550
Views
0
CrossRef citations to date
0
Altmetric
Original Research

Prognostic impact of the bone marrow tumor microenvironment, HLA-I and HLA-Ib expression in MDS and CMML progression to sAML

, , , , , , , , & show all
Article: 2323212 | Received 03 Jan 2024, Accepted 21 Feb 2024, Published online: 06 Mar 2024

References

  • Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz MJ, Le Beau MM, Bloomfield CD, Cazzola M, Vardiman JW. International consensus classification of myeloid neoplasms and acute leukemias: integrating morphologic, clinical, and genomic data. Blood. 2022 Sep 15;140(11):1200–13. doi:10.1182/blood.2022015850.
  • Arber DA, Orazi A, Hasserjian R, Thiele J, Borowitz ML, Le Beau MM, Bloomfield CD, Cazzola M, Vardiman JW. The 2016 revision to the World Health Organization classification of myeloid neoplasms and acute leukemia. Blood. 2016 May 19;127(20):2391–2405. doi:10.1182/blood-2016-03-643544.
  • Miesner M, Haferlach C, Bacher U. et al. Multilineage dysplasia (MLD) in acute myeloid leukemia (AML) correlates with MDS-related cytogenetic abnormalities and a prior history of MDS or MDS/MPN but has no independent prognostic relevance: a comparison of 408 cases classified as “AML not otherwise specified” (AML-NOS) or “AML with myelodysplasia-related changes” (AML-MRC). Blood. 2010 Oct 14;116(15):2742–2751. doi:10.1182/blood-2010-04-279794.
  • Goel H, Rahul E, Gupta I. et al. Molecular and genomic landscapes in secondary & therapy related acute myeloid leukemia. Am J Blood Res. 2021;11(5):472–497.
  • Bauer M, Vaxevanis C, Al-Ali HK. et al. Altered spatial composition of the Immune Cell Repertoire in Association to CD34+ blasts in myelodysplastic syndromes and secondary acute myeloid leukemia. Cancers. 2021 Jan 7;13(2):186. doi:10.3390/cancers13020186.
  • Ivy KS, Brent Ferrell P. Disordered Immune Regulation and its therapeutic targeting in myelodysplastic syndromes. Curr Hematol Malig Rep. 2018;13(4):244–255. doi:10.1007/s11899-018-0463-9.
  • Sallman DA, List A. The central role of inflammatory signaling in the pathogenesis of myelodysplastic syndromes. Blood. 2019 Mar 7; 133(10):1039–1048. doi:10.1182/blood-2018-10-844654.
  • Fisher DAC, Fowles JS, Zhou A, Oh ST. Inflammatory pathophysiology as a contributor to Myeloproliferative Neoplasms. Front Immunol. 2021;12:683401. doi:10.3389/fimmu.2021.683401.
  • Wen XM, Xu ZJ, Jin Y. et al. Association analyses of TP53 mutation with prognosis, tumor mutational burden, and immunological features in acute myeloid leukemia. Front Immunol. 2021;12:717527. doi:10.3389/fimmu.2021.717527.
  • Sallman DA, Komrokji R, Vaupel C. et al. Impact of TP53 mutation variant allele frequency on phenotype and outcomes in myelodysplastic syndromes. Leukemia. 2016 Mar;30(3):666–673. doi:10.1038/leu.2015.304.
  • Bewersdorf JP, Hasle V, Shallis RM. et al. Molecular, Epigenetic, and Immune Landscape of TP53- mutated (TP53-M) Acute Myeloid Leukemia (AML) and Higher Risk Myelodysplastic Syndromes (HR-MDS). Blood. 2022 Nov 15;140(Supplement 1):6247–6249. doi:10.1182/blood-2022-156460.
  • Bewersdorf JP, Xie Z, Bejar R. et al. Current landscape of translational and clinical research in myelodysplastic syndromes/neoplasms (MDS): proceedings from the 1st International Workshop on MDS (iwMDS) of the International consortium for MDS (icMDS). Blood Rev. 2023 Jul;60:101072. doi:10.1016/j.blre.2023.101072.
