|Table of Contents|

Research progress in tumor-infiltrating lymphocytes immunotherapy in solid tumors

Journal Of Modern Oncology[ISSN:1672-4992/CN:61-1415/R]

Issue:
2023 21
Page:
4055-4061
Research Field:
Publishing date:

Info

Title:
Research progress in tumor-infiltrating lymphocytes immunotherapy in solid tumors
Author(s):
ZHAO Shandong12ZHENG Meng12WANG Yan12MIAO Liyan12
1.Department of Clinical Pharmacology Research Lab,the First Affiliated Hospital of Soochow University,Jiangsu Suzhou 215000, China;2.Institute for Interdisciplinary Drug Research and Translational Sciences,Soochow University,Jiangsu Suzhou 215000,China.
Keywords:
tumor-infiltrating lymphocytessolid tumorpharmacokineticspharmacodynamics
PACS:
R730.5
DOI:
10.3969/j.issn.1672-4992.2023.21.029
Abstract:
Adoptive cell therapy(ACT) based on tumor-infiltrating lymphocytes(TILs) is one of the novel strategies for treating cancers after immune checkpoint inhibitors(ICIs),which has made great progress in patients with solid malignancies.However,unlike traditional medicine,TILs have unique pharmacokinetic characteristics(such as distribution,homing,migration and proliferation) closely related to the efficacy and safety.Hence,this article mainly summarizes recent research advances of TILs therapy,including the pharmacokinetics(PK),pharmacodynamics(PD) and possible mechanisms,in the hope of providing reference for promoting the development and clinical transformation of TILs.

References:

