Immune Cells in Hyperprogressive Disease under Immune Checkpoint-Based Immunotherapy
Abstract
:1. Introduction
2. CD8+ T Cells
2.1. Exhausted CD8+ T (Tex) Cells
2.2. Immune Checkpoint Compensation Mechanisms
2.3. IL-10/IL-10R
3. CD4+ T Cells
3.1. Regulatory T (Treg) Cells
3.2. Other Subsets of CD4+ T Cells
3.3. Exhausted CD4+ T Cells
3.4. IFN-γ
4. Monocytes
5. Macrophages
5.1. M2 Macrophages
5.2. FcγRIIb
6. DCs
6.1. PD-1
6.2. PD-L2
7. Neutrophils
8. MDSCs
9. Natural Killer (NK) Cells
10. Innate Lymphoid Cells (ILCs)
11. Conclusions and Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Frelaut, M.; le Tourneau, C.; Borcoman, E. Hyperprogression under Immunotherapy. Int. J. Mol. Sci. 2019, 20, 2674. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shen, P.; Han, L.; Ba, X.; Qin, K.; Tu, S.H. Hyperprogressive Disease in Cancers Treated with Immune Checkpoint Inhibitors. Front. Pharmacol. 2021, 12, 678409. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.P.; Wang, F.; Zhong, M.J.; Yarden, Y.; Fu, L.W. The biomarkers of hyperprogressive disease in PD-1/PD-L1 block-age therapy. Mol. Cancer 2020, 19, 81. [Google Scholar] [CrossRef]
- Wolchok, J.D.; Hoos, A.; O’Day, S.; Weber, J.S.; Hamid, O.; Lebbé, C.; Maio, M.; Binder, M.; Bohnsack, O.; Nichol, G.; et al. Guidelines for the Evaluation of Immune Therapy Activity in Solid Tumors: Immune-Related Response Criteria. Clin. Cancer Res. 2009, 15, 7412–7420. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lin, M.; Vanneste, B.G.L.; Yu, Q.; Chen, Z.; Peng, J.; Cai, X. Hyperprogression under immunotherapy: A new form of immunotherapy response?—A narrative literature review. Transl. Lung Cancer Res. 2021, 10, 3276–3291. [Google Scholar] [CrossRef] [PubMed]
- Champiat, S.; Dercle, L.; Ammari, S.; Massard, C.; Hollebecque, A.; Postel-Vinay, S.; Chaput, N.; Eggermont, A.; Marabelle, A.; Soria, J.-C.; et al. Hyperprogressive Disease Is a New Pattern of Progression in Cancer Patients Treated by Anti-PD-1/PD-L1. Clin. Cancer Res. 2017, 23, 1920–1928. [Google Scholar] [CrossRef] [Green Version]
- Saada-Bouzid, E.; Defaucheux, C.; Karabajakian, A.; Coloma, V.P.; Servois, V.; Paoletti, X.; Even, C.; Fayette, J.; Guigay, J.; Loirat, D.; et al. Hyperprogression during anti-PD-1/PD-L1 therapy in patients with recurrent and/or metastatic head and neck squamous cell carcinoma. Ann. Oncol. 2017, 28, 1605–1611. [Google Scholar] [CrossRef]
- Ferrara, R.; Mezquita, L.; Texier, M.; Lahmar, J.; Audigier-Valette, C.; Tessonnier, L.; Mazieres, J.; Zalcman, G.; Brosseau, S.; Le Moulec, S.; et al. Hyperprogressive Disease in Patients with Advanced Non-Small Cell Lung Cancer Treated with PD-1/PD-L1 Inhibitors or with Single-Agent Chemotherapy. JAMA Oncol. 2018, 4, 1543–1552. [Google Scholar] [CrossRef]
- Kanazu, M.; Edahiro, R.; Krebe, H.; Nishida, K.; Ishijima, M.; Uenami, T.; Akazawa, Y.; Yano, Y.; Yamaguchi, T.; Mori, M. Hyperprogressive disease in patients with non-small cell lung cancer treated with nivolumab: A case series. Thorac. Cancer 2018, 9, 1782–1787. [Google Scholar] [CrossRef] [Green Version]
- Russo, G.L.; Moro, M.; Sommariva, M.; Cancila, V.; Boeri, M.; Centonze, G.; Ferro, S.; Ganzinelli, M.; Gasparini, P.; Huber, V.; et al. Antibody-Fc/FcR Interac-tion on Macrophages as a Mechanism for Hyperprogressive Disease in Non-small Cell Lung Cancer Subsequent to PD-1/PD-L1 Blockade. Clin. Cancer Res. 2019, 25, 989–999. [Google Scholar] [CrossRef] [Green Version]
- Kim, C.G.; Kim, K.H.; Pyo, K.H.; Xin, C.F.; Hong, M.H.; Ahn, B.C.; Kim, Y.; Choi, S.J.; Yoon, H.I.; Lee, J.G.; et al. Hyperprogressive disease during PD-1/PD-L1 blockade in patients with non-small-cell lung cancer. Ann. Oncol. 2019, 30, 1104–1113. [Google Scholar] [CrossRef] [PubMed]
- Aoki, M.; Shoji, H.; Nagashima, K.; Imazeki, H.; Miyamoto, T.; Hirano, H.; Honma, Y.; Iwasa, S.; Okita, N.; Takashima, A.; et al. Hyperprogressive disease during nivolumab or irinotecan treatment in patients with advanced gastric cancer. ESMO Open 2019, 4, e000488. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kanjanapan, Y.; Day, D.; Wang, L.; Al-Sawaihey, H.; Abbas, E.; Namini, A.; Siu, L.L.; Hansen, A.; Razak, A.A.; Spreafico, A.; et al. Hyperprogressive disease in early-phase immunotherapy trials: Clinical predictors and association with im-mune-related toxicities. Cancer 2019, 125, 1341–1349. [Google Scholar] [CrossRef] [PubMed]
- Sasaki, A.; Nakamura, Y.; Mishima, S.; Kawazoe, A.; Kuboki, Y.; Bando, H.; Kojima, T.; Doi, T.; Ohtsu, A.; Yoshino, T.; et al. Predictive factors for hyperprogressive disease during nivolumab as anti-PD1 treatment in patients with advanced gastric cancer. Gastric Cancer 2019, 22, 793–802. [Google Scholar] [CrossRef] [Green Version]
- Lu, Z.; Zou, J.; Hu, Y.; Li, S.; Zhou, T.; Gong, J.; Li, J.; Zhang, X.; Zhou, J.; Lu, M.; et al. Serological Markers Associated with Response to Immune Checkpoint Blockade in Metastatic Gastrointestinal Tract Cancer. JAMA Netw. Open 2019, 2, e197621. [Google Scholar] [CrossRef] [Green Version]
- Matos, I.; Martin-Liberal, J.; García-Ruiz, A.; Hierro, C.; de Olza, M.O.; Viaplana, C.; Azaro, A.; Vieito, M.; Braña, I.; Mur, G.; et al. Capturing Hyperprogressive Disease with Immune-Checkpoint Inhibitors Using RECIST 1.1 Criteria. Clin. Cancer Res. 2020, 26, 1846–1855. [Google Scholar] [CrossRef] [Green Version]
- Castello, A.; Rossi, S.; Mazziotti, E.; Toschi, L.; Lopci, E. Hyperprogressive Disease in Patients with Non–Small Cell Lung Cancer Treated with Checkpoint Inhibitors: The Role of 18F-FDG PET/CT. J. Nucl. Med. 2020, 61, 821–826. [Google Scholar] [CrossRef]
