Loss of function mutations in RPL27 and RPS27 identified by whole-exome sequencing in Diamond-Blackfan anaemia

British Journal of Haematology

Volumn 168, Issue 6, 2015, Pages 854-864

  Wang, Runan ^a   Yoshida, Kenichi ^b,c   Toki, Tsutomu ^a   Sawada, Takafumi ^d   Uechi, Tamayo ^d   Okuno, Yusuke ^b,c   Sato Otsubo, Aiko ^b,c   Kudo, Kazuko ^e   Kamimaki, Isamu ^f   Kanezaki, Rika ^a   Shiraishi, Yuichi ^g   Chiba, Kenichi ^g   Tanaka, Hiroko ^g   Terui, Kiminori ^a   Sato, Tomohiko ^a   Iribe, Yuji ^h   Ohga, Shouichi ⁱ   Kuramitsu, Madoka ^j   Hamaguchi, Isao ^j   Ohara, Akira ^k   Hara, Junichi ^l   Goi, Kumiko ^m   Matsubara, Kousaku ⁿ   Koike, Kenichi ^o   Ishiguro, Akira ^p   Okamoto, Yasuhiro ^q   Watanabe, Kenichiro ^c   Kanno, Hitoshi ^h   Kojima, Seiji ^r   Miyano, Satoru ^g   Kenmochi, Naoya ^d   Ogawa, Seishi ^b,c   Ito, Etsuro ^a   more..

^a HIROSAKI UNIVERSITY   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF MIYAZAKI   (Japan)

^e SHIZUOKA CHILDREN'S HOSPITAL   (Japan)

^f SAITAMA NATIONAL HOSPITAL   (Japan)

^g THE UNIVERSITY OF TOKYO   (Japan)

^h TOKYO WOMEN'S MEDICAL UNIVERSITY   (Japan)

ⁱ KYUSHU UNIVERSITY   (Japan)

^j NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^k TOHO UNIVERSITY OMORI MEDICAL CENTER   (Japan)

^l OSAKA CITY GENERAL HOSPITAL   (Japan)

^m UNIVERSITY OF YAMANASHI   (Japan)

ⁿ NISHI KOBE MEDICAL CENTER   (Japan)

^o SHINSHU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^p NATIONAL CENTER FOR CHILD HEALTH AND DEVELOPMENT   (Japan)

^q KAGOSHIMA UNIVERSITY   (Japan)

^r NAGOYA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

more..

Author keywords

Bone marrow failure; Childhood; Diamond Blackfan; Erythropoiesis; Genetic analysis

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BLACKFAN DIAMOND ANEMIA; BRAIN DEVELOPMENT; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; EMBRYO; ERYTHROPOIESIS; FEMALE; FRAMESHIFT MUTATION; GATA1 GENE; GENE; GENE DELETION; GENE DUPLICATION; GENE EXPRESSION; GENE SEQUENCE; GENE SILENCING; GERMLINE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LOSS OF FUNCTION MUTATION; MALE; MISSENSE MUTATION; MOLECULAR PATHOLOGY; NONHUMAN; PRESCHOOL CHILD; PRIORITY JOURNAL; RNA PROCESSING; RPL13 GENE; RPL14 GENE; RPL18A GENE; RPL26 GENE; RPL27 GENE; RPL29 GENE; RPL31 GENE; RPL3L GENE; RPL6 GENE; RPL7L1T GENE; RPL8 GENE; RPS27 GENE; SPLICING DEFECT; SUBSTITUTION LINE; WHOLE EXOME SEQUENCING; ZEBRA FISH; ANIMAL; EXOME; GENETICS; INFANT; NEWBORN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PEDIGREE; PROCEDURES;

METALLOPROTEIN; NUCLEAR PROTEIN; RIBOSOMAL PROTEINS L27; RIBOSOME PROTEIN; RIBOSOME RNA; RNA BINDING PROTEIN; RPS27 PROTEIN, HUMAN;

ANEMIA, DIAMOND-BLACKFAN; ANIMALS; CHILD, PRESCHOOL; DNA MUTATIONAL ANALYSIS; ERYTHROPOIESIS; EXOME; FEMALE; GERM-LINE MUTATION; HUMANS; INFANT; INFANT, NEWBORN; MALE; METALLOPROTEINS; NUCLEAR PROTEINS; PEDIGREE; RIBOSOMAL PROTEINS; RNA, RIBOSOMAL; RNA-BINDING PROTEINS; ZEBRAFISH;

