Mechanistic insight of predictive biomarkers for antitumor PD‑1/PD‑L1 blockade: A paradigm shift towards immunome evaluation (Review)
- Authors:
- Wenjie You
- Bin Shang
- Jian Sun
- Xueqing Liu
- Lili Su
- Shujuan Jiang
-
Affiliations: Department of Respiratory and Critical Care Medicine, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250021, P.R. China, Department of Thoracic Surgery, Shandong Provincial Hospital, Cheeloo College of Medicine, Shandong University, Jinan, Shandong 250021, P.R. China, Department of Respiratory and Critical Care Medicine, Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai 200127, P.R. China - Published online on: June 11, 2020 https://doi.org/10.3892/or.2020.7643
- Pages: 424-437
-
Copyright: © You et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Mellman I, Coukos G and Dranoff G: Cancer immunotherapy comes of age. Nature. 480:480–489. 2011. View Article : Google Scholar : PubMed/NCBI | |
Butte MJ, Keir ME, Phamduy TB, Sharpe AH and Freeman GJ: Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity. 27:111–122. 2007. View Article : Google Scholar : PubMed/NCBI | |
Zou W, Wolchok JD and Chen L: PD-L1 (B7-H1) and PD-1 pathway blockade for cancer therapy: Mechanisms, response biomarkers, and combinations. Sci Transl Med. 8:328rv42016. View Article : Google Scholar : PubMed/NCBI | |
Topalian SL, Sznol M, McDermott DF, Kluger HM, Carvajal RD, Sharfman WH, Brahmer JR, Lawrence DP, Atkins MB, Powderly JD, et al: Survival, durable tumor remission, and long-term safety in patients with advanced melanoma receiving nivolumab. J Clin Oncol. 32:1020–1030. 2014. View Article : Google Scholar : PubMed/NCBI | |
Robert C, Schachter J, Long GV, Arance A, Grob JJ, Mortier L, Daud A, Carlino MS, McNeil C, Lotem M, et al: Pembrolizumab versus Ipilimumab in advanced melanoma. N Engl J Med. 372:2521–2532. 2015. View Article : Google Scholar : PubMed/NCBI | |
Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, Schadendorf D, Dummer R, Smylie M, Rutkowski P, et al: Combined nivolumab and Ipilimumab or Monotherapy in untreated melanoma. N Engl J Med. 373:23–34. 2015. View Article : Google Scholar : PubMed/NCBI | |
Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, Hassel JC, Rutkowski P, McNeil C, Kalinka-Warzocha E, et al: Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 372:320–330. 2015. View Article : Google Scholar : PubMed/NCBI | |
Borghaei H, Paz-Ares L, Horn L, Spigel DR, Steins M, Ready NE, Chow LQ, Vokes EE, Felip E, Holgado E, et al: Nivolumab versus Docetaxel in advanced nonsquamous non-small-cell lung cancer. N Engl J Med. 373:1627–1639. 2015. View Article : Google Scholar : PubMed/NCBI | |
Brahmer J, Reckamp KL, Baas P, Crino L, Eberhardt WE, Poddubskaya E, Antonia S, Pluzanski A, Vokes EE, Holgado E, et al: Nivolumab versus Docetaxel in advanced squamous-cell non-small-cell lung cancer. N Engl J Med. 373:123–135. 2015. View Article : Google Scholar : PubMed/NCBI | |
Garon EB, Rizvi NA, Hui R, Leighl N, Balmanoukian AS, Eder JP, Patnaik A, Aggarwal C, Gubens M, Horn L, et al: Pembrolizumab for the treatment of non-small-cell lung cancer. N Engl J Med. 372:2018–2028. 2015. View Article : Google Scholar : PubMed/NCBI | |
Motzer RJ, Escudier B, McDermott DF, George S, Hammers HJ, Srinivas S, Tykodi SS, Sosman JA, Procopio G, Plimack ER, et al: Nivolumab versus Everolimus in advanced renal-cell carcinoma. N Engl J Med. 373:1803–1813. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ansell SM, Lesokhin AM, Borrello I, Halwani A, Scott EC, Gutierrez M, Schuster SJ, Millenson MM, Cattry D, Freeman GJ, et al: PD-1 blockade with nivolumab in relapsed or refractory Hodgkin's lymphoma. N Engl J Med. 372:311–319. 2015. View Article : Google Scholar : PubMed/NCBI | |
Powles T, Eder JP, Fine GD, Braiteh FS, Loriot Y, Cruz C, Bellmunt J, Burris HA, Petrylak DP, Teng SL, et al: MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer. Nature. 515:558–562. 2014. View Article : Google Scholar : PubMed/NCBI | |
Rittmeyer A, Barlesi F, Waterkamp D, Park K, Ciardiello F, von Pawel J, Gadgeel SM, Hida T, Kowalski DM, Dols MC, et al: Atezolizumab versus docetaxel in patients with previously treated non-small-cell lung cancer (OAK): A phase 3, open-label, multicentre randomised controlled trial. Lancet. 389:255–265. 2017. View Article : Google Scholar : PubMed/NCBI | |
McDermott DF, Sosman JA, Sznol M, Massard C, Gordon MS, Hamid O, Powderly JD, Infante JR, Fasso M, Wang YV, et al: Atezolizumab, an Anti-programmed Death-Ligand 1 antibody, in metastatic renal cell carcinoma: Long-term safety, clinical activity, and immune correlates from a phase Ia study. J Clin Oncol. 34:833–842. 2016. View Article : Google Scholar : PubMed/NCBI | |
Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al: Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med. 366:2443–2454. 2012. View Article : Google Scholar : PubMed/NCBI | |
Fehrenbacher L, Spira A, Ballinger M, Kowanetz M, Vansteenkiste J, Mazieres J, Park K, Smith D, Artal-Cortes A, Lewanski C, et al: Atezolizumab versus docetaxel for patients with previously treated non-small-cell lung cancer (POPLAR): A multicentre, open-label, phase 2 randomised controlled trial. Lancet. 387:1837–1846. 2016. View Article : Google Scholar : PubMed/NCBI | |
Patel SP and Kurzrock R: PD-L1 expression as a predictive biomarker in cancer immunotherapy. Mol Cancer Ther. 14:847–856. 2015. View Article : Google Scholar : PubMed/NCBI | |
McLaughlin J, Han G, Schalper KA, Carvajal-Hausdorf D, Pelekanou V, Rehman J, Velcheti V, Herbst R, LoRusso P and Rimm DL: Quantitative assessment of the heterogeneity of PD-L1 expression in non-small-cell lung cancer. JAMA Oncol. 2:46–54. 2016. View Article : Google Scholar : PubMed/NCBI | |
Daud AI, Wolchok JD, Robert C, Hwu WJ, Weber JS, Ribas A, Hodi FS, Joshua AM, Kefford R, Hersey P, et al: Programmed Death-Ligand 1 expression and response to the anti-programmed Death 1 antibody pembrolizumab in melanoma. J Clin Oncol. 34:4102–4109. 2016. View Article : Google Scholar : PubMed/NCBI | |
Weber JS, Kudchadkar RR, Yu B, Gallenstein D, Horak CE, Inzunza HD, Zhao X, Martinez AJ, Wang W, Gibney G, et al: Safety, efficacy, and biomarkers of nivolumab with vaccine in ipilimumab-refractory or -naive melanoma. J Clin Oncol. 31:4311–4318. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hanahan D and Weinberg RA: Hallmarks of cancer: The next generation. Cell. 144:646–674. 2011. View Article : Google Scholar : PubMed/NCBI | |
Topalian SL, Taube JM, Anders RA and Pardoll DM: Mechanism-driven biomarkers to guide immune checkpoint blockade in cancer therapy. Nat Rev Cancer. 16:275–287. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zou W: Immunosuppressive networks in the tumour environment and their therapeutic relevance. Nat Rev Cancer. 5:263–274. 2005. View Article : Google Scholar : PubMed/NCBI | |
Greenwald RJ, Freeman GJ and Sharpe AH: The B7 family revisited. Annu Rev Immunol. 23:515–548. 2005. View Article : Google Scholar : PubMed/NCBI | |
Keir ME, Butte MJ, Freeman GJ and Sharpe AH: PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 26:677–704. 2008. View Article : Google Scholar : PubMed/NCBI | |
Freeman GJ: Structures of PD-1 with its ligands: Sideways and dancing cheek to cheek. Proc Natl Acad Sci USA. 105:10275–10276. 2008. View Article : Google Scholar : PubMed/NCBI | |
Chemnitz JM, Parry RV, Nichols KE, June CH and Riley JL: SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J Immunol. 173:945–954. 2004. View Article : Google Scholar : PubMed/NCBI | |
Reck M, Rodriguez-Abreu D, Robinson AG, Hui R, Csoszi T, Fulop A, Gottfried M, Peled N, Tafreshi A, Cuffe S, et al: Pembrolizumab versus chemotherapy for PD-L1-positive non-small-cell lung cancer. N Engl J Med. 375:1823–1833. 2016. View Article : Google Scholar : PubMed/NCBI | |
Weber JS, D'Angelo SP, Minor D, Hodi FS, Gutzmer R, Neyns B, Hoeller C, Khushalani NI, Miller WH Jr, Lao CD, et al: Nivolumab versus chemotherapy in patients with advanced melanoma who progressed after anti-CTLA-4 treatment (CheckMate 037): A randomised, controlled, open-label, phase 3 trial. Lancet Oncol. 16:375–384. 2015. View Article : Google Scholar : PubMed/NCBI | |
Rizvi NA, Mazieres J, Planchard D, Stinchcombe TE, Dy GK, Antonia SJ, Horn L, Lena H, Minenza E, Mennecier B, et al: Activity and safety of nivolumab, an anti-PD-1 immune checkpoint inhibitor, for patients with advanced, refractory squamous non-small-cell lung cancer (CheckMate 063): A phase 2, single-arm trial. Lancet Oncol. 16:257–265. 2015. View Article : Google Scholar : PubMed/NCBI | |
Ferris RL, Blumenschein G Jr, Fayette J, Guigay J, Colevas AD, Licitra L, Harrington K, Kasper S, Vokes EE, Even C, et al: Nivolumab for recurrent squamous-cell carcinoma of the head and neck. N Engl J Med. 375:1856–1867. 2016. View Article : Google Scholar : PubMed/NCBI | |
Carbone DP, Reck M, Paz-Ares L, Creelan B, Horn L, Steins M, Felip E, van den Heuvel MM, Ciuleanu TE, Badin F, et al: First-line nivolumab in stage IV or recurrent non-small-cell lung cancer. N Engl J Med. 376:2415–2426. 2017. View Article : Google Scholar : PubMed/NCBI | |
