190
Views
4
CrossRef citations to date
0
Altmetric
Review

Shwachman-Diamond syndrome: diagnosis, pathogenesis and prognosis

, &
Pages 753-767 | Received 17 Mar 2017, Accepted 10 Aug 2017, Published online: 22 Aug 2017

References

  • Shwachman H, Diamond LK, Oski FA, et al. The syndrome of pancreatic insufficiency and bone marrow dysfunction. J Pediatr. 1964;65:645–663.
  • Bodian M, Sheldon W, Lightwood R. Congenital hypoplasia of the exocrine pancreas. Acta Paediatr. 1964;53:282–293.
  • Donadieu J, Fenneteau O, Beaupain B, et al. Classification of and risk factors for hematologic complications in a French national cohort of 102 patients with Shwachman-Diamond syndrome. Haematologica. 2012;97(9):1312–1319.
  • 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.
  • Rothbaum R, Perrault J, Vlachos A, et al. Shwachman-Diamond syndrome: report from an international conference. J Pediatr. 2002;141(2):266–270.
  • Kerr EN, Elli L, Dupuis A, et al. The behavioral phenotype of school-age children with Shwachman Diamond syndrome indicates neurocognitive dysfunction with loss of Shwachman-Bodian-Diamond syndrome gene function. J Pediatr. 2010;156(3):433–438.
  • Boocock GR, Morrison JA, Popovic M, et al. Mutations in SBDS are associated with Shwachman-Diamond syndrome. Nat Genet. 2003;33(1):97–101.
  • Finch AJ, Hilcenko C, Basse N, et al. Uncoupling of GTP hydrolysis from EIF6 release on the ribosome causes Shwachman-Diamond syndrome. Genes Dev. 2011;25(9):917–929.
  • Dhanraj S, Matveev A, Li H, et al. Biallelic mutations in DNAJC21 cause Shwachman-Diamond syndrome. Blood. 2017;129(11):1557–1562.
  • Stepensky P, Chacón-Flores M, Kim KH, et al. Mutations in EFL1, an SBDS partner, are associated with infantile pancytopenia, exocrine pancreatic insufficiency and skeletal anomalies in a Shwachman-Diamond like syndrome. J Med Genet Published Online First. 2017;March 22. Doi: 10.1136/jmedgenet-2016-104366
  • Greber BJ, Boehringer D, Montellese C, et al. Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit. Nat Struct Mol Biol. 2012;19:1228–1233.
  • Mack DR, Forstner GG, Wilschanski M, et al. Shwachman syndrome: exocrine pancreatic dysfunction and variable phenotypic expression. Gastroenterology. 1996;111(6):1593–1602.
  • Toiviainen-Salo S, Raade M, Durie PR, et al. Magnetic resonance imaging findings of the pancreas in patients with Shwachman-Diamond syndrome and mutations in the SBDS gene. J Pediatr. 2008;152(3):434–436.
  • Gana S, Sainati L, Frau MR, et al. Shwachman-Diamond syndrome and Type 1 diabetes mellitus: more than a chance association? Exp Clin Endocrinol Diabetes. 2011;119(10):610–612.
  • Ip WF, Dupuis A, Ellis L, et al. Serum pancreatic enzymes define the pancreatic phenotype in patients with Shwachman-Diamond syndrome. J Pediatr. 2002;141(2):259–265.
  • Smith OP, Hann IM, Chessells JM, et al. Haematological abnormalities in Shwachman-Diamond syndrome. Br J Haematol. 1996;94(2):279–284.
  • Woods WG, Krivit W, Lubin BH, et al. Aplastic anemia associated with the Shwachman syndrome. In vivo and in vitro observations. Am J Pediatr Hematol Oncol. 1981;3(4):347–351.
  • 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.
  • Aggett PJ, Cavanagh NP, Matthew DJ, et al. Shwachman’s syndrome. A review of 21 cases. Arch Dis Child. 1980;55(5):331–347.
