Bone marrow cells from patients with Shwachman-Diamond syndrome abnormally express genes involved in ribosome biogenesis and RNA processing

British Journal of Haematology

Volumn 145, Issue 6, 2009, Pages 806-815

  Rujkijyanont, Piya ^b,c   Adams, Sally Lin ^b,c   Beyene, Joseph ^a   Dror, Yigal ^a,b,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b Research Institute   (Canada)

^c Division of Hematology/Oncology   (Canada)

Author keywords

Bone marrow failure; Gene expression; Microarray; Ribosomal proteins; Shwachman Diamond syndrome

Indexed keywords

PROTEIN P53; RIBOSOME PROTEIN;

APOPTOSIS; ARTICLE; BIOGENESIS; BONE MARROW CELL; CONTROLLED STUDY; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; PRIORITY JOURNAL; RIBOSOME; RNA PROCESSING; SHWACHMAN SYNDROME;

BONE MARROW CELLS; BONE MARROW DISEASES; CASE-CONTROL STUDIES; EXOCRINE PANCREATIC INSUFFICIENCY; GENE EXPRESSION PROFILING; HUMANS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMAL PROTEINS; RNA; RNA PROCESSING, POST-TRANSCRIPTIONAL; SYNDROME; TRANSCRIPTION, GENETIC;

EID: 66749150977     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2009.07692.x     Document Type: Article

References (64)