  • Vadakekolathu J, Minden MD, Hood T. et al. Immune landscapes predict chemotherapy resistance and immunotherapy response in acute myeloid leukemia. Sci Transl Med. 2020 Jun 3;12(546):eaaz0463. doi:10.1126/scitranslmed.aaz0463.
  • Lasry A, Nadorp B, Fornerod M. et al. An inflammatory state remodels the immune microenvironment and improves risk stratification in acute myeloid leukemia. Nat Cancer [Internet]. 2022 Dec 29 [cited 2023 Apr 24]. doi:10.1038/s43018-022-00480-0.
  • Rutella S, Vadakekolathu J, Mazziotta F. et al. Immune dysfunction signatures predict outcomes and define checkpoint blockade–unresponsive microenvironments in acute myeloid leukemia. J Clin Invest. 2022 Nov 1;132(21):e159579. doi:10.1172/JCI159579.
  • Masters SL, Gerlic M, Metcalf D. et al. NLRP1 inflammasome activation induces pyroptosis of hematopoietic progenitor cells. Immunity. 2012 Dec 14;37(6):1009–1023. doi:10.1016/j.immuni.2012.08.027.
  • Moiseev I, Tcvetkov N, Epifanovskaya O. et al. Landscape of alterations in the checkpoint system in myelodysplastic syndrome and implications for prognosis. PLoS One. 2022;17(10):e0275399. doi:10.1371/journal.pone.0275399.
  • Sallman DA, McLemore AF, Aldrich AL. et al. TP53 mutations in myelodysplastic syndromes and secondary AML confer an immunosuppressive phenotype. Blood. 2020 Jul 30;136(24):2812–2823. doi:10.1182/blood.2020006158.
  • Lübbert M, Suciu S, Baila L. et al. Low-dose decitabine versus best supportive care in elderly patients with intermediate- or high-risk myelodysplastic syndrome (MDS) ineligible for intensive chemotherapy: final results of the randomized phase III study of the European Organisation for Research and Treatment of Cancer Leukemia Group and the German MDS study Group. J Clin Oncol Off J Am Soc Clin Oncol. 2011 May 20;29(15):1987–1996.
  • Kantarjian HM, Thomas XG, Dmoszynska A. et al. Multicenter, randomized, open-label, phase III trial of decitabine versus patient choice, with physician advice, of either supportive care or low-dose cytarabine for the treatment of older patients with newly diagnosed acute myeloid leukemia. J Clin Oncol Off J Am Soc Clin Oncol. 2012 Jul 20;30(21):2670–2677. doi:10.1200/JCO.2011.38.9429.
  • Fenaux P, Mufti GJ, Hellstrom-Lindberg E. et al. Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study. Lancet Oncol. 2009 Mar;10(3):223–232. doi:10.1016/S1470-2045(09)70003-8.
  • Qiu X, Hother C, Ralfkiær UM. et al. Equitoxic doses of 5-azacytidine and 5-aza-2’deoxycytidine induce diverse immediate and overlapping heritable changes in the transcriptome. PLoS One. 2010 Sep 29;5(9):e12994. doi:10.1371/journal.pone.0012994.
  • Ørskov AD, Treppendahl MB, Skovbo A. et al. Hypomethylation and up-regulation of PD-1 in T cells by azacytidine in MDS/AML patients: a rationale for combined targeting of PD-1 and DNA methylation. Oncotarget. 2015 Apr 20;6(11):9612–9626. doi:10.18632/oncotarget.3324.
  • Youngblood B, Oestreich KJ, Ha SJ. et al. Chronic virus infection enforces demethylation of the locus that encodes PD-1 in antigen-specific CD8(+) T cells. Immunity. 2011 Sep 23;35(3):400–412. doi:10.1016/j.immuni.2011.06.015.
  • Klümper N, Ralser DJ, Bawden EG. et al. LAG3 (LAG-3, CD223) DNA methylation correlates with LAG3 expression by tumor and immune cells, immune cell infiltration, and overall survival in clear cell renal cell carcinoma. J Immunother Cancer. 2020 Mar;8(1):e000552. doi:10.1136/jitc-2020-000552.
  • Daver N, Boddu P, Garcia-Manero G. et al. Hypomethylating agents in combination with immune checkpoint inhibitors in acute myeloid leukemia and myelodysplastic syndromes. Leukemia. 2018 May;32(5):1094–1105. doi:10.1038/s41375-018-0070-8.
