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Shwachman–Diamond syndrome: implications for understanding the molecular basis of leukaemia

Published online by Cambridge University Press:  23 December 2008

Yigal Dror
Yigal Dror
Affiliation:
Cell Biology Program, Research Institute and the Marrow Failure and Myelodysplasia Program, Division of Haematology/Oncology, The Hospital for Sick Children and the University of Toronto, 555 University Avenue, Toronto, Ontario M5G 1X8, Canada. Tel. +1 416 813 8886; Fax: +1 416 813 5327; E-mail: [email protected]
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Abstract

Inherited bone marrow failure syndromes provide extremely useful genetic models for understanding leukaemogenesis because the initial genetic defect can be identified and the risk of leukaemia is very high. Shwachman–Diamond syndrome is one of the most common inherited bone marrow failure syndromes and an example of such a model. Here, I describe the malignant features of Shwachman–Diamond syndrome and discuss the potential molecular mechanisms that can lead to leukaemia.

Type
Review Article
Information
Expert Reviews in Molecular Medicine , Volume 10 , October 2008 , e38
Copyright
Copyright © Cambridge University Press 2008

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References

References

1Barabe, F. et al. (2007) Modeling the initiation and progression of human acute leukemia in mice. Science 316, 600-604CrossRefGoogle ScholarPubMed
2Hong, D. et al. (2008) Initiating and cancer-propagating cells in TEL-AML1-associated childhood leukemia. Science 319, 336-339CrossRefGoogle ScholarPubMed
3Vogelstein, B. and Kinzler, K.W. (2004) Cancer genes and the pathways they control. Nat Med 10, 789-799Google Scholar
4Garber, J.E. and Offit, K. (2005) Hereditary cancer predisposition syndromes. J Clin Oncol 23, 276-292Google Scholar
5Anderson, A.R. et al. (2006) Tumor morphology and phenotypic evolution driven by selective pressure from the microenvironment. Cell 127, 905-915CrossRefGoogle ScholarPubMed
6Folkman, J. (1990) What is the evidence that tumors are angiogenesis dependent? J Natl Cancer Inst 82, 4-6Google Scholar
7Hicklin, D.J. and Ellis, L.M. (2005) Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol 23, 1011-1027CrossRefGoogle ScholarPubMed
8Aguayo, A. et al. (2000) Angiogenesis in acute and chronic leukemias and myelodysplastic syndromes. Blood 96, 2240-2245Google Scholar
9Sloand, E.M. et al. (2006) Granulocyte colony-stimulating factor preferentially stimulates proliferation of monosomy 7 cells bearing the isoform IV receptor. Proc Natl Acad Sci U S A 103, 14483-14488CrossRefGoogle ScholarPubMed
10Liu, F. et al. (2008) Csf3r mutations in mice confer a strong clonal HSC advantage via activation of Stat5. J Clin Invest. 118, 946-955Google Scholar
11Li, X. et al. (2005) Ex vivo culture of Fancc-/- stem/progenitor cells predisposes cells to undergo apoptosis, and surviving stem/progenitor cells display cytogenetic abnormalities and an increased risk of malignancy. Blood 105, 3465-3471Google Scholar
12Li, J. et al. (2007) TNF-alpha induces leukemic clonal evolution ex vivo in Fanconi anemia group C murine stem cells. J Clin Invest 117, 3283-3295CrossRefGoogle Scholar
13Gatenby, R.A. (2006) Commentary, carcinogenesis as Darwinian evolution? Do the math! Int J Epidemiol 35, 1165-1167CrossRefGoogle ScholarPubMed
