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Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

CN 11-5983/R

Postal Subscription Code 80-967

2018 Impact Factor: 1.847

Front. Med.    2018, Vol. 12 Issue (4) : 473-480    https://doi.org/10.1007/s11684-018-0657-5
REVIEW |
Activation of phagocytosis by immune checkpoint blockade
Chia-Wei Li1, Yun-Ju Lai2, Jennifer L. Hsu1, Mien-Chie Hung1()
1. Department of Molecular and Cellular Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX 77030, USA
2. Department of Neurology, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX 77030, USA
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Abstract

Inhibition of macrophage-mediated phagocytosis has emerged as an essential mechanism for tumor immune evasion. One mechanism inhibiting the innate response is the presence of the macrophage inhibitory molecule, signal regulatory protein-α (SIRPα), on tumor-associated macrophages (TAMs) and its cognate ligand cluster of differentiation 47 (CD47) on tumor cells in the tumor microenvironment. On the basis of a recently discovered programmed death protein 1 (PD-1) in TAMs, we discuss the potential inhibitory receptors that possess new functions beyond T cell exhaustion in this review. As more and more immune receptors are found to be expressed on TAMs, the corresponding therapies may also stimulate macrophages for phagocytosis and thereby provide extra anti-tumor benefits in cancer therapy. Therefore, identification of biomarkers and combinatorial therapeutic strategies, have the potential to improve the efficacy and safety profiles of current immunotherapies.

Keywords CD47      PD-1      PD-L1      immunotherapy      TAM      phagocytosis      macrophage     
Corresponding Authors: Mien-Chie Hung   
Just Accepted Date: 09 July 2018   Issue Date: 03 September 2018
 Cite this article:   
Chia-Wei Li,Yun-Ju Lai,Jennifer L. Hsu, et al. Activation of phagocytosis by immune checkpoint blockade[J]. Front. Med., 2018, 12(4): 473-480.
 URL:  
http://academic.hep.com.cn/fmd/EN/10.1007/s11684-018-0657-5
http://academic.hep.com.cn/fmd/EN/Y2018/V12/I4/473
Fig.1  Anti-PD-1 therapy induces both TAMs and CD8+ T cell activity. (A) The expression of PD-1 on the tumor-associated macrophages (TAMs) and T cell inhibits antitumor immunity. (B) PD-1 antibody induces innate immunity by TAM phagocytosis and adaptive immunity by T cell cytolytic activity.
Group Macrophages T cells Tumors Suppressive/stimulatory Localization Targeted drug References
1 PD-1 (CD279) PD-L1 Suppressive TAMs Available [17]
PD-1 PD-L1 Suppressive [42]
PD-L1 (B7-H1; CD274)
PD-L2 (CD273)
[43]
PD-L1 PD-1 Suppressive TAMs [44]
RGMb PD-L2 Suppressive TAMs [45]
2 B7-H4 TAMs Available [46]
B7-H4 Stimulatory [47]
3 TIM3 GAL9 Suppressive TAMs Available [48]
TIM3 GAL9 Suppressive [49]
4 PVR (CD155) TIGIT Suppressive Available [50]
TIGIT PVR Suppressive [51]
CD226 PVR Stimulatory [52]
PVR (CD155) CD226 Stimulatory [53]
CD112R CD112 Suppressive [54]
5 B7-1 (CD80), B7-2 (CD86) Available [55]
CD28 B7-1, B7-2 Stimulatory [56]
CTLA-4 B7-1, B7-2 Suppressive
6 SIRPa CD47 Suppressive TAMs Available [57]
7 4-1BBL (CD137L) 4-1BB (CD137) 4-1BBL Stimulatory TAMs Available [58]
8 LILRB1 MHC I Suppressive TAMs N/A [19]
9 LRP1 CRT Stimulatory TAMs N/A [59]
10 RAGE S100 Suppressive TAMs N/A [60]
11 CD40 CD40L Stimulatory TAMs N/A [61]
