Enhanced expression of galectin-9 in triple negative breast cancer cells following radiotherapy: Implications for targeted therapy.
galectin‐9
molecular targeted therapy
radiotherapy
triple‐negative breast cancer
Journal
International journal of cancer
ISSN: 1097-0215
Titre abrégé: Int J Cancer
Pays: United States
ID NLM: 0042124
Informations de publication
Date de publication:
30 Jul 2024
30 Jul 2024
Historique:
revised:
15
05
2024
received:
18
01
2024
accepted:
27
06
2024
medline:
30
7
2024
pubmed:
30
7
2024
entrez:
30
7
2024
Statut:
aheadofprint
Résumé
Optimizations are expected in the development of immunotherapy for the treatment of Triple-negative breast cancer (TNBC). We studied the expression of galectin-9 (Gal-9) after irradiation and assessed the differential impacts of its targeting with or without radiotherapy. Tumor resections from TNBC patients who received neoadjuvant radiotherapy revealed higher levels of Gal-9 in comparison to their baseline level, only in non-responder patients. Gal-9 expression was also found to be increased in TNBC tumor biopsies and cell lines after irradiation. We investigated the therapeutic advantage of targeting Gal-9 after radiotherapy in mice. Irradiated 4T1 cells or control non-irradiated 4T1 cells were injected into BALB/c mice. Anti-Gal-9 antibody treatment decreased tumor progression only in mice injected with irradiated 4T1 cells. This proof-of-concept study demonstrates that Gal-9 could be considered as a dynamic biomarker after radiotherapy for TNBC and suggests that Gal-9 induced-overexpression could represent an opportunity to develop new therapeutic strategies for TNBC patients.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Conférence de Coordination Interrégionale EST (CCIR EST) de la Ligue contre le cancer
Informations de copyright
© 2024 The Author(s). International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.
Références
Sung H, Ferlay J, Siegel RL, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209‐249.
Siegel RL, Miller KD, Jemal A. Cancer statistics, 2019. CA Cancer J Clin. 2019;69(1):7‐34.
Pal SK, Childs BH, Pegram M. Triple negative breast cancer: unmet medical needs. Breast Cancer Res Treat. 2011;125(3):627‐636.
Balko JM, Giltnane JM, Wang K, et al. Molecular profiling of the residual disease of triple‐negative breast cancers after neoadjuvant chemotherapy identifies actionable therapeutic targets. Cancer Discov. 2014;4(2):232‐245.
Carey LA, Dees EC, Sawyer L, et al. The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res. 2007;13(8):2329‐2334.
Schmid P, Cortes J, Pusztai L, et al. Pembrolizumab for early triple‐negative breast cancer. N Engl J Med. 2020;382(9):810‐821.
Cortazar P, Zhang L, Untch M, et al. Pathological complete response and long‐term clinical benefit in breast cancer: the CTNeoBC pooled analysis. Lancet. 2014;384(9938):164‐172.
Veeraraghavan J, Natarajan M, Aravindan S, Herman TS, Aravindan N. Radiation‐triggered tumor necrosis factor (TNF) α‐NFκB cross‐signaling favors survival advantage in human neuroblastoma cells. J Biol Chem. 2011;286(24):21588‐21600.
Zang C, Liu X, Li B, et al. IL‐6/STAT3/TWIST inhibition reverses ionizing radiation‐induced EMT and radioresistance in esophageal squamous carcinoma. Oncotarget. 2017;8(7):11228‐11238.
Schröder S, Juerß D, Kriesen S, Manda K, Hildebrandt G. Immunomodulatory properties of low‐dose ionizing radiation on human endothelial cells. Int J Radiat Biol. 2019;95(1):23‐32.
Wu CT, Chen WC, Chang YH, Lin WY, Chen MF. The role of PD‐L1 in the radiation response and clinical outcome for bladder cancer. Sci Rep. 2016;6:19740.
Zhang H, Zhou F, Wang Y, et al. Eliminating radiation resistance of non‐small cell lung cancer by dihydroartemisinin through abrogating immunity escaping and promoting radiation sensitivity by inhibiting PD‐L1 expression. Front Oncol. 2020;10:595466. doi:10.3389/fonc.2020.595466
Rompré‐Brodeur A, Shinde‐Jadhav S, Ayoub M, et al. PD‐1/PD‐L1 immune checkpoint inhibition with radiation in bladder cancer: in situ and abscopal effects. Mol Cancer Ther. 2020;19(1):211‐220.
Gehre S, Meyer F, Sengedorj A, et al. Clonogenicity‐based radioresistance determines the expression of immune suppressive immune checkpoint molecules after hypofractionated irradiation of MDA‐MB‐231 triple‐negative breast cancer cells. Front Oncol. 2023;13:981239.
Grandal B, Mangiardi‐Veltin M, Laas E, et al. PD‐L1 expression after neoadjuvant chemotherapy in triple‐negative breast cancers is associated with aggressive residual disease, suggesting a potential for immunotherapy. Cancers (Basel). 2021;13(4):746.
Candas‐Green D, Xie B, Huang J, et al. Dual blockade of CD47 and HER2 eliminates radioresistant breast cancer cells. Nat Commun. 2020;11(1):4591.
