Citation: | BU Yi-chao, FU Xiu-tao, DING Zhen-bin, et al. Research progress on trained immunity in tumor multimodality therapy[J]. Chin J Clin Med, 2023, 30(5): 861-869. DOI: 10.12025/j.issn.1008-6358.2023.20231381 |
The classical immune system is divided into innate immunity and acquired immunity. The general view is that immune memory exists only in acquired immunity. However, in organisms lacking adaptive immunity, cells of the innate immune system are able to acquire memory signatures after a brief stimulus, thereby enhancing the response upon a secondary stimulus, a phenomenon known as training immunity. Trained immunity can play a unique anti-tumor role in tumors. In bladder cancer, training immunity induced by BCG vaccine has become the standard treatment for bladder cancer. The efficacy of BCG in the treatment of melanoma has also been recognized in recent years. Improving immune training during therapy through irreversible electroporation (IRE) can prolong survival in patients with pancreatic cancer. Whole β-glucan particle (WGP) can inhibit tumor lung metastasis. In breast cancer, the introduction of drugs through nanoparticles (NPs) can improve the training immune effect of targeted sites. This paper reviews the concepts, mechanisms, and current status of training immunity in the field of oncology therapy.
[1] |
KURTZ J. Specific memory within innate immune systems[J]. Trends Immunol, 2005, 26(4): 186-192. DOI: 10.1016/j.it.2005.02.001
|
[2] |
QUINTIN J, CHENG S C, VAN DER MEER J W, et al. Innate immune memory: towards a better understanding of host defense mechanisms[J]. Curr Opin Immunol, 2014, 29: 1-7. DOI: 10.1016/j.coi.2014.02.006
|
[3] |
NETEA M G, JOOSTEN L A B. Trained immunity and local innate immune memory in the lung[J]. Cell, 2018, 175(6): 1463-1465. DOI: 10.1016/j.cell.2018.11.007
|
[4] |
KLEINNIJENHUIS J, QUINTIN J, PREIJERS F, et al. Long-lasting effects of BCG vaccination on both heterologous Th1/Th17 responses and innate trained immunity[J]. J Innate Immun, 2014, 6(2): 152-158. DOI: 10.1159/000355628
|
[5] |
COOPER M A, ELLIOTT J M, KEYEL P A, et al. Cytokine-induced memory-like natural killer cells[J]. Proc Natl Acad Sci U S A, 2009, 106(6): 1915-1919. DOI: 10.1073/pnas.0813192106
|
[6] |
ROQUILLY A, MCWILLIAM H E G, JACQUELINE C, et al. Local modulation of antigen-presenting cell development after resolution of pneumonia induces long-term susceptibility to secondary infections[J]. Immunity, 2017, 47(1): 135-147. e5. DOI: 10.1016/j.immuni.2017.06.021
|
[7] |
WEIZMAN O E, SONG E, ADAMS N M, et al. Mouse cytomegalovirus-experienced ILC1s acquire a memory response dependent on the viral glycoprotein m12[J]. Nat Immunol, 2019, 20(8): 1004-1011. DOI: 10.1038/s41590-019-0430-1
|
[8] |
MARTINEZ-GONZALEZ I, MATHÄ L, STEER C A, et al. Allergen-experienced group 2 innate lymphoid cells acquire memory-like properties and enhance allergic lung inflammation[J]. Immunity, 2016, 45(1): 198-208. DOI: 10.1016/j.immuni.2016.06.017
|
[9] |
CASSONE A. The case for an expanded concept of trained immunity[J]. mBio, 2018, 9(3): e00570-e00518.
|
[10] |
NAIK S, LARSEN S B, GOMEZ N C, et al. Inflammatory memory sensitizes skin epithelial stem cells to tissue damage[J]. Nature, 2017, 550(7677): 475-480. DOI: 10.1038/nature24271
|
[11] |
ORDOVAS-MONTANES J, DWYER D F, NYQUIST S K, et al. Allergic inflammatory memory in human respiratory epithelial progenitor cells[J]. Nature, 2018, 560(7720): 649-654. DOI: 10.1038/s41586-018-0449-8
|
[12] |
JENSEN K J, LARSEN N, BIERING-SØRENSEN S, et al. Heterologous immunological effects of early BCG vaccination in low-birth-weight infants in Guinea-Bissau: a randomized-controlled trial[J]. J Infect Dis, 2015, 211(6): 956-967. DOI: 10.1093/infdis/jiu508
|
[13] |
RIECKMANN A, VILLUMSEN M, SØRUP S, et al. Vaccinations against smallpox and tuberculosis are associated with better long-term survival: a Danish case-cohort study 1971-2010[J]. Int J Epidemiol, 2017, 46(2): 695-705.