CD40 CD40L [62]
12 OX40L OX40 Stimulatory Available [63]
OX40 OX40L [64]
13 ICOSL ICOS ICOSL Stimulatory TAMs Available [65]
14 VISTA TAMs Available [66,67]
VISTA VISTA-R
Tab.1  Immune checkpoints expression across three cell types categorized into different receptor-ligand pair groups
1 Pardoll DM. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 2012; 12(4): 252–264
https://doi.org/10.1038/nrc3239 pmid: 22437870
2 Morrissey KM, Yuraszeck TM, Li CC, Zhang Y, Kasichayanula S. Immunotherapy and novel combinations in oncology: current landscape, challenges, and opportunities. Clin Transl Sci 2016; 9(2): 89–104
https://doi.org/10.1111/cts.12391 pmid: 26924066
3 Li CW, Lim SO, Hsu JL, Hung MC. Rational combination of immunotherapy for triple negative breast cancer treatment. Chin Clin Oncol 2017; 6(5): 54
https://doi.org/10.21037/cco.2017.08.04 pmid: 29129094
4 Iwai Y, Hamanishi J, Chamoto K, Honjo T. Cancer immunotherapies targeting the PD-1 signaling pathway. J Biomed Sci 2017; 24(1): 26
https://doi.org/10.1186/s12929-017-0329-9 pmid: 28376884
5 Alexander W, The checkpoint immunotherapy revolution: what started as a trickle has become a flood, despite some daunting adverse effects; new drugs, indications, and combinations continue to emerge. P T 2016; 41(3):185–191
pmid: 26957887
6 Zou W, Wolchok JD, Chen L. PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: mechanisms, response biomarkers, and combinations. Sci Transl Med 2016; 8(328): 328rv4
https://doi.org/10.1126/scitranslmed.aad7118 pmid: 26936508
7 Sharma P, Hu-Lieskovan S, Wargo JA, Ribas A. Primary, adaptive, and acquired resistance to cancer immunotherapy. Cell 2017; 168(4): 707–723
https://doi.org/10.1016/j.cell.2017.01.017 pmid: 28187290
8 Spain L, Walls G, Julve M, O’Meara K, Schmid T, Kalaitzaki E, Turajlic S, Gore M, Rees J, Larkin J. Neurotoxicity from immune-checkpoint inhibition in the treatment of melanoma: a single centre experience and review of the literature. Ann Oncol 2017; 28(2): 377–385
pmid: 28426103
9 Jaiswal S, Jamieson CH, Pang WW, Park CY, Chao MP, Majeti R, Traver D, van Rooijen N, Weissman IL. CD47 is upregulated on circulating hematopoietic stem cells and leukemia cells to avoid phagocytosis. Cell 2009; 138(2): 271–285
https://doi.org/10.1016/j.cell.2009.05.046 pmid: 19632178
10 Jiang P, Lagenaur CF, Narayanan V. Integrin-associated protein is a ligand for the P84 neural adhesion molecule. J Biol Chem 1999; 274(2): 559–562
https://doi.org/10.1074/jbc.274.2.559 pmid: 9872987
11 Majeti R, Chao MP, Alizadeh AA, Pang WW, Jaiswal S, Gibbs KD Jr, van Rooijen N, Weissman IL. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 2009; 138(2): 286–299
https://doi.org/10.1016/j.cell.2009.05.045 pmid: 19632179
12 Baccelli I, Stenzinger A, Vogel V, Pfitzner BM, Klein C, Wallwiener M, Scharpff M, Saini M, Holland-Letz T, Sinn HP, Schneeweiss A, Denkert C, Weichert W, Trumpp A. Co-expression of MET and CD47 is a novel prognosticator for survival of luminal breast cancer patients. Oncotarget 2014; 5(18): 8147–8160
https://doi.org/10.18632/oncotarget.2385 pmid: 25230070
13 Nagahara M1, Mimori K, Kataoka A, Ishii H, Tanaka F, Nakagawa T, Sato T, Ono S, Sugihara K, Mori M. Correlated expression of CD47 and SIRPA in bone marrow and in peripheral blood predicts recurrence in breast cancer patients. Clin Cancer Res 2010; 16(18): 4625–4635.