Hellmann MD, Ciuleanu TE, Pluzanski A, Lee JS, Otterson GA, Audigier-Valette C, Minenza E, Linardou H, Burgers S, Salman P, et al: Nivolumab plus Ipilimumab in lung cancer with a high tumor mutational burden. N Engl J Med. 378:2093–2104. 2018. View Article : Google Scholar : PubMed/NCBI | |
Hellmann MD, Paz-Ares L, Bernabe Caro R, Zurawski B, Kim SW, Carcereny Costa E, Park K, Alexandru A, Lupinacci L, de la Mora Jimenez E, et al: Nivolumab plus Ipilimumab in advanced non-small-cell lung cancer. N Engl J Med. 381:2020–2031. 2019. View Article : Google Scholar : PubMed/NCBI | |
Herbst RS, Baas P, Kim DW, Felip E, Perez-Gracia JL, Han JY, Molina J, Kim JH, Arvis CD, Ahn MJ, et al: Pembrolizumab versus docetaxel for previously treated, PD-L1-positive, advanced non-small-cell lung cancer (KEYNOTE-010): A randomised controlled trial. Lancet. 387:1540–1550. 2016. View Article : Google Scholar : PubMed/NCBI | |
Eggermont AMM, Blank CU, Mandala M, Long GV, Atkinson V, Dalle S, Haydon A, Lichinitser M, Khattak A, Carlino MS, et al: Adjuvant pembrolizumab versus placebo in resected stage III melanoma. N Engl J Med. 378:1789–1801. 2018. View Article : Google Scholar : PubMed/NCBI | |
Mok TSK, Wu YL, Kudaba I, Kowalski DM, Cho BC, Turna HZ, Castro G Jr, Srimuninnimit V, Laktionov KK, Bondarenko I, et al: Pembrolizumab versus chemotherapy for previously untreated, PD-L1-expressing, locally advanced or metastatic non-small-cell lung cancer (KEYNOTE-042): A randomised, open-label, controlled, phase 3 trial. Lancet. 393:1819–1830. 2019. View Article : Google Scholar : PubMed/NCBI | |
Rosenberg JE, Hoffman-Censits J, Powles T, van der Heijden MS, Balar AV, Necchi A, Dawson N, O'Donnell PH, Balmanoukian A, Loriot Y, et al: Atezolizumab in patients with locally advanced and metastatic urothelial carcinoma who have progressed following treatment with platinum-based chemotherapy: A single-arm, multicentre, phase 2 trial. Lancet. 387:1909–1920. 2016. View Article : Google Scholar : PubMed/NCBI | |
Balar AV, Galsky MD, Rosenberg JE, Powles T, Petrylak DP, Bellmunt J, Loriot Y, Necchi A, Hoffman-Censits J, Perez- Gracia JL, et al: Atezolizumab as first-line treatment in cisplatin-ineligible patients with locally advanced and metastatic urothelial carcinoma: A single-arm, multicentre, phase 2 trial. Lancet. 389:67–76. 2017. View Article : Google Scholar : PubMed/NCBI | |
Petrylak DP, Powles T, Bellmunt J, Braiteh F, Loriot Y, Morales-Barrera R, Burris HA, Kim JW, Ding B, Kaiser C, et al: Atezolizumab (MPDL3280A) monotherapy for patients with metastatic urothelial cancer: Long-term outcomes from a phase 1 study. JAMA Oncol. 4:537–544. 2018. View Article : Google Scholar : PubMed/NCBI | |
Socinski MA, Jotte RM, Cappuzzo F, Orlandi F, Stroyakovskiy D, Nogami N, Rodriguez-Abreu D, Moro-Sibilot D, Thomas CA, Barlesi F, et al: Atezolizumab for first-line treatment of metastatic Nonsquamous NSCLC. N Engl J Med. 378:2288–2301. 2018. View Article : Google Scholar : PubMed/NCBI | |
Powles T, O'Donnell PH, Massard C, Arkenau HT, Friedlander TW, Hoimes CJ, Lee JL, Ong M, Sridhar SS, Vogelzang NJ, et al: Efficacy and safety of durvalumab in locally advanced or metastatic urothelial carcinoma: Updated results from a phase 1/2 open-label study. JAMA Oncol. 3:e1724112017. View Article : Google Scholar : PubMed/NCBI | |
Taube JM, Klein A, Brahmer JR, Xu H, Pan X, Kim JH, Chen L, Pardoll DM, Topalian SL and Anders RA: Association of PD-1, PD-1 ligands, and other features of the tumor immune microenvironment with response to anti-PD-1 therapy. Clin Cancer Res. 20:5064–5074. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chen G, Huang AC, Zhang W, Zhang G, Wu M, Xu W, Yu Z, Yang J, Wang B, Sun H, et al: Exosomal PD-L1 contributes to immunosuppression and is associated with anti-PD-1 response. Nature. 560:382–386. 2018. View Article : Google Scholar : PubMed/NCBI | |
Okuma Y, Wakui H, Utsumi H, Sagawa Y, Hosomi Y, Kuwano K and Homma S: Soluble programmed cell death ligand 1 as a novel biomarker for nivolumab therapy for non-small-cell lung cancer. Clin Lung Cancer. 19:410–417.e1. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ritprajak P and Azuma M: Intrinsic and extrinsic control of expression of the immunoregulatory molecule PD-L1 in epithelial cells and squamous cell carcinoma. Oral Oncol. 51:221–228. 2015. View Article : Google Scholar : PubMed/NCBI | |
Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, et al: Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med. 366:2455–2465. 2012. View Article : Google Scholar : PubMed/NCBI | |
