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Inflammatory recruitment of healthy hematopoietic stem and progenitor cells in the acute myeloid leukemia niche – Leukemia

  • De Kouchkovsky I, Abdul-Hay M. Acute myeloid leukemia: a comprehensive review and 2016 update. Blood Cancer J 2016;6:e441.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Siegel RL, Miller KD, Fuchs HE, Jemal A. Cancer statistics, 2022. CA: A Cancer J Clin. 2022;72:7–33.


    Google Scholar
     

  • Hornick NI, Doron B, Abdelhamed S, Huan J, Harrington CA, Shen R, et al. AML suppresses hematopoiesis by releasing exosomes that contain microRNAs targeting c-MYB. Sci Signal. 2016;9:ra88.

    Article 
    PubMed 

    Google Scholar
     

  • Abdelhamed S, Butler JT, Doron B, Halse A, Nemecek E, Wilmarth PA, et al. Extracellular vesicles impose quiescence on residual hematopoietic stem cells in the leukemic niche. EMBO Rep. 2019;20:e47546.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Binder S, Luciano M, Horejs-Hoeck J. The cytokine network in acute myeloid leukemia (AML): A focus on pro- and anti-inflammatory mediators. Cytokine Growth Factor Rev. 2018;43:8–15.

    Article 
    PubMed 

    Google Scholar
     

  • Kristinsson SY, Björkholm M, Hultcrantz M, Derolf ÅR, Landgren O, Goldin LR. Chronic immune stimulation might act as a trigger for the development of acute myeloid leukemia or myelodysplastic syndromes. J Clin Oncol. 2011;29:2897–903.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Pietras EM. Inflammation: a key regulator of hematopoietic stem cell fate in health and disease. Blood .2017;130:1693–8.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schepers K, Campbell TB, Passegué E. Normal and leukemic stem cell niches: insights and therapeutic opportunities. Cell Stem Cell. 2015;16:254–67.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang TY, Dutta R, Benard B, Zhao F, Yin R, Majeti R. IL-6 blockade reverses bone marrow failure induced by human acute myeloid leukemia. Sci Transl Med. 2020;12:eaax5104.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhao JL, Ma C, O’Connell MR, Mehta A, DiLoreto R, Heath JR, et al. Conversion of danger signals into cytokine signals by hematopoietic stem and progenitor cells for regulation of stress-induced hematopoiesis. Cell Stem Cell. 2014;14:445–59.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Guzman ML, Neering SJ, Upchurch D, Grimes B, Howard DS, Rizzieri DA, et al. Nuclear factor-κB is constitutively activated in primitive human acute myelogenous leukemia cells. Blood, J Am Soc Hematol 2001;98:2301–7.


    Google Scholar
     

  • Carey A, Edwards DK, Eide CA, Newell L, Traer E, Medeiros BC, et al. Identification of Interleukin-1 by Functional Screening as a Key Mediator of Cellular Expansion and Disease Progression in Acute Myeloid Leukemia. Cell Rep. 2017;18:3204–18.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zambetti NA, Ping Z, Chen S, Kenswil KJ, Mylona MA, Sanders MA, et al. Mesenchymal inflammation drives genotoxic stress in hematopoietic stem cells and predicts disease evolution in human pre-leukemia. Cell Stem Cell. 2016;19:613–27.

    Article 
    PubMed 

    Google Scholar
     

  • Essers MAG, Offner S, Blanco-Bose WE, Waibler Z, Kalinke U, Duchosal MA, et al. IFNα activates dormant haematopoietic stem cells in vivo. Nature .2009;458:904.

    Article 
    PubMed 

    Google Scholar
     

  • Butler JT, Abdelhamed S, Kurre P. Extracellular vesicles in the hematopoietic microenvironment. Haematologica .2018;103:382–94.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ortiz A, Gui J, Zahedi F, Yu P, Cho C, Bhattacharya S, et al. An interferon-driven oxysterol-based defense against tumor-derived extracellular vesicles. Cancer Cell 2019;35:33–45. e6.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kumar B, Garcia M, Weng L, Jung X, Murakami JL, Hu X, et al. Acute myeloid leukemia transforms the bone marrow niche into a leukemia-permissive microenvironment through exosome secretion. Leukemia .2018;32:575–87.