- Hwang, I.; Park, I.; Yoon, S.-k.; Lee, J.L. Hyperprogressive Disease in Patients with Urothelial Carcinoma or Renal Cell Carcinoma Treated with PD-1/PD-L1 Inhibitors. Clin. Genitourin. Cancer 2020, 18, E122–E133. [Google Scholar] [CrossRef]
- Vaidya, P.; Bera, K.; Patil, P.D.; Gupta, A.; Jain, P.; Alilou, M.; Khorrami, M.; Velcheti, V.; Madabhushi, A. Novel, non-invasive imaging approach to identify patients with advanced non-small cell lung cancer at risk of hyperprogressive disease with immune checkpoint blockade. J. Immunother. Cancer 2020, 8, e001343. [Google Scholar] [CrossRef]
- Zhang, L.; Wu, L.; Chen, Q.; Zhang, B.; Liu, J.; Liu, S.; Mo, X.; Li, M.; Chen, Z.; Chen, L.; et al. Predicting hyperprogressive disease in patients with advanced hepatocellular carcinoma treated with anti-programmed cell death 1 therapy. eClinicalMedicine 2021, 31, 100673. [Google Scholar] [CrossRef]
- Kim, C.G.; Kim, C.; Yoon, S.E.; Kim, K.H.; Choi, S.J.; Kang, B.; Kim, H.R.; Park, S.-H.; Shin, E.-C.; Kim, Y.-Y.; et al. Hyperprogressive disease during PD-1 blockade in patients with advanced hepatocellular carcinoma. J. Hepatol. 2021, 74, 350–359. [Google Scholar] [CrossRef] [PubMed]
- Chen, S.; Gou, M.; Yan, H.; Fan, M.; Pan, Y.; Fan, R.; Qian, N.; Dai, G. Hyperprogressive Disease Caused by PD-1 Inhibitors for the Treatment of Pan-Cancer. Dis. Markers 2021, 2021, 6639366. [Google Scholar] [CrossRef] [PubMed]
- Xiao, L.-S.; Li, Q.-M.; Hu, C.-Y.; Cui, H.; Hong, C.; Huang, C.-Y.; Li, R.-N.; Dong, Z.-Y.; Zhu, H.-B.; Liu, L. Lung metastasis and lymph node metastasis are risk factors for hyperprogressive disease in primary liver cancer patients treated with immune checkpoint inhibitors. Ann. Palliat. Med. 2021, 10, 11244–11254. [Google Scholar] [CrossRef] [PubMed]
- Miyama, Y.; Morikawa, T.; Miyakawa, J.; Koyama, Y.; Kawai, T.; Kume, H.; Ushiku, T. Squamous differentiation is a potential biomarker predicting tumor progression in patients treated with pembrolizumab for urothelial carcinoma. Pathol.-Res. Pract. 2021, 219, 153364. [Google Scholar] [CrossRef] [PubMed]
- Maesaka, K.; Sakamori, R.; Yamada, R.; Tahata, Y.; Imai, Y.; Ohkawa, K.; Miyazaki, M.; Mita, E.; Ito, T.; Hagiwara, H.; et al. Hyperprogressive disease in patients with unresectable hepatocellular carcinoma receiving atezolizumab plus bevacizumab therapy. Hepatol. Res. 2022, 52, 298–307. [Google Scholar] [CrossRef]
- Tay, C.; Qian, Y.; Sakaguchi, S. Hyper-Progressive Disease: The Potential Role and Consequences of T-Regulatory Cells Foiling Anti-PD-1 Cancer Immunotherapy. Cancers 2021, 13, 48. [Google Scholar] [CrossRef]
- Pardoll, D.M. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 2012, 12, 252–264. [Google Scholar] [CrossRef] [Green Version]
- Wherry, E.J.; Kurachi, M. Molecular and cellular insights into T cell exhaustion. Nat. Rev. Immunol. 2015, 15, 486–499. [Google Scholar] [CrossRef]
- Franco, F.; Jaccard, A.; Romero, P.; Yu, Y.-R.; Ho, P.-C. Metabolic and epigenetic regulation of T-cell exhaustion. Nat. Metab. 2020, 2, 1001–1012. [Google Scholar] [CrossRef]
- Crespo, J.; Sun, H.Y.; Welling, T.H.; Tian, Z.G.; Zou, W.P. T cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment. Curr. Opin. Immunol. 2013, 25, 214–221. [Google Scholar] [CrossRef] [Green Version]
- Matsuzaki, J.; Gnjatic, S.; Mhawech-Fauceglia, P.; Beck, A.; Miller, A.; Tsuji, T.; Eppolito, C.; Qian, F.; Lele, S.; Shrikant, P.; et al. Tumor-infiltrating NY-ESO-1–specific CD8 + T cells are negatively regulated by LAG-3 and PD-1 in human ovarian cancer. Proc. Natl. Acad. Sci. USA 2010, 107, 7875–7880. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Baitsch, L.; Baumgaertner, P.; Devêvre, E.; Raghav, S.K.; Legat, A.; Barba, L.; Wieckowski, S.; Bouzourene, H.; Deplancke, B.; Romero, P.; et al. Exhaustion of tumor-specific CD8+ T cells in metastases from melanoma patients. J. Clin. Investig. 2011, 121, 2350–2360. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Thommen, D.S.; Schreiner, J.; Müller, P.; Herzig, P.; Roller, A.; Belousov, A.; Umana, P.; Pisa, P.; Klein, C.G.; Bacac, M.; et al. Progression of Lung Cancer Is Associated with Increased Dysfunction of T Cells Defined by Coexpression of Multiple Inhibitory Receptors. Cancer Immunol. Res. 2015, 3, 1344–1355. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lu, X.; Yang, L.; Yao, D.X.; Wu, X.; Li, J.P.; Liu, X.S.; Deng, L.J.; Huang, C.T.; Wang, Y.; Li, D.; et al. Tumor anti-gen-specific CD8+ T cells are negatively regulated by PD-1 and Tim-3 in human gastric cancer. Cell. Immunol. 2017, 313, 43–51. [Google Scholar] [CrossRef]
- Odorizzi, P.M.; Pauken, K.E.; Paley, M.A.; Sharpe, A.H.; Wherry, E.J. Genetic absence of PD-1 promotes accumulation of terminally differentiated exhausted CD8+ T cells. J. Exp. Med. 2015, 212, 1125–1137. [Google Scholar] [CrossRef] [PubMed]
- Wartewig, T.; Kurgyis, Z.; Keppler, S.J.; Pechloff, K.; Hameister, E.; Öllinger, R.; Maresch, R.; Buch, T.; Steiger, K.; Winter, C.; et al. PD-1 is a haploinsufficient suppressor of T cell lymphomagenesis. Nature 2017, 552, 121–125. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ratner, L.; Waldmann, T.A.; Janakiram, M.; Brammer, J.E. Rapid Progression of Adult T-Cell Leukemia–Lymphoma after PD-1 Inhibitor Therapy. N. Engl. J. Med. 2018, 378, 1947–1948. [Google Scholar] [CrossRef]
- Stein, R.G.; Ebert, S.; Schlahsa, L.; Scholz, C.J.; Braun, M.; Hauck, P.; Horn, E.; Monoranu, C.-M.; Thiemann, V.J.; Wustrow, M.P.; et al. Cognate Nonlytic Interactions between CD8+ T Cells and Breast Cancer Cells Induce Cancer Stem Cell–like Properties. Cancer Res. 2019, 79, 1507–1519. [Google Scholar] [CrossRef] [Green Version]
