Cited by 309Cancer Immunotherapy and Biomarkersinterferon and immune responsesImmunotherapy and Immune Responses

Type I interferon-mediated tumor immunity and its role in immunotherapy

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Yu, Renren, Zhu, Bo, Chen, Degao·2022·Cellular and Molecular Life Sciences

Abstract

Immune checkpoint blockade (ICB) therapies have achieved remarkable clinical responses in patients with many different types of cancer; however, most patients who receive ICB monotherapy fail to achieve long-term responses, and some tumors become immunotherapy-resistant and even hyperprogressive. Type I interferons (IFNs) have been demonstrated to inhibit tumor growth directly and indirectly by acting upon tumor and immune cells, respectively. Furthermore, accumulating evidence indicates that endo- and exogenously enhancing type I IFNs have a synergistic effect on anti-tumor immunity. Therefore, clinical trials studying new treatment strategies that combine type I IFN inducers with ICB are currently in progress. Here, we review the cellular sources of type I IFNs and their roles in the immune regulation of the tumor microenvironment. In addition, we highlight immunotherapies based on type I IFNs and combination therapy between type I IFN inducers and ICBs.

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  1. [1]Isaacs A Lindenmann J Virus interference. I. the interferon Proc R Soc Lond B Biol Sci 1957 147 258 267 26297790
  2. [2]Isaacs A Lindenmann J Valentine RC Virus interference. II. Some properties of interferon Proc R Soc Lond B Biol Sci 1957 147 268 273 26297791
  3. [3]Parker BS Rautela J Hertzog PJ Antitumour actions of interferons: implications for cancer therapy Nat Rev Cancer 2016 16 131 144 26911188
  4. [5]Pestka S Krause CD Walter MR Interferons, interferon-like cytokines, and their receptors Immunol Rev 2004 202 8 32 15546383
  5. [6]Oritani K Kanakura Y IFN-zeta/ limitin: a member of type I IFN with mild lympho-myelosuppression J Cell Mol Med 2005 9 244 254 15963247 PMC6740103
  6. [7]Lazear HM Schoggins JW Diamond MS Shared and distinct functions of type I and type III interferons Immunity 2019 50 907 923 30995506 PMC6839410
  7. [8]Platanias LC Mechanisms of type-I- and type-II-interferon-mediated signalling Nat Rev Immunol 2005 5 375 386 15864272
  8. [9]Hervas-Stubbs S Perez-Gracia JL Rouzaut A Direct effects of type I interferons on cells of the immune system Clin Cancer Res 2011 17 2619 2627 21372217
  9. [10]Stark GR Darnell JE Jr The JAK-STAT pathway at twenty Immunity 2012 36 503 514 22520844 PMC3909993
  10. [11]Borden EC Interferons alpha and beta in cancer: therapeutic opportunities from new insights Nat Rev Drug Discov 2019 18 219 234 30679806
  11. [12]Levy DE Kessler DS Pine R Darnell JE Jr Cytoplasmic activation of ISGF3, the positive regulator of interferon-alpha-stimulated transcription, reconstituted in vitro Genes Dev 1989 3 1362 1371 2606351
  12. [15]Saleiro D Platanias LC Interferon signaling in cancer Non-canonical pathways and control of intracellular immune checkpoints Semin Immunol 2019 43 101299 31771762 PMC8177745
  13. [16]Swiecki M Colonna M The multifaceted biology of plasmacytoid dendritic cells Nat Rev Immunol 2015 15 471 485 26160613 PMC4808588
  14. [17]Andzinski L Spanier J Kasnitz N Growing tumors induce a local STING dependent Type I IFN response in dendritic cells Int J Cancer 2016 139 1350 1357 27116225