EID: 84924189543     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.13229     Document Type: Article

References (32)

1. Choesmel, V., Bacqueville, D., Rouquette, J., Noaillac-Depeyre, J., Fribourg, S., Crétien, A., Leblanc, T., Tchernia, G., Da Costa, L. & Gleizes, P.E. (2007) Impaired ribosome biogenesis in Diamond-Blackfan anemia. Blood, 109, 1275-1283.
2. Cmejla, R., Cmejlova, J., Handrkova, H., Petrak, J. & Pospisilova, D. (2007) Ribosomal protein S17 gene (RPS17) is mutated in Diamond-Blackfan anemia. Human Mutation, 28, 1178-1182.
3. Doherty, L., Sheen, M.R., Vlachos, A., Choesmel, V., O'Donohue, M.F., Clinton, C., Schneider, H.E., Sieff, C.A., Newburger, P.E., Ball, S.E., Niewiadomska, E., Matysiakm M, Glader., B ., Arceci., R.J ., Farrar., J.E ., Atsidaftosm.E., Liptonm J, M., Gleizes, P.E. & Gazda, H.T. (2010) Ribosomal protein genes RPS10 and RPS26 are commonly mutated in Diamond-Blackfan anemia. The American Journal of Human Genetics, 86, 222-228.
4. Draptchinskaia, N., Gustavsson, P., Andersson, B., Pettersson, M., Willig, T.N., Dianzani, I., Ball, S., Tchernia, G., Klar, J., Matsson, H., Tentler, D., Mohandas, N., Carlsson, B. & Dahl, N. (1999) The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nature Genetics, 21, 169-175.
5. Ebert, B.L., Pretz, J., Bosco, J., Chang, C.Y., Tamayo, P., Galili, N., Raza, A., Root, D.E., Attar, E., Ellis, S.R. & Golub, T.R. (2008) Identification of RPS14 as a 5q- syndrome gene by RNA interference screen. Nature, 451, 335-339.
6. Farrar, J.E., Nater, M., Caywood, E., McDevitt, M.A., Kowalski, J., Takemoto, C.M., Talbot, C.C. Jr, Meltzer, P., Esposito, D., Beggs, A.H., Schneider, H.E., Grabowska, A., Ball, S.E., Niewiadomska, E., Sieff, C.A., Vlachos, A., Atsidaftos, E., Ellis, S.R., Lipton, J.M., Gazda, H.T. & Arceci, R.J. (2008) Abnormalities of the large ribosomal subunit protein, Rpl35a, in Diamond-Blackfan anemia. Blood, 112, 1582-1592.
7. Flygare, J., Aspesi, A., Bailey, J.C., Miyake, K., Caffrey, J.M., Karlsson, S. & Ellis, S.R. (2007) Human RPS19, the gene mutated in Diamond-Blackfan anemia, encodes a ribosomal protein required for the maturation of 40S ribosomal subunits. Blood, 109, 980-986.
8. Gazda, H.T., Grabowska, A., Merida-Long, L.B., Latawiec, E., Schneider, H.E., Lipton, J.M., Vlachos, A., Atsidaftos, E., Ball, S.E., Orfali, K.A., Niewiadomska, E., Da Costa, L., Tchernia, G., Niemeyer, C., Meerpohl, J.J., Stahl, J., Schratt, G., Glader, B., Backer, K., Wong, C., Nathan, D.G., Beggs, A.H. & Sieff, C.A. (2006) Ribosomal protein S24 gene is mutated in Diamond-Blackfan anemia. The American Journal of Human Genetics, 2006, 1110-1118.
9. Gazda, H.T., Sheen, M.R., Vlachos, A., Choesmel, V., O'Donohue, M.F., Schneider, H., Darras, N., Hasman, C., Sieff, C.A., Newburger, P.E., Ball, S.E., Niewiadomska, E., Matysiak, M., Zaucha, J.M., Glader, B., Niemeyer, C., Meerpohl, J.J., Atsidaftos, E., Lipton, J.M., Gleizes, P.E. & Beggs, A.H. (2008) Ribosomal protein L5 and L11 mutations are associated with cleft palate and abnormal thumbs in Diamond-Blackfan anemia patients. The American Journal of Human Genetics, 83, 769-780.