- Gil Del Alcazar, C.R.; Huh, S.J.; Ekram, M.B.; Trinh, A.; Liu, L.L.; Beca, F.; Zi, X.; Kwak, M.; Bergholtz, H.; Su, Y.; et al. Immune Escape in Breast Cancer During In Situ to Invasive Carcinoma Transition. Cancer Discov. 2017, 7, 1098–1115. [Google Scholar] [CrossRef] [Green Version]
- Cimino-Mathews, A.; Foote, J.B.; Emens, L.A. Immune Targeting in Breast Cancer. Oncology 2015, 29, 375–385. [Google Scholar]
- Al-Hajj, M.; Wicha, M.S.; Benito-Hernandez, A.; Morrison, S.J.; Clarke, M.F. Prospective identification of tumorigenic breast cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100, 3983–3988. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Reim, F.; Dombrowski, Y.; Ritter, C.; Buttmann, M.; Hausler, S.; Ossadnik, M.; Krockenberger, M.; Beier, D.; Beier, C.P.; Dietl, J.; et al. Immunoselection of Breast and Ovarian Cancer Cells with Trastuzumab and Natural Killer Cells: Selective Escape of CD44(high)/CD24(low)/HER2(low) Breast Cancer Stem Cells. Cancer Res. 2009, 69, 8058–8066. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, W.Q.; He, Y.J.; He, W.G.; Wu, G.S.; Zhou, X.L.; Sheng, Q.S.; Zhong, W.X.; Lu, Y.M.; Ding, Y.F.; Lu, Q.; et al. Exhausted CD8+T Cells in the Tumor Immune Microenvironment: New Pathways to Therapy. Front. Immunol. 2021, 11, 622509. [Google Scholar] [CrossRef] [PubMed]
- Huang, R.-Y.; Francois, A.; McGray, A.R.; Miliotto, A.; Odunsi, K. Compensatory upregulation of PD-1, LAG-3, and CTLA-4 limits the efficacy of single-agent checkpoint blockade in metastatic ovarian cancer. OncoImmunology 2016, 6, e1249561. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- YKawakami; Ohta, S.; Sayem, M.A.; Tsukamoto, N.; Yaguchi, T. Immune-resistant mechanisms in cancer immunothera-py. Int. J. Clin. Oncol. 2020, 25, 810–817. [Google Scholar] [CrossRef]
- Shi, H.B.; Lan, J.; Yang, J.Q. Mechanisms of Resistance to Checkpoint Blockade Therapy. Adv Exp Med Biol. 2020, 1248, 83–117. [Google Scholar]
- Camelliti, S.; Le Noci, V.; Bianchi, F.; Moscheni, C.; Arnaboldi, F.; Gagliano, N.; Balsari, A.; Garassino, M.C.; Tagliabue, E.; Sfondrini, L.; et al. Mechanisms of hyperprogressive disease after immune checkpoint inhibitor therapy: What we (don’t) know. J. Exp. Clin. Cancer Res. 2020, 39, 236. [Google Scholar] [CrossRef]
- Koyama, S.; Akbay, E.A.; Li, Y.Y.; Aref, A.R.; Skoulidis, F.; Herter-Sprie, G.S.; Buczkowski, K.A.; Liu, Y.; Awad, M.M.; Denning, W.L.; et al. STK11/LKB1 Deficiency Promotes Neutrophil Recruitment and Proinflammatory Cytokine Production to Suppress T-cell Activity in the Lung Tumor Microenvironment. Cancer Res. 2016, 76, 999–1008. [Google Scholar] [CrossRef] [Green Version]
- Sun, Z.; Fourcade, J.; Pagliano, O.; Chauvin, J.-M.; Sander, C.; Kirkwood, J.M.; Zarour, H.M. IL10 and PD-1 Cooperate to Limit the Activity of Tumor-Specific CD8+ T Cells. Cancer Res. 2015, 75, 1635–1644. [Google Scholar] [CrossRef] [Green Version]
- Richardson, J.R.; Schollhorn, A.; Gouttefangeas, C.; Schuhmacher, J. CD4+T Cells: Multitasking Cells in the Duty of Cancer Immunotherapy. Cancers 2021, 13, 596. [Google Scholar] [CrossRef]
- Togashi, Y.; Shitara, K.; Nishikawa, H. Regulatory T cells in cancer immunosuppression—Implications for anticancer therapy. Nat. Rev. Clin. Oncol. 2019, 16, 356–371. [Google Scholar] [CrossRef] [PubMed]
- Kamada, T.; Togashi, Y.; Tay, C.; Ha, D.; Sasaki, A.; Nakamura, Y.; Sato, E.; Fukuoka, S.; Tada, Y.; Tanaka, A.; et al. PD-1+ regulatory T cells amplified by PD-1 blockade promote hyperprogression of cancer. Proc. Natl. Acad. Sci. USA 2019, 116, 9999–10008. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cai, J.J.; Wang, D.S.; Zhang, G.Y.; Guo, X.L. The Role Of PD-1/PD-L1 Axis In Treg Development And Function: Implica-tions For Cancer Immunotherapy. Oncotargets Ther. 2019, 12, 8437–8445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rauch, D.A.; Conlon, K.C.; Janakiram, M.; Brammer, J.E.; Harding, J.C.; Ye, B.H.; Zang, X.; Ren, X.; Olson, S.; Cheng, X.; et al. Rapid progression of adult T-cell leukemia/lymphoma as tumor-infiltrating Tregs after PD-1 blockade. Blood 2019, 134, 1406–1414. [Google Scholar] [CrossRef]
- Simpson, T.R.; Li, F.; Montalvo-Ortiz, W.; Sepulveda, M.A.; Bergerhoff, K.; Arce, F.; Roddie, C.; Henry, J.Y.; Yagita, H.; Wolchok, J.D.; et al. Fc-dependent depletion of tumor-infiltrating regulatory T cells co-defines the efficacy of anti–CTLA-4 therapy against melanoma. J. Exp. Med. 2013, 210, 1695–1710. [Google Scholar] [CrossRef]
- Ji, Z.; Peng, Z.; Gong, J.; Zhang, X.; Li, J.; Lu, M.; Lu, Z.; Shen, L. Hyperprogression after immunotherapy in patients with malignant tumors of digestive system. BMC Cancer 2019, 19, 1–9. [Google Scholar] [CrossRef] [Green Version]
- Champiat, S.; Ferrara, R.; Massard, C.; Besse, B.; Marabelle, A.; Soria, J.-C.; Ferté, C. Hyperprogressive disease: Recognizing a novel pattern to improve patient management. Nat. Rev. Clin. Oncol. 2018, 15, 748–762. [Google Scholar] [CrossRef]
- Lee, G.H.; Lee, W.-W. Unusual CD4+CD28−T Cells and Their Pathogenic Role in Chronic Inflammatory Disorders. Immune Netw. 2016, 16, 322–329. [Google Scholar] [CrossRef] [Green Version]
- Maly, K.; Schirmer, M. The Story of CD4+ CD28− T Cells Revisited: Solved or Still Ongoing? J. Immunol. Res. 2015, 2015, 348746. [Google Scholar]
- Arasanz, H.; Zuazo, M.; Bocanegra, A.; Gato, M.; Martinez-Aguillo, M.; Morilla, I.; Fernandez, G.; Hernandez, B.; Lopez, P.; Alberdi, N.; et al. Early Detection of Hyperprogressive Dis-ease in Non-Small Cell Lung Cancer by Monitoring of Systemic T Cell Dynamics. Cancers 2020, 12, 344. [Google Scholar] [CrossRef] [Green Version]