14Vineis, P. and Berwick, M. (2006) The population dynamics of cancer, a Darwinian perspective. Int J Epidemiol 35, 1151-1159Google Scholar
15Bagby, G.C. and Meyers, G. (2007) Bone marrow failure as a risk factor for clonal evolution, prospects for leukemia prevention. Hematology Am Soc Hematol Educ Program 2007, 40-46Google Scholar
16Dror, Y. (2006) Inherited Bone Marrow Failure Syndromes (3rd Edn), BlackwellCrossRefGoogle Scholar
17Alter, B.P. (2007) Diagnosis, genetics, and management of inherited bone marrow failure syndromes. Hematology Am Soc Hematol Educ Program 2007, 29-39CrossRefGoogle Scholar
18Houghtaling, S. et al. (2003) Epithelial cancer in Fanconi anemia complementation group D2 (Fancd2) knockout mice. Genes Dev 17, 2021-2035Google Scholar
19Ruggero, D. et al. (2003) Dyskeratosis congenita and cancer in mice deficient in ribosomal RNA modification. Science 299, 259-262CrossRefGoogle ScholarPubMed
20Putz, G. et al. (2006) AML1 deletion in adult mice causes splenomegaly and lymphomas. Oncogene 25, 929-939Google Scholar
21Steele, J.M. et al. (2006) Disease progression in recently diagnosed patients with inherited marrow failure syndromes, a Canadian Inherited Marrow Failure Registry (CIMFR) report. Pediatr Blood Cancer 47, 918-925CrossRefGoogle ScholarPubMed
22Dror, Y.Shwachman-Diamond syndrome. Pediatr Blood Cancer. 2005; 45, 892-901CrossRefGoogle ScholarPubMed
23Shwachman, H. (1964) The syndrome of pancreatic insufficiency and bone marrow dysfunction. J Pediatr 65, 645-663CrossRefGoogle ScholarPubMed
24Aggett, P.J. et al. (1980) Shwachman's syndrome. A review of 21 cases. Archives of Disease in Childhood 55, 331-347Google Scholar
25Boocock, G.R. et al. (2003) Mutations in SBDS are associated with Shwachman-Diamond syndrome. Nat Genet 33, 97-101CrossRefGoogle ScholarPubMed
26Tsai, P.H. et al. (1990) Fatal cyclophosphamide-induced congestive heart failure in a 10-year-old boy with Shwachman-Diamond syndrome and severe bone marrow failure treated with allogeneic bone marrow transplantation. Am J Pediatr Hematol Oncol 12, 472-476CrossRefGoogle Scholar
27Barrios, N. et al. (1991) Bone marrow transplant in Shwachman Diamond syndrome. Br J Haematol 79, 337-338CrossRefGoogle ScholarPubMed
28Dror, Y. et al. (2001) Immune function in patients with Shwachman-Diamond syndrome. Br J Haematol 114, 712-717Google Scholar
29Hudson, E. and Aldor, T. (1970) Pancreatic insufficiency and neutropenia with associated immunoglobulin deficit. Arch Intern Med 125, 314-316CrossRefGoogle ScholarPubMed
30Aggett, P.J. et al. (1979) An inherited defect of neutrophil mobility in Shwachman syndrome. J Pediatr 94, 391-394Google Scholar
31Dror, Y. and Freedman, M.H. (1999) Shwachman-Diamond syndrome, An inherited preleukemic bone marrow failure disorder with aberrant hematopoietic progenitors and faulty marrow microenvironment. Blood 94, 3048-3054CrossRefGoogle ScholarPubMed
32Mack, D.R. et al. (1996) Shwachman syndrome, exocrine pancreatic dysfunction and variable phenotypic expression. Gastroenterology 111, 1593-1602CrossRefGoogle ScholarPubMed
33Smith, O.P. et al. (1996) Haematological abnormalities in Shwachman-Diamond syndrome. Br J Haematol 94, 279-284Google Scholar
34Dror, Y. et al. (1998) Malignant myeloid transformation with isochromosome 7q in Shwachman-Diamond syndrome. Leukemia 12, 1591-1595Google Scholar