  15. [18]Woo SR Fuertes MB Corrales L STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors Immunity 2014 41 830 842 25517615 PMC4384884
  16. [20]Wu J Sun L Chen X Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA Science 2013 339 826 830 23258412 PMC3855410
  17. [22]Zhang X Bai XC Chen ZJ Structures and mechanisms in the cGAS-STING innate immunity pathway Immunity 2020 53 43 53 32668227
  18. [23]Corrales L McWhirter SM Dubensky TW Jr Gajewski TF The host STING pathway at the interface of cancer and immunity J Clin Invest 2016 126 2404 2411 27367184 PMC4922692
  19. [25]Lv M Chen M Zhang R Manganese is critical for antitumor immune responses via cGAS-STING and improves the efficacy of clinical immunotherapy Cell Res 2020 30 966 979 32839553 PMC7785004
  20. [29]Saccheri F Pozzi C Avogadri F Bacteria-induced gap junctions in tumors favor antigen cross-presentation and antitumor immunity Sci Transl Med 2010 2 44ra57 20702856
  21. [30]Luteijn RD Zaver SA Gowen BG SLC19A1 transports immunoreactive cyclic dinucleotides Nature 2019 573 434 438 31511694 PMC6785039
  22. [31]Zhao J Xue Y Pan Y Toll-like receptor 3 agonist poly I: C reinforces the potency of cytotoxic chemotherapy via the TLR3-UNC93B1-IFN-beta signaling axis in paclitaxel-resistant colon cancer J Cell Physiol 2019 234 7051 7061 30387134
  23. [32]Sistigu A Yamazaki T Vacchelli E Cancer cell-autonomous contribution of type I interferon signaling to the efficacy of chemotherapy Nat Med 2014 20 1301 1309 25344738
  24. [33]Nunez NG Andreani V Crespo MI IFNbeta produced by TLR4-activated tumor cells is involved in improving the antitumoral immune response Cancer Res 2012 72 592 603 22139376
  25. [34]Deng L Liang H Xu M STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors Immunity 2014 41 843 852 25517616 PMC5155593
  26. [35]Vanpouille-Box C Alard A Aryankalayil MJ DNA exonuclease Trex1 regulates radiotherapy-induced tumour immunogenicity Nat Commun 2017 8 15618 28598415 PMC5472757
  27. [36]Ablasser A Schmid-Burgk JL Hemmerling I Cell intrinsic immunity spreads to bystander cells via the intercellular transfer of cGAMP Nature 2013 503 530 534 24077100 PMC4142317
  28. [37]Demaria O De Gassart A Coso S STING activation of tumor endothelial cells initiates spontaneous and therapeutic antitumor immunity Proc Natl Acad Sci U S A 2015 112 15408 15413 26607445 PMC4687570
  29. [38]Ma F Li B Yu Y Positive feedback regulation of type I interferon by the interferon-stimulated gene STING EMBO Rep 2015 16 202 212 25572843 PMC4328747
  30. [39]Ehnfors J Kost-Alimova M Persson NL Horizontal transfer of tumor DNA to endothelial cells in vivo Cell Death Differ 2009 16 749 757 19219067
  31. [40]Corrales L Glickman LH McWhirter SM Direct activation of STING in the tumor microenvironment leads to potent and systemic tumor regression and immunity Cell Rep 2015 11 1018 1030 25959818 PMC4440852
  32. [41]Zhang Y Sun Y Rao E Fatty acid-binding protein E-FABP restricts tumor growth by promoting IFN-beta responses in tumor-associated macrophages Cancer Res 2014 74 2986 2998 24713431 PMC4040301
  33. [42]Arwert EN Milford EL Rullan A STING and IRF3 in stromal fibroblasts enable sensing of genomic stress in cancer cells to undermine oncolytic viral therapy Nat Cell Biol 2020 22 758 766 32483388 PMC7611090
  34. [43]Yoon N Park MS Shigemoto T Activated human mesenchymal stem/stromal cells suppress metastatic features of MDA-MB-231 cells by secreting IFN-beta Cell Death Dis 2016 7 e2191 27077807 PMC4855669