- Zappasodi, R.; Budhu, S.; Hellmann, M.D.; Postow, M.A.; Senbabaoglu, Y.; Manne, S.; Gasmi, B.; Liu, C.L.; Zhong, H.; Li, Y.Y.; et al. Non-conventional Inhibi-tory CD4(+)Foxp3(-)PD-1(hi) T Cells as a Biomarker of Immune Checkpoint Blockade Activity. Cancer Cell 2018, 33, 1017–1032.e7. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Miggelbrink, A.M.; Jackson, J.D.; Lorrey, S.J.; Srinivasan, E.S.; Waibl-Polania, J.; Wilkinson, D.S.; Fecci, P.E. CD4 T-Cell Exhaustion: Does It Exist and What Are Its Roles in Cancer? Clin. Cancer Res. 2021, 27, 5742–5752. [Google Scholar] [CrossRef] [PubMed]
- Martini, M.; Testi, M.G.; Pasetto, M.; Picchio, M.C.; Innamorati, G.; Mazzocco, M.; Ugel, S.; Cingarlini, S.; Bronte, V.; Zanovello, P.; et al. IFN-gamma-mediated upmodulation of MHC class I expression activates tumor-specific immune response in a mouse model of prostate cancer. Vaccine 2010, 28, 3548–3557. [Google Scholar] [CrossRef] [PubMed]
- Zimmerman, M.; Yang, D.F.; Hu, X.L.; Liu, F.Y.; Singh, N.; Browning, D.; Ganapathy, V.; Chandler, P.; Choubey, D.; Abrams, S.I.; et al. IFN-gamma Upregulates Survivin and Ifi202 Expression to Induce Survival and Proliferation of Tumor-Specific T Cells. PLoS ONE 2010, 5. [Google Scholar] [CrossRef]
- Xiao, M.J.; Wang, C.H.; Zhang, J.H.; Li, Z.G.; Zhao, X.Q.; Qin, Z.H. IFN gamma Promotes Papilloma Development by Up-regulating Th17-Associated Inflammation. Cancer Res. 2009, 69, 2010–2017. [Google Scholar] [CrossRef] [Green Version]
- O’Garra, A.; Barrat, F.J.; Castro, G.; Vicari, A.; Hawrylowicz, C. Strategies for use of IL-10 or its antagonists in human disease. Immunol. Rev. 2008, 223, 114–131. [Google Scholar] [CrossRef]
- Sakai, S.; Kauffman, K.D.; Sallin, M.A.; Sharpe, A.H.; Young, H.A.; Ganusov, V.V.; Barber, D.L. CD4 T Cell-Derived IFN-gamma Plays a Minimal Role in Control of Pulmonary Mycobacterium tuberculosis Infection and Must Be Actively Re-pressed by PD-1 to Prevent Lethal Disease. PLoS Pathog. 2016, 12, e1005667. [Google Scholar] [CrossRef] [Green Version]
- Rosenkranz, D.; Weyer, S.; Tolosa, E.; Gaenslen, A.; Berg, D.; Leyhe, T.; Gasser, T.; Stoltze, L. Higher frequency of regulatory T suppressive activity cells in the elderly and increased in neurodegeneration. J. Neuroimmunol. 2007, 188, 117–127. [Google Scholar] [CrossRef]
- Shin, D.S.; Zaretsky, J.M.; Escuin-Ordinas, H.; Garcia-Diaz, A.; Hu-Lieskovan, S.; Kalbasi, A.; Grasso, C.S.; Hugo, W.; Sandoval, S.; Torrejon, D.Y.; et al. Primary Resistance to PD-1 Blockade Mediated by JAK1/2 Mutations. Cancer Discov. 2017, 7, 188–201. [Google Scholar] [CrossRef] [Green Version]
- Kato, S.; Goodman, A.; Walavalkar, V.; Barkauskas, D.A.; Sharabi, A.; Kurzrock, R. Hyperprogressors after Immunothera-py: Analysis of Genomic Alterations Associated with Accelerated Growth Rate. Clin. Cancer Res. 2017, 23, 4242–4250. [Google Scholar] [CrossRef] [Green Version]
- Zhou, J.X.; Lee, C.H.; Qi, C.F.; Wang, H.; Naghashfar, Z.; Abbasi, S.; Morse, H.C. IFN Regulatory Factor 8 Regulates MDM2 in Germinal Center B Cells. J. Immunol. 2009, 183, 3188–3194. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kratofil, R.M.; Kubes, P.; Deniset, J.F. Monocyte Conversion During Inflammation and Injury. Arterioscler. Thromb. Vasc. Biol. 2017, 37, 35–42. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Olingy, C.E.; Dinh, H.Q.; Hedrick, C.C. Monocyte heterogeneity and functions in cancer. J. Leukoc. Biol. 2019, 106, 309–322. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zasada, M.; Lenart, M.; Rutkowska-Zapała, M.; Stec, M.; Durlak, W.; Grudzień, A.; Krzeczkowska, A.; Mól, N.; Pilch, M.; Siedlar, M.; et al. Analysis of PD-1 expression in the monocyte subsets from non-septic and septic preterm neonates. PLoS ONE 2017, 12, e0186819. [Google Scholar] [CrossRef] [Green Version]
- da Mota, N.V.F.; Brunialti, M.K.C.; Santos, S.S.; Machado, F.R.; Assuncao, M.; Azevedo, L.C.P.; Salomao, R. Immuno-phenotyping of monocytes during human sepsis shows impairment in antigen presentation: A shift toward nonclassical differentiation and upregulation of fc gamma ri-receptor. Shock 2018, 50, 293–300. [Google Scholar] [CrossRef]
- Ma, C.J.; Ni, L.; Zhang, Y.; Zhang, C.L.; Wu, X.Y.; Atia, A.N.; Thayer, P.; Moorman, J.P.; Yao, Z.Q. PD-1 negatively regulates interleukin-12 expression by limiting STAT-1 phosphorylation in monocytes/macrophages duringchronic hepatitis C virus in-fection. Immunology 2011, 132, 421–431. [Google Scholar] [CrossRef]
- Zhang, Y.; Ma, C.J.; Ni, L.; Zhang, C.L.; Wu, X.Y.; Kumaraguru, U.; Li, C.F.; Moorman, J.P.; Yao, Z.Q. Cross-Talk between Programmed Death-1 and Suppressor of Cytokine Signaling-1 in Inhibition of IL-12 Production by Monocytes/Macrophages in Hepatitis C Virus Infection. J. Immunol. 2011, 186, 3093–3103. [Google Scholar] [CrossRef] [Green Version]
- Zhang, Y.; Zhou, Y.; Lou, J.; Li, J.; Bo, L.; Zhu, K.; Wan, X.; Deng, X.; Cai, Z. PD-L1 blockade improves survival in experimental sepsis by inhibiting lymphocyte apoptosis and reversing monocyte dysfunction. Crit. Care 2010, 14, R220. [Google Scholar] [CrossRef] [Green Version]
- Lamichhane, P.; Karyampudi, L.; Shreeder, B.; Krempski, J.; Bahr, D.; Daum, J.; Kalli, K.R.; Goode, E.L.; Block, M.S.; Cannon, M.J.; et al. IL10 Release upon PD-1 Blockade Sustains Immunosuppression in Ovarian Cancer. Cancer Res. 2017, 77, 6667–6678. [Google Scholar] [CrossRef] [Green Version]
- Ka, M.B.; Gondois-Rey, F.; Capo, C.; Textoris, J.; Million, M.; Raoult, D.; Olive, D.; Mege, J.L. Imbalance of Circulating Mon-ocyte Subsets and PD-1 Dysregulation in Q Fever Endocarditis: The Role of IL-10 in PD-1 Modulation. PLoS ONE 2014, 9, e107533. [Google Scholar] [CrossRef]