  • Weltgesundheitsorganisation. WHO classification of tumours of haematopoietic and lymphoid tissues. In: Swerdlow S, Campo E, Harris N, Jaffe E, Pileri S, Stein H. editor(s). World Health Organization classification of tumours. Revised 4th edition. Lyon: International Agency for Research on Cancer;2017p. 585.
  • Editorial Board. WHO classification of tumours editorial board. Haematolymphoid tumours [Internet; beta version ahead of print]. Lyon (France): International Agency for Research on Cancer; 2022 cited 2023-03-10. (WHO classification of tumours series, 5th ed.; vol. 11).
  • Bauer M, Vaxevanis C, Bethmann D. et al. Multiplex immunohistochemistry as a novel tool for the topographic assessment of the bone marrow stem cell niche. Methods Enzymol. 2020;635:67–79.
  • Graubert TA, Shen D, Ding L. et al. Recurrent mutations in the U2AF1 splicing factor in myelodysplastic syndromes. Nat Genet. 2011 Dec 11;44(1):53–57. doi:10.1038/ng.1031.
  • Babicki S, Arndt D, Marcu A. et al. Heatmapper: web-enabled heat mapping for all. Nucleic Acids Res. 2016 Jul 8;44(W1):W147–53. doi:10.1093/nar/gkw419.
  • Gu S, Xia J, Tian Y. A novel scoring system integrating molecular abnormalities with IPSS-R can improve the risk stratification in patients with MDS. BMC Cancer. 2021 Feb 6; 21(1):134. doi:10.1186/s12885-021-07864-y.
  • Hanahan D. Hallmarks of cancer: new dimensions. Cancer Discov. 2022 Jan;12(1):31–46. doi:10.1158/2159-8290.CD-21-1059.
  • Bauer M, Jasinski-Bergner S, Mandelboim O. Epstein-Barr Virus-Associated Malignancies and immune escape: the role of the tumor microenvironment and tumor cell evasion strategies. Cancers. 2021 Oct 16; 13(20):5189. doi:10.3390/cancers13205189.
  • Wickenhauser C, Bethmann D, Kappler M. et al. Tumor microenvironment, HLA class I and APM expression in HPV-Negative oral squamous cell carcinoma. Cancers. 2021 Feb 4;13(4):620. doi:10.3390/cancers13040620.
  • Samstein RM, Lee CH, Shoushtari AN. et al. Tumor mutational load predicts survival after immunotherapy across multiple cancer types. Nat Genet. 2019 Feb;51(2):202–206. doi:10.1038/s41588-018-0312-8.
  • Lawrence MS, Stojanov P, Polak P. et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature. 2013 Jul 11;499(7457):214–218. doi:10.1038/nature12213.
  • Stahl M, Goldberg AD. Immune checkpoint inhibitors in acute myeloid leukemia: novel combinations and therapeutic targets. Curr Oncol Rep. 2019 Mar 23; 21(4):37. doi:10.1007/s11912-019-0781-7.
  • Kordasti SY, Afzali B, Lim Z. et al. IL-17-producing CD4(+) T cells, pro-inflammatory cytokines and apoptosis are increased in low risk myelodysplastic syndrome. Br J Haematol. 2009 Apr;145(1):64–72. doi:10.1111/j.1365-2141.2009.07593.x.
  • Lopes MR, Traina F, de M CP. et al. IL10 inversely correlates with the percentage of CD8+ cells in MDS patients. Leuk Res. 2013 May;37(5):541–546. doi:10.1016/j.leukres.2013.01.019.
  • Galon J, Costes A, Sanchez-Cabo F. et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006 Sep 29;313(5795):1960–1964. doi:10.1126/science.1129139.
  • Salgado R, Denkert C, Demaria S. et al. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an international TILs working group 2014. Ann Oncol. 2015 Feb;26(2):259–271. doi:10.1093/annonc/mdu450.
  • Ding R, Prasanna P, Corredor G. et al. Image analysis reveals molecularly distinct patterns of TILs in NSCLC associated with treatment outcome. NPJ Precis Oncol. 2022 Jun 3;6(1):33. doi:10.1038/s41698-022-00277-5.