  35. [44]Broad RV Jones SJ Teske MC Inhibition of interferon-signalling halts cancer-associated fibroblast-dependent protection of breast cancer cells from chemotherapy Br J Cancer 2021 124 1110 1120 33398063 PMC7960738
  36. [45]Gresser I Bourali C Levy JP Increased survival in mice inoculated with tumor cells and treated with interferon preparations Proc Natl Acad Sci U S A 1969 63 51 57 5257966 PMC534033
  37. [46]Zhou L Zhang Y Wang Y A dual role of type I interferons in antitumor immunity Adv Biosyst 2020 4 e1900237 33245214
  38. [47]Chen J Cao Y Markelc B Type I IFN protects cancer cells from CD8+ T cell–mediated cytotoxicity after radiation J Clin Investig 2019 129 4224 4238 31483286 PMC6763250
  39. [48]Butterfield LH Vujanovic L Santos PM Multiple antigen-engineered DC vaccines with or without IFNalpha to promote antitumor immunity in melanoma J Immunother Cancer 2019 7 113 31014399 PMC6480917
  40. [49]Swann JB Hayakawa Y Zerafa N Type I IFN contributes to NK cell homeostasis, activation, and antitumor function J Immunol 2007 178 7540 7549 17548588
  41. [50]Marcus A Mao AJ Lensink-Vasan M Tumor-derived cGAMP triggers a STING-mediated interferon response in non-tumor cells to activate the NK cell response Immunity 2018 49 754 763 30332631 PMC6488306
  42. [51]Muller L Aigner P Stoiber D Type I Interferons and natural killer cell regulation in cancer Front Immunol 2017 8 304 28408907 PMC5374157
  43. [52]Jiang W Zhang C Tian Z Zhang J hIFN-alpha gene modification augments human natural killer cell line anti-human hepatocellular carcinoma function Gene Ther 2013 20 1062 1069 23759701
  44. [53]Riley CH Hansen M Brimnes MK Expansion of circulating CD56bright natural killer cells in patients with JAK2-positive chronic myeloproliferative neoplasms during treatment with interferon-alpha Eur J Haematol 2015 94 227 234 25082025
  45. [54]Jaillon S Ponzetta A Di Mitri D Neutrophil diversity and plasticity in tumour progression and therapy Nat Rev Cancer 2020 20 485 503 32694624
  46. [55]Andzinski L Wu CF Lienenklaus S Delayed apoptosis of tumor associated neutrophils in the absence of endogenous IFN-beta Int J Cancer 2015 136 572 583 24806531
  47. [56]Jablonska J Wu CF Andzinski L CXCR2-mediated tumor-associated neutrophil recruitment is regulated by IFN-beta Int J Cancer 2014 134 1346 1358 24154944
  48. [57]Andzinski L Kasnitz N Stahnke S Type I IFNs induce anti-tumor polarization of tumor associated neutrophils in mice and human Int J Cancer 2016 138 1982 1993 26619320
  49. [58]Jablonska J Leschner S Westphal K Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model J Clin Invest 2010 120 1151 1164 20237412 PMC2846036
  50. [59]Wu CF Andzinski L Kasnitz N The lack of type I interferon induces neutrophil-mediated pre-metastatic niche formation in the mouse lung Int J Cancer 2015 137 837 847 25604426
  51. [60]Pylaeva E Lang S Jablonska J The essential role of type I interferons in differentiation and activation of tumor-associated neutrophils Front Immunol 2016 7 629 28066438 PMC5174087
  52. [61]Sharabi A Tsokos MG Ding Y Regulatory T cells in the treatment of disease Nat Rev Drug Discov 2018 17 823 844 30310234
  53. [62]Hashimoto H Ueda R Narumi K Type I IFN gene delivery suppresses regulatory T cells within tumors Cancer Gene Ther 2014 21 532 541 25430879
  54. [63]Bacher N Raker V Hofmann C Interferon-alpha suppresses cAMP to disarm human regulatory T cells Cancer Res 2013 73 5647 5656 23878189
