Deficiency of the ribosome biogenesis gene Sbds in hematopoietic stem and progenitor cells causes neutropenia in mice by attenuating lineage progression in myelocytes

Haematologica

Volumn 100, Issue 10, 2015, Pages 1285-1293

  Zambetti, Noemi A ^a   Bindels, Eric M J ^a   Van Strien, Paulina M H ^a   Valkhof, Marijke G ^a,b   Adisty, Maria N ^a   Hoogenboezem, Remco M ^a   Sanders, Mathijs A ^a   Rommens, Johanna M ^c   Touw, Ivo P ^a   Raaijmakers, Marc H G P ^a  

^a ERASMUS MC CANCER INSTITUTE   (Netherlands)

^b SANQUIN RESEARCH   (Netherlands)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; CCAAT ENHANCER BINDING PROTEIN; CEBPA PROTEIN, MOUSE; PROTEIN; SBDS PROTEIN, MOUSE;

ADULT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BIOGENESIS; BONE MARROW CELL; CELL DIFFERENTIATION; CELL LINEAGE; DOWN REGULATION; EMBRYO; GENE; GENETIC ANALYSIS; GENOTYPE; HEPATOCYTE TRANSPLANTATION; MOUSE; NEUTROPENIA; NONHUMAN; PHENOTYPE; PROMYELOCYTE; RIBOSOME; SBDS GENE; SHWACHMAN SYNDROME; SIGNAL TRANSDUCTION; STEM CELL; ANIMAL; BONE MARROW DISEASE; CELL CYCLE; CYTOLOGY; DISEASE MODEL; EXOCRINE PANCREATIC INSUFFICIENCY; GENE DELETION; GENETICS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; KNOCKOUT MOUSE; LIPOMATOSIS; METABOLISM;

ANIMALS; APOPTOSIS; BONE MARROW DISEASES; CCAAT-ENHANCER-BINDING PROTEINS; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; DISEASE MODELS, ANIMAL; EXOCRINE PANCREATIC INSUFFICIENCY; GENE DELETION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; LIPOMATOSIS; MICE; MICE, KNOCKOUT; MYELOID CELLS; NEUTROPENIA; PROTEINS; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84943274669     PISSN: 03906078     EISSN: 15928721     Source Type: Journal    
DOI: 10.3324/haematol.2015.131573     Document Type: Article

References (50)