|
[14] |
SCHRUM J E, CRABTREE J N, DOBBS K R, et al. Cutting edge: Plasmodium falciparum induces trained innate immunity[J]. J Immunol, 2018, 200(4): 1243-1248. DOI: 10.4049/jimmunol.1701010
|
[15] |
IFRIM D C, QUINTIN J, JOOSTEN L A, et al. Trained immunity or tolerance: opposing functional programs induced in human monocytes after engagement of various pattern recognition receptors[J]. Clin Vaccine Immunol, 2014, 21(4): 534-545. DOI: 10.1128/CVI.00688-13
|
[16] |
BEKKERING S, QUINTIN J, JOOSTEN L A, et al. Oxidized low-density lipoprotein induces long-term proinflammatory cytokine production and foam cell formation via epigenetic reprogramming of monocytes[J]. Arterioscler Thromb Vasc Biol, 2014, 34(8): 1731-1738. DOI: 10.1161/ATVBAHA.114.303887
|
[17] |
SOHRABI Y, SONNTAG G V H, BRAUN L C, et al. LXR activation induces a proinflammatory trained innate immunity-phenotype in human monocytes[J]. Front Immunol, 2020, 11: 353. DOI: 10.3389/fimmu.2020.00353
|
[18] |
VAN DER HEIJDEN C D C C, KEATING S T, GROH L, et al. Aldosterone induces trained immunity: the role of fatty acid synthesis[J]. Cardiovasc Res, 2020, 116(2): 317-328.
|
[19] |
KAMADA R, YANG W J, ZHANG Y B, et al. Interferon stimulation creates chromatin marks and establishes transcriptional memory[J]. Proc Natl Acad Sci U S A, 2018, 115(39): E9162-E9171.
|
[20] |
VAN DER HEIJDEN C D C C, GROH L, KEATING S T, et al. Catecholamines induce trained immunity in monocytes in vitro and in vivo[J]. Circ Res, 2020, 127(2): 269-283. DOI: 10.1161/CIRCRESAHA.119.315800
|
[21] |
TERCAN H, RIKSEN N P, JOOSTEN L A B, et al. Trained immunity: long-term adaptation in innate immune responses[J]. Arterioscler Thromb Vasc Biol, 2021, 41(1): 55-61.
|
[22] |
NETEA M G, DOMÍNGUEZ-ANDRÉS J, BARREIRO L B, et al. Defining trained immunity and its role in health and disease[J]. Nat Rev Immunol, 2020, 20(6): 375-388. DOI: 10.1038/s41577-020-0285-6
|
[23] |
NOVAKOVIC B, HABIBI E, WANG S Y, et al. β-glucan reverses the epigenetic state of LPS-induced immunological tolerance[J]. Cell, 2016, 167(5): 1354-1368. e14. DOI: 10.1016/j.cell.2016.09.034
|
[24] |
LEE J, ZHANG T X, HWANG I, et al. Epigenetic modification and antibody-dependent expansion of memory-like NK cells in human cytomegalovirus-infected individuals[J]. Immunity, 2015, 42(3): 431-442. DOI: 10.1016/j.immuni.2015.02.013
|
[25] |
RODRIGUEZ R M, SUAREZ-ALVAREZ B, LOPEZ-LARREA C. Therapeutic epigenetic reprogramming of trained immunity in myeloid cells[J]. Trends Immunol, 2019, 40(1): 66-80. DOI: 10.1016/j.it.2018.11.006
|
[26] |
YOSHIDA K, MAEKAWA T, ZHU Y J, et al. The transcription factor ATF7 mediates lipopolysaccharide-induced epigenetic changes in macrophages involved in innate immunological memory[J]. Nat Immunol, 2015, 16(10): 1034-1043. DOI: 10.1038/ni.3257
|
[27] |
IFRIM D C, QUINTIN J, MEERSTEIN-KESSEL L, et al. Defective trained immunity in patients with STAT-1-dependent chronic mucocutaneaous candidiasis[J]. Clin Exp Immunol, 2015, 181(3): 434-440. DOI: 10.1111/cei.12642
|
[28] |
LEOPOLD WAGER C M, HOLE C R, CAMPUZANO A, et al. IFN-γ immune priming of macrophages in vivo induces prolonged STAT1 binding and protection against Cryptococcus neoformans[J]. PLoS Pathog, 2018, 14(10): e1007358. DOI: 10.1371/journal.ppat.1007358
|
[29] |
FANUCCHI S, FOK E T, DALLA E, et al. Immune genes are primed for robust transcription by proximal long noncoding RNAs located in nuclear compartments[J]. Nat Genet, 2019, 51(1): 138-150. DOI: 10.1038/s41588-018-0298-2
|
[30] |
NETEA M G, GIAMARELLOS-BOURBOULIS E J, DOMÍNGUEZ-ANDRÉS J, et al. Trained immunity: a tool for reducing susceptibility to and the severity of SARS-CoV-2 infection[J]. Cell, 2020, 181(5): 969-977. DOI: 10.1016/j.cell.2020.04.042
|
[31] |
JHA A K, HUANG S C, SERGUSHICHEV A, et al. Network integration of parallel metabolic and transcriptional data reveals metabolic modules that regulate macrophage polarization[J]. Immunity, 2015, 42(3): 419-430. DOI: 10.1016/j.immuni.2015.02.005
