Inherited bone marrow failure syndromes: a review of current practices and potential future research directions.
Journal
Current opinion in pediatrics
ISSN: 1531-698X
Titre abrégé: Curr Opin Pediatr
Pays: United States
ID NLM: 9000850
Informations de publication
Date de publication:
01 02 2023
01 02 2023
Historique:
pmc-release:
01
02
2024
pubmed:
11
11
2022
medline:
4
1
2023
entrez:
10
11
2022
Statut:
ppublish
Résumé
Recent advances in diagnosis and treatment of inherited bone marrow failure syndromes (IBMFS) have significantly improved disease understanding and patient outcomes. Still, IBMFS present clinical challenges that require further progress. This review aims to provide an overview of the current state of diagnosis and treatment modalities of the major IBMFS seen in paediatrics and present areas of prioritization for future research. Haematopoietic cell transplantation (HCT) for IBMFS has greatly improved in recent years, shifting the research and clinical focus towards cancer predispositions and adverse effects of treatment. Each year, additional novel genes and pathogenic variants are described, and genotype-phenotype mapping becomes more sophisticated. Moreover, novel therapeutics exploring disease-specific mechanisms show promise to complement HCT and treat patients who cannot undergo current treatment options. Research on IBMFS should have short-term and long-term goals. Immediate challenges include solidifying diagnostic and treatment guidelines, cancer detection and treatment, and continued optimization of HCT. Long-term goals should emphasize genotype-phenotype mapping, genetic screening tools and gene-targeted therapy.
Identifiants
pubmed: 36354296
doi: 10.1097/MOP.0000000000001196
pii: 00008480-202302000-00014
pmc: PMC9812861
mid: NIHMS1845468
doi:
Types de publication
Review
Journal Article
Research Support, N.I.H., Intramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
75-83Subventions
Organisme : Intramural NIH HHS
ID : Z99 CA999999
Pays : United States
Informations de copyright
Copyright © 2022 Wolters Kluwer Health, Inc. All rights reserved.
Références
Savage SA, Dufour C. Classical inherited bone marrow failure syndromes with high risk for myelodysplastic syndrome and acute myelogenous leukemia. Semin Hematol 2017; 54:105–114.
Arber DA, Orazi A, Hasserjian R, et al. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood 2016; 127:2391–2405.
Wegman-Ostrosky T, Savage SA. The genomics of inherited bone marrow failure: from mechanism to the clinic. Br J Haematol 2017; 177:526–542.
Nalepa G, Clapp DW. Fanconi anaemia and cancer: an intricate relationship. Nat Rev Cancer 2018; 18:168–185.
Alter BP. Fanconi anemia and the development of leukemia. Best Pract Res Clin Haematol 2014; 27:214–221.
Alter BP, Giri N, Savage SA, Rosenberg PS. Cancer in the National Cancer Institute inherited bone marrow failure syndrome cohort after fifteen years of follow-up. Haematologica 2018; 103:30–39.
Fargo JH, Rochowski A, Giri N, et al. Comparison of chromosome breakage in nonmosaic and mosaic patients with Fanconi anemia, relatives, and patients with other inherited bone marrow failure syndromes. Cytogenet Genome Res 2014;144:15--27.
Shimamura A, Alter BP. Pathophysiology and management of inherited bone marrow failure syndromes. Blood Rev 2010; 24:101–122.
Risitano AM, Marotta S, Calzone R, et al. RIAF Contributors. Twenty years of the Italian Fanconi Anemia Registry: where we stand and what remains to be learned. Haematologica 2016; 101:319–327.
Fiesco-Roa MO, Giri N, McReynolds LJ, et al. Genotype-phenotype associations in Fanconi anemia: a literature review. Blood Rev 2019; 37:100589.
Fanconi Anemia Clinical Care Guidelines. 5th Edition. Fanconi Anemia Research Fund. 2020.
Ebens CL, MacMillan ML, Wagner JE. Hematopoietic cell transplantation in Fanconi anemia: current evidence, challenges and recommendations. Expert Rev Hematol 2017; 10:81–97.
Paustian L, Chao MM, Hanenberg H, et al. Androgen therapy in Fanconi anemia: a retrospective analysis of 30 years in Germany. Pediatr Hematol Oncol 2016; 33:5–12.
