefeld, W., Memo, M., Donner, K., Laing, N.G., Marston, S., Grönholm, M., Wallgren-Pettersson, C., Abnormal actin binding of aberrant β-tropomyosins is a molecular cause of muscle weakness in TPM2-related nemaline and cap myopathy. Biochem. J. 442 (2012), 231–239.