Evolution of severe (transfusion-dependent) anaemia in myelodysplastic syndromes with 5q deletion is characterized by a macrophage-associated failure of the eythropoietic niche.
RPS14
5q deletion
erythroblastic island
erythropoiesis
myelodysplastic syndromes
Journal
British journal of haematology
ISSN: 1365-2141
Titre abrégé: Br J Haematol
Pays: England
ID NLM: 0372544
Informations de publication
Date de publication:
07 2022
07 2022
Historique:
revised:
16
02
2022
received:
04
12
2021
accepted:
13
03
2022
pubmed:
2
4
2022
medline:
28
6
2022
entrez:
1
4
2022
Statut:
ppublish
Résumé
Evolution of erythrocyte transfusion-dependent (RBC-TD) anaemia associated with haploinsufficiency of the ribosomal protein subunit S14 gene (RPS14) is a characteristic complication of myelodysplastic syndromes (MDS) with del(5q) [MDS.del(5q)]. Evaluating 39 patients with MDS.del(5q), <5% of anaemia progression was attributable to RPS14-dependent alterations of normoblasts, pro-erythroblasts, or CD34
Substances chimiques
Thalidomide
4Z8R6ORS6L
Lenalidomide
F0P408N6V4
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
114-130Subventions
Organisme : NHLBI NIH HHS
ID : R01 HL082945
Pays : United States
Informations de copyright
© 2022 The Authors. British Journal of Haematology published by British Society for Haematology and John Wiley & Sons Ltd.
Références
Germing U, Strupp C, Giagounidis A, Haas R, Gattermann N, Starke C, et al. Evaluation of dysplasia through detailed cytomorphology in 3156 patients from the Düsseldorf registry on myelodysplastic syndromes. Leuk Res. 2012;36(6):727-34.
Lefèvre C, Bondu S, Le Goff S, Kosmider O, Fontenay M. Dyserythropoiesis of myelodysplastic syndromes. Curr Opin Hematol. 2017;24(3):191-7.
Buesche G, Teoman H, Wilczak W, Ganser A, Hecker H, Wilkens L, et al. Marrow fibrosis predicts early fatal marrow failure in patients with myelodysplastic syndromes. Leukemia. 2008;22(2):313-22.
Buesche G, Teoman H, Giagounidis A, Göhring G, Schlegelberger B, Ganser A, et al. Impaired formation of erythroblastic islands is associated with erythroid failure and poor prognosis in a significant proportion of patients with myelodysplastic syndromes. Haematologica. 2016;101(5):e177-81.
Haase D, Germing U, Schanz J, Pfeilstöcker M, Nösslinger T, Hildebrandt B, et al. New insights into the prognostic impact of the karyotype in MDS and correlation with subtypes: evidence from a core dataset of 2124 patients. Blood. 2007;110(13):4385-95.
Ebert BL, Pretz J, Bosco J, Chang CY, Tamayo P, Galili N, et al. Identification of RPS14 as a 5q- syndrome gene by RNA interference screen. Nature. 2008;451(7176):335-9.
Zhou X, Hao Q, Liao J, Zhang Q, Lu H. Ribosomal protein S14 unties the MDM2-p53 loop upon ribosomal stress. Oncogene. 2013;32(3):388-96.
Wei S, Chen X, McGraw K, Zhang L, Komrokji R, Clark J, et al. Lenalidomide promotes p53 degradation by inhibiting MDM2 auto-ubiquitination in myelodysplastic syndrome with chromosome 5q deletion. Oncogene. 2013;32(9):1110-20.
Barlow JL, Drynan LF, Hewett DR, Holmes LR, Lorenzo-Abalde S, Lane AL, et al. A p53-dependent mechanism underlies macrocytic anemia in a mouse model of human 5q- syndrome. Nat Med. 2010;16(1):59-66.
Caceres G, McGraw K, Yip BH, Pellagatti A, Johnson J, Zhang L, et al. TP53 suppression promotes erythropoiesis in del(5q) MDS, suggesting a targeted therapeutic strategy in lenalidomide-resistant patients. Proc Natl Acad Sci USA. 2013;110(40):16127-32.