[1] XIA C,DONG X,LI H,et al.Cancer statistics in China and United States,2022:profiles,trends,and determinants[J].Chinese Medical Journal,2022,135(5):584-590.
[2] KIRTANE K,ELMARIAH H,CHUNG CH,et al.Adoptive cellular therapy in solid tumor malignancies:review of the literature and challenges ahead[J].Journal for Immunotherapy of Cancer,2021,9(7):e002723.
[3] TITOV A,ZMIEVSKAYA E,GANEEVA I,et al.Adoptive Immunotherapy beyond CAR T-Cells[J].Cancers,2021,13(4):743.
[4] PAIJENS ST,VLEDDER A,BRUYN M DE,et al.Tumor-infiltrating lymphocytes in the immunotherapy era[J].Cellular & Molecular Immunology,2021,18(4):842-859.
[5] WANG S,SUN J,CHEN K,et al.Perspectives of tumor-infiltrating lymphocyte treatment in solid tumors[J].BMC Medicine,2021,19(1):140.
[6] ROSENBERG SA,SPIESS P,LAFRENIERE R.A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes[J].Science(New York),1986,233(4770):1318-1321.
[7] ROSENBERG SA,PACKARD BS,AEBERSOLD PM,et al.Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma.A preliminary report[J].The New England Journal of Medicine,1988,319(25):1676-1680.
[8] GATTINONI L,FINKELSTEIN SE,KLEBANOFF CA,et al.Removal of homeostatic cytokine sinks by lymphodepletion enhances the efficacy of adoptively transferred tumor-specific CD8+ T cells[J].The Journal of Experimental Medicine,2005,202(7):907-912.
[9] DUDLEY ME,YANG JC,SHERRY R,et al.Adoptive cell therapy for patients with metastatic melanoma:evaluation of intensive myeloablative chemoradiation preparative regimens[J].Journal of Clinical Oncology,2008,26(32):5233-5239.
[10] ROSENBERG SA,YANG JC,SHERRY RM,et al.Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy[J].Clinical Cancer Research,2011,17(13):4550-4557.
[11] DANAHER P,WARREN S,DENNIS L,et al.Gene expression markers of tumor infiltrating leukocytes[J].Journal for Immunotherapy of Cancer,2017,5:18.
[12] SALGADO R,DENKERT C,DEMARIA S,et al.The evaluation of tumor-infiltrating lymphocytes(TILs)in breast cancer:recommendations by an International TILs Working Group 2014[J].Annals of Oncology,2015,26(2):259-271.
[13] SALTZ J,GUPTA R,LE HOU,et al.Spatial organization and molecular correlation of tumor-infiltrating lymphocytes using deep learning on pathology images[J].Cell Reports,2018,23(1):181-193.e7.
[14] FISHER B,PACKARD BS,READ EJ,et al.Tumor localization of adoptively transferred indium-111 labeled tumor infiltrating lymphocytes in patients with metastatic melanoma[J].Journal of Clinical Oncology,1989,7(2):250-261.
[15] GRIFFITH KD,READ EJ,CARRASQUILLO JA,et al.In vivo distribution of adoptively transferred indium-111-labeled tumor infiltrating lymphocytes and peripheral blood lymphocytes in patients with metastatic melanoma[J].Journal of the National Cancer Institute,1989,81(22):1709-1717.
[16]] PITTET MJ,GRIMM J,BERGER CR,et al.In vivo imaging of T cell delivery to tumors after adoptive transfer therapy[J].Proceedings of the National Academy of Sciences of the United States of America,2007,104(30):12457-12461.
[17] ZHAO H,WANG C,YANG Y,et al.ImmunoPET imaging of human CD8+ T cells with novel 68Ga-labeled nanobody companion diagnostic agents[J].Journal of Nanobiotechnology,2021,19(1):42.
[18] FARWELL MD,GAMACHE RF,BABAZADA H,et al.CD8-targeted PET imaging of tumor-infiltrating T cells in patients with cancer:A phase I first-in-humans study of 89Zr-Df-IAB22M2C,a radiolabeled anti-CD8 minibody[J].Journal of Nuclear Medicine,2022,63(5):720-726.
[19] HONG JJ,ROSENBERG SA,DUDLEY ME,et al.Successful treatment of melanoma brain metastases with adoptive cell therapy[J].Clinical Cancer Research,2010,16(19):4892-4898.
[20] CHANDRAN SS,SOMERVILLE RPT,YANG JC,et al.Treatment of metastatic uveal melanoma with adoptive transfer of tumour-infiltrating lymphocytes:a single-centre,two-stage,single-arm,phase 2 study[J].The Lancet Oncology,2017,18(6):792-802.
