Decoding the secret of extracellular vesicles in the immune tumor microenvironment of the glioblastoma: on the border of kingdoms.
extracellular vesicles
glioblastoma
immune responses
immune tumor microenvironment
immunotherapies
intratumoral microbiome
tumor progression
Journal
Frontiers in immunology
ISSN: 1664-3224
Titre abrégé: Front Immunol
Pays: Switzerland
ID NLM: 101560960
Informations de publication
Date de publication:
2024
2024
Historique:
received:
25
04
2024
accepted:
06
08
2024
medline:
13
9
2024
pubmed:
13
9
2024
entrez:
13
9
2024
Statut:
epublish
Résumé
Over the last decades, extracellular vesicles (EVs) have become increasingly popular for their roles in various pathologies, including cancer and neurological and immunological disorders. EVs have been considered for a long time as a means for normal cells to get rid of molecules it no longer needs. It is now well established that EVs play their biological roles also following uptake or by the interaction of EV surface proteins with cellular receptors and membranes. In this review, we summarize the current status of EV production and secretion in glioblastoma, the most aggressive type of glioma associated with high mortality. The main purpose is to shed light on the EVs as a universal mediator of interkingdom and intrakingdom communication in the context of tumor microenvironment heterogeneity. We focus on the immunomodulatory EV functions in glioblastoma-immune cross-talk to enhance immune escape and reprogram tumor-infiltrating immune cells. We critically examine the evidence that GBM-, immune cell-, and microbiome-derived EVs impact local tumor microenvironment and host immune responses, and can enter the circulatory system to disseminate and drive premetastatic niche formation in distant organs. Taking into account the current state of the art in intratumoral microbiome studies, we discuss the emerging role of bacterial EV in glioblastoma and its response to current and future therapies including immunotherapies.
Identifiants
pubmed: 39267734
doi: 10.3389/fimmu.2024.1423232
pmc: PMC11390556
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
1423232Informations de copyright
Copyright © 2024 Ghazi, Harmak, Rghioui, Kone, El Ghanmi and Badou.
Déclaration de conflit d'intérêts
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Références
NPJ Precis Oncol. 2024 May 17;8(1):103
pubmed: 38760427
Oncoimmunology. 2018 Aug 6;7(10):e1478647
pubmed: 30288344
Front Cell Infect Microbiol. 2023 Apr 27;13:1165790
pubmed: 37180444
Blood. 2012 Jan 19;119(3):756-66
pubmed: 22031862
Nat Med. 2006 Dec;12(12):1365-71
pubmed: 17115046
Front Immunol. 2022 Feb 18;12:774103