You W, Li L, Sun D, Liu X, Xia Z, Xue S, Chen B, Qin H, Ai J and Jiang H: Farnesoid X receptor constructs an immunosuppressive microenvironment and sensitizes FXRhigh PD-L1low NSCLC to Anti-PD-1 immunotherapy. Cancer Immunol Res. 7:990–1000. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ratcliffe MJ, Sharpe A, Barker C, Scorer P and Walker J: Abstract LB-094: A comparative study of PD-L1 diagnostic assays and the classification of patients as PD-L1 positive and PD-L1 negative. Cancer Res. 76 (14 Suppl):LB-094-LB-094. 2016. | |
Fujimoto D, Yamashita D, Fukuoka J, Kitamura Y, Hosoya K, Kawachi H, Sato Y, Nagata K, Nakagawa A, Tachikawa R, et al: Comparison of PD-L1 assays in non-small cell lung cancer: 22C3 pharmDx and SP263. Anticancer Res. 38:6891–6895. 2018. View Article : Google Scholar : PubMed/NCBI | |
Lim JS, Sundar R, Chenard-Poirier M, Lopez J and Yap TA: Emerging biomarkers for PD-1 pathway cancer therapy. Biomark Med. 11:53–67. 2017. View Article : Google Scholar : PubMed/NCBI | |
Noman MZ and Chouaib S: Targeting hypoxia at the forefront of anticancer immune responses. Oncoimmunology. 3:e9544632014. View Article : Google Scholar : PubMed/NCBI | |
Gowrishankar K, Gunatilake D, Gallagher SJ, Tiffen J, Rizos H and Hersey P: Inducible but not constitutive expression of PD-L1 in human melanoma cells is dependent on activation of NF-κB. PLoS One. 10:e01234102015. View Article : Google Scholar : PubMed/NCBI | |
Liu J, Hamrouni A, Wolowiec D, Coiteux V, Kuliczkowski K, Hetuin D, Saudemont A and Quesnel B: Plasma cells from multiple myeloma patients express B7-H1 (PD-L1) and increase expression after stimulation with IFN-{gamma} and TLR ligands via a MyD88-, TRAF6-, and MEK-dependent pathway. Blood. 110:296–304. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lee SJ, Jang BC, Lee SW, Yang YI, Suh SI, Park YM, Oh S, Shin JG, Yao S, Chen L, et al: Interferon regulatory factor-1 is prerequisite to the constitutive expression and IFN-gamma-induced upregulation of B7-H1 (CD274). FEBS Lett. 580:755–762. 2006. View Article : Google Scholar : PubMed/NCBI | |
Kondo A, Yamashita T, Tamura H, Zhao W, Tsuji T, Shimizu M, Shinya E, Takahashi H, Tamada K, Chen L, et al: Interferon-gamma and tumor necrosis factor-alpha induce an immunoinhibitory molecule, B7-H1, via nuclear factor-kappaB activation in blasts in myelodysplastic syndromes. Blood. 116:1124–1131. 2010. View Article : Google Scholar : PubMed/NCBI | |
Jin YH, Hou W, Kang HS, Koh CS and Kim BS: The role of interleukin-6 in the expression of PD-1 and PDL-1 on central nervous system cells following infection with Theiler's murine encephalomyelitis virus. J Virol. 87:11538–11551. 2013. View Article : Google Scholar : PubMed/NCBI | |
Xiong HY, Ma TT, Wu BT, Lin Y and Tu ZG: IL-12 regulates B7-H1 expression in ovarian cancer-associated macrophages by effects on NF-κB signalling. Asian Pac J Cancer Prev. 15:5767–5772. 2014. View Article : Google Scholar : PubMed/NCBI | |
Akbay EA, Koyama S, Carretero J, Altabef A, Tchaicha JH, Christensen CL, Mikse OR, Cherniack AD, Beauchamp EM, Pugh TJ, et al: Activation of the PD-1 pathway contributes to immune escape in EGFR-driven lung tumors. Cancer Discov. 3:1355–1363. 2013. View Article : Google Scholar : PubMed/NCBI | |
Hecht M, Buttner-Herold M, Erlenbach-Wunsch K, Haderlein M, Croner R, Grutzmann R, Hartmann A, Fietkau R and Distel LV: PD-L1 is upregulated by radiochemotherapy in rectal adenocarcinoma patients and associated with a favourable prognosis. Eur J Cancer. 65:52–60. 2016. View Article : Google Scholar : PubMed/NCBI | |
Katsuya Y, Horinouchi H, Asao T, Kitahara S, Goto Y, Kanda S, Fujiwara Y, Nokihara H, Yamamoto N, Watanabe S, et al: Expression of programmed death 1 (PD-1) and its ligand (PD-L1) in thymic epithelial tumors: Impact on treatment efficacy and alteration in expression after chemotherapy. Lung Cancer. 99:4–10. 2016. View Article : Google Scholar : PubMed/NCBI | |
Takamori S, Takada K, Tagawa T, Toyokawa G, Hirai F, Yamashita N, Okamoto T, Oki E, Yoshizumi T, Oda Y, et al: Differences in PD-L1 expression on tumor and immune cells between lung metastases and corresponding primary tumors. Surg Oncol. 27:637–641. 2018. View Article : Google Scholar : PubMed/NCBI | |
Kandoth C, McLellan MD, Vandin F, Ye K, Niu B, Lu C, Xie M, Zhang Q, McMichael JF, Wyczalkowski MA, et al: Mutational landscape and significance across 12 major cancer types. Nature. 502:333–339. 2013. View Article : Google Scholar : PubMed/NCBI | |
Alexandrov LB, Nik-Zainal S, Wedge DC, Aparicio SA, Behjati S, Biankin AV, Bignell GR, Bolli N, Borg A, Borresen-Dale AL, et al: Signatures of mutational processes in human cancer. Nature. 500:415–421. 2013. View Article : Google Scholar : PubMed/NCBI | |