  • Nacci L, Valli R, Pinto MR, et al. Parental origin of the deletion del(20q) in Shwachman-Diamond patients and loss of the paternally derived allele of the imprinted L3MBTL1 gene. Genes Chromosomes Cancer. 2017;56(1):51–58.
  • Donadieu J, Leblanc T, Bader Meunier B, et al. Analysis of risk factors for myelodysplasias, leukemias and death from infection among patients with congenital neutropenia. Experience of the French Severe Chronic Neutropenia Study Group. Haematologica. 2005;90(1):45–53.
  • Stepanovic V, Wessels D, Goldman FD, et al. The chemotaxis defect of Shwachman-Diamond syndrome leukocytes. Cell Motil Cytoskeleton. 2004;57(3):158–174.
  • Dror Y, Donadieu J, Koglmeier J, et al. Draft consensus guidelines for diagnosis and treatment of Shwachman-Diamond syndrome. Ann N Y Acad Sci. 2011;1242:40–55.
  • Pressato B, Valli R, Marletta C, et al. Cytogenetic monitoring in Shwachman-Diamond syndrome: a note on clonal progression and a practical warning. J Pediatr Hematol Oncol. 2015;37(4):307–310.
  • Mäkitie O, Ellis L, Durie PR, et al. Skeletal phenotype in patients with Shwachman-Diamond syndrome and mutations in SBDS. Clin Genet. 2004;65(2):101–112.
  • Levin TL, Mäkitie O, Berdon WE, et al. Shwachman-Bodian-Diamond syndrome: metaphyseal chondrodysplasia in children with pancreatic insufficiency and neutropenia. Pediatr Radiol. 2015;45(7):1066–1071.
  • Toiviainen-Salo S, Makitie O, Mannerkoski M, et al. Shwachman–Diamond syndrome is associated with structural brain alterations on MRI. Am J Med Genet Part A. 2008;146A:1558–1564.
  • Perobelli S, Alessandrini F, Zoccatelli G. Diffuse alterations in grey and white matter associated with cognitive impairment in Shwachman–Diamond syndrome: evidence from a multimodal approach. Neuro Image Clinical. 2015;7(2015):721–731.
  • Cipolli M. Shwachman-Diamond syndrome: clinical phenotypes. Pancreatology. 2001;1(5):543–548.
  • Mack DR. Shwachman-Diamond syndrome. J Pediatr. 2002;141(2):164–165.
  • Woloszynek JR, Rothbaum RJ, Rawls AS, et al. Mutations of the SBDS gene are present in most patients with Shwachman-Diamond syndrome. Blood. 2004;104(12):3588–3590.
  • Kuijpers TW, Nannenberg E, Alders M, et al. Congenital aplastic anemia caused by mutations in the SBDS gene: a rare presentation of Shwachman-Diamond Syndrome. Pediatrics. 2004;114(3):e387–391.
  • 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;164:866–870.
  • Topa A, Tulinius M, Oldfors A, et al. Novel myopathy in a newborn with Shwachman–Diamond syndrome and review of neonatal presentation. Am J MedGenet A. 2016;170A(5):1155–1164.
  • Carvalho CM, Zuccherato LW, Williams CL, et al. Structural variation and missense mutation in SBDS associated with Shwachman-Diamond syndrome. BMC Med Genet. 2014;15:64.
  • Zhang MY, Keel SB, Walsh T, et al. Genomic analysis of bone marrow failure and myelodysplastic syndromes reveals phenotypic and diagnostic complexity. Haematologica. 2015;100(1):42–48.
  • Keel SB, Scott A, Sanchez-Bonilla M, et al. Genetic features of myelodysplastic syndrome and aplastic anemia in pediatric and young adult patients. Haematologica. 2016;101(11):1343–1350.
  • Cesaro S, Oneto R, Messina C, et al. Haematopoietic stem cell transplantation for Shwachman-Diamond disease: a study from the European Group for blood and marrow transplantation. Br J Haematol. 2005;131(2):231–236.