[21] DAFNI U,MICHIELIN O,LLUESMA SM,et al.Efficacy of adoptive therapy with tumor-infiltrating lymphocytes and recombinant interleukin-2 in advanced cutaneous melanoma:a systematic review and meta-analysis[J].Annals of Oncology,2019,30(12):1902-1913.
[22] SARNAIK AA,HAMID O,KHUSHALANI NI,et al.Lifileucel,a tumor-infiltrating lymphocyte therapy,in metastatic melanoma[J].Journal of Clinical Oncology,2021,39(24):2656-2666.
[23] RATTO GB,ZINO P,MIRABELLI S,et al.A randomized trial of adoptive immunotherapy with tumor-infiltrating lymphocytes and interleukin-2 versus standard therapy in the postoperative treatment of resected nonsmall cell lung cancer[J].Cancer,1996,78(2):244-251.
[24] RATTO GB,MELIOLI G,ZINO P,et al.Immunotherapy with the use of tumor-infiltrating lymphocytes and interleukin-2 as adjuvant treatment in stage III non-small-cell lung cancer:A pilot study[J].The Journal of Thoracic and Cardiovascular Surgery,1995,109(6):1212-1217.
[25] CREELAN BC,WANG C,TEER JK,et al.Tumor-infiltrating lymphocyte treatment for anti-PD-1-resistant metastatic lung cancer:a phase 1 trial[J].Nature Medicine,2021,27(8):1410-1418.
[26] LEE SM,HAIGENTZ M,VILLARUZ LC,et al.A phase 2 study to assess the efficacy and safety of autologous tumor-infiltrating lymphocytes(TIL,LN-145) alone and in combination with anti-PD-L1 inhibitor durvalumab in patients with locally advanced or metastatic NSCLC[J].Journal of Clinical Oncology,2018,36(15_suppl):TPS3107.
[27] STEVANOVIC S,DRAPER LM,LANGHAN MM,et al.Complete regression of metastatic cervical cancer after treatment with human papillomavirus-targeted tumor-infiltrating T cells[J].Journal of Clinical Oncology,2015,33(14):1543-1550.
[28] STEVANOVIC S,HELMAN SR,WUNDERLICH JR,et al.A phase II study of tumor-infiltrating lymphocyte therapy for human papillomavirus-associated epithelial cancers[J].Clinical Cancer Research,2019,25(5):1486-1493.
[29] HUANG H,NIE CP,LIU XF,et al.Phase I study of adjuvant immunotherapy with autologous tumor-infiltrating lymphocytes in locally advanced cervical cancer[J].The Journal of Clinical Investigation,2022,132(15):e157726.
[30] GUO J,LUO N,AI G,et al.Eradicating tumor in a recurrent cervical cancer patient with autologous tumor-infiltrating lymphocytes and a modified lymphodepleting regimen[J].Journal for Immunotherapy of Cancer,2022,10(2):e003887.
[31] JAZAERI AA,ZSIROS E,AMARIA RN,et al.Safety and efficacy of adoptive cell transfer using autologous tumor infiltrating lymphocytes(LN-145) for treatment of recurrent,metastatic,or persistent cervical carcinoma[J].Journal of Clinical Oncology,2019,37(15_suppl):2538.
[32] ZACHARAKIS N,CHINNASAMY H,BLACK M,et al.Immune recognition of somatic mutations leading to complete durable regression in metastatic breast cancer[J].Nature Medicine,2018,24(6):724-730.
[33] ZACHARAKIS N,HUQ LM,SEITTER SJ,et al.Breast cancers are immunogenic:Immunologic analyses and a phase II pilot clinical trial using mutation-reactive autologous lymphocytes[J].Journal of Clinical Oncology,2022,40(16):1741-1754.
[34] SONG H,WANG H,GONG M,et al.Augmentation of antitumor function of tumor-infiltrating lymphocytes against triple-negative breast cancer by PD-1 blockade[J].Cell Biology International,2022,46(2):278-287.
[35] AOKI Y,TAKAKUWA K,KODAMA S,et al.Use of adoptive transfer of tumor-infiltrating lymphocytes alone or in combination with cisplatin-containing chemotherapy in patients with epithelial ovarian cancer[J].Cancer Research,1991,51(7):1934-1939.
[36] FREEDMAN RS,EDWARDS CL,KAVANAGH JJ,et al.Intraperitoneal adoptive immunotherapy of ovarian carcinoma with tumor-infiltrating lymphocytes and low-dose recombinant interleukin-2:a pilot trial[J].Journal of Immunotherapy with Emphasis on Tumor Immunology,1994,16(3):198-210.
