Transcriptome analysis reveals a ribosome constituents disorder involved in the RPL5 downregulated zebrafish model of Diamond-Blackfan anemia

BMC Medical Genomics

Volumn 9, Issue 1, 2016, Pages

  Wan, Yang ^a   Zhang, Qian ^b   Zhang, Zhaojun ^b   Song, Binfeng ^c   Wang, Xiaomin ^a   Zhang, Yingchi ^a   Jia, Qiong ^c   Cheng, Tao ^a   Zhu, Xiaofan ^a   Leung, Anskar Yu Hung ^d   Yuan, Weiping ^a   Jia, Haibo ^c   Fang, Xiangdong ^b  

^a INSTITUTE OF HEMATOLOGY AND BLOOD DISEASES HOSPITAL   (China)

^b Chinese Academy of Sciences and China National Center for Bioinformation   (China)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^d UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

DBA; ncRNA seq; RNA seq; RPL5; Zebrafish

Indexed keywords

AMINOACYL TRANSFER RNA; LONG UNTRANSLATED RNA; MICRORNA; RIBOSOME PROTEIN; RPL5 PROTEIN; SMALL UNTRANSLATED RNA; TRANSCRIPTOME; UNCLASSIFIED DRUG; HEMOGLOBIN; MORPHOLINO OLIGONUCLEOTIDE; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOGENESIS; BLACKFAN DIAMOND ANEMIA; CELL CYCLE; CELL CYCLE G1 PHASE; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE S PHASE; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA REPLICATION; DOWN REGULATION; ERYTHROPOIESIS; GENE EXPRESSION; GENE TARGETING; HAPLOINSUFFICIENCY; HEMATOPOIESIS; MOLECULAR PATHOLOGY; MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN STRUCTURE; PURE RED CELL ANEMIA; RIBOSOME; RNA PROCESSING; RNA SEQUENCE; RNA SYNTHESIS; RNA TRANSLATION; SPLICEOSOME; UPREGULATION; ZEBRA FISH; ANIMAL; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; METABOLISM; NONMAMMALIAN EMBRYO; SIGNAL TRANSDUCTION;

ANEMIA, DIAMOND-BLACKFAN; ANIMALS; DISEASE MODELS, ANIMAL; DOWN-REGULATION; EMBRYO, NONMAMMALIAN; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HEMATOPOIESIS; HEMOGLOBINS; MICRORNAS; MORPHOLINOS; RIBOSOMES; RNA, LONG NONCODING; SIGNAL TRANSDUCTION; TRANSCRIPTOME; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84960502270     PISSN: None     EISSN: 17558794     Source Type: Journal    
DOI: 10.1186/s12920-016-0174-9     Document Type: Article

References (58)