  55. [64]Anz D Rapp M Eiber S Suppression of Intratumoral CCL22 by type I Interferon inhibits migration of regulatory T cells and blocks cancer progression Can Res 2015 75 4483 4493 26432403
  56. [65]Hirata A Hashimoto H Shibasaki C Intratumoral IFN-alpha gene delivery reduces tumor-infiltrating regulatory T cells through the downregulation of tumor CCL17 expression Cancer Gene Ther 2019 26 334 343 30420718
  57. [66]Sisirak V Faget J Gobert M Impaired IFN-alpha production by plasmacytoid dendritic cells favors regulatory T-cell expansion that may contribute to breast cancer progression Cancer Res 2012 72 5188 5197 22836755
  58. [67]Li K Shi H Zhang B Myeloid-derived suppressor cells as immunosuppressive regulators and therapeutic targets in cancer Signal Transduct Target Ther 2021 6 362 34620838 PMC8497485
  59. [68]Zoglmeier C Bauer H Noerenberg D CpG blocks immunosuppression by myeloid-derived suppressor cells in tumor-bearing mice Clin Cancer Res 2011 17 1765 1775 21233400
  60. [69]Field AK Tytell AA Lampson GP Hilleman MR Inducers of interferon and host resistance. II. Multistranded synthetic polynucleotide complexes Proc Natl Acad Sci U S A 1967 58 1004 1010 5233831 PMC335739
  61. [70]Chen J Sun HW Yang YY Reprogramming immunosuppressive myeloid cells by activated T cells promotes the response to anti-PD-1 therapy in colorectal cancer Signal Transduct Target Ther 2021 6 4 33414378 PMC7791142
  62. [71]Huang L Li L Lemos H Cutting edge: DNA sensing via the STING adaptor in myeloid dendritic cells induces potent tolerogenic responses J Immunol 2013 191 3509 3513 23986532 PMC3788571
  63. [73]Drobits B Holcmann M Amberg N Imiquimod clears tumors in mice independent of adaptive immunity by converting pDCs into tumor-killing effector cells J Clin Invest 2012 122 575 585 22251703 PMC3266798
  64. [74]Adamus T Kortylewski M The revival of CpG oligonucleotide-based cancer immunotherapies Contemp Oncol (Pozn) 2018 22 56 60 29628795 PMC5885070
  65. [75]Aranda F Vacchelli E Obrist F Trial watch: toll-like receptor agonists in oncological indications Oncoimmunology 2014 3 e29179 25083332 PMC4091055
  66. [77]Sagiv-Barfi I Czerwinski DK Levy S Eradication of spontaneous malignancy by local immunotherapy Sci Transl Med 2018 10 4eaan488 PMC5997264 29386357
  67. [78]Nuhn L De Koker S Van Lint S Nanoparticle-conjugate TLR7/8 agonist localized immunotherapy provokes safe antitumoral responses Adv Mater 2018 30 e1803397 30276880
  68. [79]Kim SY Kim S Kim JE Lyophilizable and multifaceted toll-like receptor 7/8 agonist-loaded nanoemulsion for the reprogramming of tumor microenvironments and enhanced cancer immunotherapy ACS Nano 2019 13 12671 12686 31589013
  69. [80]Perry JL Tian S Sengottuvel N Pulmonary delivery of nanoparticle-bound toll-like receptor 9 agonist for the treatment of metastatic lung cancer ACS Nano 2020 14 7200 7215 32463690 PMC7531260
  70. [81]Vollmer J Krieg AM Immunotherapeutic applications of CpG oligodeoxynucleotide TLR9 agonists Adv Drug Deliv Rev 2009 61 195 204 19211030
  71. [82]Brody JD Ai WZ Czerwinski DK In situ vaccination with a TLR9 agonist induces systemic lymphoma regression: a phase I/II study J Clin Oncol 2010 28 4324 4332 20697067 PMC2954133
  72. [83]Tozer GM Kanthou C Baguley BC Disrupting tumour blood vessels Nat Rev Cancer 2005 5 423 435 15928673
  73. [84]Wang K Donnelly CR Jiang C STING suppresses bone cancer pain via immune and neuronal modulation Nat Commun 2021 12 4558 34315904 PMC8316360