[37] PEDERSEN M,WESTERGAARD MCW,MILNE K,et al.Adoptive cell therapy with tumor-infiltrating lymphocytes in patients with metastatic ovarian cancer:a pilot study[J].Oncoimmunology,2018,7(12):e1502905.
[38] LI J,CHEN QY,HE J,et al.Phase I trial of adoptively transferred tumor-infiltrating lymphocyte immunotherapy following concurrent chemoradiotherapy in patients with locoregionally advanced nasopharyngeal carcinoma[J].Oncoimmunology,2015,4(2):e976507.
[39] SHI J,LI M,YANG R.Tumor-infiltrating lymphocytes as a feasible adjuvant immunotherapy for osteosarcoma with a poor response to neoadjuvant chemotherapy[J].Immunotherapy,2020,12(9):641-652.
[40] LEIDNER RS,SUKARI A,CHUNG CH,et al.A phase 2,multicenter study to evaluate the efficacy and safety of autologous tumor infiltrating lymphocytes(LN-145) for the treatment of patients with recurrent and/or metastatic squamous cell carcinoma of the head and neck(HNSCC)[J].Journal of Clinical Oncology,2018,36(15_suppl):TPS6096.
[41] POCH M,HALL M,JOERGER A,et al.Expansion of tumor infiltrating lymphocytes(TIL)from bladder cancer[J].Oncoimmunology,2018,7(9):e1476816.
[42] BRAUN MW,ABDELHAKIM H,LI M,et al.Adherent cell depletion promotes the expansion of renal cell carcinoma infiltrating T cells with optimal characteristics for adoptive transfer[J].Journal for Immunotherapy of Cancer,2020,8(2):e000706.
[43] AYDIN AM,HALL M,BUNCH BL,et al.Expansion of tumor-infiltrating lymphocytes(TIL) from penile cancer patients[J].International Immunopharmacology,2021,94:107481.
[44] KO A,COWARD VS,GOKGOZ N,et al.Investigating the potential of isolating and expanding tumour-infiltrating lymphocytes from adult sarcoma[J].Cancers,2022,14(3):548.
[45] LIU Z,MENG Q,BARTEK J,et al.Tumor-infiltrating lymphocytes(TILs)from patients with glioma[J].Oncoimmunology,2017,6(2):e1252894.
[46] MENG Q,LIU Z,RANGELOVA E,et al.Expansion of tumor-reactive T cells from patients with pancreatic cancer[J].Journal of Immunotherapy(Hagerstown,Md.1997),2016,39(2):81-89.
[47] HUSE M.The T-cell-receptor signaling network[J].Journal of Cell Science,2009,122(Pt 9):1269-1273.
[48] POL JG,CAUDANA P,PAILLET J,et al.Effects of interleukin-2 in immunostimulation and immunosuppression[J].The Journal of Experimental Medicine,2020,217(1):e20191247.
[49] KVERNELAND AH,CHAMBERLAIN CA,BORCH TH,et al.Adoptive cell therapy with tumor-infiltrating lymphocytes supported by checkpoint inhibition across multiple solid cancer types[J].Journal for Immunotherapy of Cancer,2021,9(10):e003499.
[50] RADVANYI LG,BERNATCHEZ C,ZHANG M,et al.Specific lymphocyte subsets predict response to adoptive cell therapy using expanded autologous tumor-infiltrating lymphocytes in metastatic melanoma patients[J].Clinical Cancer Research,2012,18(24):6758-6770.
[51] ZHOU J,SHEN X,HUANG J,et al.Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy[J].Journal of Immunology(Baltimore,Md.1950),2005,175(10):7046-7052.
[52] KRISTENSEN NP,HEEKE C,TVINGSHOLM SA,et al.Neoantigen-reactive CD8+ T cells affect clinical outcome of adoptive cell therapy with tumor-infiltrating lymphocytes in melanoma[J].The Journal of Clinical Investigation,2022,132(2):e150535.
[53] KIM SP,VALE NR,ZACHARAKIS N,et al.Adoptive cellular therapy with autologous tumor-infiltrating lymphocytes and T-cell receptor-engineered T cells targeting common p53 neoantigens in human solid tumors[J].Cancer Immunology Research,2022,10(8):932-946.
[54] CHU J,WANG C,MA Q,et al.Coupling programmed cell death 1-positive tumor-infiltrating T cells with anti-programmed cell death 1 antibody improves the efficacy of adoptive T-cell therapy[J].Cytotherapy,2022,24(3):291-301.
