Bone Marrow Microenvironment Signalling and Chemoresistance in Acute Myeloid Leukemia

Authors

  • Iva Babic Department of Stem Cell Transplantation, University of Zagreb, Zagreb, Croatia Author
  • Radost Dimitrova Department of Clinical Immunology, Medical University of Plovdiv, Plovdiv, Bulgaria Author
  • Sanne Van Dijk Department of Haematopathology, Erasmus University Rotterdam, Rotterdam, Netherlands Author

DOI:

https://doi.org/10.5281/zenodo.22238172

Keywords:

Acute Myeloid Leukaemia, Bone Marrow Microenvironment, CXCR4, Chemoresistance, Leukaemic Niche

Abstract

Graphical abstract

Leukaemic blasts sheltering in the marrow niche survive chemotherapy that kills their circulating counterparts. The mechanism has been characterised in unusualdetail, the drugs to disrupt it exist and are licensed for other purposes, and after two decades the clinical  benefit remains unproven. Objectives: To review the published evidence on bone marrow microenvironment signalling as a mediator of chemoresistance in acute myeloid leukaemia: which interactions confer protection, how they have been demonstrated, which have been targeted clinically, and why the translation has been slower than the biology predicted. Material and Methods: Narrative review of mechanistic studies, preclinical models, early-phase trials and randomised evaluations indexed in PubMed and the major haematology journals. Studies were eligible if they characterised a marrow microenvironment interaction contributing to chemoresistance in acute
leukaemia, or reported clinical evaluation of an agent targeting one. No new patient data were generated and no patients were recruited; every estimate quoted is one published by the original investigators. Results: CXCR4 is overexpressed in 25 to 30 per cent of patients with acute myeloid leukaemia, and high expression is associated with poor prognosis. Its ligand CXCL12 is produced by marrow mesenchymal stromal cells and anchors blasts in contact with stroma and extracellular matrix, which generate growth-promoting and anti-apoptotic signals. Stromal co-culture confers chemoresistance in vitro and co-treatment with a CXCR4 antagonist restores chemosensitivity. In murine models, adding a CXCR4 antagonist to cytarabine reduced leukaemic burden and improved survival. Clinical translation has proceeded through a phase 1/2 chemosensitisation study in relapsed and refractory disease and, more recently, a randomised, double-blind, placebo-controlled phase 2 trial in which 128 patients in first remission received high-dose cytarabine with a selective CXCR4 antagonist or placebo. Conclusion: The mechanism is well established and reproducible across models, and the therapeutic principle remains largely untested at scale. Two decades after the interaction was described, the randomised evidence amounts to a single phase 2 trial of 128 patients. Abbreviations: AML – Acute Myeloid Leukaemia, ALL – Acute Lymphoblastic Leukaemia, BM – Bone Marrow, BMSC – Bone Marrow Stromal Cell, CXCR4 – CXC Chemokine Receptor 4, CXCL12 – CXC Motif Chemokine Ligand 12, SDF-1 – Stromal Cell-Derived Factor 1, VLA-4 – Very Late Antigen 4, VCAM-1 – Vascular Cell Adhesion Molecule 1, LSC – Leukaemic Stem Cell, MRD – Measurable Residual Disease, HSC – Haematopoietic Stem Cell, PDX – Patient-Derived Xenograft.

References

Döhner, H., Wei, AH., Appelbaum, FR., Craddock, C., DiNardo, CD., Dombret, H., et al. (2022) Diagnosis and management of AML in adults: 2022 recommendations from an international expert panel on behalf of the ELN. Blood, 140(12): 1345-1377.

Kantarjian, H., Kadia, T., DiNardo, C., Daver, N., Borthakur, G., Jabbour, E., et al. (2021) Acute myeloid leukemia: current progress and future directions. Blood Cancer J, 11: 41.

Cho, BS., Kim, HJ., Konopleva, M. (2017) Targeting the CXCL12/CXCR4 axis in acute myeloid leukemia: from bench to bedside. Korean J Intern Med, 32(2): 248-257.

Vanegas, NP., Vernot, JP. (2015) Targeting the microenvironment in acute myeloid leukemia. Curr Cancer Drug Targets, 15(4): 267-283.

Schepers, K., Campbell, TB., Passegué, E. (2015) Normal and leukemic stem cell niches: insights and therapeutic opportunities. Cell Stem Cell, 16(3): 254-267.

Poggi, A., Villa, F., Fernadez, JLC., Costa, D., Zocchi, MR., Benelli, R. (2021) Hematopoietic cell kinase (HCK) is a player of the crosstalk between hematopoietic cells and bone marrow niche through CXCL12/CXCR4 axis. Front Immunol, 12: 638496.

Peled, A., Petit, I., Kollet, O., Magid, M., Ponomaryov, T., Byk, T., et al. (1999) Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science, 283(5403): 845-848.

Burger, JA., Kipps, TJ. (2006) CXCR4: a key receptor in the crosstalk between tumor cells and their microenvironment. Blood, 107(5): 1761-1767.