https://doi.org/10.1158/1078-0432.CCR-10-0349 pmid: :2070561335
14 Suzuki S, Yokobori T, Tanaka N, Sakai M, Sano A, Inose T, Sohda M, Nakajima M, Miyazaki T, Kato H, Kuwano H. CD47 expression regulated by the miR-133a tumor suppressor is a novel prognostic marker in esophageal squamous cell carcinoma. Oncol Rep 2012; 28(2): 465–472
https://doi.org/10.3892/or.2012.1831 pmid: 22641236
15 Yoshida K, Tsujimoto H, Matsumura K, Kinoshita M, Takahata R, Matsumoto Y, Hiraki S, Ono S, Seki S, Yamamoto J, Hase K. CD47 is an adverse prognostic factor and a therapeutic target in gastric cancer. Cancer Med 2015; 4(9): 1322–1333
https://doi.org/10.1002/cam4.478 pmid: 26077800
16 Wang H, Tan M, Zhang S, Li X, Gao J, Zhang D, Hao Y, Gao S, Liu J, Lin B. Expression and significance of CD44, CD47 and c-met in ovarian clear cell carcinoma. Int J Mol Sci 2015; 16(2): 3391–3404
https://doi.org/10.3390/ijms16023391 pmid: 25658794
17 Gordon SR, Maute RL, Dulken BW, Hutter G, George BM, McCracken MN, Gupta R, Tsai JM, Sinha R, Corey D, Ring AM, Connolly AJ, Weissman IL. PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature 2017; 545(7655): 495–499
https://doi.org/10.1038/nature22396 pmid: 28514441
18 Liu X, Kwon H, Li Z, Fu YX. Is CD47 an innate immune checkpoint for tumor evasion? J Hematol Oncol 2017; 10(1): 12
https://doi.org/10.1186/s13045-016-0381-z pmid: 28077173
19 Barkal AA, Weiskopf K, Kao KS, Gordon SR, Rosental B, Yiu YY, George BM, Markovic M, Ring NG, Tsai JM, McKenna KM, Ho PY, Cheng RZ, Chen JY, Barkal LJ, Ring AM, Weissman IL, Maute RL. Engagement of MHC class I by the inhibitory receptor LILRB1 suppresses macrophages and is a target of cancer immunotherapy. Nat Immunol 2018; 19(1): 76–84
https://doi.org/10.1038/s41590-017-0004-z pmid: 29180808
20 Riley JL. PD-1 signaling in primary T cells. Immunol Rev 2009; 229(1): 114–125
https://doi.org/10.1111/j.1600-065X.2009.00767.x pmid: 19426218
21 Fuertes Marraco SA, Neubert NJ, Verdeil G, Speiser DE. Inhibitory receptors beyond T cell exhaustion. Front Immunol 2015; 6: 310
https://doi.org/10.3389/fimmu.2015.00310 pmid: 26167163
22 Chen L, Han X. Anti-PD-1/PD-L1 therapy of human cancer: past, present, and future. J Clin Invest 2015; 125(9): 3384–3391
https://doi.org/10.1172/JCI80011 pmid: 26325035
23 Riella LV, Paterson AM, Sharpe AH, Chandraker A. Role of the PD-1 pathway in the immune response. Am J Transplant 2012; 12(10): 2575–2587
https://doi.org/10.1111/j.1600-6143.2012.04224.x pmid: 22900886
24 Lim SO, Li CW, Xia W, Cha JH, Chan LC, Wu Y, Chang SS, Lin WC, Hsu JM, Hsu YH, Kim T, Chang WC, Hsu JL, Yamaguchi H, Ding Q, Wang Y, Yang Y, Chen CH, Sahin AA, Yu D, Hortobagyi GN, Hung MC. Deubiquitination and stabilization of PD-L1 by CSN5. Cancer Cell 2016; 30(6): 925–939
https://doi.org/10.1016/j.ccell.2016.10.010 pmid: 27866850
25 Liu X, Pu Y, Cron K, Deng L, Kline J, Frazier WA, Xu H, Peng H, Fu YX, Xu MM. CD47 blockade triggers T cell-mediated destruction of immunogenic tumors. Nat Med 2015; 21(10): 1209–1215
https://doi.org/10.1038/nm.3931 pmid: 26322579