- Said, E.A.; Dupuy, F.P.; Trautmann, L.; Zhang, Y.W.; Shi, Y.; El-Far, M.; Hill, B.J.; Noto, A.; Ancuta, P.; Peretz, Y.; et al. Pro-grammed death-1-induced interleukin-10 production by monocytes impairs CD4(+) T cell activation during HIV infection. Nat. Med. 2010, 16, 452–459. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xia, Q.; Wei, L.; Zhang, Y.; Sheng, J.; Wu, W.; Zhang, Y. Immune Checkpoint Receptors Tim-3 and PD-1 Regulate Monocyte and T Lymphocyte Function in Septic Patients. Mediat. Inflamm. 2018, 2018, 1632902. [Google Scholar] [CrossRef] [PubMed]
- Ouyang, W.; O’Garra, A. IL-10 Family Cytokines IL-10 and IL-22: From Basic Science to Clinical Translation. Immunity 2019, 50, 871–891. [Google Scholar] [CrossRef] [PubMed]
- Gordon, S.R.; Maute, R.L.; Dulken, B.W.; Hutter, G.; George, B.M.; McCracken, M.N.; Gupta, R.; Tsai, J.M.; Sinha, R.; Corey, D.; et al. PD-1 expression by tumour-associated macrophages inhibits phagocytosis and tumour immunity. Nature 2017, 545, 495–499. [Google Scholar] [CrossRef]
- Lavin, Y.; Kobayashi, S.; Leader, A.; Amir, E.D.; Elefant, N.; Bigenwald, C.; Remark, R.; Sweeney, R.; Becker, C.D.; Lev-ine, J.H.; et al. Innate Immune Landscape in Early Lung Adenocarcinoma by Paired Single-Cell Analyses. Cell 2017, 169, 750–765. [Google Scholar] [CrossRef] [Green Version]
- Korehisa, S.; Oki, E.; Iimori, M.; Nakaji, Y.; Shimokawa, M.; Saeki, H.; Okano, S.; Oda, Y.; Maehara, Y. Clinical significance of programmed cell death-ligand 1 expression and the immune microenvironment at the invasive front of colorectal cancers with high microsatellite instability. Int. J. Cancer 2017, 142, 822–832. [Google Scholar] [CrossRef] [Green Version]
- Adams, T.A.; Vail, P.J.; Ruiz, A.; Mollaee, M.; McCue, P.A.; Knudsen, E.S.; Witkiewicz, A.K. Composite analysis of immu-nological and metabolic markers defines novel subtypes of triple negative breast cancer. Mod. Pathol. 2018, 31, 288–298. [Google Scholar] [CrossRef]
- Harada, K.; Dong, X.; Estrella, J.S.; Correa, A.M.; Xu, Y.; Hofstetter, W.L.; Sudo, K.; Onodera, H.; Suzuki, K.; Suzuki, A.; et al. Tumor-associated macrophage infiltration is highly associated with PD-L1 expression in gastric adenocarcinoma. Gastric Cancer 2017, 21, 31–40. [Google Scholar] [CrossRef]
- Scholz, A.; Lang, V.; Henschler, R.; Czabanka, M.; Vajkoczy, P.; Chavakis, E.; Drynski, J.; Harter, P.N.; Mittelbronn, M.; Dumont, D.J.; et al. Angiopoietin-2 promotes myeloid cell infiltration in a beta(2)-integrin-dependent manner. Blood 2011, 118, 5050–5059. [Google Scholar] [CrossRef]
- Wu, X.Q.; Giobbie-Hurder, A.; Liao, X.Y.; Connelly, C.; Connolly, E.M.; Li, J.J.; Manos, M.P.; Lawrence, D.; McDermott, D.; Severgnini, M.; et al. Angiopoietin-2 as a Bi-omarker and Target for Immune Checkpoint Therapy. Cancer Immunol. Res. 2017, 5, 17–28. [Google Scholar] [CrossRef] [Green Version]
- Wang, F.; Li, B.; Wei, Y.; Zhao, Y.; Wang, L.; Zhang, P.; Yang, J.; He, W.; Chen, H.; Jiao, Z.; et al. Tumor-derived exosomes induce PD1+ macrophage population in human gastric cancer that promotes disease progression. Oncogenesis 2018, 7, 1–11. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hugo, W.; Zaretsky, J.M.; Sun, L.; Song, C.; Moreno, B.H.; Hu-Lieskovan, S.; Berent-Maoz, B.; Pang, J.; Chmielowski, B.; Cherry, G.; et al. Genomic and Transcriptomic Features of Response to Anti-PD-1 Therapy in Metastatic Melanoma. Cell 2016, 165, 35–44. [Google Scholar] [CrossRef] [Green Version]
- Kang, T.H.; Jung, S.T. Boosting therapeutic potency of antibodies by taming Fc domain functions. Exp. Mol. Med. 2019, 51, 1–9. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chiu, M.L.; Goulet, D.R.; Teplyakov, A.; Gilliland, G.L. Antibody Structure and Function: The Basis for Engineering Therapeutics. Antibodies 2019, 8, 55. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vidarsson, G.; Dekkers, G.; Rispens, T. IgG Subclasses and Allotypes: From Structure to Effector Functions. Front. Immunol. 2014, 5, 520. [Google Scholar] [CrossRef] [Green Version]
- Kretschmer, A.; Schwanbeck, R.; Valerius, T.; Rosner, T. Antibody Isotypes for Tumor Immunotherapy. Transfus. Med. Hemotherapy 2017, 44, 320–326. [Google Scholar] [CrossRef] [Green Version]
- Chen, X.; Song, X.M.; Li, K.; Zhang, T. Fc gamma R-Binding Is an Important Functional Attribute for Immune Checkpoint Antibodies in Cancer Immunotherapy. Front. Immunol. 2019, 10, 292. [Google Scholar] [CrossRef]
- Yu, J.; Song, Y.; Tian, W. How to select IgG subclasses in developing anti-tumor therapeutic antibodies. J. Hematol. Oncol. 2020, 13, 45. [Google Scholar] [CrossRef]
- Arlauckas, S.P.; Garris, C.S.; Kohler, R.H.; Kitaoka, M.; Cuccarese, M.F.; Yang, K.S.; Miller, M.A.; Carlson, J.C.; Freeman, G.J.; Anthony, R.M.; et al. In vivo imaging reveals a tumor-associated macrophage–mediated resistance pathway in anti–PD-1 therapy. Sci. Transl. Med. 2017, 9, eaal3604. [Google Scholar] [CrossRef] [Green Version]
- Knorr, D.A.; Ravetch, J.V. Immunotherapy and Hyperprogression: Unwanted Outcomes, Unclear Mechanism. Clin. Cancer Res. 2019, 25, 904–906. [Google Scholar] [CrossRef] [Green Version]
- Swisher, J.F.A.; Haddad, D.A.; McGrath, A.G.; Boekhoudt, G.H.; Feldman, G.M. IgG4 can induce an M2-like phenotype in human monocyte-derived macrophages through Fc gamma RI. Mabs 2014, 6, 1377–1384. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Versteven, M.; Van den Bergh, J.M.J.; Marcq, E.; Smits, E.L.J.; Van Tendeloo, V.F.I.; Hobo, W.; Lion, E. Dendritic Cells and Programmed Death-1 Blockade: A Joint Venture to Combat Cancer. Front. Immunol. 2018, 9, 394. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Laoui, D.; Keirsse, J.; Morias, Y.; van Overmeire, E.; Geeraerts, X.; Elkrim, Y.; Kiss, M.; Bolli, E.; Lahmar, Q.; Sichien, D.; et al. The tumour microenviron-ment harbours ontogenically distinct dendritic cell populations with opposing effects on tumour immunity. Nat. Commun. 2016, 7, 13720. [Google Scholar]