10. Gazda, H.T., Preti, M., Sheen, M.R., O'Donohue, M.F., Vlachos, A., Davies, S.M., Kattamis, A., Doherty, L., Landowski, M., Buros, C., Ghazvinian, R., Sieff, C.A., Newburger, P.E., Niewiadomska, E., Matysiak, M., Glader, B., Atsidaftos, E., Lipton, J.M., Gleizes, P.E. & Beggs, A.H. (2012) Frameshift mutation in p53 regulator RPL26 is associated with multiple physical abnormalities and a specific pre-ribosomal RNA processing defect in diamond-blackfan anemia. Human Mutation, 33, 1037-1044.
11. Gerrard, G., Valgañón, M., Foong, H.E., Kasperaviciute, D., Iskander, D., Game, L., Müller, M., Aitman, T.J., Roberts, I., de la Fuente, J., Foroni, L. & Karadimitris, A. (2013) Target enrichment and high-throughput sequencing of 80 ribosomal protein genes to identify mutations associated with Diamond-Blackfan anaemia. British Journal of Haematology, 162, 530-536.
12. Hadjiolova, K.V., Nicoloso, M., Mazan, S., Hadjiolov, A.A. & Bachellerie, J.P. (1993) Alternative pre-rRNA processing pathways in human cells and their alteration by cycloheximide inhibition of protein synthesis. European Journal of Biochemistry, 212, 211-215.
13. Idol, R.A., Robledo, S., Du, H.Y., Crimmins, D.L., Wilson, D.B. & Ladenson, J.H. (2007) Cells depleted for RPS19, a protein associated with Diamond Blackfan anemia, show defects in 18S ribosomal RNA synthesis and small ribosomal subunit production. Blood Cells Molecules and Diseases, 39, 35-43.
14. Ito, E., Konno, Y., Toki, T. & Terui, K. (2010) Molecular pathogenesis in Diamond-Blackfan anemia. International Journal of Hematology, 92, 413-418.
15. Konno, Y., Toki, T., Tandai, S., Xu, G., Wang, R.N., Terui, K., Ohga, S., Hara, T., Hama, A., Kojima, S., Hasegawa, D., Kosaka, Y., Yanagisawa, R., Koike, K., Kanai, R., Imai, T., Hongo, T., Park, M.J., Sugita, K. & Ito, E. (2010) Mutations in the ribosomal protein genes in Japanese patients with Diamond-Blackfan anemia. Haematologica, 95, 1293-1299.
16. Kunishima, S., Okuno, Y., Yoshida, K., Shiraishi, Y., Sandada, M., Muramatsu, H., Chiba, K., Tanaka, H., Miyazaki, K., Sakai, M., Ohtake, M., Kobayashi, R., Iguchi, A., Niimi, G., Otsu, M., Takahashi, Y., Miyano, S., Saito, H., Kojima, S. & Ogawa, S. (2013) ACTN1 mutations cause congenital macrothrombocytopenia. The American Journal of Human Genetics, 92, 431-438.
17. Kuramitsu, M., Sato-Otsubo, A., Morio, T., Takagi, M., Toki, T., Terui, K., Wang, R., Kanno, H., Ohga, S., Ohara, A., Kojima, S., Kitoh, T., Goi, K., Kudo, K., Matsubayashi, T., Mizue, N., Ozeki, M., Masumi, A., Momose, H., Takizawa, K., Mizukami, T., Yamaguchi, K., Ogawa, S., Ito, E. & Hamaguchi, I. (2012) Extensive gene deletions in Japanese patients with Diamond-Blackfan anemia. Blood, 119, 2376-2384.
18. Li, H. & Durbin, R. (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25, 1754-1760.
19. Lipton, J.M., Atsidaftos, E., Zyskind, I. & Vlachos, A. (2006) Improving clinical care and elucidating the pathophysiology of Diamond Blackfan anemia: an update from the Diamond Blackfan Anemia Registry. Pediatric Blood & Cancer, 46, 558-564.
20. McGowan, K.A. & Mason, P.J. (2011) Animal models of Diamond Blackfan anemia. Seminars in Hematology, 48, 106-116.