26 Soto-Pantoja DR, Terabe M, Ghosh A, Ridnour LA, DeGraff WG, Wink DA, Berzofsky JA, Roberts DD. CD47 in the tumor microenvironment limits cooperation between antitumor T-cell immunity and radiotherapy. Cancer Res 2014; 74(23): 6771–6783
https://doi.org/10.1158/0008-5472.CAN-14-0037-T pmid: 25297630
27 Yang L, Zhang Y. Tumor-associated macrophages: from basic research to clinical application. J Hematol Oncol 2017; 10(1): 58
https://doi.org/10.1186/s13045-017-0430-2 pmid: 28241846
28 Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014; 41(1): 49–61
https://doi.org/10.1016/j.immuni.2014.06.010 pmid: 25035953
29 Alderton GK. Tumour immunology: turning macrophages on, off and on again. Nat Rev Immunol 2014; 14(3): 136–137
https://doi.org/10.1038/nri3634 pmid: 24566906
30 Zijlmans HJ, Fleuren GJ, Baelde HJ, Eilers PH, Kenter GG, Gorter A. The absence of CCL2 expression in cervical carcinoma is associated with increased survival and loss of heterozygosity at 17q11.2. J Pathol 2006; 208(4): 507–517
https://doi.org/10.1002/path.1918 pmid: 16435282
31 Tsutsui S, Yasuda K, Suzuki K, Tahara K, Higashi H, Era S. Macrophage infiltration and its prognostic implications in breast cancer: the relationship with VEGF expression and microvessel density. Oncol Rep 2005; 14(2): 425–431
pmid: 16012726
32 Ries CH, Cannarile MA, Hoves S, Benz J, Wartha K, Runza V, Rey-Giraud F, Pradel LP, Feuerhake F, Klaman I, Jones T, Jucknischke U, Scheiblich S, Kaluza K, Gorr IH, Walz A, Abiraj K, Cassier PA, Sica A, Gomez-Roca C, de Visser KE, Italiano A, Le Tourneau C, Delord JP, Levitsky H, Blay JY, Rüttinger D. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell 2014; 25(6): 846–859
https://doi.org/10.1016/j.ccr.2014.05.016 pmid: 24898549
33 Mok S, Koya RC, Tsui C, Xu J, Robert L, Wu L, Graeber T, West BL, Bollag G, Ribas A. Inhibition of CSF-1 receptor improves the antitumor efficacy of adoptive cell transfer immunotherapy. Cancer Res 2014; 74(1): 153–161
https://doi.org/10.1158/0008-5472.CAN-13-1816 pmid: 24247719
34 Han Y, Chen Z, Yang Y, Jiang Z, Gu Y, Liu Y, Lin C, Pan Z, Yu Y, Jiang M, Zhou W, Cao X. Human CD14+ CTLA-4+ regulatory dendritic cells suppress T-cell response by cytotoxic T-lymphocyte antigen-4-dependent IL-10 and indoleamine-2,3-dioxygenase production in hepatocellular carcinoma. Hepatology 2014; 59(2): 567–579
https://doi.org/10.1002/hep.26694 pmid: 23960017
35 Komohara Y, Jinushi M, Takeya M. Clinical significance of macrophage heterogeneity in human malignant tumors. Cancer Sci 2014; 105(1): 1–8
https://doi.org/10.1111/cas.12314 pmid: 24168081
36 Li CW, Lim SO, Xia W, Lee HH, Chan LC, Kuo CW, Khoo KH, Chang SS, Cha JH, Kim T, Hsu JL, Wu Y, Hsu JM, Yamaguchi H, Ding Q, Wang Y, Yao J, Lee CC, Wu HJ, Sahin AA, Allison JP, Yu D, Hortobagyi GN, Hung MC. Glycosylation and stabilization of programmed death ligand-1 suppresses T-cell activity. Nat Commun 2016; 7: 12632
https://doi.org/10.1038/ncomms12632 pmid: 27572267
37 Jiao S, Xia W, Yamaguchi H, Wei Y, Chen MK, Hsu JM, Hsu JL, Yu WH, Du Y, Lee HH, Li CW, Chou CK, Lim SO, Chang SS, Litton J, Arun B, Hortobagyi GN, Hung MC. PARP inhibitor upregulates PD-L1 expression and enhances cancer-associated immunosuppression. Clin Cancer Res 2017; 23(14): 3711–3720