  74. [85]Xu N Palmer DC Robeson AC STING agonist promotes CAR T cell trafficking and persistence in breast cancer J Exp Med 2021 218 e20200844 33382402 PMC7780733
  75. [86]Lara PN Jr Douillard JY Nakagawa K Randomized phase III placebo-controlled trial of carboplatin and paclitaxel with or without the vascular disrupting agent vadimezan (ASA404) in advanced non-small-cell lung cancer J Clin Oncol 2011 29 2965 2971 21709202
  76. [88]Cheng N Watkins-Schulz R Junkins RD A nanoparticle-incorporated STING activator enhances antitumor immunity in PD-L1-insensitive models of triple-negative breast cancer JCI Insight 2018 3 e120638 30429378 PMC6302949
  77. [89]Jang SC Economides KD Moniz RJ ExoSTING, an extracellular vesicle loaded with STING agonists, promotes tumor immune surveillance Commun Biol 2021 4 497 33888863 PMC8062530
  78. [93]Yang X Zhang X Fu ML Targeting the tumor microenvironment with interferon-beta bridges innate and adaptive immune responses Cancer Cell 2014 25 37 48 24434209 PMC3927846
  79. [94]Salvagno C Ciampricotti M Tuit S Therapeutic targeting of macrophages enhances chemotherapy efficacy by unleashing type I interferon response Nat Cell Biol 2019 21 511 521 30886344 PMC6451630
  80. [95]Burnette BC Liang H Lee Y The efficacy of radiotherapy relies upon induction of type i interferon-dependent innate and adaptive immunity Cancer Res 2011 71 2488 2496 21300764 PMC3070872
  81. [96]Feng X Tubbs A Zhang C ATR inhibition potentiates ionizing radiation-induced interferon response via cytosolic nucleic acid-sensing pathways EMBO J 2020 39 e104036 32484965 PMC7361286
  82. [97]Frank MJ Reagan PM Bartlett NL In situ vaccination with a TLR9 agonist and local low-dose radiation induces systemic responses in untreated indolent lymphoma Cancer Discov 2018 8 1258 1269 30154192 PMC6171524
  83. [98]Poh A First oncolytic viral therapy for melanoma Cancer Discov 2016 6 6 26552414
  84. [99]Ramelyte E Tastanova A Balazs Z Oncolytic virotherapy-mediated anti-tumor response: a single-cell perspective Cancer Cell 2021 39 394 406 33482123
  85. [100]Desjardins A Gromeier M Herndon JE 2nd Recurrent glioblastoma treated with recombinant poliovirus N Engl J Med 2018 379 150 161 29943666 PMC6065102
  86. [101]Brown MC Mosaheb MM Mohme M Viral infection of cells within the tumor microenvironment mediates antitumor immunotherapy via selective TBK1-IRF3 signaling Nat Commun 2021 12 1858 33767151 PMC7994570
  87. [102]Zamarin D Holmgaard RB Subudhi SK Localized oncolytic virotherapy overcomes systemic tumor resistance to immune checkpoint blockade immunotherapy Sci Transl Med 2014 6 226ra232 PMC4106918 24598590
  88. [103]Melero I Quetglas JI Reboredo M Strict requirement for vector-induced type I interferon in efficacious antitumor responses to virally encoded IL12 Cancer Res 2015 75 497 507 25527611
  89. [104]Komdeur FL Singh A van de Wall S First-in-human phase I clinical trial of an SFV-based RNA replicon cancer vaccine against HPV-induced cancers Mol Ther 2021 29 611 625 33160073 PMC7854293
  90. [105]Bourgeois-Daigneault MC Roy DG Aitken AS Neoadjuvant oncolytic virotherapy before surgery sensitizes triple-negative breast cancer to immune checkpoint therapy Sci Transl Med 2018 10 eaao1641 29298865
  91. [106]Roy DG Geoffroy K Marguerie M Adjuvant oncolytic virotherapy for personalized anti-cancer vaccination Nat Commun 2021 12 2626 33976179 PMC8113265