21. Mirabello, L., Macari, E.R., Jessop, L., Ellis, S.R., Myers, T., Giri, N., Taylor, A.M., McGrath, K.E., Humphries, J.M., Ballew, B.J., Yeager, M., Boland, J.F., He, J., Hicks, B.D., Burdett, L., Alter, B.P., Zon, L. & Savage, S.A. (2014) Whole-exome sequencing and functional studies identify RPS29 as a novel gene mutated in multi-case Diamond-Blackfan anemia families. Blood, 124, 24-32.
22. Narla, A. & Ebert, B.J. (2010) Ribosomepathies: human disorders of ribosome dysfunction. Blood, 115, 3196-3205.
23. Rouquette, J., Choesmel, V. & Gleizes, P.E. (2005) Nuclear export and cytoplasmic processing of precursors to the 40S ribosomal subunits in mammalian cells. EMBO Journal, 24, 2862-2872.
24. Sankaran, V.G., Ghazvinian, R., Do, R., Thiru, P., Vergilio, J.A., Beggs, A.H., Sieff, C.A., Orkin, S.H., Nathan, D.G., Lander, E.S. & Gazda, H.T. (2012) Exome sequencing identifies GATA1 mutations resulting Diamond-Blackfan anemia. The Journal of Clinical Investigation, 122, 2439-2443.
25. Torihara, H., Uechi, T., Chakraborty, A., Shinya, M., Sakai, N. & Kenmochi, N. (2011) Erythropoiesis failure due to RPS19 deficiency is independent of an activated Tp53 response in a zebrafish model of Diamond-Blackfan anaemia. British Journal of Haematology, 152, 648-654.
26. Uechi, T., Nakajima, Y., Nakao, A., Torihara, H., Chakraborty, A., Inoue, K. & Kenmochi, N. (2006) Ribosomal protein gene knockdown causes developmental defects in zebrafish. PLoS ONE, 1, e37.
27. Vlachos, A., Ball, S., Dahl, N., Alter, B.P., Sheth, S., Ramenghi, U., Meerpohl, J., Karlsson, S., Liu, J.M., Leblanc, T., Paley, C., Kang, E.M., Leder, E.J., Atsidaftos, E., Shimamura, A., Bessler, M., Glader, B. & Lipton, J.M. (2008) Diagnosing and treating Diamond Blackfan anaemia: results of an international clinical consensus conference. British Journal of Haematology, 142, 859-876.
28. Vlachos, A., Rosenberg, P.S., Atsidaftos, E., Alter, B.P. & Lipton, J.M. (2012) Incidence of neoplasia in Diamond Blackfan anemia: a report from the Diamond Blackfan Anemia Registry. Blood, 119, 3815-3819.
29. Willig, T.N., Draptchinskaia, N., Dianzani, I., Ball, S., Niemeyer, C., Ramenghi, U., Orfali, K., Gustavsson, P., Garelli, E., Brusco, A., Tiemann, C., Pérignon, J.L., Bouchier, C., Cicchiello, L., Dahl, N., Mohandas, N. & Tchernia, G. (1999) Mutations in ribosomal protein S19 gene and diamond blackfan anemia: wide variations in phenotypic expression. Blood, 94, 4294-4306.
30. Xiong, X., Zhao, Y., He, H. & Sun, Y. (2011) Ribosomal protein S27-like and S27 interplay with p53-MDM2 axis as a target, a substrate and a regulator. Oncogene, 30, 1798-1811.
31. Yoshida, K., Sanada, M., Shiraishi, Y., Nowak, D., Nagata, Y., Yamamoto, R., Sato, Y., Sato-Otsubo, A., Kon, A., Nagasaki, M., Chalkidis, G., Suzuki, Y., Shiosaka, M., Kawahata, R., Yamaguchi, T., Otsu, M., Obara, N., Sakata-Yanagimoto, M., Ishiyama, K., Mori, H., Nolte, F., Hofmann, W.K., Miyawaki, S., Sugano, S., Haferlach, C., Koeffler, H.P., Shih, L.Y., Haferlach, T., Chiba, S., Nakauchi, H., Miyano, S. & Ogawa, S. (2011) Frequent pathway mutations of splicing machinery in myelodysplasia. Nature, 478, 64-69.
32. Zhang, Y. & Lu, H. (2009) Signaling to p53: ribosomal proteins find their way. Cancer Cell, 16, 369-377.