  • Toiviainen-Salo S, Pitkänen O, Holmström M, et al. Myocardial function in patients with Shwachman-Diamond syndrome: aspects to consider before stem cell transplantation. Pediatr Blood Cancer. 2008;51(4):461–467.
  • Sauer M, Zeidler C, Meissner B, et al. Substitution of cyclophosphamide and busulfan by fludarabine, treosulfan and melphalan in a preparative regimen for children and adolescents with Shwachman-Diamond syndrome. Bone Marrow Transplant. 2007;39(3):143–147.
  • Bahtla D, Davies SM, Shenoy S, et al. Reduced-intensity conditioning is effective and safe for transplantation of patients with Shwachman-Diamond syndrome. Bone Marrow Transplant. 2008;42(3):159–165.
  • Woods WG, Roloff JS, Lukens JN, et al. The occurrence of leukemia in patients with the Shwachman syndrome. J Pediatr. 1981;99(3):425–428.
  • Dalle JH, De Latour RP. Allogeneic hematopoietic stem cell transplantation for inherited bone marrow failure syndromes. Int J Hematol. 2016;103:373–379.
  • Lindsley RC, Saber W, Mar BG, et al. Prognostic mutations in myelodysplastic syndrome after stem-cell transplantation. N Engl J Med. 2017;376(6):536–547.
  • Menne TB, Goyenechea B, Nuria 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.
  • Austin KM, Gupta ML Jr, Coats SA, et al. Mitotic spindle destabilization and genomic instability in Shwachman-Diamond syndrome. J Clin Invest. 2008;118(4):1511–1518.
  • Ball HL, Zhang B, Riches JJ, et al. Shwachman-Bodian Diamond syndrome is a multi-functional protein implicated in cellular stress responses. Hum Mol Genet. 2009;18(19):3684–3695.
  • Raaijmakers MHGP, Mukherjee S, Guo S, et al. Bone progenitor dysfunction induces myelodysplasia and secondary leukemia. Nature. 2010;464(7290):852–857.
  • Orelio C, Kuijpers TW. Shwachman-Diamond syndrome neutrophils have altered chemoattractant-induced F-actin polymerization and polarization characteristics. Haematologica. 2009;94:409–413.
  • Zhang S, Shi M, Hui CC, et al. Loss of the mouse ortholog of the Shwachman-Diamond syndrome gene (Sbds) results in early embryonic lethality. Mol Cell Biol. 2006;26(17):6656–6663.
  • Austin KM, Leary RJ, Shimamura A. The Shwachman-Diamond SBDS protein localizes to the nucleolus. Blood. 2005;106(4):1253–1258.
  • Nakashima E, Mabuchi A, Makita Y, et al. Novel SBDS mutations caused by gene conversion in Japanese patients with Shwachman-Diamond syndrome. Hum Genet. 2004;114(4):345–348.
  • Nicolis E, Bonizzato A, Assael BM, et al. Identification of novel mutations in patients with Shwachman-Diamond syndrome. Hum Mutat. 2005;25(4):410.
  • Shammas C, Menne TF, Hilcenko C, et al. Structural and mutational analysis of the SBDS protein family. Insight into the leukemia-associated Shwachman-Diamond Syndrome. J Biol Chem. 2005;280(19):19221–19229.
  • Maserati E, Minelli A, Pressato B, et al. Shwachman syndrome as mutator phenotype responsible for myeloid dysplasia/neoplasia through karyotype instability and chromosomes 7 and 20 anomalies. Genes Chromosomes Cancer. 2006;45(4):375–382.
  • Taneichi H, Kanegane H, Futatani T, et al. Clinical and genetic analyses of presumed Shwachman-Diamond syndrome in Japan. Int J Hematol. 2006;84(1):60–62.
  • Costa E, Duque F, Oliveira J, et al. Identification of a novel AluSx-mediated deletion of exon 3 in the SBDS gene in a patient with Shwachman-Diamond syndrome. Blood Cells Mol Dis. 2007;39(1):96–101.