Pollard JA, Furutani E, Liu S, et al. Metformin for treatment of cytopenias in children and young adults with Fanconi anemia. Blood Adv 2022; 6:3803–3811.
Thompson AS, Saba N, McReynolds LJ, et al. The causes of Fanconi anemia in South Asia and the Middle East: a case series and review of the literature. Mol Genet Genomic Med 2021; 9:e1693.
Nicoletti E, Rao G, Bueren JA, et al. Mosaicism in Fanconi anemia: concise review and evaluation of published cases with focus on clinical course of blood count normalization. Ann Hematol 2020; 99:913–924.
Mehta PA, Ebens C. Fanconi anemia. In: Adam MP, Mirzaa GM, Pagon RA, et al. , editors. GeneReviews [Internet]. Seattle, WA: University of Washington; 1993-2022. https://www.ncbi.nlm.nih.gov/books/NBK1401/
Altintas B, Giri N, McReynolds LJ, et al. Genotype-phenotype and outcome associations in patients with Fanconi anemia: the National Cancer Institute cohort. Haematologica 2022; [Epub ahead of print.
Alter BP, Rosenberg PS, Giri N, et al. Telomere length is associated with disease severity and declines with age in dyskeratosis congenita. Haematologica 2012; 97:353–359.
Ballew BJ, Savage SA. Updates on the biology and management of dyskeratosis congenita and related telomere biology disorders. Expert Rev Hematol 2013; 6:327–337.
Telomere biology disorders: diagnosis and management guidelines. Second edition. Team Telomere. 2022.
Revy P, Kannengiesser C, Bertuch AA. Genetics of human telomere biology disorders Nature Reviews Genetics 2022
Savage SA, Niewisch MR. Dyskeratosis congenita and related telomere biology disorders. In: Adam MP, Mirzaa GM, Pagon RA, et al ., editors. GeneReviews [Internet]. Seattle, WA: University of Washington, Seattle; 1993-2022. PMID: 20301779.
Niewisch MR, Giri N, McReynolds LJ, et al. Disease progression and clinical outcomes in telomere biology disorders. Blood 2022; 139:1807–1819.
Bhoopalan SV, Wlodarski M, Reiss U, et al. Reduced-intensity conditioning-based hematopoietic cell transplantation for dyskeratosis congenita: single-center experience and literature review. Pediatr Blood Cancer 2021; 68:e29177.
Khincha PP, Wentzensen IM, Giri N, et al. Response to androgen therapy in patients with dyskeratosis congenita. Br J Haematol 2014; 165:349–357.
Nguyen THD. Structural biology of human telomerase: progress and prospects. Biochem Soc Trans 2021; 49:1927–1939.
Belaya Z, Golounina O, Nikitin A, et al. Multiple bilateral hip fractures in a patient with dyskeratosis congenita caused by a novel mutation in the PARN gene. Osteoporos Int 2021; 32:1227–1231.
Dorgaleleh S, Naghipoor K, Hajimohammadi Z, et al. Molecular insight of dyskeratosis congenita: defects in telomere length homeostasis. J Clin Transl Res 2022; 8:20–30.
Zeng T, Lv G, Chen X, et al. CD8 + T-cell senescence and skewed lymphocyte subsets in young dyskeratosis congenita patients with PARN and DKC1 mutations. J Clin Lab Anal 2020; 34:e23375.
Sharma R, Sahoo SS, Honda M, et al. Gain-of-function mutations in RPA1 cause a syndrome with short telomeres and somatic genetic rescue. Blood 2022; 139:1039–1051.
Grill S, Nandakumar J. Molecular mechanisms of telomere biology disorders. J Biol Chem 2021; 296:100064.
Niewisch MR, Savage SA. An update on the biology and management of dyskeratosis congenita and related telomere biology disorders. Expert Rev Hematol 2019; 12:1037–1052.
Bezzerri V, Cipolli M. Shwachman-Diamond syndrome: molecular mechanisms and current perspectives. Mol Diagn Ther 2019; 23:281–290.
Kallen ME, Dulau-Florea A, Wang W, Calvo KR. Acquired and germline predisposition to bone marrow failure: diagnostic features and clinical implications. Semin Hematol 2019; 56:69–82.