Herbst RS, Soria JC, Kowanetz M, Fine GD, Hamid O, Gordon MS, Sosman JA, McDermott DF, Powderly JD, Gettinger SN, et al: Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients. Nature. 515:563–567. 2014. View Article : Google Scholar : PubMed/NCBI | |
Rizvi NA, Hellmann MD, Snyder A, Kvistborg P, Makarov V, Havel JJ, Lee W, Yuan J, Wong P, Ho TS, et al: Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science. 348:124–128. 2015. View Article : Google Scholar : PubMed/NCBI | |
Forde PM, Chaft JE, Smith KN, Anagnostou V, Cottrell TR, Hellmann MD, Zahurak M, Yang SC, Jones DR, Broderick S, et al: Neoadjuvant PD-1 blockade in resectable lung cancer. N Engl J Med. 378:1976–1986. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wang Z, Duan J, Cai S, Han M, Dong H, Zhao J, Zhu B, Wang S, Zhuo M, Sun J, et al: Assessment of blood tumor mutational burden as a potential biomarker for immunotherapy in patients with non-small cell lung cancer with use of a next-generation sequencing cancer gene panel. JAMA Oncol. 5:696–702. 2019. View Article : Google Scholar : PubMed/NCBI | |
Lipson EJ, Sharfman WH, Drake CG, Wollner I, Taube JM, Anders RA, Xu H, Yao S, Pons A, Chen L, et al: Durable cancer regression off-treatment and effective reinduction therapy with an anti-PD-1 antibody. Clin Cancer Res. 19:462–468. 2013. View Article : Google Scholar : PubMed/NCBI | |
Li GM: Mechanisms and functions of DNA mismatch repair. Cell Res. 18:85–98. 2008. View Article : Google Scholar : PubMed/NCBI | |
Le DT, Uram JN, Wang H, Bartlett BR, Kemberling H, Eyring AD, Skora AD, Luber BS, Azad NS, Laheru D, et al: PD-1 blockade in tumors with mismatch-repair deficiency. N Engl J Med. 372:2509–2520. 2015. View Article : Google Scholar : PubMed/NCBI | |
Le DT, Durham JN, Smith KN, Wang H, Bartlett BR, Aulakh LK, Lu S, Kemberling H, Wilt C, Luber BS, et al: Mismatch repair deficiency predicts response of solid tumors to PD-1 blockade. Science. 357:409–413. 2017. View Article : Google Scholar : PubMed/NCBI | |
Schumacher TN and Schreiber RD: Neoantigens in cancer immunotherapy. Science. 348:69–74. 2015. View Article : Google Scholar : PubMed/NCBI | |
McGranahan N, Furness AJ, Rosenthal R, Ramskov S, Lyngaa R, Saini SK, Jamal-Hanjani M, Wilson GA, Birkbak NJ, Hiley CT, et al: Clonal neoantigens elicit T cell immunoreactivity and sensitivity to immune checkpoint blockade. Science. 351:1463–1469. 2016. View Article : Google Scholar : PubMed/NCBI | |
Van Allen EM, Golay HG, Liu Y, Koyama S, Wong K, Taylor-Weiner A, Giannakis M, Harden M, Rojas-Rudilla V, Chevalier A, et al: Long-term benefit of PD-L1 blockade in lung cancer associated with JAK3 activation. Cancer Immunol Res. 3:855–863. 2015. View Article : Google Scholar : PubMed/NCBI | |
Azuma K, Ota K, Kawahara A, Hattori S, Iwama E, Harada T, Matsumoto K, Takayama K, Takamori S, Kage M, et al: Association of PD-L1 overexpression with activating EGFR mutations in surgically resected nonsmall-cell lung cancer. Ann Oncol. 25:1935–1940. 2014. View Article : Google Scholar : PubMed/NCBI | |
Parsa AT, Waldron JS, Panner A, Crane CA, Parney IF, Barry JJ, Cachola KE, Murray JC, Tihan T, Jensen MC, et al: Loss of tumor suppressor PTEN function increases B7-H1 expression and immunoresistance in glioma. Nat Med. 13:84–88. 2007. View Article : Google Scholar : PubMed/NCBI | |
Marzec M, Zhang Q, Goradia A, Raghunath PN, Liu X, Paessler M, Wang HY, Wysocka M, Cheng M, Ruggeri BA, et al: Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc Natl Acad Sci USA. 105:20852–20857. 2008. View Article : Google Scholar : PubMed/NCBI | |
Yadav M, Jhunjhunwala S, Phung QT, Lupardus P, Tanguay J, Bumbaca S, Franci C, Cheung TK, Fritsche J, Weinschenk T, et al: Predicting immunogenic tumour mutations by combining mass spectrometry and exome sequencing. Nature. 515:572–576. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zaretsky JM, Garcia-Diaz A, Shin DS, Escuin-Ordinas H, Hugo W, Hu-Lieskovan S, Torrejon DY, Abril-Rodriguez G, Sandoval S, Barthly L, et al: Mutations associated with acquired resistance to PD-1 blockade in melanoma. N Engl J Med. 375:819–829. 2016. View Article : Google Scholar : PubMed/NCBI | |
Skoulidis F, Goldberg ME, Greenawalt DM, Hellmann MD, Awad MM, Gainor JF, Schrock AB, Hartmaier RJ, Trabucco SE, Gay L, et al: STK11/LKB1 mutations and PD-1 inhibitor resistance in KRAS-mutant lung adenocarcinoma. Cancer Discov. 8:822–835. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chen F, Zhuang X, Lin L, Yu P, Wang Y, Shi Y, Hu G and Sun Y: New horizons in tumor microenvironment biology: Challenges and opportunities. BMC Med. 13:452015. View Article : Google Scholar : PubMed/NCBI | |