  92. [107]Zamarin D Ricca JM Sadekova S PD-L1 in tumor microenvironment mediates resistance to oncolytic immunotherapy J Clin Invest 2018 128 1413 1428 29504948 PMC5873884
  93. [108]Walsh SR Bastin D Chen L Type I IFN blockade uncouples immunotherapy-induced antitumor immunity and autoimmune toxicity J Clin Invest 2019 129 518 530 30422820 PMC6355222
  94. [109]Evgin L Huff AL Wongthida P Oncolytic virus-derived type I interferon restricts CAR T cell therapy Nat Commun 2020 11 3187 32581235 PMC7314766
  95. [110]Fend L Yamazaki T Remy C Immune checkpoint blockade, immunogenic chemotherapy or IFN-alpha blockade boost the local and abscopal effects of oncolytic virotherapy Cancer Res 2017 77 4146 4157 28536278
  96. [111]Tsuchiya N Zhang R Iwama T Type I interferon delivery by iPSC-derived myeloid cells elicits antitumor Immunity via XCR1(+) dendritic cells Cell Rep 2019 29 162 175 31577946
  97. [112]Sharma P Hu-Lieskovan S Wargo JA Ribas A Primary, adaptive, and acquired resistance to cancer immunotherapy Cell 2017 168 707 723 28187290 PMC5391692
  98. [113]Meric-Bernstam F Larkin J Tabernero J Bonini C Enhancing anti-tumour efficacy with immunotherapy combinations The Lancet 2021 397 1010 1022 33285141
  99. [114]Jacquelot N Yamazaki T Roberti MP Sustained Type I interferon signaling as a mechanism of resistance to PD-1 blockade Cell Res 2019 29 846 861 31481761 PMC6796942
  100. [115]Da Gama DJ Parakh S Andrews MC Autoantibodies may predict immune-related toxicity: results from a phase I study of intralesional bacillus calmette-guerin followed by ipilimumab in patients with advanced metastatic melanoma Front Immunol 2018 9 411 29552014 PMC5840202
  101. [116]Bald T Landsberg J Lopez-Ramos D Immune cell-poor melanomas benefit from PD-1 blockade after targeted type I IFN activation Cancer Discov 2014 4 674 687 24589924
  102. [117]Brockwell NK Owen KL Zanker D Neoadjuvant interferons: critical for effective PD-1-based immunotherapy in TNBC Cancer Immunol Res 2017 5 871 884 28848054
  103. [118]Aznar MA Planelles L Perez-Olivares M Immunotherapeutic effects of intratumoral nanoplexed poly I:C J Immunother Cancer 2019 7 116 31046839 PMC6498680
  104. [119]Bhagchandani S Johnson JA Irvine DJ Evolution of Toll-like receptor 7/8 agonist therapeutics and their delivery approaches: from antiviral formulations to vaccine adjuvants Adv Drug Deliv Rev 2021 175 113803 34058283 PMC9003539
  105. [125]Wang S Campos J Gallotta M Intratumoral injection of a CpG oligonucleotide reverts resistance to PD-1 blockade by expanding multifunctional CD8+ T cells Proc Natl Acad Sci U S A 2016 113 E7240 E7249 27799536 PMC5135381
  106. [126]Ribas A Medina T Kummar S SD-101 in Combination with pembrolizumab in advanced melanoma: results of a phase Ib, multicenter study Cancer Discov 2018 8 1250 1257 30154193 PMC6719557
  107. [127]Smith M Garcia-Martinez E Pitter MR Trial Watch: Toll-like receptor agonists in cancer immunotherapy Oncoimmunology 2018 7 e1526250 30524908 PMC6279325
  108. [128]Cheng Y Lemke-Miltner CD Wongpattaraworakul W In situ immunization of a TLR9 agonist virus-like particle enhances anti-PD1 therapy J Immunother Cancer 2020 8 e000940 33060147 PMC7566437
  109. [129]Ribas A Medina T Kirkwood JM Overcoming PD-1 blockade resistance with CpG-A toll-like receptor 9 agonist vidutolimod in patients with metastatic melanoma Cancer Discov 2021 10.1158/2159-8290 34326162 PMC8799774 · DOI