Nelson AS, Myers KC. Diagnosis, treatment, and molecular pathology of Shwachman-Diamond syndrome. Hematol Oncol Clin North Am 2018; 32:687–700.
Farooqui SM, Ward R, Aziz M. Shwachman-Diamond syndrome. StatPearls [Internet]. Treasure Island, FL: StatPearls Publishing; 2022. PMID: 29939643.
Dhanraj S, Matveev A, Li H, et al. Biallelic mutations in DNAJC21 cause Shwachman-Diamond syndrome. Blood 2017; 129:1557–1562.
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 Shwachman-Diamond like syndrome. J Med Genet 2017; 54:558–566.
Carapito R, Konantz M, Paillard C, et al. Mutations in signal recognition particle SRP54 cause syndromic neutropenia with Shwachman-Diamond-like features. J Clin Invest 2017; 127:4090–4103.
Goobie S, Popovic M, Morrison J, et al. Shwachman-Diamond syndrome with exocrine pancreatic dysfunction and bone marrow failure maps to the centromeric region of chromosome 7. Am J Hum Genet 2001; 68:1048–1054.
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.
Mack DR, Forstner GG, Wilschanski M, et al. Shwachman syndrome: exocrine pancreatic dysfunction and variable phenotypic expression. Gastroenterology 1996; 111:1593–1602.
Bhatla 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; 42:159–165.
Cesaro S, Pillon M, Sauer M, et al. Long-term outcome after allogeneic hematopoietic stem cell transplantation for Shwachman-Diamond syndrome: a retrospective analysis and a review of the literature by the Severe Aplastic Anemia Working Party of the European Society for Blood and Marrow Transplantation (SAAWP-EBMT). Bone Marrow Transplant 2020; 55:1796–1809.
Shimamura A. Molecular alterations governing predisposition to myelodysplastic syndromes: insights from Shwachman-Diamond syndrome. Best Pract Res Clin Haematol 2021; 34:101252.
Xia J, Miller CA, Baty J, et al. Somatic mutations and clonal hematopoiesis in congenital neutropenia. Blood 2018; 131:408–416.
Touw IP. Congenital neutropenia: disease models guiding new treatment strategies. Curr Opin Hematol 2022; 29:27–33.
Myers KC, Furutani E, Weller E, et al. Clinical features and outcomes of patients with Shwachman-Diamond syndrome and myelodysplastic syndrome or acute myeloid leukaemia: a multicentre, retrospective, cohort study. Lancet Haematol 2020; 7:e238–e246.
Sieff C. Diamond-Blackfan anemia. In: Adam MP, Mirzaa GM, Pagon RA, et al ., editors. GeneReviews [Internet]. Seattle, WA: University of Washington, Seattle; 1993-2022. PMID: 20301769.
Vlachos A, Rosenberg PS, Atsidaftos E, et al. Increased risk of colon cancer and osteogenic sarcoma in Diamond-Blackfan anemia. Blood 2018; 132:2205–2208.
Flygare J, Aspesi A, Bailey JC, et al. Human RPS19, the gene mutated in Diamond-Blackfan anemia, encodes a ribosomal protein required for the maturation of 40S ribosomal subunits. Blood 2007; 109:980–986.
Choesmel V, Bacqueville D, Rouquette J, et al. Impaired ribosome biogenesis in Diamond-Blackfan anemia. Blood 2007; 109:1275–1283.
Cmejla R, Blafkova J, Stopka T, et al. Ribosomal protein S19 gene mutations in patients with Diamond-Blackfan anemia and identification of ribosomal protein S19 pseudogenes. Blood Cells Mol Dis 2000; 26:124–132.
Ulirsch JC, Verboon JM, Kazerounian S, et al. The genetic landscape of Diamond-Blackfan anemia. Am J Hum Genet 2018; 103:930–947.
Vlachos A, Ball S, Dahl N, et al. Diagnosing and treating Diamond Blackfan anaemia: results of an international clinical consensus conference. Br J Haematol 2008; 142:859–876.
Lipton JM, Atsidaftos E, Zyskind I, Vlachos A. Improving clinical care and elucidating the pathophysiology of Diamond Blackfan anemia: an update from the Diamond Blackfan Anemia Registry. Pediatr Blood Cancer 2006; 46:558–564.