  • Minelli A, Nacci L, Valli R, et al. Structural variation in SBDS gene, with loss of exon 3, in two Shwachman-Diamond patients. Blood Cells Mol Dis. 2016;60:33–35.
  • Erdos M, Alapia K, Balogh I, et al. Severe Shwachman-Diamond syndrome phenotype caused by compound heterozygous missense mutations in the SBDS gene. Exp Hematol. 2006;34:1517–1521.
  • Qiu XB1, Shao YM, Miao S, et al. The diversity of the DnaJ/Hsp40 family, the crucial partners for Hsp70 chaperones. Cell Mol Life Sci. 2006;63:2560–2570.
  • Tafforeau L, Zorbas C, Langhendries JL, et al. The complexity of human ribosome biogenesis revealed by systematic nucleolar screening of pre-rRNA processing factors. Mol Cell. 2013;51:539–551.
  • Tummala H, Walne AJ, Williams M, et al. DNAJC21 mutations link a cancer-prone bone marrow failure syndrome to corruption in 60S ribosome subunit maturation. Am J Hum Genet. 2016;99:115–124.
  • Woolford JL Jr, Baserga SJ. Ribosome biogenesis in the yeast Saccharomyces cerevisiae. Genetics. 2013;195(3):643–681.
  • Kaschner LA, Sharma R, Shrestha OK, et al. A conserved domain important for association of eukaryotic J-protein co-chaperones Jjj1 and Zuo1 with the ribosome. Biochim Biophys Acta. 2015;1853(5):1035–1045.
  • Gijsbers A, García-Márquez A, Luviano A, et al. Guanine nucleotide exchange in the ribosomal GTPase EFL1 is modulated by the protein mutated in the Shwachman-Diamond syndrome. Biochem Biophys Res Commun. 2013;437(3):349–354.
  • García-Márquez A, Gijsbers A, De La Mora E, et al. Defective guanine nucleotide exchange in the elongation factor-like 1 (EFL1) GTPase by mutations in the Shwachman-Diamond syndrome protein. J Biol Chem. 2015;290(29):17669–17678.
  • Rujkijyanont P, Beyene J, Wei K, et al. Leukaemia-related gene expression in bone marrow cells from patients with the preleukaemic disorder Shwachman-Diamond syndrome. Br J Haematol. 2007;137(6):537–544.
  • Rujkijyanont P, Adams SL, Beyene J, et al. Bone marrow cells from patients with Shwachman-Diamond syndrome abnormally express genes involved in ribosome biogenesis and RNA processing. Br J Haematol. 2009;145(6):806–815.
  • Pressato B, Valli R, Marletta C, et al. Deletion of chromosome 20 in bone marrow of patients with Shwachman-Diamond syndrome, loss of the EIF6 gene and benign prognosis. Br J Haematol. 2012;157(4):503–505.
  • Valli R, De Paoli E, Nacci L, et al. Novel recurrent chromosome anomalies in Shwachman-Diamond syndrome. Pediatr Blood Cancer. 2017;64:8.
  • Dror Y. Shwachman-Diamond syndrome. Pediatr Blood Cancer. 2005;45(7):892–901.
  • Pressato B, Marletta C, Montalbano G, et al. Improving the definition of the structure of the isochromosome i(7)(q10) in Shwachman-Diamond syndrome. Br J Haematol. 2010;150(5):632–633.
  • Minelli A, Maserati E, Nicolis E, et al. The isochromosome i(7)(q10) carrying c.258+2t>c mutation of the SBDS gene does not promote development of myeloid malignancies in patients with Shwachman syndrome. Leukemia. 2009;23(4):708–711.
  • Valli R, Pressato B, Marletta C, et al. Different loss of material in recurrent chromosome 20 interstitial deletions in Shwachman-Diamond syndrome and in myeloid neoplasms. Mol Cytogenet. 2013;6(1):56.
  • Ganapathi KA, Shimamura A. Ribosomal dysfunction and inherited marrow failure. Br J Haematol. 2008;141:376–387.