- Keirsse, J.; Van Damme, H.; Van Ginderachter, J.A.; Laoui, D. Exploiting tumor-associated dendritic cell heterogeneity for novel cancer therapies. J. Leukoc. Biol. 2017, 102, 317–324. [Google Scholar] [CrossRef]
- Krempski, J.; Karyampudi, L.; Behrens, M.D.; Erskine, C.L.; Hartmann, L.; Dong, H.; Goode, E.L.; Kalli, K.R.; Knutson, K.L. Tumor-Infiltrating Programmed Death Receptor-1+ Dendritic Cells Mediate Immune Suppression in Ovarian Cancer. J. Immunol. 2011, 186, 6905–6913. [Google Scholar] [CrossRef] [Green Version]
- Karyampudi, L.; Lamichhane, P.; Krempski, J.; Kalli, K.R.; Behrens, M.D.; Vargas, D.M.; Hartmann, L.C.; Janco, J.M.T.; Dong, H.D.; Hedin, K.E.; et al. PD-1 Blunts the Function of Ovarian Tumor-Infiltrating Den-dritic Cells by Inactivating NF-kappa B. Cancer Res. 2016, 76, 239–250. [Google Scholar] [CrossRef] [Green Version]
- Zhao, Y.; Harrison, D.L.; Song, Y.; Ji, J.; Huang, J.; Hui, E. Antigen-Presenting Cell-Intrinsic PD-1 Neutralizes PD-L1 in cis to Attenuate PD-1 Signaling in T Cells. Cell Rep. 2018, 24, 379–390.e6. [Google Scholar] [CrossRef] [Green Version]
- Patsoukis, N.; Wang, Q.; Strauss, L.; Boussiotis, V.A. Revisiting the PD-1 pathway. Sci. Adv. 2020, 6, eabd2712. [Google Scholar] [CrossRef]
- Zak, K.M.; Grudnik, P.; Magiera, K.; Domling, A.; Dubin, G.; Holak, T.A. Structural Biology of the Immune Checkpoint Receptor PD-1 and Its Ligands PD-L1/PD-L2. Structure 2017, 25, 1163–1174. [Google Scholar] [CrossRef]
- Qin, W.T.; Hu, L.P.; Zhang, X.L.; Jiang, S.H.; Li, J.; Zhang, Z.G.; Wang, X. The Diverse Function of PD-1/PD-L Pathway Beyond Cancer. Front. Immunol. 2019, 10, 2298. [Google Scholar] [CrossRef]
- Pentcheva-Hoang, T.; Egen, J.G.; Wojnoonski, K.; Allison, J.P. B7-1 and B7-2 Selectively Recruit CTLA-4 and CD28 to the Immunological Synapse. Immunity 2004, 21, 401–413. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Keir, M.E.; Butte, M.J.; Freeman, G.J.; Sharpe, A.H. PD-1 and Its Ligands in Tolerance and Immunity. Annu. Rev. Immunol. 2008, 26, 677–704. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karunarathne, D.S.; Horne-Debets, J.M.; Huang, J.; Faleiro, R.; Leow, C.Y.; Amante, F.; Watkins, T.S.; Miles, J.; Dwyer, P.J.; Stacey, K.; et al. Programmed Death-1 Ligand 2-Mediated Regulation of the PD-L1 to PD-1 Axis Is Essential for Establishing CD4+ T Cell Immunity. Immunity 2016, 45, 333–345. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kuipers, H.; Muskens, F.; Willart, M.; Hijdra, D.; van Assema, F.B.J.; Coyle, A.J.; Hoogsteden, H.C.; Lambrecht, B.N. Con-tribution of the PD-1 ligands/PD-1 signaling pathway to dendritic cell-mediated CD4+ T cell activation. Eur. J. Immunol. 2006, 36, 2472–2482. [Google Scholar] [CrossRef]
- Dulos, J.; Carven, G.J.; van Boxtel, S.J.; Evers, S.; Driessen-Engels, L.J.A.; Hobo, W.; Gorecka, M.A.; de Haan, A.F.J.; Mulders, P.; Punt, C.J.A.; et al. PD-1 Blockade Augments Th1 and Th17 and Suppresses Th2 Responses in Peripheral Blood From Patients with Prostate and Advanced Melanoma Cancer. J. Immunother. 2012, 35, 169–178. [Google Scholar] [CrossRef]
- Akbay, E.A.; Koyama, S.; Liu, Y.; Dries, R.; Bufe, L.E.; Silkes, M.; Alath, M.; Magee, D.M.; Jones, R.; Jinushi, M.; et al. Interleukin-17A Promotes Lung Tumor Progression through Neu-trophil Attraction to Tumor Sites and Mediating Resistance to PD-1 Blockade. J. Thorac. Oncol. 2017, 12, 1268–1279. [Google Scholar] [CrossRef] [Green Version]
- Liu, Y.; Cheng, Y.; Xu, Y.; Wang, Z.; Du, X.; Li, C.; Peng, J.; Gao, L.; Liang, X.; Ma, C. Increased expression of programmed cell death protein 1 on NK cells inhibits NK-cell-mediated anti-tumor function and indicates poor prognosis in digestive can-cers. Oncogene 2017, 36, 6143–6153. [Google Scholar] [CrossRef] [Green Version]
- Zhang, T.; Song, X.M.; Xu, L.L.; Ma, J.; Zhang, Y.J.; Gong, W.F.; Zhang, Y.L.; Zhou, X.S.; Wang, Z.B.; Wang, Y.L.; et al. The binding of an anti-PD-1 antibody to Fc gamma RI has a profound impact on its biological functions. Cancer Immunol. Immunother. 2018, 67, 1079–1090. [Google Scholar] [CrossRef] [Green Version]
- Tarnawski, R.; Fowler, J.; Skladowski, K.; Swierniak, A.; Suwinski, R.; Maciejewski, B.; Wygoda, A. How fast is repopula-tion of tumor cells during the treatment gap? Int. J. Radiat. Oncol. Biol. Phys. 2002, 54, 229–236. [Google Scholar] [CrossRef]
- Lagadec, C.; Vlashi, E.; Della Donna, L.; Dekmezian, C.; Pajonk, F. Radiation-Induced Reprogramming of Breast Cancer Cells. Stem Cells 2012, 30, 833–844. [Google Scholar] [CrossRef] [Green Version]
- Demicheli, R.; Retsky, M.W.; Hrushesky, W.J.M.; Baum, M.; Gukas, I.D. The effects of surgery on tumor growth: A century of investigations. Ann. Oncol. 2008, 19, 1821–1828. [Google Scholar] [CrossRef] [PubMed]
- Strannegård, Ö.; Thorén, F.B. Opposing effects of immunotherapy in melanoma using multisubtype interferon-alpha–can tumor immune escape after immunotherapy accelerate disease progression? OncoImmunology 2016, 5, e1091147. [Google Scholar] [CrossRef] [Green Version]
- Zhang, H.; Houghton, A.M. Good cops turn bad: The contribution of neutrophils to immune-checkpoint inhibitor treatment failures in cancer. Pharmacol. Ther. 2021, 217, 107662. [Google Scholar] [CrossRef] [PubMed]
