Monocyte-macrophage polarization and recruitment pathways in the tumour microenvironment of B-cell acute lymphoblastic leukaemia.

Adolescent Adult Aged Antigens, CD / metabolism Coculture Techniques Female Human Umbilical Vein Endothelial Cells Humans Macrophages / metabolism Male Middle Aged Monocytes / metabolism Neoplasm Proteins / metabolism Precursor B-Cell Lymphoblastic Leukemia-Lymphoma / drug therapy Tumor Microenvironment

acute lymphoblastic leukaemia bone marrow microenvironment chemokines macrophages mesenchymal stromal cells monocytes

Journal

British journal of haematology

ISSN: 1365-2141

Titre abrégé: Br J Haematol

Pays: England

ID NLM: 0372544

Informations de publication

Date de publication:
06 2021

Historique:

revised: 18 12 2020

received: 07 09 2020

accepted: 21 12 2020

pubmed: 14 3 2021

medline: 28 9 2021

entrez: 13 3 2021

Statut: ppublish

Résumé

B-cell acute lymphoblastic leukaemia (B-ALL) reprograms the surrounding bone marrow (BM) stroma to create a leukaemia-supportive niche. To elucidate the contribution of immune cells to the leukaemic microenvironment, we investigated the involvement of monocyte/macrophage compartments, as well as several recruitment pathways in B-ALL development. Immunohistochemistry analyses showed that CD68-expressing macrophages were increased in leukaemic BM biopsies, compared to controls and predominantly expressed the M2-like markers CD163 and CD206. Furthermore, the "non-classical" CD14

Identifiants

DOI: 10.1111/bjh.17330 PMID: 33713428

pubmed: 33713428

doi: 10.1111/bjh.17330

doi:

Substances chimiques

Antigens, CD 0

Neoplasm Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

Pagination

1157-1171

Informations de copyright

Références

Ceppi F, Cazzaniga G, Colombini A, Biondi A, Conter V. Risk factors for relapse in childhood acute lymphoblastic leukemia: prediction and prevention. Expert Rev Hematol. 2015;8(1):57-70.

Jabbour E, Pui CH, Kantarjian H. Progress and innovations in the management of adult acute lymphoblastic leukemia. JAMA Oncol. 2018;4:1413-20.

Portale F, Beneforti L, Fallati A, Biondi A, Palmi C, Cazzaniga G, et al. Activin A contributes to the definition of a pro-oncogenic bone marrow microenvironment in t(12;21) preleukemia. Exp Hematol. 2019;73:7-12.e4.

Portale F, Cricri G, Bresolin S, Lupi M, Gaspari S, Silvestri D, et al. ActivinA: a new leukemia-promoting factor conferring migratory advantage to B-cell precursor-acute lymphoblastic leukemic cells. Haematologica. 2019;104:533-45.

de Rooij B, Polak R, van den Berk LCJ, Stalpers F, Pieters R, den Boer ML. Acute lymphoblastic leukemia cells create a leukemic niche without affecting the CXCR4/CXCL12 axis. Haematologica. 2017;102:e389-e393.

de Vasconcellos JF, Laranjeira AB, Zanchin NI, Otubo R, Vaz TH, Cardoso AA, et al. Increased CCL2 and IL-8 in the bone marrow microenvironment in acute lymphoblastic leukemia. Pediatr Blood Cancer. 2011;56:568-77.

Ma Z, Zhao X, Deng M, Huang Z, Wang J, Wu Y, et al. Bone marrow mesenchymal stromal cell-derived periostin promotes B-ALL progression by modulating CCL2 in leukemia cells. Cell Rep. 2019;26:1533-43 e4.

Mantovani A, Marchesi F, Malesci A, Laghi L, Allavena P. Tumour-associated macrophages as treatment targets in oncology. Nat Rev Clin Oncol. 2017;14:399-416.

Bottazzi B, Polentarutti N, Acero R, Balsari A, Boraschi D, Ghezzi P, et al. Regulation of the macrophage content of neoplasms by chemoattractants. Science. 1983;220:210-2.