Nervi, B., Ramirez, P., Rettig, MP., Uy, GL., Holt, MS., Ritchey, JK., et al. (2009) Chemosensitization of acute myeloid leukemia (AML) following mobilization by the CXCR4 antagonist AMD3100. Blood, 113(24): 6206-6214.

Uy, GL., Rettig, MP., Motabi, IH., McFarland, K., Trinkaus, KM., Hladnik, LM., et al. (2012) A phase 1/2 study of chemosensitization with the CXCR4 antagonist plerixafor in relapsed or refractory acute myeloid leukemia. Blood, 119(17): 3917-3924.

Broxmeyer, HE., Orschell, CM., Clapp, DW., Hangoc, G., Cooper, S., Plett, PA., et al. (2005) Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med, 201(8): 1307-1318.

Kuhne, MR., Mulvey, T., Belanger, B., Chen, S., Pan, C., Chong, C., et al. (2013) BMS-936564/MDX-1338: a fully human anti-CXCR4 antibody induces apoptosis in vitro and shows antitumor activity in vivo in hematologic malignancies. Clin Cancer Res, 19(2): 357-366.

Sison, EAR., Magoon, D., Li, L., Annesley, CE., Rau, RE., Small, D., Brown, P. (2014) Plerixafor as a chemosensitizing agent in pediatric acute lymphoblastic leukemia: efficacy and potential mechanisms of resistance to CXCR4 inhibition. Oncotarget, 5(19): 8947-8958.

Zeng, Z., Shi, YX., Samudio, IJ., Wang, RY., Ling, X., Frolova, O., et al. (2009) Targeting the leukemia microenvironment by CXCR4 inhibition overcomes resistance to kinase inhibitors and chemotherapy in AML. Blood, 113(24): 6215-6224.

Konopleva, MY., Jordan, CT. (2011) Leukemia stem cells and microenvironment: biology and therapeutic targeting. J Clin Oncol, 29(5): 591-599.

Bhatt, S., Rettig, MP., Uy, GL., et al. (2026) Inhibition of high CXCR4 with motixafortide and absence of single-cell MRD predict outcome after AML consolidation. Blood.

Chien, S., Beyer, T., Nourigat-Sabo, C., et al. (2019) Targeting adhesion molecules and the hypoxic niche in acute myeloid leukemia. Curr Opin Hematol, 26(2): 88-95.

Hawkins, ED., Duarte, D., Akinduro, O., Khorshed, RA., Passaro, D., Nowicka, M., et al. (2019) Defining the in vivo characteristics of acute myeloid leukemia cells behavior by intravital imaging. Immunol Cell Biol, 97(3): 229-235.

Li, X., Guo, H., Duan, H., Yang, Y., Meng, J., Liu, J., Wang, C., Xu, H. (2015) Improving chemotherapeutic efficiency in acute myeloid leukemia treatments by chemically synthesized peptide interfering with CXCR4/CXCL12 axis. Sci Rep, 5: 16228.

Ishikawa, F., Yoshida, S., Saito, Y., Hijikata, A., Kitamura, H., Tanaka, S., et al. (2007) Chemotherapy-resistant human AML stem cells home to and engraft within the bone-marrow endosteal region. Nat Biotechnol, 25(11): 1315-1321.

Matsunaga, T., Takemoto, N., Sato, T., Takimoto, R., Tanaka, I., Fujimi, A., et al. (2003) Interaction between leukemic-cell VLA-4 and stromal fibronectin is a decisive factor for minimal residual disease of acute myelogenous leukemia. Nat Med, 9(9): 1158-1165.

Jacamo, R., Chen, Y., Wang, Z., Ma, W., Zhang, M., Spaeth, EL., et al. (2014) Reciprocal leukemia-stroma VCAM-1/VLA-4-dependent activation of NF-kappaB mediates chemoresistance. Blood, 123(17): 2691-2702.

Moschoi, R., Imbert, V., Nebout, M., Chiche, J., Mary, D., Prebet, T., et al. (2016) Protective mitochondrial transfer from bone marrow stromal cells to acute myeloid leukemic cells during chemotherapy. Blood, 128(2): 253-264.

Zeijlemaker, W., Grob, T., Meijer, R., Hanekamp, D., Kelder, A., Carbaat-Ham, JC., et al. (2019) CD34+CD38- leukemic stem cell frequency to predict outcome in acute myeloid leukemia. Leukemia, 33(5): 1102-1112.

Schuurhuis, GJ., Heuser, M., Freeman, S., Béné, MC., Buccisano, F., Cloos, J., et al. (2018) Minimal/measurable residual disease in AML: a consensus document from the European LeukemiaNet MRD Working Party. Blood, 131(12): 1275-1291.

Graphical abstract

Published

2025-08-25

Issue

Section

Articles

How to Cite

Bone Marrow Microenvironment Signalling and Chemoresistance in Acute Myeloid Leukemia. (2025). Annals of Leukemia Research, 6(1), 16-21. https://doi.org/10.5281/zenodo.22238172