  • Narla A, Ebert BL. Ribosomopathies: human disorders of ribosome dysfunction. Blood. 2010;115(16):3196–3205.
  • Yelick PC, Trainor PA. Ribosomopathies: global process, tissue specific defects. Rare Dis. 2015;3:e1025185.
  • Draptchinskaia N, Gustavsson P, Andersson B, et al. The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat Genet. 1999;21(2):169–175.
  • Heiss NS, Knight SW, Vulliamy TJ, et al. X-linked dyskeratosis congenita is caused by mutations in a highly conserved gene with putative nucleolar functions. Nat Genet. 1998;19:32–38.
  • Ridanpaa M, Sulisalo T, De La Chapelle A, et al. Genetic and physical mapping of the cartilage-hair hypoplasia locus on 9p13. Am J Hum Genet. 1995;57:A201.
  • Treacher Collins Syndrome Collaborative Group. Positional cloning of a gene involved in the pathogenesis of Treacher Collins syndrome. Nat Genet. 1996;12:130–136.
  • Kadakia S, Helman SN, Badhey AK, et al. Treacher Collins syndrome: the genetics of a craniofacial disease. Int J Pediatr Otorhinolaryngol. 2014;78:893–898.
  • Boultwood J, Fidler C, Strickson AJ, et al. Narrowing and genomic annotation of the commonly deleted region of the 5q- syndrome. Blood. 2002;93:4638–4641.
  • Boultwood J, Pellagatti A, McKenzie AN, et al. Advances in the 5q- syndrome. Blood. 2010;116:5803–5811.
  • Sahoo T, Bacino CA, German JR, et al. Identification of novel deletions of 15q11q13 in Angelman syndrome by array-CGH: molecular characterization and genotype-phenotype correlations. Eur J Hum Genet. 2007;15:943–949.
  • Sahoo T, Del Gaudio D, German JR, et al. Prader-Willi phenotype caused by paternal deficiency for the HBII-85 C/D box small nucleolar RNA cluster. Nat Genet. 2008;40:719–721.
  • Armistead J, Khatkar S, Meyer B, et al. Mutation of a gene essential for ribosome biogenesis, EMG1, causes Bowen-Conradi syndrome. Am J Hum Genet. 2009;84:728–739.
  • Chagnon P, Michaud J, Mitchell G, et al. A missense mutation (R565W) in cirhin (FLJ14728) in North American Indian childhood cirrhosis. Am J Hum Genet. 2002;71:1443–1449.
  • Nakhoul H, Ke J, Zhou X, et al. Ribosomopathies: mechanisms of disease. Clin Med Insights Blood Disord. 2014;7:7–16.
  • Xue S, Barna M. Specialized ribosomes: a new frontier in gene regulation and organism biology. Mol Cell Biol. 2010;13:335–369.
  • Farley KI, Baserga SJ. Probing the mechanisms underlying human disease in making ribosomes. Biochem Soc Trans. 2016;44:1035–1044.
  • 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.
  • De Keersmaecker K. A novel mouse model provides insights into the neutropenia associated with the ribosomopathy Shwachman-Diamond syndrome. Haematologica. 2015;100(10):1237–1239.
  • Zambetti NA, Bindels EM, Van Strien PM, et al. Deficiency of the ribosome biogenesis gene Sbds in hematopoietic stem and progenitor cells causes neutropenia in mice by attenuating lineage progression in myelocytes. Haematologica. 2015;100(10):1285–1293.
  • Tourlakis ME, Zhang S, Ball HL, et al. In vivo senescence in the Sbds-deficient murine pancreas: cell-type specific consequences of translation insufficiency. PLoS Genet. 2015;11(6):e1005288.
  • Minelli A, Nicolis E, Cannioto Z, et al. Incidence of Shwachman-Diamond syndrome. Pediatr Blood Cancer. 2012;59(7):1334–1335.
  • Ikeda F, Yoshida K, Toki T, et al. Exome sequencing identified RPS15A as a novel causative gene for Diamond-Blackfan anemia. Haematologica. 2017;102(3):e93–e96.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.