https://doi.org/10.1158/1078-0432.CCR-16-3215 pmid: 28167507
38 Zhang J, Bu X, Wang H, Zhu Y, Geng Y, Nihira NT, Tan Y, Ci Y, Wu F, Dai X, Guo J, Huang YH, Fan C, Ren S, Sun Y, Freeman GJ, Sicinski P, Wei W. Cyclin D-CDK4 kinase destabilizes PD-L1 via Cul3(SPOP) to control cancer immune surveillance. Nature 2017; 553(7686): 91–95
https://doi.org/10.1038/nature25015
39 Burr ML, Sparbier CE, Chan YC, Williamson JC, Woods K, Beavis PA, Lam EYN, Henderson MA, Bell CC, Stolzenburg S, Gilan O, Bloor S, Noori T, Morgens DW, Bassik MC, Neeson PJ, Behren A, Darcy PK, Dawson SJ, Voskoboinik I, Trapani JA, Cebon J, Lehner PJ, Dawson MA. CMTM6 maintains the expression of PD-L1 and regulates anti-tumour immunity. Nature 2017; 549(7670): 101–105
https://doi.org/10.1038/nature23643 pmid: 28813417
40 Mezzadra R, Sun C, Jae LT, Gomez-Eerland R, de Vries E, Wu W, Logtenberg MEW, Slagter M, Rozeman EA, Hofland I, Broeks A, Horlings HM, Wessels LFA, Blank CU, Xiao Y, Heck AJR, Borst J, Brummelkamp TR, Schumacher TNM. Identification of CMTM6 and CMTM4 as PD-L1 protein regulators. Nature 2017; 549(7670): 106–110
https://doi.org/10.1038/nature23669 pmid: 28813410
41 Li CW, Lim SO, Chung EM, Kim YS, Park AH, Yao J, Cha JH, Xia W, Chan LC, Kim T, Chang SS, Lee HH, Chou CK, Liu YL, Yeh HC, Perillo EP, Dunn AK, Kuo CW, Khoo KH, Hsu JL, Wu Y, Hsu JM, Yamaguchi H, Huang TH, Sahin AA, Hortobagyi GN, Yoo SS, Hung MC. Eradication of triple-negative breast cancer cells by targeting glycosylated PD-L1. Cancer Cell 2018; 33(2):187–201.e10
https://doi.org/10.1016/j.ccell.2018.01.009 pmid: 29438695
42 Dong H, Zhu G, Tamada K, Chen L. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med 1999; 5(12): 1365–1369
https://doi.org/10.1038/70932 pmid: 10581077
43 Rodríguez-García M, Porichis F, de Jong OG, Levi K, Diefenbach TJ, Lifson JD, Freeman GJ, Walker BD, Kaufmann DE, Kavanagh DG. Expression of PD-L1 and PD-L2 on human macrophages is up-regulated by HIV-1 and differentially modulated by IL-10. J Leukoc Biol 2011; 89(4): 507–515
https://doi.org/10.1189/jlb.0610327 pmid: 21097698
44 Wu K, Kryczek I, Chen L, Zou W, Welling TH. Kupffer cell suppression of CD8+ T cells in human hepatocellular carcinoma is mediated by B7-H1/programmed death-1 interactions. Cancer Res 2009; 69(20): 8067–8075
https://doi.org/10.1158/0008-5472.CAN-09-0901 pmid: 19826049
45 Xiao Y, Yu S, Zhu B, Bedoret D, Bu X, Francisco LM, Hua P, Duke-Cohan JS, Umetsu DT, Sharpe AH, DeKruyff RH, Freeman GJ. RGMb is a novel binding partner for PD-L2 and its engagement with PD-L2 promotes respiratory tolerance. J Exp Med 2014; 211(5): 943–959
https://doi.org/10.1084/jem.20130790 pmid: 24752301
46 Kryczek I, Zou L, Rodriguez P, Zhu G, Wei S, Mottram P, Brumlik M, Cheng P, Curiel T, Myers L, Lackner A, Alvarez X, Ochoa A, Chen L, Zou W. B7-H4 expression identifies a novel suppressive macrophage population in human ovarian carcinoma. J Exp Med 2006; 203(4): 871–881
https://doi.org/10.1084/jem.20050930 pmid: 16606666