Matsushima K, Larsen CG, DuBois GC, Oppenheim JJ. Purification and characterization of a novel monocyte chemotactic and activating factor produced by a human myelomonocytic cell line. J Exp Med. 1989;169:1485-90.

Nasrollahzadeh E, Razi S, Keshavarz-Fathi M, Mazzone M, Rezaei N. Pro-tumorigenic functions of macrophages at the primary, invasive and metastatic tumor site. Cancer Immunol Immunother. 2020;69:1673-97.

Xu R, Li Y, Yan H, Zhang E, Huang X, Chen Q, et al. CCL2 promotes macrophages-associated chemoresistance via MCPIP1 dual catalytic activities in multiple myeloma. Cell Death Dis. 2019;10(10):781.

Galletti G, Caligaris-Cappio F, Bertilaccio MT. B cells and macrophages pursue a common path toward the development and progression of chronic lymphocytic leukemia. Leukemia. 2016;30:2293-301.

Boissard F, Laurent C, Ramsay AG, Quillet-Mary A, Fournie JJ, Poupot M, et al. Nurse-like cells impact on disease progression in chronic lymphocytic leukemia. Blood Cancer J. 2016;6:e381.

Galletti G, Scielzo C, Barbaglio F, Rodriguez TV, Riba M, Lazarevic D, et al. Targeting macrophages sensitizes chronic lymphocytic leukemia to apoptosis and inhibits disease progression. Cell Rep. 2016;14:1748-60.

Al-Matary YS, Botezatu L, Opalka B, Hones JM, Lams RF, Thivakaran A, et al. Acute myeloid leukemia cells polarize macrophages towards a leukemia supporting state in a Growth factor independence 1 dependent manner. Haematologica. 2016;101:1216-27.

Marchesi F, Cirillo M, Bianchi A, Gately M, Olimpieri OM, Cerchiara E, et al. High density of CD68+/CD163+ tumour-associated macrophages (M2-TAM) at diagnosis is significantly correlated to unfavorable prognostic factors and to poor clinical outcomes in patients with diffuse large B-cell lymphoma. Hematol Oncol. 2015;33:110-2.

Kaku Y, Imaoka H, Morimatsu Y, Komohara Y, Ohnishi K, Oda H, et al. Overexpression of CD163, CD204 and CD206 on alveolar macrophages in the lungs of patients with severe chronic obstructive pulmonary disease. PLoS One. 2014;9:e87400.

Komohara Y, Hirahara J, Horikawa T, Kawamura K, Kiyota E, Sakashita N, et al. AM-3K, an anti-macrophage antibody, recognizes CD163, a molecule associated with an anti-inflammatory macrophage phenotype. J Histochem Cytochem. 2006;54:763-71.

Anfray C, Ummarino A, Andon FT, Allavena P. Current strategies to target tumor-associated-macrophages to improve anti-tumor immune responses. Cells. 2019;9:46.

Etzerodt A, Moulin M, Doktor TK, Delfini M, Mossadegh-Keller N, Bajenoff M, et al. Tissue-resident macrophages in omentum promote metastatic spread of ovarian cancer. J Exp Med. 2020;217.

Kiss M, Van Gassen S, Movahedi K, Saeys Y, Laoui D. Myeloid cell heterogeneity in cancer: not a single cell alike. Cell. Immunol. 2018;330:188-201.

Fronkova E, Mejstrikova E, Avigad S, Chik KW, Castillo L, Manor S, et al. Minimal residual disease (MRD) analysis in the non-MRD-based ALL IC-BFM 2002 protocol for childhood ALL: is it possible to avoid MRD testing? Leukemia. 2008;22:989-97.

Conter V, Bartram CR, Valsecchi MG, Schrauder A, Panzer-Grumayer R, Moricke A, et al. Molecular response to treatment redefines all prognostic factors in children and adolescents with B-cell precursor acute lymphoblastic leukemia: results in 3184 patients of the AIEOP-BFM ALL 2000 study. Blood. 2010;115:3206-14.