    Article 
    PubMed 

    Google Scholar
     

  • Doron B, Abdelhamed S, Butler JT, Hashmi SK, Horton TM, Kurre P. Transmissible ER stress reconfigures the AML bone marrow compartment. Leukemia. 2019;33:918–30.

    Article 
    PubMed 

    Google Scholar
     

  • Pietras EM, Lakshminarasimhan R, Techner J-M, Fong S, Flach J, Binnewies M, et al. Re-entry into quiescence protects hematopoietic stem cells from the killing effect of chronic exposure to type I interferons. J Exp Med. 2014;211:245–62.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ju J-M, Jung MH, Nam G, Kim W, Oh S, Kim HD, et al. Escape from thymic deletion and anti-leukemic effects of T cells specific for hematopoietic cell-restricted antigen. Nat Commun. 2018;9:225.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Deng M, Gui X, Kim J, Xie L, Chen W, Li Z, et al. LILRB4 signalling in leukaemia cells mediates T cell suppression and tumour infiltration. Nature 2018;562:605–9.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yan F, Shen N, Pang JX, Zhang YW, Rao EY, Bode AM, et al. Fatty acid-binding protein FABP4 mechanistically links obesity with aggressive AML by enhancing aberrant DNA methylation in AML cells. Leukemia .2017;31:1434–42.

    Article 
    PubMed 

    Google Scholar
     

  • Li J-M, Petersen CT, Li J-X, Panjwani R, Chandra DJ, Giver CR, et al. Modulation of immune checkpoints and graft-versus-leukemia in allogeneic transplants by antagonizing vasoactive intestinal peptide signaling. Cancer Res. 2016;76:6802–15.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Curran E, Chen X, Corrales L, Kline DE, others. STING pathway activation stimulates potent immunity against acute myeloid leukemia. Cell Rep. (2016).

  • Ratajczak M, Adamiak M, Deptala A, Domagala-Kulawik J, Ratajczak J, Kucia M. Myeloablative Conditioning for Transplantation Induces State of Sterile Inflammation in the Bone Marrow: Implications for Optimizing Homing and Engraftment of Hematopoietic Stem Cells. Antioxidant & Redox Signaling. 2022;37:1254–65.

    Article 

    Google Scholar
     

  • Pietras EM, Reynaud D, Kang Y-A, Carlin D, Calero-Nieto FJ, Leavitt AD, et al. Functionally distinct subsets of lineage-biased multipotent progenitors control blood production in normal and regenerative conditions. Cell Stem Cell. 2015;17:35–46.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Krivtsov AV, Twomey D, Feng Z, Stubbs MC, Wang Y, Faber J, et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL–AF9. Nature. 2006;442:818–22.

    Article 
    PubMed 

    Google Scholar
     

  • Bernt KM, Zhu N, Sinha AU, Vempati S, Faber J, Krivtsov AV, et al. MLL-rearranged leukemia is dependent on aberrant H3K79 methylation by DOT1L. Cancer Cell 2011;20:66–78.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stavropoulou V, Kaspar S, Brault L, Sanders MA, Juge S, Morettini S, et al. MLL-AF9 expression in hematopoietic stem cells drives a highly invasive AML expressing EMT-related genes linked to poor outcome. Cancer Cell. 2016;30:43–58.

