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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

CN 11-5983/R

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Front. Med.    2023, Vol. 17 Issue (1) : 105-118    https://doi.org/10.1007/s11684-022-0934-1
RESEARCH ARTICLE
CD47 blockade improves the therapeutic effect of osimertinib in non-small cell lung cancer
Wei-Bang Yu1, Yu-Chi Chen1, Can-Yu Huang1, Zi-Han Ye1, Wei Shi1, Hong Zhu2, Jia-Jie Shi1, Jun Chen3, Jin-Jian Lu1,4,5()
1. State Key Laboratory of Quality Research in Chinese Medicine, Institute of Chinese Medical Sciences, University of Macau, Macao 999078, China
2. Zhejiang Province Key Laboratory of Anti-Cancer Drug Research, College of Pharmaceutical Sciences, and Cancer Center of Zhejiang University, Zhejiang University, Hangzhou 310000, China
3. Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou 510000, China
4. Department of Pharmaceutical Sciences, Faculty of Health Sciences, University of Macau, Macao 999078, China
5. MoE Frontiers Science Center for Precision Oncology, University of Macau, Macao 999078, China
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Abstract

The third-generation epidermal growth factor receptor (EGFR) inhibitor osimertinib (OSI) has been approved as the first-line treatment for EGFR-mutant non-small cell lung cancer (NSCLC). This study aims to explore a rational combination strategy for enhancing the OSI efficacy. In this study, OSI induced higher CD47 expression, an important anti-phagocytic immune checkpoint, via the NF-κB pathway in EGFR-mutant NSCLC HCC827 and NCI-H1975 cells. The combination treatment of OSI and the anti-CD47 antibody exhibited dramatically increasing phagocytosis in HCC827 and NCI-H1975 cells, which highly relied on the antibody-dependent cellular phagocytosis effect. Consistently, the enhanced phagocytosis index from combination treatment was reversed in CD47 knockout HCC827 cells. Meanwhile, combining the anti-CD47 antibody significantly augmented the anticancer effect of OSI in HCC827 xenograft mice model. Notably, OSI induced the surface exposure of “eat me” signal calreticulin and reduced the expression of immune-inhibitory receptor PD-L1 in cancer cells, which might contribute to the increased phagocytosis on cancer cells pretreated with OSI. In summary, these findings suggest the multidimensional regulation by OSI and encourage the further exploration of combining anti-CD47 antibody with OSI as a new strategy to enhance the anticancer efficacy in EGFR-mutant NSCLC with CD47 activation induced by OSI.
Keywords osimertinib      anti-CD47 antibody      combination strategy      ADCP      EGFR     
Corresponding Author(s): Jin-Jian Lu   
Just Accepted Date: 01 September 2022   Online First Date: 23 November 2022    Issue Date: 15 March 2023
 Cite this article:   
Wei-Bang Yu,Yu-Chi Chen,Can-Yu Huang, et al. CD47 blockade improves the therapeutic effect of osimertinib in non-small cell lung cancer[J]. Front. Med., 2023, 17(1): 105-118.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-022-0934-1
https://academic.hep.com.cn/fmd/EN/Y2023/V17/I1/105
Fig.1  OSI upregulates the CD47 expression in HCC827 and NCI-H1975 cell lines. (A) After the treatment with 125 nmol/L OSI for 48 h in cancer cells with different mutation background, the CD47 expression on the membrane was detected by flow cytometry. (B and D) Flow cytometry and Western blot assay were performed to determine CD47 expression after the treatment of different dosages of OSI for 1 h and/or 48 h in HCC827 cells. (C and E) The CD47 expression level was determined by flow cytometry and Western blot after the treatment of 125 nmol/L OSI for 24 h and 48 h in HCC827 cells. (F) The HCC827 xenograft mice were treated with vehicle or OSI (0.5 mg/kg) as described in the materials and methods section. After the mice were sacrificed, CD47 expression in three independent tumor tissues of each group was obtained and detected through flow cytometry.
GenesAnalysisSequences
CD47qRT-PCRForward: 5′-AGAAGGTGAAACGATCATCGAGC-3′
Reverse: 5′-CTCATCCATACCACCGGATCT-3′