Mantovani A, Allavena P, Sica A and Balkwill F: Cancer-related inflammation. Nature. 454:436–444. 2008. View Article : Google Scholar : PubMed/NCBI | |
Yang L, Pang Y and Moses HL: TGF-beta and immune cells: An important regulatory axis in the tumor microenvironment and progression. Trends Immunol. 31:220–227. 2010. View Article : Google Scholar : PubMed/NCBI | |
Pauken KE and Wherry EJ: Overcoming T cell exhaustion in infection and cancer. Trends Immunol. 36:265–276. 2015. View Article : Google Scholar : PubMed/NCBI | |
Li HY, McSharry M, Bullock B, Nguyen TT, Kwak J, Poczobutt JM, Sippel TR, Heasley LE, Weiser-Evans MC, Clambey ET, et al: The tumor microenvironment regulates sensitivity of murine lung tumors to PD-1/PD-L1 antibody blockade. Cancer Immunol Res. 5:767–777. 2017. View Article : Google Scholar : PubMed/NCBI | |
Smyth MJ, Ngiow SF, Ribas A and Teng MW: Combination cancer immunotherapies tailored to the tumour microenvironment. Nat Rev Clin Oncol. 13:143–158. 2016. View Article : Google Scholar : PubMed/NCBI | |
Tumeh PC, Harview CL, Yearley JH, Shintaku IP, Taylor EJ, Robert L, Chmielowski B, Spasic M, Henry G, Ciobanu V, et al: PD-1 blockade induces responses by inhibiting adaptive immune resistance. Nature. 515:568–571. 2014. View Article : Google Scholar : PubMed/NCBI | |
Chen PL, Roh W, Reuben A, Cooper ZA, Spencer CN, Prieto PA, Miller JP, Bassett RL, Gopalakrishnan V, Wani K, et al: Analysis of immune signatures in longitudinal tumor samples yields insight into biomarkers of response and mechanisms of resistance to immune checkpoint blockade. Cancer Discov. 6:827–837. 2016. View Article : Google Scholar : PubMed/NCBI | |
Daud AI, Loo K, Pauli ML, Sanchez-Rodriguez R, Sandoval PM, Taravati K, Tsai K, Nosrati A, Nardo L, Alvarado MD, et al: Tumor immune profiling predicts response to anti-PD-1 therapy in human melanoma. J Clin Invest. 126:3447–3452. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kim R, Keam B, Kim S, Kim M, Kim SH, Kim JW, Kim YJ, Kim TM, Jeon YK, Kim DW, et al: Differences in tumor microenvironments between primary lung tumors and brain metastases in lung cancer patients: Therapeutic implications for immune checkpoint inhibitors. BMC Cancer. 19:192019. View Article : Google Scholar : PubMed/NCBI | |
Chen DS and Mellman I: Elements of cancer immunity and the cancer-immune set point. Nature. 541:321–330. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kim CG, Jang M, Kim Y, Leem G, Kim KH, Lee H, Kim TS, Choi SJ, Kim HD, Han JW, et al: VEGF-A drives TOX-dependent T cell exhaustion in anti-PD-1-resistant microsatellite stable colorectal cancers. Sci Immunol. 4:eaay05552019. View Article : Google Scholar : PubMed/NCBI | |
Ngiow SF, Young A, Jacquelot N, Yamazaki T, Enot D, Zitvogel L and Smyth MJ: A threshold level of intratumor CD8+ T-cell PD1 expression dictates therapeutic response to Anti-PD1. Cancer Res. 75:3800–3811. 2015. View Article : Google Scholar : PubMed/NCBI | |
Davis RJ, Moore EC, Clavijo PE, Friedman J, Cash H, Chen Z, Silvin C, Van Waes C and Allen C: Anti-PD-L1 efficacy Can Be enhanced by inhibition of myeloid-derived suppressor cells with a selective inhibitor of PI3Kδ/γ. Cancer Res. 77:2607–2619. 2017. View Article : Google Scholar : PubMed/NCBI | |
Mao Y, Eissler N, Blanc KL, Johnsen JI, Kogner P and Kiessling R: Targeting suppressive myeloid cells potentiates checkpoint inhibitors to control spontaneous neuroblastoma. Clin Cancer Res. 22:3849–3859. 2016. View Article : Google Scholar : PubMed/NCBI | |
Stone TW and Darlington LG: Endogenous kynurenines as targets for drug discovery and development. Nat Rev Drug Discov. 1:609–620. 2002. View Article : Google Scholar : PubMed/NCBI | |
Llosa NJ, Cruise M, Tam A, Wicks EC, Hechenbleikner EM, Taube JM, Blosser RL, Fan H, Wang H, Luber BS, et al: The vigorous immune microenvironment of microsatellite instable colon cancer is balanced by multiple counter-inhibitory checkpoints. Cancer Discov. 5:43–51. 2015. View Article : Google Scholar : PubMed/NCBI | |
Higgs BW, Robbins PB, Blake-Haskins JA, Zhu W, Morehouse C, Brohawn PZ, Rebelatto MC, Yao Y, Jin X, Shi L and Ranade K: 15LBA High tumoral IFNγ mRNA, PD-L1 protein, and combined IFNγ mRNA/PD-L1 protein expression associates with response to durvalumab (anti-PD-L1) monotherapy in NSCLC patients. Eur J Cancer. 51 (Suppl):S7172015. View Article : Google Scholar | |