    Article 
    PubMed 

    Google Scholar
     

  • Chen X, Burkhardt DB, Hartman AA, Hu X, Eastman AE, Sun C, et al. MLL-AF9 initiates transformation from fast-proliferating myeloid progenitors. Nat Commun. 2019;10:5767.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kelly-Scumpia KM, Scumpia PO, Delano MJ, Weinstein JS, Cuenca AG, Wynn JL, et al. Type I interferon signaling in hematopoietic cells is required for survival in mouse polymicrobial sepsis by regulating CXCL10. J Exp Med. 2010;207:319–26.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Baldridge MT, King KY, Boles NC, Weksberg DC, Goodell MA. Quiescent haematopoietic stem cells are activated by IFN-γ in response to chronic infection. Nature. 2010;465:793–7.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kanayama M, Izumi Y, Yamauchi Y, Kuroda S, Shin T, Ishikawa S, et al. CD86-based analysis enables observation of bona fide hematopoietic responses. Blood. 2020;136:1144–54.

    Article 
    PubMed 

    Google Scholar
     

  • Cai Z, Kotzin JJ, Ramdas B, Chen S, Nelanuthala S, Palam LR, et al. Inhibition of inflammatory signaling in Tet2 mutant preleukemic cells mitigates stress-induced abnormalities and clonal hematopoiesis. Cell Stem Cell 2018;23:833–49.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Welner RS, Amabile G, Bararia D, Czibere A, Yang H, Zhang H, et al. Treatment of chronic myelogenous leukemia by blocking cytokine alterations found in normal stem and progenitor cells. Cancer Cell 2015;27:671–81.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kleppe M, Kwak M, Koppikar P, Riester M, Keller M, Bastian L, et al. JAK–STAT pathway activation in malignant and nonmalignant cells contributes to MPN pathogenesis and therapeutic responseJAK–STAT pathway activation in malignant and nonmalignant cells in MPN. Cancer Discov. 2015;5:316–31.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Holicek P, Truxova I, Rakova J, Salek C, Hensler M, Kovar M, et al. Type I interferon signaling in malignant blasts contributes to treatment efficacy in AML patients. Cell Death Dis. 2023;14:209.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • de Laval B, Maurizio J, Kandalla P, Brisou G, Simonnet L, Huber C, et al. C/EBPβ-dependent epigenetic memory induces trained immunity in hematopoietic stem cells. Cell Stem Cell. 2020;26:657–74.

    Article 
    PubMed 

    Google Scholar
     

  • Abdelhamed S, Butler JT, Jung S, Chen D-W, Jenkins G, Gao L, et al. Rational biomarker development for the early and minimally invasive monitoring of AML. Blood Adv. 2021;5:4515–20.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bogeska R, Mikecin A-M, Kaschutnig P, Fawaz M, Büchler-Schäff M, Le D, et al. Inflammatory exposure drives long-lived impairment of hematopoietic stem cell self-renewal activity and accelerated aging. Cell Stem Cell. 2022;29:1273–84.e8.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schepers K, Pietras EM, Reynaud D, Flach J, Binnewies M, Garg T, et al. Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem Cell. 2013;13:285–99.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Miraki-Moud F, Anjos-Afonso F, Hodby KA, Griessinger E, Rosignoli G, Lillington D, et al. Acute myeloid leukemia does not deplete normal hematopoietic stem cells but induces cytopenias by impeding their differentiation. Proc Natl Acad Sci. 2013;110:13576–81.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Boyd AL, Reid JC, Salci KR, Aslostovar L, Benoit YD, Shapovalova Z, et al. Acute myeloid leukaemia disrupts endogenous myelo-erythropoiesis by compromising the adipocyte bone marrow niche. Nat Cell Biol. 2017;19:1336–47.