β-actinqRT-PCRForward: 5′-AGCGAGCATCCCCCAAAGTT-3′
Reverse: 5′-GGGCACGAAGGCTCATCATT-3′
EGFRsiRNASense: 5′-GCCUGAGAGUGGAGGUAAC-3′
Antisense: 5′-GUUACCUCCACUCUCAGGC-3′
p65siRNASense: 5′-GAUCAAUGGCUACACAGGATT-3′
Antisense: 5′-UCCUGUGUAUCCAUUGAUCTT-3′
Negative controlsiRNASense:5′-UUCUCCGAACGUGUCACGUTT-3′
Antisense: 5′-ACGUGACACGUUCGGAGAATT-3′
Tab.1  Primers and siRNA sequences
Fig.2  OSI induces higher CD47 expression through the NF-κB pathway. (A) The CD47 mRNA levels were detected by qRT-PCR in HCC827 cells after the treatment of OSI (125 nmol/L) for 24 h and 48 h. (B and C) The CD47 expression was determined by flow cytometry and Western blot in HCC827 cells pretreated with OSI (125 nmol/L) or siRNA of EGFR for 48 h. (D) Western blot assay was used to determine the related protein levels in HCC827 cells pretreated with siRNA of p65 for 6 h, followed by the addition of OSI (125 nmol/L) for another 42 h. (E) Cytoplasm–nucleus fractionation of HCC827 cells pretreated with OSI (125 nmol/L) was conducted, and the related proteins were detected by Western blot. Actin and Histone H3 were the internal controls for cytoplasmic and nuclear proteins, respectively.
Fig.3  The combination of OSI and B6H12 shows dramatically enhanced phagocytosis in vitro and a better anticancer effect in vivo. (A) Flow cytometry assay was used to determine the binding of CD47 and SIRPα after the OSI treatment (125 nmol/L) for 48 h, followed by the coculture with recombinant human SIRPα antibody. (B) HCC827 or NCI-H1975 cells pretreated with OSI (125 nmol/L) were labeled with CFSE and cocultured with BMDMs (3:1) for 2 h in the presence or absence of anti-CD47 antibody (B6H12, 10 μg/mL). The mixed cells were then stained with APC-labeled anti-F4/80 antibody and analyzed by flow cytometry. Phagocytosis rate was calculated as the percentage of F4/80+ and CFSE+ double-positive macrophages in all F4/80+ macrophages. (C–E) The HCC827 xenograft mice were treated with vehicle, OSI (0.5 mg/kg), B6H12 (250 μg per mouse), or the combination of OSI and B6H12 as described in the materials and methods section. The tumor volume and mice body weight were recorded every other day for about 3 weeks. The tumor morphology from each mouse on day 20 was obtained after the sacrifice.
Fig.4  OSI dramatically enhances the phagocytosis by B6H12 via the ADCP effect. (A) The expression of CD47 in HCC827/CD47KO and normal HCC827 cells was detected by Western blot. (B) HCC827 and HCC827/CD47KO cells were labeled with CFSE and cocultured with BMDMs (3:1) for 2 h, and the mixed cells were then stained with APC-labeled anti-F4/80 antibody and analyzed by flow cytometry. The phagocytosis rate was calculated as the percentage of F4/80+ and CFSE+ double-positive macrophages in all F4/80+ macrophages. (C) HCC827/CD47KO cells were cocultured with BMDMs in the presence of isotype or B6H12 after the OSI treatment (125 nmol/L) for 48 h. Phagocytosis rate was calculated as mentioned above. (D) HCC827 cells pretreated with OSI (125 nmol/L) were stained with CFSE, cocultured with BMDMs (3:1) for another 2 h in the presence of B6H12 and/or anti-CD16/32 antibody, and analyzed by flow cytometry. The phagocytosis rate was calculated as described previously.
Fig.5  OSI induces higher expression of calreticulin and downregulates PD-L1 on the membrane of HCC827 cells. (A and B) The calreticulin expression on the membrane was detected by flow cytometry and immunofluorescence after the treatment of OSI (125 nmol/L) for 48 h. (C and D) The PD-L1 expression in HCC827 cells pretreated with OSI (125 nmol/L) was measured by flow cytometry and Western blot, respectively.
Fig.6  Schematic representation of the combination strategy of OSI and CD47 blockade in NSCLC. OSI induced the upregulation of CD47 through the NF-κB pathway. The anti-CD47 antibody blocked the interaction of CD47 and SIRPα. The binding between Fc region of anti-CD47 antibody and FcγR enhanced the ADCP effect. In addition, OSI induced the membrane exposure of calreticulin and reduced the expression of PD-L1.
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