1. Anderson, S.J., Lauritsen, J.P., Hartman, M.G., Foushee, A.M., Lefebvre, J.M., Shinton, S.A., Gerhardt, B., Hardy, R.R., Oravecz, T. Wiest, D.L. (2007) Ablation of ribosomal protein L22 selectively impairs alphabeta T cell development by activation of a p53-dependent checkpoint. Immunity, 26, 759 772. (Pubitemid 46907667)
2. Antoine, M. Kiefer, P. (1998) Functional characterization of transcriptional regulatory elements in the upstream region and intron 1 of the human S6 ribosomal protein gene. Biochemical Journal, 336 (Pt 2), 327 335. (Pubitemid 28564388)
3. Austin, K.M., Leary, R.J. Shimamura, A. (2005) The Shwachman-Diamond SBDS protein localizes to the nucleolus. Blood, 106, 1253 1258. (Pubitemid 41129587)
4. Boocock, G.R., Morrison, J.A., Popovic, M., Richards, N., Ellis, L., Durie, P.R. Rommens, J.M. (2003) Mutations in SBDS are associated with Shwachman-Diamond syndrome. Nature Genetics, 33, 97 101. (Pubitemid 36068690)
5. Chung, S. Perry, R.P. (1993) The importance of downstream delta-factor binding elements for the activity of the rpL32 promoter. Nucleic Acids Research, 21, 3301 3308.
6. Colombo, P. Fried, M. (1992) Functional elements of the ribosomal protein L7a (rpL7a) gene promoter region and their conservation between mammals and birds. Nucleic Acids Research, 20, 3367 3373.
7. Curcic, D., Glibetic, M., Larson, D.E. Sells, B.H. (1997) GA-binding protein is involved in altered expression of ribosomal protein L32 gene. Journal of Cellular Biochemistry, 65, 287 307. (Pubitemid 27190686)
8. Davies, B. Fried, M. (1995) The L19 ribosomal protein gene (RPL19): gene organization, chromosomal mapping, and novel promoter region. Genomics, 25, 372 380.
9. Dror, Y. (2005) Shwachman-Diamond syndrome. Pediatric Blood & Cancer, 45, 892 901. (Pubitemid 41552156)
10. Dror, Y. Freedman, M.H. (1999) Shwachman-Diamond syndrome: An inherited preleukemic bone marrow failure disorder with aberrant hematopoietic progenitors and faulty marrow microenvironment. Blood, 94, 3048 3054. (Pubitemid 29512709)
11. Dror, Y. Freedman, M.H. (2001) Shwachman-Diamond syndrome marrow cells show abnormally increased apoptosis mediated through the Fas pathway. Blood, 97, 3011 3016.
12. Dror, Y. Freedman, M.H. (2002) Shwachman-diamond syndrome. British Journal of Haematology, 118, 701 713.
13. Dror, Y., Ginzberg, H., Dalal, I., Cherepanov, V., Downey, G., Durie, P., Roifman, C.M. Freedman, M.H. (2001) Immune function in patients with Shwachman-Diamond syndrome. British Journal of Haematology, 114, 712 717. (Pubitemid 32953656)
14. Dror, Y., Durie, P., Ginzberg, H., Herman, R., Banerjee, A., Champagne, M., Shannon, K., Malkin, D. Freedman, M.H. (2002) Clonal evolution in marrows of patients with Shwachman-Diamond syndrome: a prospective 5-year follow-up study. Experimental Hematology, 30, 659 669. (Pubitemid 34835684)
15. Du, J., Shi, Y., Pan, Y., Jin, X., Liu, C., Liu, N., Han, Q., Lu, Y., Qiao, T. Fan, D. (2005) Regulation of multidrug resistance by ribosomal protein l6 in gastric cancer cells. Cancer Biology & Therapy, 4, 242 247. (Pubitemid 41351325)
16. Efron, B. Tibshirani, R. (2007) On testing the significance of sets of genes. Annals of Applied Statistics, 1, 107 129.
17. Ganapathi, K.A., Austin, K.M., Lee, C.S., Dias, A., Malsch, M.M., Reed, R. Shimamura, A. (2007) The human Shwachman-Diamond syndrome protein, SBDS, associates with ribosomal RNA. Blood, 110, 1458 1465. (Pubitemid 47443960)
18. Genuario, R.R. Perry, R.P. (1996) The GA-binding protein can serve as both an activator and repressor of ribosomal protein gene transcription. Journal of Biological Chemistry, 271, 4388 4395. (Pubitemid 26074149)
19. Genuario, R.R., Kelley, D.E. Perry, R.P. (1993) Comparative utilization of transcription factor GABP by the promoters of ribosomal protein genes rpL30 and rpL32. Gene Expression, 3, 279 288. (Pubitemid 2043173)
20. Goldstone, S.D. Lavin, M.F. (1993) Isolation of a cDNA clone, encoding the ribosomal protein S20, downregulated during the onset of apoptosis in a human leukaemic cell line. Biochemical and Biophysical Research Communications, 196, 619 623.
21. Gordon, S., Akopyan, G., Garban, H. Bonavida, B. (2006) Transcription factor YY1: structure, function, and therapeutic implications in cancer biology. Oncogene, 25, 1125 1142. (Pubitemid 43297928)
22. Hariharan, N. Perry, R.P. (1989) A characterization of the elements comprising the promoter of the mouse ribosomal protein gene RPS16. Nucleic Acids Research, 17, 5323 5337. (Pubitemid 19173361)
23. Hariharan, N., Kelley, D.E. Perry, R.P. (1989) Equipotent mouse ribosomal protein promoters have a similar architecture that includes internal sequence elements. Genes and Development, 3, 1789 1800.