pubmed: 35250965
Nat Cell Biol. 2008 Dec;10(12):1470-6
pubmed: 19011622
Sci Rep. 2021 Nov 2;11(1):21504
pubmed: 34728682
Science. 2012 Aug 31;337(6098):1111-5
pubmed: 22821982
J Clin Neurosci. 2009 Jun;16(6):748-54
pubmed: 19324552
J Autoimmun. 2011 Nov;37(3):242-53
pubmed: 21795021
J Cell Mol Med. 2018 Mar;22(3):2001-2006
pubmed: 29377463
Nature. 2014 Mar 6;507(7490):118-23
pubmed: 24487619
Oncogene. 2020 Jan;39(2):428-442
pubmed: 31485019
Cancer Discov. 2018 Apr;8(4):403-416
pubmed: 29567829
Science. 2018 May 25;360(6391):
pubmed: 29798856
Mol Cell Proteomics. 2018 Feb;17(2):205-215
pubmed: 29203497
J Pathol. 2008 Sep;216(1):15-24
pubmed: 18553315
EBioMedicine. 2019 Mar;41:225-235
pubmed: 30737083
Front Cell Neurosci. 2022 Sep 09;16:819363
pubmed: 36159398
Cancer Epidemiol Biomarkers Prev. 2019 Dec;28(12):2030-2037
pubmed: 31519703
Nat Commun. 2014 Nov 25;5:5488
pubmed: 25421927
Int J Cancer. 2015 Oct 1;137(7):1630-42
pubmed: 25802036
Biomed Pharmacother. 2018 Dec;108:1451-1459
pubmed: 30372847
Front Immunol. 2021 Jul 09;12:679425
pubmed: 34305910
Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2019 Mar;11(2):e1523
pubmed: 29701017
Cell. 2019 Aug 8;178(4):795-806.e12
pubmed: 31398337
Br J Cancer. 2021 Aug;125(3):313-323
pubmed: 33824481
Circulation. 2021 Apr 6;143(14):1426-1449
pubmed: 33819075
Front Cell Dev Biol. 2023 Mar 07;11:1060000
pubmed: 36960410
Cell Death Dis. 2020 Oct 22;11(10):896
pubmed: 33093453
J Immunol. 2012 Aug 15;189(4):1747-56
pubmed: 22786771
Front Pharmacol. 2018 Feb 28;9:169
pubmed: 29541030
J Extracell Vesicles. 2014 Aug 04;3:
pubmed: 25143819
Cell Rep. 2020 Feb 18;30(7):2065-2074.e4
pubmed: 32075753
J Neuroimmunol. 2016 Jan 15;290:103-8
pubmed: 26711578
Thromb Haemost. 2014 Dec;112(6):1219-29
pubmed: 25209750
Semin Cell Dev Biol. 2015 Apr;40:17-26
pubmed: 25721810
ACS Nano. 2020 Dec 22;14(12):16698-16711
pubmed: 33232124
Pol Arch Med Wewn. 2008 Jun;118(6):345-50
pubmed: 18619189
Oncoimmunology. 2018 Jan 16;7(4):e1412909
pubmed: 29632728
Trends Cell Biol. 2023 Aug;33(8):667-681
pubmed: 36737375
Proc Natl Acad Sci U S A. 2012 Mar 13;109(11):4146-51
pubmed: 22315426
Front Immunol. 2019 Apr 09;10:683
pubmed: 31024540
Int J Mol Sci. 2023 Apr 03;24(7):
pubmed: 37047660
Parasitol Res. 2015 May;114(5):1865-73
pubmed: 25855345
N Engl J Med. 2023 Feb 2;388(5):427-438
pubmed: 36724329
J Extracell Vesicles. 2022 Jan;11(1):e12151
pubmed: 35041249
Sci Rep. 2019 Jan 14;9(1):96
pubmed: 30643174
Stem Cells Int. 2018 May 27;2018:9863194
pubmed: 29977309
J Extracell Vesicles. 2012 Sep 11;1:
pubmed: 24009881
Blood. 2004 Nov 1;104(9):2761-6
pubmed: 15242875
Oncoimmunology. 2021 Feb 10;10(1):1883890