  110. [131]Weihrauch MR Richly H von Bergwelt-Baildon MS Phase I clinical study of the toll-like receptor 9 agonist MGN1703 in patients with metastatic solid tumours Eur J Cancer 2015 51 146 156 25480557
  111. [132]Thomas M Ponce-Aix S Navarro A Immunotherapeutic maintenance treatment with toll-like receptor 9 agonist lefitolimod in patients with extensive-stage small-cell lung cancer: results from the exploratory, controlled, randomized, international phase II IMPULSE study Ann Oncol 2018 29 2076 2084 30137193 PMC6225892
  112. [133]Kapp K Volz B Oswald D Beneficial modulation of the tumor microenvironment and generation of anti-tumor responses by TLR9 agonist lefitolimod alone and in combination with checkpoint inhibitors Oncoimmunology 2019 8 e1659096 31741757 PMC6844329
  113. [134]Reilley MJ Morrow B Ager CR TLR9 activation cooperates with T cell checkpoint blockade to regress poorly immunogenic melanoma J Immunother Cancer 2019 7 323 31771649 PMC6880482
  114. [135]Fu J Kanne DB Leong M STING agonist formulated cancer vaccines can cure established tumors resistant to PD-1 blockade Sci Transl Med 2015 7 283ra252 283ra252 PMC4504692 25877890
  115. [136]Wang H Hu S Chen X cGAS is essential for the antitumor effect of immune checkpoint blockade Proc Natl Acad Sci U S A 2017 114 1637 1642 28137885 PMC5320994
  116. [137]Harding SM Benci JL Irianto J Mitotic progression following DNA damage enables pattern recognition within micronuclei Nature 2017 548 466 470 28759889 PMC5857357
  117. [143]Lhuillier C Vanpouille-Box C Galluzzi L Emerging biomarkers for the combination of radiotherapy and immune checkpoint blockers Semin Cancer Biol 2018 52 125 134 29258856 PMC6004231
  118. [144]Kang J Demaria S Formenti S Current clinical trials testing the combination of immunotherapy with radiotherapy J Immunother Cancer 2016 4 51 27660705 PMC5028964
  119. [145]Vacchelli E Bloy N Aranda F Trial watch: immunotherapy plus radiation therapy for oncological indications Oncoimmunology 2016 5 e1214790 27757313 PMC5048768
  120. [146]Hui R Ozguroglu M Villegas A Patient-reported outcomes with durvalumab after chemoradiotherapy in stage III, unresectable non-small-cell lung cancer (PACIFIC): a randomised, controlled, phase 3 study Lancet Oncol 2019 20 1670 1680 31601496
  121. [147]Mayadev J Nunes AT Li M CALLA: Efficacy and safety of concurrent and adjuvant durvalumab with chemoradiotherapy versus chemoradiotherapy alone in women with locally advanced cervical cancer: a phase III, randomized, double-blind, multicenter study Int J Gynecol Cancer 2020 30 1065 1070 32447296 PMC7398223
  122. [148]Senan S Okamoto I Lee GW Design and rationale for a phase III, randomized, placebo-controlled trial of durvalumab with or without tremelimumab after concurrent chemoradiotherapy for patients With limited-stage small-cell lung cancer: the ADRIATIC study Clin Lung Cancer 2020 21 e84 e88 31948903
  123. [149]Kwon ED Drake CG Scher HI Ipilimumab versus placebo after radiotherapy in patients with metastatic castration-resistant prostate cancer that had progressed after docetaxel chemotherapy (CA184-043): a multicentre, randomised, double-blind, phase 3 trial Lancet Oncol 2014 15 700 712 24831977 PMC4418935
  124. [150]Chan HY Choi J Jackson C Lim M Combination immunotherapy strategies for glioblastoma J Neurooncol 2021 151 375 391 33611705