24. Harris, S.A., Dudov, K.P. Bowman, L.H. (1992) Comparison of the mouse L32 ribosomal protein promoter elements in mouse myoblasts, fibers, and L cells. Journal of Cellular Biochemistry, 50, 178 189.
25. He, H. Sun, Y. (2007) Ribosomal protein S27L is a direct p53 target that regulates apoptosis. Oncogene, 26, 2707 2716. (Pubitemid 46663829)
26. He, J., Navarrete, S., Jasinski, M., Vulliamy, T., Dokal, I., Bessler, M. Mason, P.J. (2002) Targeted disruption of Dkc1, the gene mutated in X-linked dyskeratosis congenita, causes embryonic lethality in mice. Oncogene, 21, 7740 7744. (Pubitemid 35398819)
27. Hofmann, K. Bucher, P. (1995) The FHA domain: a putative nuclear signalling domain found in protein kinases and transcription factors. Trends in Biochemical Sciences, 20, 347 349.
28. Hubbell, E., Liu, W.M. Mei, R. (2002) Robust estimators for expression analysis. Bioinformatics, 18, 1585 1592. (Pubitemid 36097723)
29. Ihaka, R. Gentleman, R. (1996) A language for data analysis and graphics. Journal of Computational Graphical and Statistics, 5, 299 314.
30. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U. Speed, T.P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249 264.
31. Kim, S.Y., Lee, M.Y., Cho, K.C., Choi, Y.S., Choi, J.S., Sung, K.W., Kwon, O.J., Kim, H.S., Kim, I.K. Jeong, S.W. (2003) Alterations in mRNA expression of ribosomal protein S9 in hydrogen peroxide-treated neurotumor cells and in rat hippocampus after transient ischemia. Neurochemical Research, 28, 925 931. (Pubitemid 36438411)
32. Kirn-Safran, C.B., Dayal, S., Martin-DeLeon, P.A. Carson, D.D. (2000) Cloning, expression, and chromosome mapping of the murine Hip/Rpl29 gene. Genomics, 68, 210 219.
33. Koonin, E.V., Wolf, Y.I. Aravind, L. (2001) Prediction of the archaeal exosome and its connections with the proteasome and the translation and transcription machineries by a comparative-genomic approach. Genome Research, 11, 240 252. (Pubitemid 32166533)
34. Lai, C.H., Chou, C.Y., Ch'ang, L.Y., Liu, C.S. Lin, W. (2000) Identification of novel human genes evolutionarily conserved in Caenorhabditis elegans by comparative proteomics. Genome Research, 10, 703 713. (Pubitemid 30333199)
35. Liu, W.M., Mei, R., Di, X., Ryder, T.B., Hubbell, E., Dee, S., Webster, T.A., Harrington, C.A., Ho, M.H., Baid, J. Smeekens, S.P. (2002) Analysis of high density expression microarrays with signed-rank call algorithms. Bioinformatics, 18, 1593 1599. (Pubitemid 36097724)
36. Liu, J.J., Zhang, J., Ramanan, S., Julian, J., Carson, D.D. Hooi, S.C. (2004) Heparin/heparan sulfate interacting protein plays a role in apoptosis induced by anticancer drugs. Carcinogenesis, 25, 873 879. (Pubitemid 38886073)
37. Luscombe, N.M., Austin, S.E., Berman, H.M. Thornton, J.M. (2000) An overview of the structures of protein-DNA complexes. Genome Biology, 1, REVIEWS001.
38. Menne, T.F., Goyenechea, B., Sanchez-Puig, N., Wong, C.C., Tonkin, L.M., Ancliff, P.J., Brost, R.L., Costanzo, M., Boone, C. Warren, A.J. (2007) The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast. Nature Genetics, 39, 486 495. (Pubitemid 46514776)
39. Meyuhas, O. Klein, A. (1990) The mouse ribosomal protein L7 gene. Its primary structure and functional analysis of the promoter region. Journal of Biological Chemistry, 265, 11465 11473.
40. Meyuhas, O. Perry, R.P. (1980) Construction and identification of cDNA clones for mouse ribosomal proteins: application for the study of r-protein gene expression. Gene, 10, 113 129. (Pubitemid 10000613)
41. Newberry, E.P., Latifi, T. Towler, D.A. (1999) The RRM domain of MINT, a novel Msx2 binding protein, recognizes and regulates the rat osteocalcin promoter. Biochemistry, 38, 10678 10690.
42. Overman, P.F., Rhoads, D.D., Tasheva, E.S., Pyle, M.M. Roufa, D.J. (1993) Multiple regulatory elements ensure accurate transcription of a human ribosomal protein gene. Somatic Cell and Molecular Genetics, 19, 347 362. (Pubitemid 23292986)
43. Rujkijyanont, P., Beyene, J., Wei, K., Khan, F. Dror, Y. (2007) Leukaemia-related gene expression in bone marrow cells from patients with the preleukaemic disorder Shwachman-Diamond syndrome. British Journal of Haematology, 137, 537 544. (Pubitemid 46817337)
44. Rujkijyanont, P., Watanabe, K., Ambekar, C., Wang, H., Schimmer, A., Beyene, J. Dror, Y. (2008) SBDS-deficient cells undergo accelerated apoptosis through the Fas-pathway. Haematologica, 93, 363 371.
45. Safrany, G. Perry, R.P. (1995) The relative contributions of various transcription factors to the overall promoter strength of the mouse ribosomal protein L30 gene. European Journal of Biochemistry, 230, 1066 1072.