Ascierto ML, McMiller TL, Berger AE, Danilova L, Anders RA, Netto GJ, Xu H, Pritchard TS, Fan J, Cheadle C, et al: The intratumoral balance between metabolic and immunologic gene expression is associated with Anti-PD-1 response in patients with renal cell carcinoma. Cancer Immunol Res. 4:726–733. 2016. View Article : Google Scholar : PubMed/NCBI | |
Francisco LM, Salinas VH, Brown KE, Vanguri VK, Freeman GJ, Kuchroo VK and Sharpe AH: PD-L1 regulates the development, maintenance, and function of induced regulatory T cells. J Exp Med. 206:3015–3029. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ding ZC, Lu X, Yu M, Lemos H, Huang L, Chandler P, Liu K, Walters M, Krasinski A, Mack M, et al: Immunosuppressive myeloid cells induced by chemotherapy attenuate antitumor CD4+ T-cell responses through the PD-1-PD-L1 axis. Cancer Res. 74:3441–3453. 2014. View Article : Google Scholar : PubMed/NCBI | |
Platten M, Wick W and Van den Eynde BJ: Tryptophan catabolism in cancer: Beyond IDO and tryptophan depletion. Cancer Res. 72:5435–5440. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ayers M, Lunceford J, Nebozhyn M, Murphy E, Loboda A, Kaufman DR, Albright A, Cheng JD, Kang SP, Shankaran V, et al: IFN-γ-related mRNA profile predicts clinical response to PD-1 blockade. J Clin Invest. 127:2930–2940. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhang X, Zeng Y, Qu Q, Zhu J, Liu Z, Ning W, Zeng H, Zhang N, Du W, Chen C, et al: PD-L1 induced by IFN-γ from tumor-associated macrophages via the JAK/STAT3 and PI3K/AKT signaling pathways promoted progression of lung cancer. Int J Clin Oncol. 22:1026–1033. 2017. View Article : Google Scholar : PubMed/NCBI | |
Quandt D, Jasinski-Bergner S, Muller U, Schulze B and Seliger B: Synergistic effects of IL-4 and TNFα on the induction of B7-H1 in renal cell carcinoma cells inhibiting allogeneic T cell proliferation. J Transl Med. 12:1512014. View Article : Google Scholar : PubMed/NCBI | |
Ni XY, Sui HX, Liu Y, Ke SZ, Wang YN and Gao FG: TGF-β of lung cancer microenvironment upregulates B7H1 and GITRL expression in dendritic cells and is associated with regulatory T cell generation. Oncol Rep. 28:615–621. 2012. View Article : Google Scholar : PubMed/NCBI | |
Rodriguez-Garcia M, Porichis F, de Jong OG, Levi K, Diefenbach TJ, Lifson JD, Freeman GJ, Walker BD, Kaufmann DE and 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. 89:507–515. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kondou R, Iizuka A, Nonomura C, Miyata H, Ashizawa T, Nagashima T, Ohshima K, Urakami K, Kusuhara M, Yamaguchi K, et al: Classification of tumor microenvironment immune types based on immune response-associated gene expression. Int J Oncol. 54:219–228. 2019.PubMed/NCBI | |
Spranger S, Spaapen RM, Zha Y, Williams J, Meng Y, Ha TT and Gajewski TF: Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells. Sci Transl Med. 5:200ra1162013. View Article : Google Scholar : PubMed/NCBI | |
Zhao J, Wen X, Tian L, Li T, Xu C, Wen X, Melancon MP, Gupta S, Shen B, Peng W, et al: Irreversible electroporation reverses resistance to immune checkpoint blockade in pancreatic cancer. Nat Commun. 10:8992019. View Article : Google Scholar : PubMed/NCBI | |
Liu P, Zhao L, Pol J, Levesque S, Petrazzuolo A, Pfirschke C, Engblom C, Rickelt S, Yamazaki T, Iribarren K, et al: Crizotinib-induced immunogenic cell death in non-small cell lung cancer. Nat Commun. 10:14862019. View Article : Google Scholar : PubMed/NCBI | |
Nikolich-Zugich J, Slifka MK and Messaoudi I: The many important facets of T-cell repertoire diversity. Nat Rev Immunol. 4:123–132. 2004. View Article : Google Scholar : PubMed/NCBI | |
Ruggiero E, Nicolay JP, Fronza R, Arens A, Paruzynski A, Nowrouzi A, Urenden G, Lulay C, Schneider S, Goerdt S, et al: High-resolution analysis of the human T-cell receptor repertoire. Nat Commun. 6:80812015. View Article : Google Scholar : PubMed/NCBI | |
Zheng Y, Wang T, Tu X, Huang Y, Zhang H, Tan D, Jiang W, Cai S, Zhao P, Song R, et al: Gut microbiome affects the response to anti-PD-1 immunotherapy in patients with hepatocellular carcinoma. J Immunother Cancer. 7:1932019. View Article : Google Scholar : PubMed/NCBI | |
Sunakawa Y, Inoue E, Matoba R, Kawakami H, Sato Y, Nakajima TE, Muro K, Ichikawa W and Fujii M: DELIVER (JACCRO GC-08) trial: Discover novel host-related immune-biomarkers for nivolumab in advanced gastric cancer. Future Oncol. 15:2441–2447. 2019. View Article : Google Scholar : PubMed/NCBI | |