  125. [151]Lan Y Moustafa M Knoll M Simultaneous targeting of TGF-beta/PD-L1 synergizes with radiotherapy by reprogramming the tumor microenvironment to overcome immune evasion Cancer Cell 2021 39 1388 1403 34506739
  126. [152]Andtbacka RH Kaufman HL Collichio F Talimogene laherparepvec improves durable response rate in patients with advanced melanoma J Clin Oncol 2015 33 2780 2788 26014293
  127. [153]Puzanov I Milhem MM Minor D Talimogene laherparepvec in combination with ipilimumab in previously untreated, unresectable stage IIIB-IV melanoma J Clin Oncol 2016 34 2619 2626 27298410 PMC7189507
  128. [154]Ribas A Dummer R Puzanov I Oncolytic virotherapy promotes intratumoral T cell Infiltration and improves Anti-PD-1 immunotherapy Cell 2017 170 1109 1119 28886381 PMC8034392
  129. [156]Harrington KJ Kong A Mach N Talimogene laherparepvec and pembrolizumab in recurrent or metastatic squamous cell carcinoma of the head and neck (MASTERKEY-232): a multicenter, phase 1b study Clin Cancer Res 2020 26 5153 5161 32669371
  130. [160]Kuryk L Moller AW Jaderberg M Combination of immunogenic oncolytic adenovirus ONCOS-102 with anti-PD-1 pembrolizumab exhibits synergistic antitumor effect in humanized A2058 melanoma huNOG mouse model Oncoimmunology 2019 8 e1532763 30713786 PMC6343802
  131. [164]Panagioti E Kurokawa C Viker K Immunostimulatory bacterial antigen-armed oncolytic measles virotherapy significantly increases the potency of anti-PD1 checkpoint therapy J Clin Invest 2021 131 e141614 34196308 PMC8245183
  132. [165]Mender I Zhang A Ren Z Telomere Stress Potentiates STING-Dependent Anti-tumor Immunity Cancer Cell 2020 38 400 411 32619407 PMC7494563
  133. [166]Si W Liang H Bugno J Lactobacillus rhamnosus GG induces cGAS/STING- dependent type I interferon and improves response to immune checkpoint blockade Gut 2021 71 521 533 33685966 PMC8710942

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Sorted by citations

Authors
Yu, R., Zhu, B., & Chen, D.
Affiliations
Army Medical University (CN)
Corresponding author
  • Zhu, Bo
  • Chen, Degao
Venue
Cellular and Molecular Life Sciences
Published
2022-03
Volume
79
Issue
3
Pages
191-191
ISSN
  • 1420-682X (ISSN-L)
  • 1420-9071
OpenAlex
W4220735045
Cited by
309
References
18
Citations by year
2026: 52 · 2025: 86 · 2024: 86 · 2023: 73 · 2022: 12
FWCI
7.91
Type
journal article
Language
en
Open access
Locations
  • Cellular and Molecular Life Sciences (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
National Natural Science Foundation of China (82003018, 81925030)
Topics
  • Health Sciences › Medicine › Oncology › Cancer Immunotherapy and Biomarkers
  • Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
  • Life Sciences › Immunology and Microbiology › Immunology › Immunotherapy and Immune Responses
Keywords
type I interferon, antitumor immunity, immune checkpoint blockade, cancer immunotherapy, combination therapy, tumor microenvironment, interferon inducers, immunotherapy resistance, hyperprogression
MeSH terms
Cancer-Associated Fibroblasts, Myeloid-Derived Suppressor Cells, Immune Checkpoint Inhibitors, Animals, Combined Modality Therapy, Dendritic Cells, Humans, Immunotherapy, Interferon Type I, Killer Cells, Natural, Macrophages, Neoplasms, Neutrophils, Signal Transduction, Lymphocytes, Tumor-Infiltrating, Models, Immunological, Endothelial Cells, Oncolytic Virotherapy, T-Lymphocytes, Regulatory, Toll-Like Receptors, Mice, Tumor Microenvironment

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

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