47 Dangaj D, Lanitis E, Zhao A, Joshi S, Cheng Y, Sandaltzopoulos R, Ra HJ, Danet-Desnoyers G, Powell DJ Jr, Scholler N. Novel recombinant human b7-h4 antibodies overcome tumoral immune escape to potentiate T-cell antitumor responses. Cancer Res 2013; 73(15): 4820–4829
https://doi.org/10.1158/0008-5472.CAN-12-3457 pmid: 23722540
48 Dong J, Cheng L, Zhao M, Pan X, Feng Z, Wang D. Tim-3-expressing macrophages are functionally suppressed and expanded in oral squamous cell carcinoma due to virus-induced Gal-9 expression. Tumour Biol 2017; 39(5): 1010428317701651
https://doi.org/10.1177/1010428317701651 pmid: 28466780
49 Li H, Wu K, Tao K, Chen L, Zheng Q, Lu X, Liu J, Shi L, Liu C, Wang G, Zou W. Tim-3/galectin-9 signaling pathway mediates T-cell dysfunction and predicts poor prognosis in patients with hepatitis B virus-associated hepatocellular carcinoma. Hepatology 2012; 56(4): 1342–1351
https://doi.org/10.1002/hep.25777 pmid: 22505239
50 Yu X, Harden K, Gonzalez LC, Francesco M, Chiang E, Irving B, Tom I, Ivelja S, Refino CJ, Clark H, Eaton D, Grogan JL. The surface protein TIGIT suppresses T cell activation by promoting the generation of mature immunoregulatory dendritic cells. Nat Immunol 2009; 10(1): 48–57
https://doi.org/10.1038/ni.1674 pmid: 19011627
51 Li M, Xia P, Du Y, Liu S, Huang G, Chen J, Zhang H, Hou N, Cheng X, Zhou L, Li P, Yang X, Fan Z. T-cell immunoglobulin and ITIM domain (TIGIT) receptor/poliovirus receptor (PVR) ligand engagement suppresses interferon-g production of natural killer cells via b-arrestin 2-mediated negative signaling. J Biol Chem 2014; 289(25): 17647–17657
https://doi.org/10.1074/jbc.M114.572420 pmid: 24817116
52 Tahara-Hanaoka S, Shibuya K, Onoda Y, Zhang H, Yamazaki S, Miyamoto A, Honda S, Lanier LL, Shibuya A. Functional characterization of DNAM-1 (CD226) interaction with its ligands PVR (CD155) and nectin-2 (PRR-2/CD112). Int Immunol 2004; 16(4): 533–538
https://doi.org/10.1093/intimm/dxh059 pmid: 15039383
53 Guillemin GJ, Brew BJ. Microglia, macrophages, perivascular macrophages, and pericytes: a review of function and identification. J Leukoc Biol 2004; 75(3): 388–397
https://doi.org/10.1189/jlb.0303114 pmid: 14612429
54 Zhu Y, Paniccia A, Schulick AC, Chen W, Koenig MR, Byers JT, Yao S, Bevers S, Edil BH. Identification of CD112R as a novel checkpoint for human T cells. J Exp Med 2016; 213(2): 167–176
https://doi.org/10.1084/jem.20150785 pmid: 26755705
55 Galdiero M, Pisciotta MG, Gorga F, Petrillo G, Marinelli A, Galdiero E. Modulation of costimulatory molecules CD80/CD86 on B cells and macrophages by stress proteins GroEL, GroES and DnaK. Int J Immunopathol Pharmacol 2005; 18(4): 637–644
https://doi.org/10.1177/039463200501800404 pmid: 16388710
56 Zang X, Allison JP. The B7 family and cancer therapy: costimulation and coinhibition. Clin Cancer Res. 2007; 13(18 Pt 1): 5271–5279
https://doi.org/DOI:0.1158/1078-0432.CCR-07-1030 pmid: 17875755