1. Narla A, Ebert BL. Ribosomopathies: human disorders of ribosome dysfunction. Blood. 2010;115(16):3196-205.
2. Natalia DPG, Björn A, Monica P, Thiébaut N, Irma D, Sarah B, Gil T, Joakim K, Hans M, et al. The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat Genet. 1999;21:7.
3. Vlachos A, Blanc L, Lipton JM. Diamond Blackfan anemia: a model for the translational approach to understanding human disease. Expert Rev Hematol. 2014;7(3):359-72.
4. Vlachos A, Rosenberg PS, Atsidaftos E, Alter BP, Lipton JM. Incidence of neoplasia in Diamond Blackfan anemia: a report from the Diamond Blackfan anemia registry. Blood. 2012;119(16):3815-9.
5. Vlachos A, Muir E. How I treat Diamond-Blackfan anemia. Blood. 2010;116(19):3715-23.
6. Vlachos A, Dahl N, Dianzani I, Lipton JM. Clinical utility gene card for: Diamond-Blackfan Anemia - update 2013. Eur J Human Genet. 2013;21(4).
7. Mirabello L, Macari ER, Jessop L, Ellis SR, Myers T, Giri N, Taylor AM, McGrath KE, Humphries JM, Ballew BJ, et al. Whole-exome sequencing and functional studies identify RPS29 as a novel gene mutated in multicase Diamond-Blackfan anemia families. Blood. 2014;124(1):24-32.
8. Rosorius O. Human ribosomal protein l5 contains defined nuclear localization and export signals. J Biol Chem. 2000;275(16):12061-8.
9. Gazda HT, Sheen MR, Vlachos A, Choesmel V, O'Donohue MF, Schneider H, Darras N, Hasman C, Sieff CA, Newburger PE, et al. Ribosomal protein L5 and L11 mutations are associated with cleft palate and abnormal thumbs in Diamond-Blackfan anemia patients. Am J Hum Genet. 2008;83(6):769-80.
10. Garcon L, Ge J, Manjunath SH, Mills JA, Apicella M, Parikh S, Sullivan LM, Podsakoff GM, Gadue P, French DL, et al. Ribosomal and hematopoietic defects in induced pluripotent stem cells derived from Diamond Blackfan anemia patients. Blood. 2013;122(6):912-21.
11. Donati G, Peddigari S, Mercer CA, Thomas G. 5S ribosomal RNA is an essential component of a nascent ribosomal precursor complex that regulates the Hdm2-p53 checkpoint. Cell Reports. 2013;4(1):87-98.
12. Fumagalli S, Thomas G. The role of p53 in ribosomopathies. Semin Hematol. 2011;48(2):97-105.
13. Torihara H, Uechi T, Chakraborty A, Shinya M, Sakai N, Kenmochi N. Erythropoiesis failure due to RPS19 deficiency is independent of an activated Tp53 response in a zebrafish model of Diamond-Blackfan anaemia. Br J Haematol. 2011;152(5):648-54.
14. Jaako P, Flygare J, Olsson K, Quere R, Ehinger M, Henson A, Ellis S, Schambach A, Baum C, Richter J, et al. Mice with ribosomal protein S19 deficiency develop bone marrow failure and symptoms like patients with Diamond-Blackfan anemia. Blood. 2011;118(23):6087-96.
15. Moniz H, Gastou M, Leblanc T, Hurtaud C, Cretien A, Lecluse Y, Raslova H, Larghero J, Croisille L, Faubladier M, et al. Primary hematopoietic cells from DBA patients with mutations in RPL11 and RPS19 genes exhibit distinct erythroid phenotype in vitro. Cell Death Dis. 2012;3:e356.
16. Lawrie CH. microRNA expression in erythropoiesis and erythroid disorders. Br J Haematol. 2010;150(2):144-51.
17. Paralkar VR, Mishra T, Luan J, Yao Y, Kossenkov AV, Anderson SM, Dunagin M, Pimkin M, Gore M, Sun D, et al. Lineage and species-specific long noncoding RNAs during erythro-megakaryocytic development. Blood. 2014;123(12):1927-37.
18. Starczynowski DT, Kuchenbauer F, Argiropoulos B, Sung S, Morin R, Muranyi A, Hirst M, Hogge D, Marra M, Wells RA, et al. Identification of miR-145 and miR-146a as mediators of the 5q- syndrome phenotype. Nat Med. 2010;16(1):49-58.