Wang NH, Lei Z, Yang HN, et al. Radiation‐induced PD‐L1 expression in tumor and its microenvironment facilitates cancer‐immune escape: a narrative review. Ann Transl Med. 2022;10(24):1406.
Lv Y, Ma X, Ma Y, Du Y, Feng J. A new emerging target in cancer immunotherapy: galectin‐9 (LGALS9). Genes Dis. 2022;10(6):2366‐2382.
Yang RY, Rabinovich GA, Liu FT. Galectins: structure, function and therapeutic potential. Expert Rev Mol Med. 2008;10:e17.
Gieseke F, Kruchen A, Tzaribachev N, Bentzien F, Dominici M, Müller I. Proinflammatory stimuli induce galectin‐9 in human mesenchymal stromal cells to suppress T‐cell proliferation. Eur J Immunol. 2013;43(10):2741‐2749.
Zheng S, Song J, Linghu D, et al. Galectin‐9 blockade synergizes with ATM inhibition to induce potent anti‐tumor immunity. Int J Biol Sci. 2023;19(3):981‐993.
Zhu C, Anderson AC, Schubart A, et al. The Tim‐3 ligand galectin‐9 negatively regulates T helper type 1 immunity. Nat Immunol. 2005;6(12):1245‐1252.
Wu C, Thalhamer T, Franca RF, et al. Galectin‐9‐CD44 interaction enhances stability and function of adaptive regulatory T cells. Immunity. 2014;41(2):270‐282.
Cao A, Alluqmani N, Buhari FHM, et al. Galectin‐9 binds IgM‐BCR to regulate B cell signaling. Nat Commun. 2018;9:3288.
Daley D, Mani VR, Mohan N, et al. Dectin‐1 activation on macrophages by galectin‐9 promotes pancreatic carcinoma and peritumoral immune‐tolerance. Nat Med. 2017;23(5):556‐567.
Lv R, Bao Q, Li Y. Regulation of M1‐type and M2‐type macrophage polarization in RAW264.7 cells by galectin‐9. Mol Med Rep. 2017;16(6):9111‐9119.
Schlichtner S, Yasinska IM, Lall GS, et al. T lymphocytes induce human cancer cells derived from solid malignant tumors to secrete galectin‐9 which facilitates immunosuppression in cooperation with other immune checkpoint proteins. J Immunother Cancer. 2023;11(1):e005714. doi:10.1136/jitc‐2022‐005714
Pally D, Banerjee M, Hussain S, et al. Galectin‐9 signaling drives breast cancer invasion through extracellular matrix. ACS Chem Biol. 2022;17(6):1376‐1386.
Aanhane E, Schulkens IA, Heusschen R, et al. Different angioregulatory activity of monovalent galectin‐9 isoforms. Angiogenesis. 2018;21(3):545‐555.
Chou SY, Yen SL, Huang CC, Huang EY. Galectin‐1 is a poor prognostic factor in patients with glioblastoma multiforme after radiotherapy. BMC Cancer. 2018;18(1):105.
Ju MH, Byun KD, Park EH, Lee JH, Han SH. Association of galectin 9 expression with immune cell infiltration, programmed cell death ligand‐1 expression, and patient's clinical outcome in triple‐negative breast cancer. Biomedicine. 2021;9(10):1383.
Gameiro SR, Jammeh ML, Wattenberg MM, Tsang KY, Ferrone S, Hodge JW. Radiation‐induced immunogenic modulation of tumor enhances antigen processing and calreticulin exposure, resulting in enhanced T‐cell killing. Oncotarget. 2014;5(2):403‐416.
Karekla E, Liao WJ, Sharp B, et al. Ex vivo explant cultures of non‐small cell lung carcinoma enable evaluation of primary tumor responses to anticancer therapy. Cancer Res. 2017;77(8):2029‐2039.
Yang R, Sun L, Li CF, et al. Galectin‐9 interacts with PD‐1 and TIM‐3 to regulate T cell death and is a target for cancer immunotherapy. Nat Commun. 2021;12(1):832.
Bos PD, Plitas G, Rudra D, Lee SY, Rudensky AY. Transient regulatory T cell ablation deters oncogene‐driven breast cancer and enhances radiotherapy. J Exp Med. 2013;210(11):2435‐2466.
Zhang Y, Xue S, Hao Q, Liu F, Huang W, Wang J. Galectin‐9 and PSMB8 overexpression predict unfavorable prognosis in patients with AML. J Cancer. 2021;12(14):4257‐4263.
Lee M, Hamilton JAG, Talekar GR, et al. Obesity‐induced galectin‐9 is a therapeutic target in B‐cell acute lymphoblastic leukemia. Nat Commun. 2022;13(1):1157.
Spitzenberger F, Graessler J, Schroeder HE. Molecular and functional characterization of galectin 9 mRNA isoforms in porcine and human cells and tissues. Biochimie. 2001;83(9):851‐862.
Yang R, Sun L, Li CF, et al. Development and characterization of anti‐galectin‐9 antibodies that protect T cells from galectin‐9‐induced cell death. J Biol Chem. 2022;298(4):101821.