|
[32] |
CHENG S C, QUINTIN J, CRAMER R A, et al. mTOR- and HIF-1α-mediated aerobic glycolysis as metabolic basis for trained immunity[J]. Science, 2014, 345(6204): 1250684. DOI: 10.1126/science.1250684
|
[33] |
ARTS R J, NOVAKOVIC B, TER HORST R, et al. Glutaminolysis and fumarate accumulation integrate immunometabolic and epigenetic programs in trained immunity[J]. Cell Metab, 2016, 24(6): 807-819. DOI: 10.1016/j.cmet.2016.10.008
|
[34] |
BEKKERING S, ARTS R J W, NOVAKOVIC B, et al. Metabolic induction of trained immunity through the mevalonate pathway[J]. Cell, 2018, 172(1-2): 135-146. e9. DOI: 10.1016/j.cell.2017.11.025
|
[35] |
KAUFMANN E, SANZ J, DUNN J L, et al. BCG educates hematopoietic stem cells to generate protective innate immunity against tuberculosis[J]. Cell, 2018, 172(1-2): 176-190. e19. DOI: 10.1016/j.cell.2017.12.031
|
[36] |
MIYAKE M, NISHIMURA N, ODA Y, et al. Intravesical Bacillus Calmette-Guerin treatment-induced sleep quality deterioration in patients with non-muscle invasive bladder cancer: functional outcome assessment based on a questionnaire survey and actigraphy[J]. Support Care Cancer, 2022, 30(1): 887-895. DOI: 10.1007/s00520-021-06468-3
|
[37] |
VAN PUFFELEN J H, KEATING S T, OOSTERWIJK E, et al. Trained immunity as a molecular mechanism for BCG immunotherapy in bladder cancer[J]. Nat Rev Urol, 2020, 17(9): 513-525. DOI: 10.1038/s41585-020-0346-4
|
[38] |
YANG J, JONES M S, RAMOS R I, et al. Insights into local tumor microenvironment immune factors associated with regression of cutaneous melanoma metastases by Mycobacterium bovis bacille Calmette-Guérin[J]. Front Oncol, 2017, 7: 61.
|
[39] |
BENITEZ M L R, BENDER C B, OLIVEIRA T L, et al. Mycobacterium bovis BCG in metastatic melanoma therapy[J]. Appl Microbiol Biotechnol, 2019, 103(19): 7903-7916. DOI: 10.1007/s00253-019-10057-0
|
[40] |
GELLER A E, SHRESTHA R, WOESTE M R, et al. The induction of peripheral trained immunity in the pancreas incites anti-tumor activity to control pancreatic cancer progression[J]. Nat Commun, 2022, 13(1): 759. DOI: 10.1038/s41467-022-28407-4
|
[41] |
LIU J J, GUNN L, HANSEN R, et al. Combined yeast-derived beta-glucan with anti-tumor monoclonal antibody for cancer immunotherapy[J]. Exp Mol Pathol, 2009, 86(3): 208-214. DOI: 10.1016/j.yexmp.2009.01.006
|
[42] |
WOESTE M R, SHRESTHA R, GELLER A E, et al. Irreversible electroporation augments β-glucan induced trained innate immunity for the treatment of pancreatic ductal adenocarcinoma[J]. J Immunother Cancer, 2023, 11(4): e006221. DOI: 10.1136/jitc-2022-006221
|
[43] |
RUARUS A H, VROOMEN L G P H, GEBOERS B, et al. Percutaneous irreversible electroporation in locally advanced and recurrent pancreatic cancer (PANFIRE-2): a multicenter, prospective, single-arm, phaseⅡstudy[J]. Radiology, 2020, 294(1): 212-220. DOI: 10.1148/radiol.2019191109
|
[44] |
DING C L, SHRESTHA R, ZHU X J, et al. Inducing trained immunity in pro-metastatic macrophages to control tumor metastasis[J]. Nat Immunol, 2023, 24(2): 239-254. DOI: 10.1038/s41590-022-01388-8
|
[45] |
ZANGANEH S, HUTTER G, SPITLER R, et al. Iron oxide nanoparticles inhibit tumour growth by inducing pro-inflammatory macrophage polarization in tumour tissues[J]. Nat Nanotechnol, 2016, 11(11): 986-994. DOI: 10.1038/nnano.2016.168
|
[46] |
CHEN Q, SUN L J, CHEN Z J. Regulation and function of the cGAS-STING pathway of cytosolic DNA sensing[J]. Nat Immunol, 2016, 17(10): 1142-1149. DOI: 10.1038/ni.3558
|
[47] |
ZARENEZHAD E, KANAAN M H G, ABDOLLAH S S, et al. Metallic nanoparticles: their potential role in breast cancer immunotherapy via trained immunity provocation[J]. Biomedicines, 2023, 11(5): 1245. DOI: 10.3390/biomedicines11051245
|
[48] |
LEBRE F, BOLAND J B, GOUVEIA P, et al. Pristine graphene induces innate immune training[J]. Nanoscale, 2020, 12(20): 11192-11200. DOI: 10.1039/C9NR09661B
|