Boultwood J. The role of haploinsufficiency of RPS14 and p53 activation in the molecular pathogenesis of the 5q- syndrome. Pediatr Rep. 2011;3(Suppl 2):e10.
Schneider RK, Schenone M, Ferreira MV, Kramann R, Joyce CE, Hartigan C, et al. Rps14 haploinsufficiency causes a block in erythroid differentiation mediated by S100A8 and S100A9. Nat Med. 2016;22(3):288-97.
Burwick N, Shimamura A, Liu JM. Non-diamond Blackfan anemia disorders of ribosome function: Shwachman diamond syndrome and 5q- syndrome. Semin Hematol. 2011;48(2):136-43.
Rojas SM, Díez-Campelo M, Luño E, Cabrero M, Pedro C, Calabuig M, et al. Transfusion dependence development and disease evolution in patients with MDS and del(5q) and without transfusion needs at diagnosis. Leuk Res. 2014;38(3):304-9.
Greenberg PL, Tuechler H, Schanz J, Sanz G, Garcia-Manero G, Solé F, et al. Revised international prognostic scoring system for myelodysplastic syndromes. Blood. 2012;120(12):2454-65.
Malcovati L, Germing U, Kuendgen A, Della Porta MG, Pascutto C, Invernizzi R, et al. Time-dependent prognostic scoring system for predicting survival and leukemic evolution in myelodysplastic syndromes. J Clin Oncol. 2007;25(23):3503-10.
Hosono N, Makishima H, Mahfouz R, Przychodzen B, Yoshida K, Jerez A, et al. Recurrent genetic defects on chromosome 5q in myeloid neoplasms. Oncotarget. 2017;8(4):6483-95.
Jädersten M, Saft L, Smith A, Kulasekararaj A, Pomplun S, Göhring G, et al. TP53 mutations in low-risk myelodysplastic syndromes with del(5q) predict disease progression. J Clin Oncol. 2011;29(15):1971-9.
Bersanelli M, Travaglino E, Meggendorfer M, Matteuzzi T, Sala C, Mosca E, et al. Classification and personalized prognostic assessment on the basis of clinical and genomic features in myelodysplastic syndromes. J Clin Oncol. 2021;39(11):1223-33.
Chasis JA, Mohandas N. Erythroblastic islands: niches for erythropoiesis. Blood. 2008;112:470-8.
Yeo JH, Lam YW, Fraser ST. Cellular dynamics of mammalian red blood cell production in the erythroblastic Island niche. Biophys Rev. 2019;11(6):873-94.
Greenberg P, Cox C, LeBeau MM, Fenaux P, Morel P, Sanz G, et al. International scoring system for evaluating prognosis in myelodysplastic syndromes (see comments) (published erratum appeared in blood 1998 Feb 1;91 (3):1100). Blood. 1997;89(6):2079-88.
List AF, Bennett JM, Sekeres MA, Skikne B, Fu T, Shammo JM, et al. Extended survival and reduced risk of AML progression in erythroid-responsive lenalidomide-treated patients with lower-risk del(5q) MDS. Leukemia. 2014;28(5):1033-40.
List A, Dewald G, Bennett J, Giagounidis A, Raza A, Feldman E, et al. Lenalidomide in the myelodysplastic syndrome with chromosome 5q deletion. N Engl J Med. 2006;355(14):1456-65.
Göhring G, Giagounidis A, Büsche G, Kreipe HH, Zimmermann M, Hellström-Lindberg E, et al. Patients with del(5q) MDS who fail to achieve sustained erythroid or cytogenetic remission after treatment with lenalidomide have an increased risk for clonal evolution and AML progression. Ann Hematol. 2010;89(4):365-74.
Hasserjian RP, Orazi A, Brunning RD, Germing U, Le Beau MM, Porwit A, et al. Myelodysplastic syndromes. In: Swerdlow SS, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al., editors. WHO classification of tumors of haematopoietic and lymphoid tissues. Revised. 4th ed. Lyon: IARC; 2017. p. 97-120.
Bessis M. L'ilot erythroblastique. Unite functionelle de la moelle osseuse. Rev Hematol. 1958;13:8-11.