pubmed: 33628625
Cancer Res. 2014 Oct 15;74(20):5758-71
pubmed: 25261234
Science. 2018 Mar 23;359(6382):1366-1370
pubmed: 29567708
Front Immunol. 2018 May 23;9:1111
pubmed: 29875772
BMC Cancer. 2018 Jan 6;18(1):47
pubmed: 29306323
PLoS Comput Biol. 2013;9(6):e1003107
pubmed: 23840181
Neuro Oncol. 2016 Jan;18(1):58-69
pubmed: 26433199
Philos Trans R Soc Lond B Biol Sci. 2018 Jan 5;373(1737):
pubmed: 29158317
Curr Biol. 2009 Dec 1;19(22):1875-85
pubmed: 19896381
Nano Lett. 2020 Jan 8;20(1):11-21
pubmed: 31858807
Brain Tumor Pathol. 2019 Apr;36(2):29-39
pubmed: 30859343
Nat Commun. 2019 Jul 5;10(1):3000
pubmed: 31278254
Curr Opin Genet Dev. 2015 Feb;30:17-24
pubmed: 25616158
Front Cell Dev Biol. 2022 Nov 16;10:996805
pubmed: 36467419
Lancet Oncol. 2019 Feb;20(2):e77-e91
pubmed: 30712808
Front Mol Biosci. 2023 Mar 14;10:1172797
pubmed: 36999160
Neurooncol Adv. 2022 Feb 15;4(1):vdac017
pubmed: 35990703
Neuro Oncol. 2022 Sep 1;24(9):1454-1468
pubmed: 35157758
Front Immunol. 2023 May 16;14:1173518
pubmed: 37261362
Front Immunol. 2018 May 07;9:957
pubmed: 29780392
Elife. 2019 Aug 30;8:
pubmed: 31469364
Cell. 1983 Jul;33(3):967-78
pubmed: 6307529
J Extracell Vesicles. 2015 Oct 05;4:28665
pubmed: 26443722
Cell Metab. 2008 Jan;7(1):11-20
pubmed: 18177721
Nat Genet. 2013 Oct;45(10):1141-9
pubmed: 23917401
Science. 2020 Aug 21;369(6506):936-942
pubmed: 32820119
Adv Sci (Weinh). 2022 Jul;9(21):e2200470
pubmed: 35603968
Tissue Barriers. 2017 Oct 2;5(4):e1373208
pubmed: 28956703
iScience. 2020 Aug 21;23(8):101420
pubmed: 32795915
Clin Chim Acta. 2019 Jan;488:116-121
pubmed: 30395864
Nature. 2020 Apr;580(7802):269-273
pubmed: 32106218
Acta Biomater. 2019 Jun;91:248-257
pubmed: 31003032
Front Immunol. 2018 May 08;9:1004
pubmed: 29867979
Curr Cancer Drug Targets. 2017;17(3):221-235
pubmed: 27528364
Nat Rev Nephrol. 2017 Dec;13(12):731-749
pubmed: 29081510
Ann Oncol. 2017 Jul 1;28(7):1457-1472
pubmed: 28863449
J Extracell Vesicles. 2021 Jul;10(9):e12120
pubmed: 34262675
Lancet. 2017 Sep 30;390(10102):1603-1610
pubmed: 28705462
Oncotarget. 2010 Nov;1(7):552-62
pubmed: 21317451
Mol Neurobiol. 2019 Jun;56(6):4566-4581
pubmed: 30353492
Oncoimmunology. 2015 Jun 24;5(4):e1062968
pubmed: 27141372
Trends Mol Med. 2015 Apr;21(4):233-44
pubmed: 25771098
PLoS One. 2012;7(7):e42064
pubmed: 22848702
Proc Natl Acad Sci U S A. 2013 Apr 30;110(18):7312-7
pubmed: 23589885
Biochim Biophys Acta Rev Cancer. 2017 Dec;1868(2):372-393
pubmed: 28669749
Cancer Cell. 2018 Apr 9;33(4):570-580
pubmed: 29634945
CA Cancer J Clin. 2019 Jan;69(1):7-34
pubmed: 30620402
Cell. 2019 Apr 4;177(2):428-445.e18
pubmed: 30951670
Kidney Int. 2010 Nov;78(9):838-48