- Sacdalan, D.B.; Lucero, J.A.; Sacdalan, D.L. Prognostic utility of baseline neutrophil-to-lymphocyte ratio in patients re-ceiving immune checkpoint inhibitors: A review and meta-analysis. Oncotargets Ther. 2018, 11, 955–965. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Howard, R.; Kanetsky, P.A.; Egan, K.M. Exploring the prognostic value of the neutrophil-to-lymphocyte ratio in cancer. Sci. Rep. 2019, 9, 1–10. [Google Scholar] [CrossRef] [Green Version]
- Mezquita, L.; Auclin, E.; Ferrara, R.; Charrier, M.; Remon, J.; Planchard, D.; Ponce, S.; Ares, L.P.; Leroy, L.; Audigier-Valette, C.; et al. Association of the Lung Immune Prognostic Index with Immune Checkpoint Inhibitor Outcomes in Patients with Advanced Non–Small Cell Lung Cancer. JAMA Oncol. 2018, 4, 351–357. [Google Scholar] [CrossRef]
- Banna, G.L.; Di Quattro, R.; Malatino, L.; Fornarini, G.; Addeo, A.; Maruzzo, M.; Urzia, V.; Rundo, F.; Lipari, H.; De Giorgi, U.; et al. Neutrophil-to-lymphocyte ratio and lactate dehydrogenase as biomarkers for urothelial cancer treated with immunotherapy. Clin. Transl. Oncol. 2020, 22, 2130–2135. [Google Scholar] [CrossRef]
- Ferrara, R.; Russo, G.L.; Signorelli, D.; Proto, C.; Prelaj, A.; Galli, G.; de Toma, A.; Viscardi, G.; Lobefaro, R.; Brambilla, M.; et al. Circulating and tumor-associated neutrophil subtypes discriminate hyperprogressive disease (HPD) from convention-al progression (PD) upon immune checkpoint inhibitors (ICI) in advanced non-small cell lung cancer (NSCLC) patients (pts) and in vivo models. J. Clin. Oncol. 2020, 38, 9547. [Google Scholar] [CrossRef]
- Tesi, R. MDSC; the Most Important Cell You Have Never Heard Of. Trends Pharmacol. Sci. 2019, 40, 4–7. [Google Scholar] [CrossRef]
- Marvel, D.; Gabrilovich, D.I. Myeloid-derived suppressor cells in the tumor microenvironment: Expect the unexpected. J. Clin. Investig. 2015, 125, 3356–3364. [Google Scholar] [CrossRef]
- Groux, H.; Bigler, M.; E De Vries, J.; Roncarolo, M.G. Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells. J. Exp. Med. 1996, 184, 19–29. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Herbst, R.S.; Soria, J.-C.; Kowanetz, M.; Fine, G.D.; Hamid, O.; Gordon, M.S.; Sosman, J.A.; McDermott, D.F.; Powderly, J.D.; Gettinger, S.N.; et al. Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature 2014, 515, 563–567. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hsu, J.; Hodgins, J.J.; Marathe, M.; Nicolai, C.J.; Bourgeois-Daigneault, M.C.; Trevino, T.N.; Azimi, C.S.; Scheer, A.K.; Randolph, H.E.; Thompson, T.W.; et al. Contribution of NK cells to immunotherapy mediated by PD-1/PD-L1 blockade. J. Clin. Investig. 2018, 128, 4654–4668. [Google Scholar] [CrossRef] [PubMed]
- Solaymani-Mohammadi, S.; Lakhdari, O.; Minev, I.; Shenouda, S.; Frey, B.; Billeskov, R.; Singer, S.; Berzofsky, J.A.; Eckmann, L.; Kagnoff, M.F. Lack of the programmed death-1 receptor renders host susceptible to enteric microbial infection through impairing the production of the mucosal natural killer cell effector molecules. J. Leukoc. Biol. 2016, 99, 475–482. [Google Scholar] [CrossRef] [Green Version]
- Vivier, E.; Artis, D.; Colonna, M.; Diefenbach, A.; Di Santo, J.P.; Eberl, G.; Koyasu, S.; Locksley, R.M.; McKenzie, A.N.J.; Mebius, R.E.; et al. Innate Lymphoid Cells: 10 Years On. Cell 2018, 174, 1054–1066. [Google Scholar] [CrossRef] [Green Version]
- Colonna, M. Innate Lymphoid Cells: Diversity, Plasticity, and Unique Functions in Immunity. Immunity 2018, 48, 1104–1117. [Google Scholar] [CrossRef] [Green Version]
- Castellanos, J.G.; Longman, R.S. The balance of power: Innate lymphoid cells in tissue inflammation and repair. J. Clin. Investig. 2019, 129, 2640–2650. [Google Scholar] [CrossRef] [Green Version]
- Chiossone, L.; Dumas, P.-Y.; Vienne, M.; Vivier, E. Natural killer cells and other innate lymphoid cells in cancer. Nat. Rev. Immunol. 2018, 18, 671–688. [Google Scholar] [CrossRef]
- Fung, K.Y.; Nguyen, P.M.; Putoczki, T. The expanding role of innate lymphoid cells and their T-cell counterparts in gas-trointestinal cancers. Mol. Immunol. 2019, 110, 48–56. [Google Scholar] [CrossRef]
- Kirchberger, S.; Royston, D.J.; Boulard, O.; Thornton, E.; Franchini, F.; Szabady, R.L.; Harrison, O.; Powrie, F. Innate lym-phoid cells sustain colon cancer through production of interleukin-22 in a mouse model. J. Exp. Med. 2013, 210, 917–931. [Google Scholar] [CrossRef]
- Irshad, S.; Flores-Borja, F.; Lawler, K.; Monypenny, J.; Evans, R.; Male, V.; Gordon, P.; Cheung, A.; Gazinska, P.; Noor, F.; et al. ROR gamma t+ Innate Lymphoid Cells Promote Lymph Node Metasta-sis of Breast Cancers. Cancer Res. 2017, 77, 1083–1096. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Carrega, P.; Loiacono, F.; Di Carlo, E.; Scaramuccia, A.; Mora, M.; Conte, R.; Benelli, R.; Spaggiari, G.M.; Cantoni, C.; Campana, S.; et al. NCR+ILC3 concentrate in human lung cancer and associate with intratumoral lymphoid structures. Nat. Commun. 2015, 6, 8280. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xiong, D.; Wang, Y.; Singavi, A.K.; Mackinnon, A.; George, B.; You, M. Immunogenomic Landscape Contributes to Hyperprogressive Disease after Anti-PD-1 Immunotherapy for Cancer. iScience 2018, 9, 258–277. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vacca, P.; Pesce, S.; Greppi, M.; Fulcheri, E.; Munari, E.; Olive, D.; Mingari, M.C.; Moretta, A.; Moretta, L.; Marcenaro, E. PD-1 is expressed by and regulates human group 3 innate lymphoid cells in human decidua. Mucosal Immunol. 2019, 12, 624–631. [Google Scholar] [CrossRef] [PubMed]
- Tumino, N.; Martini, S.; Munari, E.; Scordamaglia, F.; Besi, F.; Mariotti, F.R.; Bogina, G.; Mingari, M.C.; Vacca, P.; Moretta, L. Presence of innate lymphoid cells in pleural effusions of primary and metastatic tumors: Functional analysis and expression of PD-1 receptor. Int. J. Cancer 2019, 145, 1660–1668. [Google Scholar] [CrossRef]