19. Kaushik K, Leonard VE, Shamsudheen KV, Lalwani MK, Jalali S, Patowary A, Joshi A, Scaria V, Sivasubbu S. Dynamic expression of long non-coding RNAs (lncRNAs) in adult zebrafish. PLoS One. 2013;8(12):e83616.
20. Haque S, Kaushik K, Leonard VE, Kapoor S, Sivadas A, Joshi A, Scaria V, Sivasubbu S. Short stories on zebrafish long noncoding RNAs. Zebrafish. 2014;11(6):499-508.
21. Pauli A, Valen E, Lin MF, Garber M, Vastenhouw NL, Levin JZ, Fan L, Sandelin A, Rinn JL, Regev A, et al. Systematic identification of long noncoding RNAs expressed during zebrafish embryogenesis. Genome Res. 2012;22(3):577-91.
22. Alvarez-Dominguez JR, Hu W, Yuan B, Shi J, Park SS, Gromatzky AA, van Oudenaarden A, Lodish HF. Global discovery of erythroid long noncoding RNAs reveals novel regulators of red cell maturation. Blood. 2014;123(4):570-81.
23. Jia Q, Zhang Q, Zhang Z, Wang Y, Zhang W, Zhou Y, Wan Y, Cheng T, Zhu X, Fang X, et al. Transcriptome analysis of the zebrafish model of Diamond-Blackfan anemia from RPS19 deficiency via p53-dependent and -independent pathways. PLoS One. 2013;8(8):e71782.
24. Zhang Z, Jia H, Zhang Q, Wan Y, Zhou Y, Jia Q, Zhang W, Yuan W, Cheng T, Zhu X, et al. Assessment of hematopoietic failure due to Rpl11 deficiency in a zebrafish model of Diamond-Blackfan anemia by deep sequencing. BMC Genomics. 2013;14:896.
25. Song B, Zhang Q, Zhang Z, Wan Y, Jia Q, Wang X, Zhu X, Leung AY, Cheng T, Fang X, et al. Systematic transcriptome analysis of the zebrafish model of diamond-blackfan anemia induced by RPS24 deficiency. BMC Genomics. 2014;15:759.
26. Amsterdam A, Nissen RM, Sun Z, Swindell EC, Farrington S, Hopkins N. Identification of 315 genes essential for early zebrafish development. Proc Natl Acad Sci U S A. 2004;101(35):12792-7.
27. Boglev Y, Badrock AP, Trotter AJ, Du Q, Richardson EJ, Parslow AC, Markmiller SJ, Hall NE, de Jong-Curtain TA, Ng AY, et al. Autophagy induction is a Tor- and Tp53-independent cell survival response in a zebrafish model of disrupted ribosome biogenesis. PLoS Genet. 2013;9(2):e1003279.
28. Lu X, Li X, He Q, Gao J, Gao Y, Liu B, Liu F. miR-142-3p regulates the formation and differentiation of hematopoietic stem cells in vertebrates. Cell Res. 2013;23(12):1356-68.
29. Wang L, Fu C, Fan H, Du T, Dong M, Chen Y, Jin Y, Zhou Y, Deng M, Gu A, et al. miR-34b regulates multiciliogenesis during organ formation in zebrafish. Development. 2013;140(13):2755-64.
30. Bertrand JY, Kim AD, Teng S, Traver D. CD41+ cc-myb + precursors colonize the zebrafish pronephros by a novel migration route to initiate adult hematopoiesis. Development. 2008;135(10):1853-62.
31. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, Pfeffer S, Rice A, Kamphorst AO, Landthaler M, et al. A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 2007;129(7):1401-14.
32. Bartel DP. MicroRNAs: Target recognition and regulatory functions. Cell. 2009;136(2):215-33.
33. Sood R, Liu P. Novel insights into the genetic controls of primitive and definitive hematopoiesis from zebrafish models. Advances Hematol. 2012;2012:830703.
34. Patterson LJ, Gering M, Patient R. Scl is required for dorsal aorta as well as blood formation in zebrafish embryos. Blood. 2005;105(9):3502-11.
35. Mudumana SP, Hentschel D, Liu Y, Vasilyev A, Drummond IA. odd skipped related1 reveals a novel role for endoderm in regulating kidney versus vascular cell fate. Development. 2008;135(20):3355-67.
36. Young SRL, Mumaw C, Marrs JA, Skalnik DG. Antisense targeting of CXXC finger protein 1 inhibits genomic cytosine methylation and primitive hematopoiesis in zebrafish. J Biol Chem. 2006;281(48):37034-44.