    Article 
    PubMed 

    Google Scholar
     

  • Akinduro O, Weber TS, Ang H, Haltalli M, Ruivo N, Duarte D, et al. Proliferation dynamics of acute myeloid leukaemia and haematopoietic progenitors competing for bone marrow space. Nat Commun. 2018;9:519.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Corces-Zimmerman MR, Hong W-J, Weissman IL, Medeiros BC, Majeti R. Preleukemic mutations in human acute myeloid leukemia affect epigenetic regulators and persist in remission. Proc Natl Acad Sci. 2014;111:2548–53.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Caiado F, Pietras EM, Manz MG. Inflammation as a regulator of hematopoietic stem cell function in disease, aging, and clonal selection. J Exp Med. 2021;218:e20201541.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Hormaechea-Agulla D, Matatall KA, Le DT, Kain B, Long X, Kus P, et al. Chronic infection drives Dnmt3a-loss-of-function clonal hematopoiesis via IFNγ signaling. Cell Stem Cell. 2021;28:1428–42.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Matatall KA, Jeong M, Chen S, Sun D, Chen F, Mo Q, et al. Chronic infection depletes hematopoietic stem cells through stress-induced terminal differentiation. Cell Rep. 2016;17:2584–95.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tall AR, Fuster JJ. Clonal hematopoiesis in cardiovascular disease and therapeutic implications. Nat Cardiovasc Res. 2022;1:116–24.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gómez AM, Martínez C, González M, Luque A, Melen GJ, Martínez J, et al. Chemokines and relapses in childhood acute lymphoblastic leukemia: a role in migration and in resistance to antileukemic drugs. Blood Cells, Mol, Dis. 2015;55:220–7.

    Article 
    PubMed 

    Google Scholar
     

  • Lee Y, Chittezhath M, André V, Zhao H, Poidinger M, Biondi A, et al. Protumoral role of monocytes in human B-cell precursor acute lymphoblastic leukemia: involvement of the chemokine CXCL10. Blood, J Am Soc Hematol. 2012;119:227–37.


    Google Scholar
     

  • Sarris AH, Broxmeyer HE, Wirthmueller U, Karasavvas N, Cooper S, Lu L, et al. Human interferon-inducible protein 10: expression and purification of recombinant protein demonstrate inhibition of early human hematopoietic progenitors. J Exp Med. 1993;178:1127–32.

    Article 
    PubMed 

    Google Scholar
     

  • Aldinucci D, Poletto D, Nanni P, Degan M, Rupolo M, Pinto A, et al. CD40L induces proliferation, self-renewal, rescue from apoptosis, and production of cytokines by CD40-expressing AML blasts. Exp Hematol. 2002;30:1283–92.

    Article 
    PubMed 

    Google Scholar
     

  • Argiropoulos B, Palmqvist L, Yung E, Kuchenbauer F, Heuser M, Sly LM, et al. Linkage of Meis1 leukemogenic activity to multiple downstream effectors including Trib2 and Ccl3. Exp Hematol. 2008;36:845–59.

    Article 
    PubMed 

    Google Scholar
     

  • Kornblau SM, Mccue D, Singh N, Chen W, Estrov Z, Coombes KR. Recurrent expression signatures of cytokines and chemokines are present and are independently prognostic in acute myelogenous leukemia and myelodysplasia. Blood .2010;116:4251–61.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Vijay V, Miller R, Vue GS, Pezeshkian MB, Maywood M, Ast AM, et al. Interleukin-8 blockade prevents activated endothelial cell mediated proliferation and chemoresistance of acute myeloid leukemia. Leuk Res. 2019;84:106180.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Vadakekolathu J, Minden MD, Hood T, Church SE, Reeder S, Altmann H, et al. Immune landscapes predict chemotherapy resistance and immunotherapy response in acute myeloid leukemia. Sci Transl Med. 2020;12:eaaz0463.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stevens AM, Miller JM, Munoz JO, Gaikwad AS, Redell MS. Interleukin-6 levels predict event-free survival in pediatric AML and suggest a mechanism of chemotherapy resistance. Blood Adv 2017;1:1387–97.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lasry A, Nadorp B, Fornerod M, Nicolet D, Wu H, Walker CJ, et al. An inflammatory state remodels the immune microenvironment and improves risk stratification in acute myeloid leukemia. Nature Cancer. 2022;4:27–42.

  • Bertoli S, Picard M, Bérard E, Griessinger E, Larrue C, Mouchel PL, et al. Dexamethasone in hyperleukocytic acute myeloid leukemia. Haematologica. 2018;103:988–98.

    Article 
    PubMed 
    PubMed Central 

    Google Scholar