Verma D, Zanetti C, Godavarthy PS, Kumar R, Minciacchi VR, Pfeiffer J, et al. Bone marrow niche-derived extracellular matrix-degrading enzymes influence the progression of B-cell acute lymphoblastic leukemia. Leukemia. 2020;34:1540-52.

Vilchis-Ordonez A, Contreras-Quiroz A, Vadillo E, Dorantes-Acosta E, Reyes-López A, Quintela-Nuñez del Prado HM, et al. Bone marrow cells in acute lymphoblastic leukemia create a proinflammatory microenvironment influencing normal hematopoietic differentiation fates. Biomed Res Int. 2015;2015:386165.

Ferretti E, Bertolotto M, Deaglio S, Tripodo C, Ribatti D, Audrito V, et al. A novel role of the CX3CR1/CX3CL1 system in the cross-talk between chronic lymphocytic leukemia cells and tumor microenvironment. Leukemia. 2011;25:1268-77.

Marchica V, Toscani D, Corcione A, Bolzoni M, Storti P, Vescovini R, et al. Bone Marrow CX3CL1/Fractalkine is a new player of the pro-angiogenic microenvironment in multiple myeloma patients. Cancers. 2019;11(3):321.

Villani AC, Satija R, Reynolds G, Sarkizova S, Shekhar K, Fletcher J, et al. Single-cell RNA-seq reveals new types of human blood dendritic cells, monocytes, and progenitors. Science. 2017;356:eaah4573.

Merah-Mourah F, Cohen SO, Charron D, Mooney N, Haziot A. Identification of novel human monocyte subsets and evidence for phenotypic groups defined by interindividual variations of expression of adhesion molecules. Sci Rep. 2020;10:4397.

Ahmad F, Dobel T, Schmitz M, Schakel K. Current concepts on 6-sulfo LacNAc expressing monocytes (slanMo). Front Immunol. 2019;10:948.

Piao C, Zhang WM, Li TT, Zhang CC, Qiu S, Liu Y, et al. Complement 5a stimulates macrophage polarization and contributes to tumor metastases of colon cancer. Exp Cell Res. 2018;366:127-38.

Bonavita E, Gentile S, Rubino M, Maina V, Papait R, Kunderfranco P, et al. PTX3 is an extrinsic oncosuppressor regulating complement-dependent inflammation in cancer. Cell. 2015;160:700-14.

Garlanda C, Bottazzi B, Magrini E, Inforzato A, Mantovani A. PTX3, a humoral pattern recognition molecule, in innate immunity, tissue repair, and cancer. Physiol Rev. 2018;98:623-39.

Sun W, Malvar J, Sposto R, Verma A, Wilkes JJ, Dennis R, et al. Outcome of children with multiply relapsed B-cell acute lymphoblastic leukemia: a therapeutic advances in childhood leukemia & lymphoma study. Leukemia. 2018;32:2316-25.

Witkowski MT, Dolgalev I, Evensen NA, Ma C, Chambers T, Roberts KG, et al. Extensive remodeling of the immune microenvironment in B cell acute lymphoblastic leukemia. Cancer Cell. 2020.

Wang Q, Lu Y, Li R, Jiang Y, Zheng Y, Qian J, et al. Therapeutic effects of CSF1R-blocking antibodies in multiple myeloma. Leukemia. 2018;32:176-83.

Sousa S, Brion R, Lintunen M, Kronqvist P, Sandholm J, Monkkonen J, et al. Human breast cancer cells educate macrophages toward the M2 activation status. Breast Cancer Res 2015;17:101.

Zhang QW, Liu L, Gong CY, Shi HS, Zeng YH, Wang XZ, et al. Prognostic significance of tumor-associated macrophages in solid tumor: a meta-analysis of the literature. PLoS One. 2012;7:e50946.