35Dror, Y. et al. (2002) Clonal evolution in marrows of patients with Shwachman-Diamond syndrome, a prospective 5-year follow-up study. Exp Hematol 30, 659-669Google Scholar
36Mandel, K. et al. (2002) A practical, comprehensive classification for pediatric myelodysplastic syndromes, the CCC system. J Pediatr Hematol Oncol 24, 596-605CrossRefGoogle ScholarPubMed
37Huijgens, P.C. et al. (1977) Syndrome of Shwachman and leukaemia. Scand J Haematol 18, 20-24Google Scholar
38Okcu, F., Roberts, W.M. and Chan, K.W. (1998) Bone marrow transplantation in Shwachman-Diamond syndrome, report of two cases and review of the literature. Bone Marrow Transplant 21, 849-851CrossRefGoogle ScholarPubMed
39Passmore, S.J. et al. (1995) Pediatric myelodysplasia, a study of 68 children and a new prognostic scoring system. Blood 85, 1742-1750Google Scholar
40Hsu, J.W. et al. (2002) Bone marrow transplantation in Shwachman-Diamond syndrome. Bone Marrow Transplant 30, 255-258Google Scholar
41Lai, C.H. et al. (2000) Identification of novel human genes evolutionarily conserved in Caenorhabditis elegans by comparative proteomics. Genome Res 10, 703-713Google Scholar
42Shammas, C. et al. (2005) Structural and mutational analysis of the SBDS protein family. Insight into the leukemia-associated Shwachman-Diamond Syndrome. J Biol Chem 280, 19221-19229Google Scholar
43Woloszynek, J.R. et al. (2004) Mutations of the SBDS gene are present in most patients with Shwachman-Diamond syndrome. Blood 104, 3588-3590CrossRefGoogle ScholarPubMed
44Austin, K.M., Leary, R.J. and Shimamura, A. (2005) The Shwachman-Diamond SBDS protein localizes to the nucleolus. Blood 106, 1253-1258Google Scholar
45Zhang, S. et al. (2006) Loss of the mouse ortholog of the shwachman-diamond syndrome gene (Sbds) results in early embryonic lethality. Mol Cell Biol 26, 6656-6663Google Scholar
46Ganapathi, K.A. et al. (2007) The human Shwachman-Diamond syndrome protein, SBDS, associates with ribosomal RNA. Blood 110, 1458-1465CrossRefGoogle ScholarPubMed
47Savchenko, A. et al. The Shwachman-Bodian-Diamond syndrome protein family is involved in RNA metabolism. J Biol Chem 280, 19213-19220CrossRefGoogle Scholar
48Menne, T.F. et al. (2007) The Shwachman-Bodian-Diamond syndrome protein mediates translational activation of ribosomes in yeast. Nat Genet 39, 486-495CrossRefGoogle ScholarPubMed
49Dror, Y. and Freedman, M.H. (2001) Shwachman-Diamond syndrome marrow cells show abnormally increased apoptosis mediated through the Fas pathway. Blood 97, 3011-3016CrossRefGoogle ScholarPubMed
50Rujkijyanont, P. et al. (2008) SBDS-deficient cells undergo accelerated apoptosis through the Fas-pathway. Haematologica 93, 363-371CrossRefGoogle ScholarPubMed
51Stepanovic, V. et al. (2004) The chemotaxis defect of Shwachman-Diamond Syndrome leukocytes. Cell Motil Cytoskel 57, 158-174Google Scholar
52Wessels, D. et al. (2006) The Shwachman-Bodian-Diamond syndrome gene encodes an RNA-binding protein that localizes to the pseudopod of Dictyostelium amoebae during chemotaxis. J Cell Sci 119, 370-379CrossRefGoogle Scholar
53Austin, K.M. et al. (2008) Mitotic spindle destabilization and genomic instability in Shwachman-Diamond syndrome. J Clin Invest 118, 1511-1518Google Scholar
54Rosenberg, P.S. et al. (2006) The incidence of leukemia and mortality from sepsis in patients with severe congenital neutropenia receiving long-term G-CSF therapy. Blood 107, 4628-4635CrossRefGoogle ScholarPubMed