Porter J, Galanello R, Saglio G, et al. Relative response of patients with myelodysplastic syndromes and other transfusion-dependent anaemias to deferasirox (ICL670): a 1-yr prospective study. Eur J Haematol 2008; 80:168–176.
Cappellini MD, Piga A. Current status in iron chelation in hemoglobinopathies. Curr Mol Med 2008; 8:663–674.
Sakaguchi H, Yoshida N. Recent advances in hematopoietic cell transplantation for inherited bone marrow failure syndromes. Int J Hematol 2022; 116:16–27.
Takafuji S, Mori T, Nishimura N, et al. Usefulness of functional splicing analysis to confirm precise disease pathogenesis in Diamond-Blackfan anemia caused by intronic variants in RPS19 . Pediatr Hematol Oncol 2021; 38:515–527.
van Dooijeweert B, Broeks MH, van Beers EJ, et al. Dried blood spot metabolomics reveals a metabolic fingerprint with diagnostic potential for Diamond Blackfan anaemia. Br J Haematol 2021; 193:1185–1193.
Macečková Z, Kubíčková A, De Sanctis JB, Hajdúch M. Effect of glucocorticosteroids in Diamond-Blackfan anaemia: maybe not as elusive as it seems. Int J Mol Sci 2022; 23:1886.
Dorn KM, Burns KD, Trout MAR, et al. Diamond-Blackfan anemia: a case report and review of the literature. Neonatology 2021; 118:500–504.
McReynolds LJ, Calvo KR, Holland SM. Germline GATA2 mutation and bone marrow failure. Hematol Oncol Clin North Am 2018; 32:713–728.
Hsu AP, McReynolds LJ, Holland SM. GATA2 deficiency. Curr Opin Allergy Clin Immunol 2015; 15:104–109.
Fabozzi F, Strocchio L, Mastronuzzi A, Merli P. GATA2 and marrow failure. Best Pract Res Clin Haematol 2021; 34:101278.
Hsu AP, Sampaio EP, Khan J, et al. Mutations in GATA2 are associated with the autosomal dominant and sporadic monocytopenia and mycobacterial infection (MonoMAC) syndrome. Blood 2011; 118:2653–2655.
Dickinson RE, Griffin H, Bigley V, et al. Exome sequencing identifies GATA-2 mutation as the cause of dendritic cell, monocyte, B and NK lymphoid deficiency. Blood 2011; 118:2656–2658.
Hahn CN, Chong CE, Carmichael CL, et al. Heritable GATA2 mutations associated with familial myelodysplastic syndrome and acute myeloid leukemia. Nat Genet 2011; 43:1012–1017.
Ostergaard P, Simpson MA, Connell FC, et al. Mutations in GATA2 cause primary lymphedema associated with a predisposition to acute myeloid leukemia (Emberger syndrome). Nat Genet 2011; 43:929–931.
Wlodarski MW, Hirabayashi S, Pastor V, et al. Prevalence, clinical characteristics, and prognosis of GATA2-related myelodysplastic syndromes in children and adolescents. Blood 2016; 127:1387–1397. quiz 1518.
Bogaert DJ, Laureys G, Naesens L, et al. GATA2 deficiency and haematopoietic stem cell transplantation: challenges for the clinical practitioner. Br J Haematol 2020; 188:768–773.
Wlodarski MW, Collin M, Horwitz MS. GATA2 deficiency and related myeloid neoplasms. Semin Hematol 2017; 54:81–86.
Cuellar-Rodriguez J, Gea-Banacloche J, Freeman AF, et al. Successful allogeneic hematopoietic stem cell transplantation for GATA2 deficiency. Blood 2011; 118:3715–3720.
Maeurer M, Magalhaes I, Andersson J, et al. Allogeneic hematopoietic cell transplantation for GATA2 deficiency in a patient with disseminated human papillomavirus disease. Transplantation 2014; 98:e95–e96.
Hofmann I, Avagyan S, Stetson A, et al. Comparison of outcomes of myeloablative allogeneic stem cell transplantation for pediatric patients with bone marrow failure, myelodysplastic syndrome and acute myeloid leukemia with and without germline GATA2 mutations. Biol Blood Marrow Transplant 2020; 26:1124–1130.