57 Willingham SB, Volkmer JP, Gentles AJ, Sahoo D, Dalerba P, Mitra SS, Wang J, Contreras-Trujillo H, Martin R, Cohen JD, Lovelace P, Scheeren FA, Chao MP, Weiskopf K, Tang C, Volkmer AK, Naik TJ, Storm TA, Mosley AR, Edris B, Schmid SM, Sun CK, Chua MS, Murillo O, Rajendran P, Cha AC, Chin RK, Kim D, Adorno M, Raveh T, Tseng D, Jaiswal S, Enger PO, Steinberg GK, Li G, So SK, Majeti R, Harsh GR, van de Rijn M, Teng NN, Sunwoo JB, Alizadeh AA, Clarke MF, Weissman IL. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci USA 2012; 109(17): 6662–6667
https://doi.org/10.1073/pnas.1121623109 pmid: 22451913
58 Wang Q, Zhang P, Zhang Q, Wang X, Li J, Ma C, Sun W, Zhang L. Analysis of CD137 and CD137L expression in human primary tumor tissues. Croat Med J 2008; 49(2): 192–200
https://doi.org/10.3325/cmj.2008.2.192 pmid: 18461674
59 Chao MP, Jaiswal S, Weissman-Tsukamoto R, Alizadeh AA, Gentles AJ, Volkmer J, Weiskopf K, Willingham SB, Raveh T, Park CY, Majeti R, Weissman IL. Calreticulin is the dominant pro-phagocytic signal on multiple human cancers and is counterbalanced by CD47. Sci Transl Med 2010; 2(63):63ra94
https://doi.org/10.1126/scitranslmed.3001375 pmid: 21178137
60 Leclerc E, Fritz G, Vetter SW, Heizmann CW. Binding of S100 proteins to RAGE: an update. Biochim Biophys Acta 2009; 1793(6): 993–1007
https://doi.org/10.1016/j.bbamcr.2008.11.016 pmid: 19121341
61 Kinouchi M, Miura K, Mizoi T, Ishida K, Fujibuchi W, Sasaki H, Ohnuma S, Saito K, Katayose Y, Naitoh T, Motoi F, Shiiba K, Egawa S, Shibata C, Unno M. Infiltration of CD40-positive tumor-associated macrophages indicates a favorable prognosis in colorectal cancer patients. Hepatogastroenterology 2013; 60(121): 83–88
pmid: 22687258
62 Elgueta R, Benson MJ, de Vries VC, Wasiuk A, Guo Y, Noelle RJ. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol Rev 2009; 229(1): 152–172
https://doi.org/10.1111/j.1600-065X.2009.00782.x pmid: 19426221
63 Karulf M, Kelly A, Weinberg AD, Gold JA. OX40 ligand regulates inflammation and mortality in the innate immune response to sepsis. J Immunol 2010; 185(8): 4856–4862
https://doi.org/10.4049/jimmunol.1000404 pmid: 20844189
64 Croft M, So T, Duan W, Soroosh P. The significance of OX40 and OX40L to T-cell biology and immune disease. Immunol Rev 2009; 229(1): 173–191
https://doi.org/10.1111/j.1600-065X.2009.00766.x pmid: 19426222
65 Zhang Y, Luo Y, Qin SL, Mu YF, Qi Y, Yu MH, Zhong M. The clinical impact of ICOS signal in colorectal cancer patients. OncoImmunology 2016; 5(5): e1141857
https://doi.org/10.1080/2162402X.2016.1141857 pmid: 27467961
66 Lines JL, Pantazi E, Mak J, Sempere LF, Wang L, O’Connell S, Ceeraz S, Suriawinata AA, Yan S, Ernstoff MS, Noelle R. VISTA is an immune checkpoint molecule for human T cells. Cancer Res 2014; 74(7): 1924–1932
https://doi.org/10.1158/0008-5472.CAN-13-1504 pmid: 24691993
67 Nowak EC, Lines JL, Varn FS, Deng J, Sarde A, Mabaera R, Kuta A, Le Mercier I, Cheng C, Noelle RJ. Immunoregulatory functions of VISTA. Immunol Rev 2017; 276(1): 66–79
https://doi.org/10.1111/imr.12525 pmid: 28258694
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[2] Yingyan Yu. Molecular classification and precision therapy of cancer: immune checkpoint inhibitors[J]. Front. Med., 2018, 12(2): 229-235.