37. Zhang Y, Morimoto K, Danilova N, Zhang B, Lin S. Zebrafish models for dyskeratosis congenita reveal critical roles of p53 activation contributing to hematopoietic defects through RNA processing. PLoS One. 2012;7(1):e30188.
38. Burns CE, Galloway JL, Smith AC, Keefe MD, Cashman TJ, Paik EJ, Mayhall EA, Amsterdam AH, Zon LI. A genetic screen in zebrafish defines a hierarchical network of pathways required for hematopoietic stem cell emergence. Blood. 2009;113(23):5776-82.
39. Craven SE, French D, Ye W, de Sauvage F, Rosenthal A. Loss of Hspa9b in zebrafish recapitulates the ineffective hematopoiesis of the myelodysplastic syndrome. Blood. 2005;105(9):3528-34.
40. Uechi T, Nakajima Y, Chakraborty A, Torihara H, Higa S, Kenmochi N. Deficiency of ribosomal protein S19 during early embryogenesis leads to reduction of erythrocytes in a zebrafish model of Diamond-Blackfan anemia. Hum Mol Genet. 2008;17(20):3204-11.
41. Suzuki HI, Yamagata K, Sugimoto K, Iwamoto T, Kato S, Miyazono K. Modulation of microRNA processing by p53. Nature. 2009;460(7254):529-33.
42. Payne EM, Virgilio M, Narla A, Sun H, Levine M, Paw BH, Berliner N, Look AT, Ebert BL, Khanna-Gupta A. L-Leucine improves the anemia and developmental defects associated with Diamond-Blackfan anemia and del(5q) MDS by activating the mTOR pathway. Blood. 2012;120(11):2214-24.
43. Jaako P, Debnath S, Olsson K, Bryder D, Flygare J, Karlsson S. Dietary L-leucine improves the anemia in a mouse model for Diamond-Blackfan anemia. Blood. 2012;120(11):2225-8.
44. Westerfield M, Doerry E, Douglas S. Zebrafish in the Net. Trends Genet TIG. 1999;15(6):248-9.
45. Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Deve Dynamics Off Publication Am Assoc Anatomists. 1995;203(3):253-310.
46. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511-5.
47. Roberts A, Trapnell C, Donaghey J, Rinn JL, Pachter L. Improving RNA-Seq expression estimates by correcting for fragment bias. Genome Biol. 2011;12(3):R22.
48. Jiang H, Wong WH. Statistical inferences for isoform expression in RNA-Seq. Bioinformatics. 2009;25(8):1026-32.
49. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks (vol 7, pg 562, 2012). Nat Protoc. 2014;9(10):2513.
50. Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G. CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res. 2007;35:W345-9.
51. Punta M, Coggill PC, Eberhardt RY, Mistry J, Tate J, Boursnell C, Pang N, Forslund K, Ceric G, Clements J, et al. The Pfam protein families database. Nucleic Acids Res. 2012;40(D1):D290-301.
52. Rice P, Longden I, Bleasby A. EMBOSS: The European molecular biology open software suite. Trends Genet. 2000;16(6):276-7.
53. Huang PJ, Liu YC, Lee CC, Lin WC, Gan RR, Lyu PC, Tang P. DSAP: deep-sequencing small RNA analysis pipeline. Nucleic Acids Res. 2010;38(Web Server issue):W385-91.
54. da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44-57.
55. Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009;37(1):1-13.
56. Schmitt T, Ogris C, Sonnhammer EL. FunCoup 3.0: database of genome-wide functional coupling networks. Nucleic Acids Res. 2014;42(Database issue):D380-8.
57. Cline MS, Smoot M, Cerami E, Kuchinsky A, Landys N, Workman C, Christmas R, Avila-Campilo I, Creech M, Gross B, et al. Integration of biological networks and gene expression data using Cytoscape. Nat Protoc. 2007;2(10):2366-82.
58. Thompson MA, Ransom DG, Pratt SJ, MacLennan H, Kieran MW, Detrich HW, Vail B, Huber TL, Paw B, Brownlie AJ, et al. The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis. Dev Biol. 1998;197(2):248-69.