  • Dhatchinamoorthy K, Colbert JD, Rock KL. Cancer Immune Evasion Through Loss of MHC class I antigen presentation. Front Immunol. 2021;12:636568. doi:10.3389/fimmu.2021.636568.
  • Boddu P, Kantarjian H, Garcia-Manero G. The emerging role of immune checkpoint based approaches in AML and MDS. Leuk Lymphoma. 2018 Apr;59(4):790–802. doi:10.1080/10428194.2017.1344905.
  • Lee JH, Shklovskaya E, Lim SY. et al. Transcriptional downregulation of MHC class I and melanoma de- differentiation in resistance to PD-1 inhibition. Nat Commun. 2020 Apr 20;11(1):1897. doi:10.1038/s41467-020-15726-7.
  • Lei Q, Wang D, Sun K. Resistance mechanisms of anti-PD1/PDL1 therapy in solid tumors. Front Cell Dev Biol. 2020;8:672. doi:10.3389/fcell.2020.00672.
  • Kuba K, Inoue H, Matsumura S. et al. A retrospective analysis of tumor infiltrating lymphocytes in head and neck squamous cell carcinoma patients treated with nivolumab. Sci Rep. 2022 Dec 29;12(1):22557. doi:10.1038/s41598-022-27237-0.
  • Penter L, Liu Y, Wolff JO. et al. Mechanisms of response and resistance to combined decitabine and ipilimumab for advanced myeloid disease. Blood. 2023 Jan 27. 2022018246.
  • Wang X, Li M. Correlate tumor mutation burden with immune signatures in human cancers. BMC Immunol. 2019 Jan 11; 20(1):4. doi:10.1186/s12865-018-0285-5.
  • Griffiths EA, Srivastava P, Matsuzaki J. et al. NY-ESO-1 vaccination in combination with Decitabine Induces Antigen-Specific T-lymphocyte Responses in patients with myelodysplastic syndrome. Clin Cancer Res Off J Am Assoc Cancer Res. 2018 Mar 1;24(5):1019–1029. doi:10.1158/1078-0432.CCR-17-1792.
  • Abaza Y, Zeidan AM. Immune checkpoint inhibition in acute myeloid leukemia and myelodysplastic syndromes. Cells. 2022 Jul 20; 11(14):2249. doi:10.3390/cells11142249.
  • Wong KK, Hassan R, Yaacob NS. Hypomethylating agents and immunotherapy: Therapeutic Synergism in acute myeloid leukemia and myelodysplastic syndromes. Front Oncol. 2021;11:624742. doi:10.3389/fonc.2021.624742.
  • Serrano A, Castro-Vega I, Redondo M. Role of gene methylation in antitumor immune response: implication for tumor progression. Cancers. 2011 Mar 29; 3(2):1672–1690. doi:10.3390/cancers3021672.
  • Nangalia J, Grinfeld J, Green AR. Pathogenesis of myeloproliferative disorders. Annu Rev Pathol. 2016 May 23; 11(1):101–126. doi:10.1146/annurev-pathol-012615-044454.
  • Yang G, Wang X, Huang S. et al. Generalist in allogeneic hematopoietic stem cell transplantation for MDS or AML: epigenetic therapy. Front Immunol. 2022;13:1034438. doi:10.3389/fimmu.2022.1034438.
  • Yang H, Bueso-Ramos C, DiNardo C. et al. Expression of PD-L1, PD-L2, PD-1 and CTLA4 in myelodysplastic syndromes is enhanced by treatment with hypomethylating agents. Leukemia. 2014 Jun;28(6):1280–1288. doi:10.1038/leu.2013.355.
  • Yang X, Ma L, Zhang X. Targeting PD-1/PD-L1 pathway in myelodysplastic syndromes and acute myeloid leukemia. Exp Hematol Oncol. 2022 Mar 2; 11(1):11. doi:10.1186/s40164-022-00263-4.
  • Saxena K, Herbrich SM, Pemmaraju N. et al. A phase 1b/2 study of azacitidine with PD-L1 antibody avelumab in relapsed/refractory acute myeloid leukemia. Cancer. 2021 Oct 15;127(20):3761–3771. doi:10.1002/cncr.33690.