[55] PARKHURST M,GROS A,PASETTO A,et al.Isolation of T-cell receptors specifically reactive with mutated tumor-associated antigens from tumor-infiltrating lymphocytes based on CD137 expression[J].Clinical Cancer Research,2017,23(10):2491-2505.
[56] DUHEN R,BALLESTEROS-MERINO C,FRYE A K,et al.Neoadjuvant anti-OX40(MEDI6469)therapy in patients with head and neck squamous cell carcinoma activates and expands antigen-specific tumor-infiltrating T cells[J].Nature Communications,2021,12(1):1047.
[57] KRISHNA S,LOWERY FJ,COPELAND AR,et al.Stem-like CD8 T cells mediate response of adoptive cell immunotherapy against human cancer[J].Science(New York),2020,370(6522):1328-1334.
[58] DIAZ-CANO I,PAZ-ARES L,OTANO I.Adoptive tumor infiltrating lymphocyte transfer as personalized immunotherapy[J].International Review of Cell and Molecular Biology,2022,370:163-192.
[59] FREEMAN P,MIELGO A.Cancer-associated fibroblast mediated inhibition of CD8+ cytotoxic T cell accumulation in tumours:Mechanisms and therapeutic opportunities[J].Cancers,2020,12(9):2687.
[60] LI X,XIANG Y,LI F,et al.WNT/β-Catenin signaling pathway regulating T cell-inflammation in the tumor microenvironment[J].Frontiers in Immunology,2019,10:2293.
[61] GALLUZZI L,SPRANGER S,FUCHS E,et al.WNT signaling in cancer immunosurveillance[J].Trends in Cell Biology,2019,29(1):44-65.
[62] XIA L,OYANG L,LIN J,et al.The cancer metabolic reprogramming and immune response[J].Molecular Cancer,2021,20(1):28.
[63] WANG Y,WANG C,HUANG M,et al.Pilot study of a novel nanobody 68 Ga-NODAGA-SNA006 for instant PET imaging of CD8+ T cells[J].European Journal of Nuclear Medicine and Molecular Imaging,2022,49(13):4394-4405.
[64] SEITTER SJ,SHERRY RM,YANG JC,et al.Impact of prior treatment on the efficacy of adoptive transfer of tumor-infiltrating lymphocytes in patients with metastatic melanoma[J].Clinical Cancer Research,2021,27(19):5289-5298.
[65] FORGET MA,HAYMAKER C,HESS KR,et al.Prospective analysis of adoptive TIL therapy in patients with metastatic melanoma:Response,impact of anti-CTLA4,and biomarkers to predict clinical outcome[J].Clinical Cancer Research,2018,24(18):4416-4428.
[66] SABERIAN C,AMARIA RN,NAJJAR AM,et al.Randomized phase II trial of lymphodepletion plus adoptive cell transfer of tumor-infiltrating lymphocytes,with or without dendritic cell vaccination,in patients with metastatic melanoma[J].Journal for Immunotherapy of Cancer,2021,9(5):e002449.
[67] BORCH TH,HARBST K,RANA AH,et al.Clinical efficacy of T-cell therapy after short-term BRAF-inhibitor priming in patients with checkpoint inhibitor-resistant metastatic melanoma[J].Journal for Immunotherapy of Cancer,2021,9(7):e002703.
[68] ZHANG J,ENDRES S,KOBOLD S.Enhancing tumor T cell infiltration to enable cancer immunotherapy[J].Immunotherapy,2019,11(3):201-213.
[69] BINNEWIES M,POLLACK JL,RUDOLPH J,et al.Targeting TREM2 on tumor-associated macrophages enhances immunotherapy[J].Cell Reports,2021,37(3):109844.
[70] WANG Y,WANG C,QIU J,et al.Targeting CD96 overcomes PD-1 blockade resistance by enhancing CD8+ TIL function in cervical cancer[J].Journal for Immunotherapy of Cancer,2022,10(3):e003667.
[71] WU J,CHEN Z,WICKSTRM SL,et al.Interleukin-33 is a novel immunosuppressor that protects cancer cells from TIL killing by a macrophage-mediated shedding mechanism[J].Advanced Science(Weinheim,Baden-Wurttemberg,Germany),2021,8(21):e2101029.
[72] CHAMBERLAIN CA,BENNETT EP,KVERNELAND AH,et al.Highly efficient PD-1-targeted CRISPR-Cas9 for tumor-infiltrating lymphocyte-based adoptive T cell therapy[J].Molecular Therapy Oncolytics,2022,24:417-428.

Memo

Memo:
National Natural Science Foundation of China(No.82104318);国家自然科学基金(编号:82104318)
Last Update: 2023-09-28