Komohara Y, Niino D, Saito Y, Ohnishi K, Horlad H, Ohshima K, et al. Clinical significance of CD163(+) tumor-associated macrophages in patients with adult T-cell leukemia/lymphoma. Cancer Sci. 2013;104:945-51.

Kowalska W. Expression of CD163 and HLA-DR molecules on the monocytes in chronic lymphocytic leukemia patients. Folia Histochem. Cytobiol. 2020;58:17-24.

Marchesi F, Piemonti L, Fedele G, Destro A, Roncalli M, Albarello L, et al. The chemokine receptor CX3CR1 is involved in the neural tropism and malignant behavior of pancreatic ductal adenocarcinoma. Can Res. 2008;68:9060-9.

Gurler Main H, Xie J, Muralidhar GG, Elfituri O, Xu H, Kajdacsy-Balla AA, et al. Emergent role of the fractalkine axis in dissemination of peritoneal metastasis from epithelial ovarian carcinoma. Oncogene. 2017;36:3025-36.

Tardaguila M, Mira E, Garcia-Cabezas MA, Feijoo AM, Quintela-Fandino M, Azcoitia I, et al. CX3CL1 promotes breast cancer via transactivation of the EGF pathway. Can Res. 2013;73:4461-73.

Popovic M, Laumonnier Y, Burysek L, Syrovets T, Simmet T. Thrombin-induced expression of endothelial CX3CL1 potentiates monocyte CCL2 production and transendothelial migration. J Leukoc Biol. 2008;84:215-23.

Sierra-Filardi E, Nieto C, Dominguez-Soto A, Barroso R, Sanchez-Mateos P, Puig-Kroger A, et al. CCL2 shapes macrophage polarization by GM-CSF and M-CSF: identification of CCL2/CCR2-dependent gene expression profile. J Immunol. 2014;192:3858-67.

Li Y, Zheng Y, Li T, Wang Q, Qian J, Lu Y, et al. Chemokines CCL2, 3, 14 stimulate macrophage bone marrow homing, proliferation, and polarization in multiple myeloma. Oncotarget. 2015;6:24218-29.

Lenkiewicz A, Bujko K, Brzezniakiewicz-Janus K, Xu B, Ratajczak MZ. The complement cascade as a mediator of human malignant hematopoietic cell trafficking. Front Immunol. 2019;10:1292.

Edwards DK, Watanabe-Smith K, Rofelty A, Damnernsawad A, Laderas T, Lamble A, et al. CSF1R inhibitors exhibit antitumor activity in acute myeloid leukemia by blocking paracrine signals from support cells. Blood. 2019;133:588-99.

Zucca E, Rondeau S, Vanazzi A, Ostenstad B, Mey UJM, Rauch D, et al. Short regimen of rituximab plus lenalidomide in follicular lymphoma patients in need of first-line therapy. Blood. 2019;134:353-62.

Schulz A, Durr C, Zenz T, Dohner H, Stilgenbauer S, Lichter P, et al. Lenalidomide reduces survival of chronic lymphocytic leukemia cells in primary cocultures by altering the myeloid microenvironment. Blood. 2013;121:2503-11.

Banerjee P, Zhang R, Ivan C, Galletti G, Clise-Dwyer K, Barbaglio F, et al. Trabectedin reveals a strategy of immunomodulation in chronic lymphocytic leukemia. Cancer Immunol Res. 2019;7:2036-51.

Adams S, Kozhaya L, Martiniuk F, Meng TC, Chiriboga L, Liebes L, et al. Topical TLR7 agonist imiquimod can induce immune-mediated rejection of skin metastases in patients with breast cancer. Clinical Cancer Res. 2012;18:6748-57.

Kyi C, Roudko V, Sabado R, Saenger Y, Loging W, Mandeli J, et al. Therapeutic immune modulation against solid cancers with intratumoral Poly-ICLC: A Pilot Trial. Clin Cancer Res. 2018;24:4937-48.