55Kuijpers, T.W. et al. (2005) Hematologic abnormalities in Shwachman Diamond syndrome, lack of genotype-phenotype relationship. Blood 106, 356-361Google Scholar
56Davies, S.M. et al. (1997) Unrelated donor bone marrow transplantation for children and adolescents with aplastic anaemia or myelodysplasia. Br J Haematol 96, 749-756Google Scholar
57Freedman, M.H. et al. (2000) Myelodysplasia syndrome and acute myeloid leukemia in patients with congenital neutropenia receiving G-CSF therapy. Blood 96, 429-436Google Scholar
58Majeed, F. et al. (2005) Mutation analysis of SBDS in pediatric acute myeloblastic leukemia. Pediatr Blood Cancer 45, 920-924Google Scholar
59Hershkovits, B.S., Dagan, J. and Freier, S. (1999) Increased spontaneous chromosomal breakage in Shwachman syndrome. J Pediatr Gastroenterol Nutr 28, 449-450Google ScholarPubMed
60Tada, H. et al. (1987) A case of Shwachman syndrome with increased spontaneous chromosome breakage. Hum Genet 77, 289-291Google Scholar
61Fraccaro, M., Scappaticci, S. and Arico, M. (1988) Shwachman syndrome and chromosome breakage. Hum Genet 79, 194Google Scholar
62Koiffmann, C.P. et al. (1991) Is Shwachman syndrome (McKusick 26040) a chromosome breakage syndrome? Hum Genet 87, 106-107CrossRefGoogle ScholarPubMed
63Maserati, E. et al. (2006) Shwachman syndrome as mutator phenotype responsible for myeloid dysplasia/neoplasia through karyotype instability and chromosomes 7 and 20 anomalies. Genes Chromosomes Cancer 45, 375-382Google Scholar
64Thornley, I. et al. (2002) Abnormal telomere shortening in leucocytes of children with Shwachman-Diamond syndrome. Br J Haematol 117, 189-192CrossRefGoogle ScholarPubMed
65Calado, R.T. et al. (2007) Mutations in the SBDS gene in acquired aplastic anemia. Blood 110, 1141-1146CrossRefGoogle ScholarPubMed
66Hao, L.Y., Strong, M.A. and Greider, C.W. (2004) Phosphorylation of H2AX at short telomeres in T cells and fibroblasts. J Biol Chem. 279, 45148-45154CrossRefGoogle Scholar
67Counter, C.M. et al. (1992) Telomere shortening associated with chromosome instability is arrested in immortal cells which express telomerase activity. EMBO J 11, 1921-1929Google Scholar
68Smogorzewska, A. et al. (2002) DNA ligase IV-dependent NHEJ of deprotected mammalian telomeres in G1 and G2. Curr Biol 12, 1635-1644Google Scholar
69Londono-Vallejo, J.A. (2008) Telomere instability and cancer. Biochimie 90, 73-82Google Scholar
70Dokal, I. (2000) Dyskeratosis congenita in all its forms. Br J Haematol 110, 768-779Google Scholar
71Vlachos, A., Klein, G.W. and Lipton, J.M. (2001) The Diamond Blackfan Anemia Registry, tool for investigating the epidemiology and biology of Diamond-Blackfan anemia. J Pediatr Hematol Oncol 23, 377-382Google Scholar
72Taskinen, M. et al. (2008) Extended follow-up of the Finnish cartilage-hair hypoplasia cohort confirms high incidence of non-Hodgkin lymphoma and basal cell carcinoma. Am J Med Genet A 146A, 2370-2375Google Scholar
73Ebert, B.L. et al. (2008) Identification of RPS14 as a 5q-syndrome gene by RNA interference screen. Nature 451, 335-339Google Scholar
74Amsterdam, A. et al. (2004) Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biol 2, e139.CrossRefGoogle ScholarPubMed
75Rujkijyanont, P. et al. (2007) Leukaemia-related gene expression in bone marrow cells from patients with the preleukaemic disorder Shwachman-Diamond syndrome. Br J Haematol 137, 537-544CrossRefGoogle ScholarPubMed