46. Savchenko, A., Krogan, N., Cort, J.R., Evdokimova, E., Lew, J.M., Yee, A.A., Sanchez-Pulido, L., Andrade, M.A., Bochkarev, A., Watson, J.D., Kennedy, M.A., Greenblatt, J., Hughes, T., Arrowsmith, C.H., Rommens, J.M. Edwards, A.M. (2005) The Shwachman-Bodian-Diamond syndrome protein family is involved in RNA metabolism. Journal of Biological Chemistry, 280, 19213 19220. (Pubitemid 41379628)
47. Selenko, P., Gregorovic, G., Sprangers, R., Stier, G., Rhani, Z., Kramer, A. Sattler, M. (2003) Structural basis for the molecular recognition between human splicing factors U2AF65 and SF1/mBBP. Molecular Cell, 11, 965 976. (Pubitemid 36566318)
48. Shammas, C., Menne, T.F., Hilcenko, C., Michell, S.R., Goyenechea, B., Boocock, G.R., Durie, P.R., Rommens, J.M. Warren, A.J. (2005) Structural and mutational analysis of the SBDS protein family. Insight into the leukemia-associated Shwachman-Diamond Syndrome. Journal of Biological Chemistry, 280, 19221 19229. (Pubitemid 41379629)
49. Shi, Y., Zhai, H., Wang, X., Han, Z., Liu, C., Lan, M., Du, J., Guo, C., Zhang, Y., Wu, K. Fan, D. (2004) Ribosomal proteins S13 and L23 promote multidrug resistance in gastric cancer cells by suppressing drug-induced apoptosis. Experimental Cell Research, 296, 337 346. (Pubitemid 38624654)
50. Shwachman, H., Diamond, L.K., Oski, F.A. Khaw, K.T. (1964) The Syndrome of Pancreatic Insufficiency and Bone Marrow Dysfunction. Journal of Pediatrics, 65, 645 663.
51. Smith, O.P., Hann, I.M., Chessells, J.M., Reeves, B.R. Milla, P. (1996) Haematological abnormalities in Shwachman-Diamond syndrome. British Journal of Haematology, 94, 279 284. (Pubitemid 26247985)
52. Smyth, G.K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Statistical Applications in Genetics and Molecular Biology, 3, Article3.
53. Takagi, M., Sueishi, M., Saiwaki, T., Kametaka, A. Yoneda, Y. (2001) A novel nucleolar protein, NIFK, interacts with the forkhead associated domain of Ki-67 antigen in mitosis. Journal of Biological Chemistry, 276, 25386 25391.
54. Takagi, M., Absalon, M.J., McLure, K.G. Kastan, M.B. (2005) Regulation of p53 translation and induction after DNA damage by ribosomal protein L26 and nucleolin. Cell, 123, 49 63. (Pubitemid 41414528)
55. Virbasius, J.V. Scarpulla, R.C. (1994) Activation of the human mitochondrial transcription factor A gene by nuclear respiratory factors: a potential regulatory link between nuclear and mitochondrial gene expression in organelle biogenesis. Proceedings of the National Academy of Sciences of the United States of America, 91, 1309 1313. (Pubitemid 24059000)
56. Wang, H., Zhao, L.N., Li, K.Z., Ling, R., Li, X.J. Wang, L. (2006) Overexpression of ribosomal protein L15 is associated with cell proliferation in gastric cancer. BMC Cancer, 6, 91.
57. Wessels, D., Srikantha, T., Yi, S., Kuhl, S., Aravind, L. Soll, D.R. (2006) The Shwachman-Bodian-Diamond syndrome gene encodes an RNA-binding protein that localizes to the pseudopod of Dictyostelium amoebae during chemotaxis. Journal of Cell Science, 119, 370 379. (Pubitemid 43210705)
58. Wu, L.F., Hughes, T.R., Davierwala, A.P., Robinson, M.D., Stoughton, R. Altschuler, S.J. (2002) Large-scale prediction of Saccharomyces cerevisiae gene function using overlapping transcriptional clusters. Nature Genetics, 31, 255 265.
59. Yanagida, M., Hayano, T., Yamauchi, Y., Shinkawa, T., Natsume, T., Isobe, T. Takahashi, N. (2004) Human fibrillarin forms a sub-complex with splicing factor 2-associated p32, protein arginine methyltransferases, and tubulins alpha 3 and beta 1 that is independent of its association with preribosomal ribonucleoprotein complexes. Journal of Biological Chemistry, 279, 1607 1614. (Pubitemid 38084425)
60. Yoganathan, T., Bhat, N.K. Sells, B.H. (1992) A positive regulator of the ribosomal protein gene, beta factor, belongs to the ETS oncoprotein family. Biochemical Journal, 287 (Pt 2), 349 353.
61. Yoo, Y.A., Kim, M.J., Park, J.K., Chung, Y.M., Lee, J.H., Chi, S.G., Kim, J.S. Yoo, Y.D. (2005) Mitochondrial ribosomal protein L41 suppresses cell growth in association with p53 and p27Kip1. Molecular and Cellular Biology, 25, 6603 6616. (Pubitemid 41023234)
62. Yoshihama, M., Uechi, T., Asakawa, S., Kawasaki, K., Kato, S., Higa, S., Maeda, N., Minoshima, S., Tanaka, T., Shimizu, N. Kenmochi, N. (2002) The human ribosomal protein genes: sequencing and comparative analysis of 73 genes. Genome Research, 12, 379 390. (Pubitemid 34233012)
63. Zhang, Y., Wolf, G.W., Bhat, K., Jin, A., Allio, T., Burkhart, W.A. Xiong, Y. (2003) Ribosomal protein L11 negatively regulates oncoprotein MDM2 and mediates a p53-dependent ribosomal-stress checkpoint pathway. Molecular and Cellular Biology, 23, 8902 8912. (Pubitemid 37433388)
64. Zhang, S., Shi, M., Hui, C.C. Rommens, J.M. (2006) Loss of the mouse ortholog of the shwachman-diamond syndrome gene (Sbds) results in early embryonic lethality. Molecular and Cellular Biology, 26, 6656 6663. (Pubitemid 44277900)