Sangiorgio VFI, Geyer JT, Margolskee E, Al-Kawaaz M, Mathew S, Tam W, et al. Myeloid neoplasms with isolated del(5q) and JAK2 V617F mutation: a "grey zone" combination of myelodysplastic and myeloproliferative features? Haematologica. 2020;105(6):e276-9.
Bartels S, Vogtmann J, Schipper E, Büsche G, Schlue J, Lehmann U, et al. Combination of myeloproliferative neoplasm driver gene activation with mutations of splice factor or epigenetic modifier genes increases risk of rapid blastic progression. Eur J Haematol. 2021;106(4):520-8.
Saft L, Karimi M, Ghaderi M, Matolcsy A, Mufti GJ, Kulasekararaj A, et al. p53 protein expression independently predicts outcome in patients with lower-risk myelodysplastic syndromes with del(5q). Haematologica. 2014;99(6):1041-9.
Henderson CR. Estimation of variance and covariance components. Biometrics. 1953;9:226-52.
Breslow NE, Clayton DG. Approximate inference in generalized linear mixed models. J Am Stat Assoc. 1993;88:9-25.
Hedeker D, Gibbons RD. Mixreg: a computer program for mixed-effects regression analysis with autocorrelated errors. Comput Methods Programs Biomed. 1996;49:229-52.
Garderet L, Kobari L, Mazurier C, De Witte C, Giarratana MC, Pérot C, et al. Unimpaired terminal erythroid differentiation and preserved enucleation capacity in myelodysplastic 5q(del) clones: a single cell study. Haematologica. 2010;95(3):398-405.
Yang Z, Keel SB, Shimamura A, Liu L, Gerds AT, Li HY, et al. Delayed globin synthesis leads to excess heme and the macrocytic anemia of diamond Blackfan anemia and del(5q) myelodysplastic syndrome. Sci Transl Med. 2016;8(338):338ra67.
Yip BH, Vuppusetty C, Attwood M, Giagounidis A, Germing U, Lamikanra AA, et al. Activation of the mTOR signaling pathway by L-leucine in 5q- syndrome and other RPS14-deficient erythroblasts. Leukemia. 2013;27(8):1760-3.
Boultwood J, Yip BH, Vuppusetty C, Pellagatti A, Wainscoat JS. Activation of the mTOR pathway by the amino acid (L)-leucine in the 5q- syndrome and other ribosomopathies. Adv Biol Regul. 2013;53(1):8-17.
Mei Y, Zhao B, Basiorka AA, Yang J, Cao L, Zhang J, et al. Age-related inflammatory bone marrow microenvironment induces ineffective erythropoiesis mimicking del(5q) MDS. Leukemia. 2018;32(4):1023-33.
Grigorakaki C, Morceau F, Chateauvieux S, Dicato M, Diederich M. Tumor necrosis factor α-mediated inhibition of erythropoiesis involves GATA-1/GATA-2 balance impairment and PU.1 over-expression. Biochem Pharmacol. 2011;82:156-66.
Jacobs-Helber SM, Roh KH, Bailey D, Dessypris EN, Ryan JJ, Chen J, et al. Tumor necrosis factor-alpha expressed constitutively in erythroid cells or induced by erythropoietin has negative and stimulatory roles in normal erythropoiesis and erythroleukemia. Blood. 2003;101:524-31.
Buck I, Morceau F, Cristofanon S, Heintz C, Chateauvieux S, Reuter S, et al. Tumor necrosis factor alpha inhibits erythroid differentiation in human erythropoietin-dependent cells involving p38 MAPK pathway, GATA-1 and FOG-1 downregulation and GATA-2 upregulation. Biochem Pharmacol. 2008;76(10):1229-39.
Bibikova E, Youn MY, Danilova N, Ono-Uruga Y, Konto-Ghiorghi Y, Ochoa R, et al. TNF-mediated inflammation represses GATA1 and activates p38 MAP kinase in RPS19-deficient hematopoietic progenitors. Blood. 2014;124(25):3791-8.
Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C, van Zoelen MA, et al. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med. 2007;13(9):1042-9.