pubmed: 20703216
ACS Nano. 2021 Aug 24;15(8):13826-13838
pubmed: 34382768
ACS Nano. 2014 Feb 25;8(2):1525-37
pubmed: 24410085
Front Oncol. 2022 Aug 08;12:781741
pubmed: 36003766
Front Cell Neurosci. 2018 Aug 03;12:235
pubmed: 30123112
Front Cell Infect Microbiol. 2013 Sep 06;3:49
pubmed: 24032108
Nat Commun. 2017 Sep 20;8(1):626
pubmed: 28931823
Nat Rev Neurol. 2018 Aug;14(8):482-495
pubmed: 29985475
J Immunother Cancer. 2017 Aug 15;5(1):65
pubmed: 28806909
Oncotarget. 2015 Oct 13;6(31):31413-27
pubmed: 26429879
Front Immunol. 2019 Feb 28;10:202
pubmed: 30873152
J Neurosci. 2007 Oct 17;27(42):11214-27
pubmed: 17942716
Exp Cell Res. 2017 Sep 15;358(2):421-426
pubmed: 28189637
Int J Mol Sci. 2023 Jan 10;24(2):
pubmed: 36674857
Sci Rep. 2017 Aug 1;7(1):7072
pubmed: 28765539
Cancer Res. 2017 May 1;77(9):2306-2317
pubmed: 28202510
Trends Cell Biol. 2015 Jun;25(6):364-72
pubmed: 25683921
Neuro Oncol. 2015 Aug;17(8):1064-75
pubmed: 25355681
Nature. 2015 Nov 19;527(7578):329-35
pubmed: 26524530
J Cell Biol. 2013 Feb 18;200(4):373-83
pubmed: 23420871
Asian Pac J Cancer Prev. 2013;14(1):309-14
pubmed: 23534743
Cell Commun Signal. 2021 Apr 23;19(1):47
pubmed: 33892745
Trends Mol Med. 2013 Aug;19(8):460-73
pubmed: 23773831
BMJ. 2017 Mar 15;356:j831
pubmed: 28298355
Neuro Oncol. 2018 Oct 9;20(11):1536-1546
pubmed: 29718366
Front Cell Dev Biol. 2020 Oct 02;8:573511
pubmed: 33134295
PLoS One. 2012;7(9):e45399
pubmed: 23028984
PLoS One. 2008;3(11):e3769
pubmed: 19020659
J Transl Med. 2012 Jan 05;10:5
pubmed: 22221959
Science. 2020 Feb 7;367(6478):
pubmed: 32029601
Proc Natl Acad Sci U S A. 2012 Jul 31;109(31):E2110-6
pubmed: 22753494
Nat Commun. 2017 Sep 27;8(1):709
pubmed: 28955033
Braz J Med Biol Res. 2013 Oct;46(10):824-30
pubmed: 24141609
FASEB J. 2009 May;23(5):1541-57
pubmed: 19109410
JCI Insight. 2017 Aug 3;2(15):
pubmed: 28768910
Bioconjug Chem. 2016 Oct 19;27(10):2225-2238
pubmed: 27547843
Neuro Oncol. 2022 Feb 1;24(2):184-196
pubmed: 34581817
Proteomics. 2007 Sep;7(17):3143-53
pubmed: 17787032
Front Immunol. 2024 May 28;15:1397486
pubmed: 38863709
Science. 2020 May 29;368(6494):973-980
pubmed: 32467386
Nat Commun. 2019 Jun 3;10(1):2402
pubmed: 31160588
Front Immunol. 2021 May 31;12:679954
pubmed: 34135908
Oncoimmunology. 2015 Mar 19;4(6):e1008371
pubmed: 26155418
Acta Pharm Sin B. 2020 Aug;10(8):1534-1548
pubmed: 32963948
Neurooncol Adv. 2020 May 06;2(1):vdaa056
pubmed: 32642708
Science. 2018 Nov 9;362(6415):
pubmed: 30409859
Nat Rev Mol Cell Biol. 2018 Apr;19(4):213-228
pubmed: 29339798
Trends Cell Biol. 2006 Sep;16(9):443-52
pubmed: 16879967
Philos Trans R Soc Lond B Biol Sci. 2018 Jan 5;373(1737):
pubmed: 29158308