1. Shwachman H, Diamond LK, Oski FA, Khaw KT. The Syndrome of Pancreatic Insufficiency and Bone Marrow Dysfunction. J Pediatr. 1964;65:645-663.
2. Huang JN, Shimamura A. Clinical spectrum and molecular pathophysiology of Shwachman-Diamond syndrome. Curr Opin Hematol. 2011;18(1):30-35.
3. Tamary H, Alter BP. Current diagnosis of inherited bone marrow failure syndromes. Pediatr Hematol Oncol. 2007;24(2):87-99.
4. Mack DR, Forstner GG, Wilschanski M, Freedman MH, Durie PR. Shwachman syndrome: Exocrine pancreatic dysfunction and variable phenotypic expression. Gastroenterology. 1996;111(6):1593-1602.
5. Ginzberg H, Shin J, Ellis L, et al. Shwachman syndrome: phenotypic manifestations of sibling sets and isolated cases in a large patient cohort are similar. J Pediatr. 1999;135(1):81-88.
6. Dror Y. Shwachman-Diamond syndrome. Pediatr Blood Cancer. 2005;45(7):892-901.
7. Donadieu J, Fenneteau O, Beaupain B, et al. Classification of and risk factors for hemato-logic complications in a French national cohort of 102 patients with Shwachman-Diamond syndrome. Haematologica. 2012; 97(9):1312-1319.
8. Myers KC, Bolyard AA, Otto B, et al. Variable Clinical Presentation of Shwachman-Diamond Syndrome: Update from the North American Shwachman-Diamond Syndrome Registry. J Pediatr. 2014;164(4):866-870.
9. Boocock GR, Morrison JA, Popovic M, et al. Mutations in SBDS are associated with Shwachman-Diamond syndrome. Nat Genet. 2003;33(1):97-101.
10. Finch AJ, Hilcenko C, Basse N, et al. Uncoupling of GTP hydrolysis from eIF6 release on the ribosome causes Shwachman-Diamond syndrome. Gene Dev. 2011;25(9): 917-929.
11. Menne TF, Goyenechea B, Sanchez-Puig N, et al. The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast. Nat Genet. 2007;39(4):486-495.
12. Wong CC, Traynor D, Basse N, Kay RR, Warren AJ. Defective ribosome assembly in Shwachman-Diamond syndrome. Blood. 2011;118(16):4305-4312.
13. Burwick N, Coats SA, Nakamura T, Shimamura A. Impaired ribosomal subunit association in Shwachman-Diamond syndrome. Blood. 2012;120(26):5143-5152.
14. De Keersmaecker K, Sulima SO, Dinman JD. Ribosomopathies and the paradox of cellular hypo- to hyperproliferation. Blood. 2015; 125(9):1377-1382.
15. Ruggero D, Shimamura A. Marrow failure: a window into ribosome biology. Blood. 2014;124(18):2784-2792.
16. Zhang S, Shi M, Hui CC, Rommens JM. Loss of the mouse ortholog of the shwach-man-diamond syndrome gene (Sbds) results in early embryonic lethality. Mol Cell Biol. 2006;26(17):6656-6663.
17. Rawls AS, Gregory AD, Woloszynek JR, Liu FL, Link DC. Lentiviral-mediated RNAi inhibition of Sbds in murine hematopoietic progenitors impairs their hematopoietic potential. Blood. 2007;110(7):2414-2422.
18. Zhang P, Iwasaki-Arai J, Iwasaki H, et al. Enhancement of hematopoietic stem cell repopulating capacity and self-renewal in the absence of the transcription factor C/EBP alpha. Immunity. 2004;21(6):853-863.
19. Wòlfler A, Oorschot AADV, Haanstra JR, et al. Lineage-instructive function of C/EBP alpha in multipotent hematopoietic cells and early thymic progenitors. Blood. 2010;116 (20):4116-4125.
20. Ye M, Zhang H, Amabile G, et al. C/EBPa controls acquisition and maintenance of adult haematopoietic stem cell quiescence. Nat Cell Biol. 2013;15(4):385-394.
21. Tourlakis ME, Zhong J, Gandhi R, et al. Deficiency of Sbds in the Mouse Pancreas Leads to Features of Shwachman-Diamond Syndrome, With Loss of Zymogen Granules. Gastroenterology. 2012;143 (2):481-492.
22. Gröschel S, Sanders MA, Hoogenboezem R et al. A Single Oncogenic Enhancer Rearrangement Causes Concomitant EVI1 and GATA2 Deregulation in Leukemia. Cell. 2014;157(2):369-381.
23. Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102(43):15545-15550.
24. Flodby P, Barlow C, Kylefjord H, Ahrlund-Richter L, Xanthopoulos KG. Increased hepatic cell proliferation and lung abnormalities in mice deficient in CCAAT/enhancer binding protein alpha. J Biol Chem. 1996;271(40):24753-24760.
25. Aggett PJ, Cavanagh NPC, Matthew DJ, Pincott JR, Sutcliffe J, Harries JT. Shwachman's Syndrome. A Review of 21 Cases. Arch Dis Child. 1980;55(5):331-347.
26. Raaijmakers MH, Mukherjee S, Guo S, et al. Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature. 2010;464(7290):852-857.
27. Manz MG, Boettcher S. Emergency granu-lopoiesis. Nat Rev Immunol. 2014;14(5):302-314.