Klei TR, Meinderts SM, van den Berg TK, van Bruggen R. From the cradle to the grave: the role of macrophages in erythropoiesis and erythrophagocytosis. Front Immunol. 2017;8:73 eCollection 2017.
Jacobsen RN, Perkins AC, Levesque JP. Macrophages and regulation of erythropoiesis. Curr Opin Hematol. 2015;22(3):212-9.
Luo Y, Shao L, Chang J, Feng W, Liu YL, Cottler-Fox MH, et al. M1 and M2 macrophages differentially regulate hematopoietic stem cell self-renewal and ex vivo expansion. Blood Adv. 2018;2:859-70.
Lopez-Yrigoyen M, Yang CT, Fidanza A, Cassetta L, Taylor AH, McCahill A, et al. Genetic programming of macrophages generates an in vitro model for the human erythroid Island niche. Nat Commun. 2019;10(1):881.
Li W, Wang Y, Zhao H, Zhang H, Xu Y, Wang S, et al. Identification and transcriptome analysis of erythroblastic Island macrophages. Blood. 2019;134(5):480-91.
Wei Q, Boulais PE, Zhang D, Pinho S, Tanaka M, Frenette PS. Maea expressed by macrophages, but not erythroblasts, maintains postnatal murine bone marrow erythroblastic islands. Blood. 2019;133(11):1222-32.
Anselmo A, Lauranzano E, Soldani C, Ploia C, Angioni R, D'amico G, et al. Identification of a novel agrin-dependent pathway in cell signaling and adhesion within the erythroid niche. Cell Death Differ. 2016;23(8):1322-30.
Lévesque JP, Summers KM, Bisht K, Millard SM, Winkler IG, Pettit AR. Macrophages form erythropoietic niches and regulate iron homeostasis to adapt erythropoiesis in response to infections and inflammation. Exp Hematol. 2021;103:1-14.
Li W, Guo R, Song Y, Jiang Z. Erythroblastic Island macrophages shape normal erythropoiesis and drive associated disorders in erythroid hematopoietic diseases. Front Cell Dev Biol. 2021;8:613885 eCollection 2020.
Mukherjee K, Bieker JJ. Transcriptional control of gene expression and the heterogeneous cellular identity of Erythroblastic Island macrophages. Front Genet. 2021;12:756028 eCollection 2021.
Wei Q, Pinho S, Dong S, Pierce H, Li H, Nakahara F, et al. MAEA is an E3 ubiquitin ligase promoting autophagy and maintenance of haematopoietic stem cells. Nat Commun. 2021;12:2522.
List A, Kurtin S, Roe DJ, Buresh A, Mahadevan D, Fuchs D, et al. Efficacy of lenalidomide in myelodysplastic syndromes. N Engl J Med. 2005;352(6):549-57.
Poli A, Ratti S, Finelli C, Mongiorgi S, Clissa C, Lonetti A, et al. Nuclear translocation of PKC-α is associated with cell cycle arrest and erythroid differentiation in myelodysplastic syndromes (MDSs). FASEB J. 2018;32:681-92.
Cappellini A, Mongiorgi S, Finelli C, Fazio A, Ratti S, Marvi MV, et al. Phospholipase C beta1 (PI-PLCbeta1)/cyclin D3/protein kinase C (PKC) alpha signaling modulation during iron-induced oxidative stress in myelodysplastic syndromes (MDS). FASEB J. 2020;34(11):15400-16.
Deleschaux C, Moras M, Lefevre SD, Ostuni MA. An overview of different strategies to recreate the physiological environment in experimental erythropoiesis. Int J Mol Sci. 2020;21(15):5263.
Teodorescu P, Pasca S, Dima D, Tomuleasa C, Ghiaur G. Targeting the microenvironment in MDS: the final frontier. Front Pharmacol. 2020;11:1044 eCollection 2020.
Ribezzo F, Snoeren IAM, Ziegler S, Stoelben J, Olofsen PA, Henic A, et al. Rps14, Csnk1a1 and miRNA145/miRNA146a deficiency cooperate in the clinical phenotype and activation of the innate immune system in the 5q- syndrome. Leukemia. 2019;33(7):1759-72.