[3] Yan Yang, Jian Chen, Di Lin, Xujian Xu, Jun Cheng, Changgui Sun. Prevalence and drug resistance characteristics of carbapenem-resistant Enterobacteriaceae in Hangzhou, China[J]. Front. Med., 2018, 12(2): 182-188.
[4] Yue Zhao, Wenjun Long, Caiqi Du, Huanhuan Yang, Shimin Wu, Qin Ning, Xiaoping Luo. Prevalence of vitamin D deficiency in girls with idiopathic central precocious puberty[J]. Front. Med., 2018, 12(2): 174-181.
[5] Min Yu, Zonghai Li. Natural killer cells in hepatocellular carcinoma: current status and perspectives for future immunotherapeutic approaches[J]. Front. Med., 2017, 11(4): 509-521.
[6] Limin Mao, Minglei Guo, Daozhong Jin, Bing Xue, John Q. Wang. Group III metabotropic glutamate receptors and drug addiction[J]. Front Med, 2013, 7(4): 445-451.
[7] Chun Yang, Xiaomin Li, Nan Wang, Shixia Xu, Jianjun Yang, Zhiqiang Zhou. Tramadol reinforces antidepressant effects of ketamine with increased levels of brain-derived neurotrophic factor and tropomyosin-related kinase B in rat hippocampus[J]. Front Med, 2012, 6(4): 411-415.
[8] Qiang Gao, Yinghong Shi, Xiaoying Wang, Jian Zhou, Shuangjian Qiu, Jia Fan. Translational medicine in hepatocellular carcinoma[J]. Front Med, 2012, 6(2): 122-133.
[9] Min Cheng, Jian Zhang, Wen Jiang, Yongyan Chen, Zhigang Tian. Natural killer cell lines in tumor immunotherapy[J]. Front Med, 2012, 6(1): 56-66.
[10] Qi-De LIN, Li-Hua QIU. Pathogenesis, diagnosis, and treatment of recurrent spontaneous abortion with immune type[J]. Front Med Chin, 2010, 4(3): 275-279.
[11] Qi MEI MM, Zhe CAO MM, Hua XIONG MD, Yuan CHEN MD, . Preliminary results of gentamycin combined with sodium bicarbonate for prevention of irinotecan-induced diarrhea[J]. Front. Med., 2009, 3(4): 470-474.
[12] Rong WANG, Shangwei WU, Xue LI, Ping HE, Yunde LIU. Detection of AmpC β-lactamase and drug resistance of Enterobacter cloacae[J]. Front Med Chin, 2009, 3(1): 72-75.
[13] Hui QIU, Hui ZHANG, Zuohua FENG. 4-1BBL expressed by eukaryotic cells activates immune cells and suppresses the progression of murine tumor[J]. Front Med Chin, 2009, 3(1): 20-25.
[14] LIU Hongchun, CAO Zhongwei, JIN Jianjun, WANG Jiyao. Blockage of receptor-interacting protein 2 expression by small interfering RNA in murine macrophages[J]. Front. Med., 2008, 2(2): 166-170.
[15] CHU Deyong, LI Conglei, SHEN Jilong, WU Qiang. Paeoniflorin prevents hepatic fibrosis of by inhibiting TGF-β1 production from macrophages in mice[J]. Front. Med., 2008, 2(2): 154-165.
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