- Hepworth, M.R.; Fung, T.C.; Masur, S.H.; Kelsen, J.R.; McConnell, F.M.; Dubrot, J.; Withers, D.R.; Hugues, S.; Farrar, M.A.; Reith, W.; et al. Group 3 innate lymphoid cells mediate intes-tinal selection of commensal bacteria-specific CD4(+) T cells. Science 2015, 348, 1031–1035. [Google Scholar] [CrossRef] [Green Version]
Reference | Year | Country | Cancer Types | Incidence, n (%) | Clinical Relevance |
---|---|---|---|---|---|
Champiat et al. [6] | 2017 | France | Pan-cancer | 12/131 (9%) | HPD was associated with a higher age (>65 years old) and a worse OS, but not associated with higher tumor burden or any specific tumor type. |
Saâda-Bouzid et al. [7] | 2017 | France | R/M HNSCC | 10/34 (29%) | HPD significantly correlated with a regional recurrence, but not with local or distant recurrence. HPD was associated with a shorter PFS, but not with OS. |
Ferrara et al. [8] | 2018 | France | NSCLC | 56/406 (13.8%) | HPD was associated with high metastatic burden and poor prognosis. |
Kanazu et al. [9] | 2018 | Japan | NSCLC | 5/87 (5.7%) | HPD was thought to be associated with poor quality of life and survival. |
Lo Russo et al. [10] | 2019 | Italy | NSCLC | 39/152 (25.7%) | Pretreatment tissue samples from all patients with HPD showed tumor infiltration by M2-like CD163+CD33+PD-L1+ clustered epithelioid macrophages. |
Kim et al. [11] | 2019 | South Korea | R/M NSCLC | 55/263 (20.9%) | A lower frequency of effector/memory subsets (CCR7−CD45RA− T cells among the total CD8+ T cells) and a higher frequency of severely exhausted populations (TIGIT+ T cells among PD-1+CD8+ T cells) in peripheral blood were associated with HPD and inferior survival rate. |
Aoki et al. [12] | 2019 | Japan | AGC | 19/100 (19.0%) | HPD was observed more frequently after nivolumab compared with irinotecan, which was associated with a poor prognosis after nivolumab but not so clearly after irinotecan. |
Kanjanapan et al. [13] | 2019 | Canada | Pan-cancer | 12/182 (6.6%) | HPD was not associated with CSAEs, age, tumor type, or the type of immunotherapy but was more common in females. |
Sasaki et al. [14] | 2019 | Japan | AGC | 13/62 (21.0%) | Elevations in ANC and CRP levels upon nivolumab treatment might indicate HPD. |
Lu et al. [15] | 2019 | China | Metastatic GTC | 5/56 (8.9%) | Baseline serum levels of MCP-1, LIF, and CD-152 were associated with HPD. |
Matos et al. [16] | 2020 | Spain | Pan-cancer | 29/270 (10.7%) | The HPD progressor group had a significantly lower OS when compared with the non-HPD progressor group. |
Castello et al. [17] | 2020 | Italy | NSCLC | 14/46 (30.4%) | HPD status was associated with tumor burden. The derived neutrophil-to-lymphocyte ratio and platelet count were significantly associated with HPD status. |
Hwang et al. [18] | 2020 | South Korea | RCC/UC | 13/203 (6.4%) | HPD developed predominantly in patients with UC, and the incidence of HPD in patients with RCC was negligible. UC and creatinine above 1.2 mg/dL were independent predictive factors for HPD. A 30% increase in lymphocyte number following PD-1/PD-L1 inhibitor treatment was a negative predictor of HPD. |
Vaidya et al. [19] | 2020 | USA | Advanced NSCLC | 19/109 (17.4%) | Image-based radiomics markers extracted from baseline CTs might help identify patients at risk of HPD. |
Zhang et al. [20] | 2020 | China | Advanced HCC | 10/69 (14.5%) | Haemoglobin level, portal vein tumour thrombus, and Child-Pugh score were significantly associated with HPD. Patients with HPD had a significantly shorter OS than that of the patients with non-HPD. |
Kim et al. [21] | 2021 | South Korea | Advanced HCC | 24/189 (12.7%) | Patients with HPD had worse PFS and OS compared to patients with progressive disease without HPD. An elevated neutrophil-to-lymphocyte ratio (>4.125) was associated with HPD and an inferior survival rate. |
Chen et al. [22] | 2021 | China | Pan-cancer | 38/377 (10.1%) | Patients with HPD had lower OS than those without HPD. KRAS status was significantly associated with HPD in patients with colorectal cancer. The rapid increase of characteristic tumor markers within 1 month was associated with the occurrence of HPD. |
Xiao et al. [23] | 2021 | China | PLC | 13/129 (10.1%) | The PFS of HPD patients was significantly worse than that of non-HPD patients. Compared with the non-HPD patients, lung metastasis, and lymph node metastasis were independent risk factors of HPD. |
Miyama et al. [24] | 2021 | Japan | UC | 6/23 (26.1%) | Squamous differentiation may be a novel biomarker for predicting HPD in patients with UC who receive pembrolizumab. |
Maesaka et al. [25] | 2022 | Japan | Unresectable HCC | 9/88 (10.2%) | Patients with HPD had larger and more intrahepatic tumors, higher levels of α-fetoprotein and lactate dehydrogenase, and higher NLR at baseline than patients without HPD. NLR of ≥3 at baseline was identified as the only independent factor associated with HPD in multivariate analysis. |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Wei, Z.; Zhang, Y. Immune Cells in Hyperprogressive Disease under Immune Checkpoint-Based Immunotherapy. Cells 2022, 11, 1758. https://doi.org/10.3390/cells11111758
Wei Z, Zhang Y. Immune Cells in Hyperprogressive Disease under Immune Checkpoint-Based Immunotherapy. Cells. 2022; 11(11):1758. https://doi.org/10.3390/cells11111758
Chicago/Turabian StyleWei, Zhanqi, and Yuewei Zhang. 2022. "Immune Cells in Hyperprogressive Disease under Immune Checkpoint-Based Immunotherapy" Cells 11, no. 11: 1758. https://doi.org/10.3390/cells11111758