Matson V, Fessler J, Bao R, Chongsuwat T, Zha Y, Alegre ML, Luke JJ and Gajewski TF: The commensal microbiome is associated with anti-PD-1 efficacy in metastatic melanoma patients. Science. 359:104–108. 2018. View Article : Google Scholar : PubMed/NCBI | |
Jin Y, Dong H, Xia L, Yang Y, Zhu Y, Shen Y, Zheng H, Yao C, Wang Y and Lu S: The diversity of gut microbiome is associated with favorable responses to anti-programmed death 1 immunotherapy in Chinese patients with NSCLC. J Thorac Oncol. 14:1378–1389. 2019. View Article : Google Scholar : PubMed/NCBI | |
Ivanov II and Littman DR: Modulation of immune homeostasis by commensal bacteria. Curr Opin Microbiol. 14:106–114. 2011. View Article : Google Scholar : PubMed/NCBI | |
Sivan A, Corrales L, Hubert N, Williams JB, Aquino-Michaels K, Earley ZM, Benyamin FW, Lei YM, Jabri B, Alegre ML, et al: Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science. 350:1084–1089. 2015. View Article : Google Scholar : PubMed/NCBI | |
Vetizou M, Pitt JM, Daillere R, Lepage P, Waldschmitt N, Flament C, Rusakiewicz S, Routy B, Roberti MP, Duong CP, et al: Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science. 350:1079–1084. 2015. View Article : Google Scholar : PubMed/NCBI | |
Dong M, Meng Z, Kuerban K, Qi F, Liu J, Wei Y, Wang Q, Jiang S, Feng M and Ye L: Diosgenin promotes antitumor immunity and PD-1 antibody efficacy against melanoma by regulating intestinal microbiota. Cell Death Dis. 9:10392018. View Article : Google Scholar : PubMed/NCBI | |
Weide B, Martens A, Hassel JC, Berking C, Postow MA, Bisschop K, Simeone E, Mangana J, Schilling B, Di Giacomo AM, et al: Baseline biomarkers for outcome of melanoma patients treated with pembrolizumab. Clin Cancer Res. 22:5487–5496. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zer A, Sung MR, Walia P, Khoja L, Maganti M, Labbe C, Shepherd FA, Bradbury PA, Feld R, Liu G, et al: Correlation of neutrophil to lymphocyte ratio and absolute neutrophil count with outcomes with PD-1 axis inhibitors in patients with advanced non-small-cell lung cancer. Clin Lung Cancer. 19:426–434.e1. 2018. View Article : Google Scholar : PubMed/NCBI | |
Diem S, Kasenda B, Spain L, Martin-Liberal J, Marconcini R, Gore M and Larkin J: Serum lactate dehydrogenase as an early marker for outcome in patients treated with anti-PD-1 therapy in metastatic melanoma. Br J Cancer. 114:256–261. 2016. View Article : Google Scholar : PubMed/NCBI | |
Gibney GT, Kudchadkar RR, DeConti RC, Thebeau MS, Czupryn MP, Tetteh L, Eysmans C, Richards A, Schell MJ, Fisher KJ, et al: Safety, correlative markers, and clinical results of adjuvant nivolumab in combination with vaccine in resected high-risk metastatic melanoma. Clin Cancer Res. 21:712–720. 2015. View Article : Google Scholar : PubMed/NCBI | |
Niemeijer AN, Leung D, Huisman MC, Bahce I, Hoekstra OS, van Dongen G, Boellaard R, Du S, Hayes W, Smith R, et al: Whole body PD-1 and PD-L1 positron emission tomography in patients with non-small-cell lung cancer. Nat Commun. 9:46642018. View Article : Google Scholar : PubMed/NCBI | |
Bensch F, van der Veen EL, Lub-de Hooge MN, Jorritsma- Smit A, Boellaard R, Kok IC, Oosting SF, Schroder CP, Hiltermann TJN, van der Wekken AJ, et al: 89Zr-atezolizumab imaging as a non-invasive approach to assess clinical response to PD-L1 blockade in cancer. Nat Med. 24:1852–1858. 2018. View Article : Google Scholar : PubMed/NCBI | |
Sun R, Limkin EJ, Vakalopoulou M, Dercle L, Champiat S, Han SR, Verlingue L, Brandao D, Lancia A, Ammari S, et al: A radiomics approach to assess tumour-infiltrating CD8 cells and response to anti-PD-1 or anti-PD-L1 immunotherapy: An imaging biomarker, retrospective multicohort study. Lancet Oncol. 19:1180–1191. 2018. View Article : Google Scholar : PubMed/NCBI | |
Joyce JA and Fearon DT: T cell exclusion, immune privilege, and the tumor microenvironment. Science. 348:74–80. 2015. View Article : Google Scholar : PubMed/NCBI | |
Kluger HM, Zito CR, Barr ML, Baine MK, Chiang VL, Sznol M, Rimm DL, Chen L and Jilaveanu LB: Characterization of PD-L1 expression and associated T-cell infiltrates in metastatic melanoma samples from variable anatomic sites. Clin Cancer Res. 21:3052–3060. 2015. View Article : Google Scholar : PubMed/NCBI | |
Rooney MS, Shukla SA, Wu CJ, Getz G and Hacohen N: Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell. 160:48–61. 2015. View Article : Google Scholar : PubMed/NCBI | |
Feng Z, Puri S, Moudgil T, Wood W, Hoyt CC, Wang C, Urba WJ, Curti BD, Bifulco CB and Fox BA: Multispectral imaging of formalin-fixed tissue predicts ability to generate tumor-infiltrating lymphocytes from melanoma. J Immunother Cancer. 3:472015. View Article : Google Scholar : PubMed/NCBI |