76Ferrari, A. et al. (1990) Simultaneous occurrence of larynx carcinoma and acute blastic transformation in a patient with essential thrombocythemia. Haematologica 75, 488-489Google Scholar
77Loging, W.T. and Reisman, D. (1999) Elevated expression of ribosomal protein genes L37, RPP-1, and S2 in the presence of mutant p53. Cancer Epidemiol Biomarkers Prev 8, 1011-1016Google Scholar
78Kondoh, N. et al. (2001) Enhanced expression of S8, L12, L23a, L27 and L30 ribosomal protein mRNAs in human hepatocellular carcinoma. Anticancer Res 21, 2429-2433Google Scholar
79Carlsson, G. et al. (2004) Kostmann syndrome, severe congenital neutropenia associated with defective expression of Bcl-2, constitutive mitochondrial release of cytochrome c, and excessive apoptosis of myeloid progenitor cells. Blood 103, 3355-3361CrossRefGoogle ScholarPubMed
80Mempel, K. et al. (1991) Increased serum levels of granulocyte colony-stimulating factor in patients with severe congenital neutropenia. Blood 77, 1919-1922Google Scholar
81Ballmaier, M. et al. (1997) Thrombopoietin in patients with congenital thrombocytopenia and absent radii, elevated serum levels, normal receptor expression, but defective reactivity to thrombopoietin. Blood 90, 612-619Google Scholar
82Aizawa, S. et al. (1999) Bone marrow stroma from refractory anemia of myelodysplastic syndrome is defective in its ability to support normal CD34-positive cell proliferation and differentiation in vitro. Leuk Res 23, 239-246CrossRefGoogle ScholarPubMed
83Leung, E.W. et al. (2006) Shwachman-Diamond syndrome, an inherited model of a plastic anaemia with accelerated angiogenesis. Br J Haematol 133, 558-561Google Scholar
84Gasparini, G. et al. (2005) Angiogenic inhibitors, a new therapeutic strategy strategy in oncology. Nat Clin Pract Oncol 2, 562-577CrossRefGoogle ScholarPubMed
85List, A. et al. (2005) Efficacy of lenalidomide in myelodysplastic syndromes. N Engl J Med 352, 549-557CrossRefGoogle ScholarPubMed
86Pellagatti, A. et al. (2007) Lenalidomide inhibits the malignant clone and up-regulates the SPARC gene mapping to the commonly deleted region in 5q- syndrome patients. Proc Natl Acad Sci U S A 104, 11406-11411Google Scholar
87Kornfeld, S.J. et al. (1995) Shwachman-Diamond syndrome associated with hypogammaglobulinemia and growth hormone deficiency. J Allergy Clin Immunol. 96, 247-250CrossRefGoogle ScholarPubMed
88Pinkerton, C.R. et al. (2002) Immunodeficiency-related lymphoproliferative disorders, prospective data from the United Kingdom Children's Cancer Study Group Registry. Br J Haematol 118, 456-461CrossRefGoogle ScholarPubMed
89Guerra, N. et al. (2008) NKG2D-deficient mice are defective in tumor surveillance in models of spontaneous malignancy. Immunity 28, 571-580CrossRefGoogle ScholarPubMed

Further reading, resources and contacts

Bagby, G.C. and Meyers, G. (2007) Bone marrow failure as a risk factor for clonal evolution, prospects for leukemia prevention. Hematology American Society of Hematology Education Program Book 2007, 40-46.CrossRefGoogle Scholar
Bagby, G.C. and Meyers, G. (2007) Bone marrow failure as a risk factor for clonal evolution, prospects for leukemia prevention. Hematology American Society of Hematology Education Program Book 2007, 40-46.CrossRefGoogle Scholar