Bortnick R, Wlodarski M, de Haas V, et al. Hematopoietic stem cell transplantation in children and adolescents with GATA2-related myelodysplastic syndrome. Bone Marrow Transplant 2021; 56:2732–2741.
Nichols-Vinueza DX, Parta M, Shah NN, et al. Donor source and posttransplantation cyclophosphamide influence outcome in allogeneic stem cell transplantation for GATA2 deficiency. Br J Haematol 2022; 196:169–178.
Frangoul H, Altshuler D, Cappellini MD, et al. CRISPR-Cas9 gene editing for sickle cell disease and β-thalassemia. N Engl J Med 2021; 384:252–260.
Davidsson J, Puschmann A, Tedgård U, et al. SAMD9 and SAMD9L in inherited predisposition to ataxia, pancytopenia, and myeloid malignancies. Leukemia 2018; 32:1106–1115.
Sahoo SS, Kozyra EJ, Wlodarski MW. Germline predisposition in myeloid neoplasms: unique genetic and clinical features of GATA2 deficiency and SAMD9/SAMD9L syndromes. Best Pract Res Clin Haematol 2020; 33:101197.
Kennedy AL, Shimamura A. Genetic predisposition to MDS: clinical features and clonal evolution. Blood 2019; 133:1071–1085.
Nagamachi A, Matsui H, Asou H, et al. Haploinsufficiency of SAMD9L, an endosome fusion facilitator, causes myeloid malignancies in mice mimicking human diseases with monosomy 7. Cancer Cell 2013; 24:305–317.
Narumi S, Amano N, Ishii T, et al. SAMD9 mutations cause a novel multisystem disorder, MIRAGE syndrome, and are associated with loss of chromosome 7. Nat Genet 2016; 48:792–797.
Gorcenco S, Komulainen-Ebrahim J, Nordborg K, et al. Ataxia-pancytopenia syndrome with SAMD9L mutations. Neurol Genet 2017; 3:e183.
Tesi B, Davidsson J, Voss M, et al. Gain-of-function SAMD9L mutations cause a syndrome of cytopenia, immunodeficiency, MDS, and neurological symptoms. Blood 2017; 129:2266–2279.
Chin X, Sreedharan AV, Tan EC, et al. MIRAGE syndrome caused by a De Novo c.3406G>C (p. Glu1136Gln) mutation in the SAMD9 gene presenting with neonatal adrenal insufficiency and recurrent intussusception: a case report. Front Endocrinol (Lausanne) 2021; 12:742495.
Thiede C, Prange-Krex G, Freiberg-Richter J, et al. Buccal swabs but not mouthwash samples can be used to obtain pretransplant DNA fingerprints from recipients of allogeneic bone marrow transplants. Bone Marrow Transplant 2000; 25:575–577.
University of Chicago Hematopoietic Malignancies Cancer Risk Team. How I diagnose and manage individuals at risk for inherited myeloid malignancies. Blood 2016; 128:1800–1813.
Locatelli F, Strahm B. How I treat myelodysplastic syndromes of childhood. Blood 2018; 131:1406–1414.
Sarthy J, Zha J, Babushok D, et al. Poor outcome with hematopoietic stem cell transplantation for bone marrow failure and MDS with severe MIRAGE syndrome phenotype. Blood Adv 2018; 2:120–125.
Sahoo SS, Pastor VP, Panda PK, et al. SAMD9 and SAMD9L germline disorders in patients Enrolled in studies of the European working group of MDS in childhood (EWOG-MDS): prevalence, outcome, phenotype and functional characterisation. Blood 2018; 132:613.
Thomas ME3rd, Abdelhamed S, Hiltenbrand R, et al. Pediatric MDS and bone marrow failure-associated germline mutations in SAMD9 and SAMD9L impair multiple pathways in primary hematopoietic cells. Leukemia 2021; 35:3232–3244.
Inaba T, Nagamachi A. Revertant somatic mosaicism as a cause of cancer. Cancer Sci 2021; 112:1383–1389.
Sahoo SS, Pastor VB, Goodings C, Voss RK, et al. Clinical evolution, genetic landscape and trajectories of clonal hematopoiesis in SAMD9/SAMD9L syndromes. Nat Med 2021; 27:1806–1817.