28. Satake S, Hirai H, Hayashi Y, et al. C/EBP beta Is Involved in the Amplification of Early Granulocyte Precursors during Candidemia-Induced "Emergency" Granulopoiesis. J Immunol. 2012;189(9):4546-4555.
29. Borregaard N, Sehested M, Nielsen BS, Sengelov H, Kjeldsen L. Biosynthesis of Granule Proteins in Normal Human Bone-Marrow Cells. Gelatinase Is a Marker of Terminal Neutrophil Differentiation. Blood. 1995;85(3):812-817.
30. Borregaard N, Cowland JB. Granules of the human neutrophilic polymorphonuclear leukocyte. Blood. 1997;89(10):3503-3521.
31. Bainton DF, Ullyot JL, Farquhar MG. The development of neutrophilic polymor-phonuclear leukocytes in human bone marrow. J Exp Med. 1971;134(4):907-934.
32. Wang QF, Cleaves R, Kummalue T, Nerlov C, Friedman AD. Cell cycle inhibition mediated by the outer surface of the C/EBPalpha basic region is required but not sufficient for granulopoiesis. Oncogene. 2003;22(17): 2548-2557.
33. Walkley CR, Purton LE, Snelling HJ, et al. Identification of the molecular requirements for an RAR alpha-mediated cell cycle arrest during granulocytic differentiation. Blood. 2004;103(4):1286-1295.
34. Bush TS, St Coeur M, Resendes KK, Rosmarin AG. GA-binding protein (GABP) and Sp1 are required, along with retinoid receptors, to mediate retinoic acid responsiveness of CD18 (beta 2 leukocyte integrin): a novel mechanism of transcriptional regulation in myeloid cells. Blood. 2003;101(1): 311-317.
35. Fumagalli S, Thomas G. The role of p53 in ribosomopathies. Semin Hematol. 2011;48 (2):97-105.
36. Elghetany MT, Alter BP. p53 protein overex-pression in bone marrow biopsies of patients with Shwachman-Diamond syndrome has a prevalence similar to that of patients with refractory anemia. Arch Pathol Lab Med. 2002;126(4):452-455.
37. Kastner P, Lawrence HJ, Waltzinger C, Ghyselinck NB, Chambon P, Chan S. Positive and negative regulation of granu-lopoiesis by endogenous RARalpha. Blood. 2001;97(5):1314-1320.
38. Labrecque J, Allan D, Chambon P, Iscove NN, Lohnes D, Hoang T. Impaired granulo-cytic differentiation in vitro in hematopoiet-ic cells lacking retinoic acid receptors alpha1 and gamma. Blood. 1998;92(2):607-615.
39. Signer RAJ, Magee JA, Salic A, Morrison SJ. Haematopoietic stem cells require a highly regulated protein synthesis rate. Nature. 2014;509(7498):49-54.
40. Perdahl EB, Naprstek BL, Wallace WC, Lipton JM. Erythroid Failure in Diamond-Blackfan Anemia Is Characterized by Apoptosis. Blood. 1994;83(3):645-650.
41. Dutt S, Narla A, Lin K, et al. Haploinsufficiency for ribosomal protein genes causes selective activation of p53 in human erythroid progenitor cells. Blood. 2011;117(9):2567-2576.
42. Dror Y, Freedman MH. Shwachman-Diamond syndrome: An inherited preleukemic bone marrow failure disorder with aberrant hematopoietic progenitors and faulty marrow microenvironment. Blood. 1999;94(9):3048-3054.
43. Provost E, Wehner KA, Zhong XG, et al. Ribosomal biogenesis genes play an essential and p53-independent role in zebrafish pancreas development. Development. 2012;139(17):3232-3241.
44. Mercuri A, Cannata E, Perbellini O, et al. Immunophenotypic analysis of hematopoiesis in patients suffering from Shwachman-Bodian-Diamond syndrome. Eur J Haematol. 2014. Nov 17. [Epub ahead of print].
45. Saunders EF, Gall G, Freedman MH. Granulopoiesis in Shwachman's syndrome (pancreatic insufficiency and bone marrow dysfunction). Pediatrics. 1979;64(4):515-519.
46. Dror Y, Freedman MH. Shwachman-Diamond syndrome marrow cells show abnormally increased apoptosis mediated through the Fas pathway. Blood. 2001; 97(10):3011-3016.
47. Glaubach T, Minella AC, Corey SJ. Cellular stress pathways in pediatric bone marrow failure syndromes: many roads lead to neu-tropenia. Pediatr Res. 2014;75(1 2):189-195.
48. Yost CC, Denis MM, Lindemann S, et al. Activated polymorphonuclear leukocytes rapidly synthesize retinoic acid receptor-alpha: a mechanism for translational control of transcriptional events. J Exp Med. 2004; 200(5):671-680.
49. Ludwig LS, Gazda HT, Eng JC, et al. Altered translation of GATA1 in Diamond-Blackfan anemia. Nat Med. 2014;20(7):748-753.
50. Tulpule A, Kelley JM, Lensch MW, et al. Pluripotent stem cell models of Shwachman-Diamond syndrome reveal a common mechanism for pancreatic and hematopoietic dysfunction. Cell Stem Cell. 2013;12(6):727-736.