Int J Mol Sci. 2020 Jul 27;21(15):
pubmed: 32727112
Cell Cycle. 2018;17(4):428-438
pubmed: 29468929
Pathog Dis. 2018 Mar 1;76(2):
pubmed: 29718270
J Extracell Vesicles. 2016 Jul 05;5:30741
pubmed: 27389011
Cell. 2013 Oct 10;155(2):462-77
pubmed: 24120142
Nat Rev Rheumatol. 2014 Jun;10(6):356-64
pubmed: 24535546
J Neuropathol Exp Neurol. 2006 Jun;65(6):529-39
pubmed: 16783163
J Cell Biol. 1985 Sep;101(3):942-8
pubmed: 2993317
J Autoimmun. 2018 Dec;95:100-123
pubmed: 30509385
Bioscience. 2015 Aug 1;65(8):783-797
pubmed: 26955082
Cancer Cell. 2021 Oct 11;39(10):1317-1341
pubmed: 34506740
Proteomics. 2011 Jul;11(13):2745-51
pubmed: 21630462
Int J Mol Sci. 2019 Dec 22;21(1):
pubmed: 31877909
Nat Cell Biol. 2007 Jun;9(6):654-9
pubmed: 17486113
Nat Rev Microbiol. 2019 Jan;17(1):13-24
pubmed: 30397270
JCI Insight. 2016;1(2):
pubmed: 26973881
J Immunol Methods. 2004 Nov;294(1-2):15-22
pubmed: 15604012
Nat Protoc. 2020 Jan;15(1):40-67
pubmed: 31776460
Neuro Oncol. 2016 Apr;18(4):497-506
pubmed: 26385614
Cancer Res. 2009 Jul 1;69(13):5601-9
pubmed: 19549916
Immunohorizons. 2021 Aug 17;5(8):647-658
pubmed: 34404719
Proc Natl Acad Sci U S A. 2016 Feb 23;113(8):E968-77
pubmed: 26858453
Nat Rev Mol Cell Biol. 2022 May;23(5):369-382
pubmed: 35260831
Sci Transl Med. 2015 Dec 16;7(318):318ra200
pubmed: 26676607
J Genet Genomics. 2017 Nov 20;44(11):519-530
pubmed: 29169920
Cell Death Differ. 2008 Jan;15(1):183-91
pubmed: 17932498
J Extracell Vesicles. 2022 Jan;11(1):e12190
pubmed: 35041301
Cell Rep. 2020 Feb 25;30(8):2489-2500.e5
pubmed: 32101730
PLoS One. 2012;7(12):e50946
pubmed: 23284651
Oncotarget. 2015 May 10;6(13):11327-41
pubmed: 25857301
Nature. 2020 Mar;579(7800):567-574
pubmed: 32214244
Immunol Cell Biol. 2018 May 8;:
pubmed: 29738615
Mol Cancer. 2019 Mar 30;18(1):59
pubmed: 30925927
Cancer Gene Ther. 2023 Mar;30(3):481-496
pubmed: 36494582
J Extracell Vesicles. 2015 May 14;4:27066
pubmed: 25979354
J Biochem Mol Biol. 2003 Jan 31;36(1):49-59
pubmed: 12542975
Front Immunol. 2018 Jun 28;9:1486
pubmed: 30002658
J Immunol. 2009 Sep 15;183(6):3720-30
pubmed: 19692638
Neurosci Lett. 2018 Oct 15;685:173-178
pubmed: 30153495
Cancers (Basel). 2019 Sep 06;11(9):
pubmed: 31500086
Crit Rev Clin Lab Sci. 2019 Dec 22;57(4):227-252
pubmed: 31865806
Mol Nutr Food Res. 2014 Jul;58(7):1561-73
pubmed: 24842810
Cell Metab. 2021 May 4;33(5):988-1000.e7
pubmed: 33761313
Transl Clin Pharmacol. 2018 Sep;26(3):103-110
pubmed: 32055558
Clin Exp Immunol. 2018 Mar;191(3):301-310
pubmed: 29105068
Cell Microbiol. 2016 Nov;18(11):1525-1536
pubmed: 27673272
Cells. 2021 Feb 28;10(3):
pubmed: 33670924
Nat Cell Biol. 2019 Jan;21(1):9-17
pubmed: 30602770
J Biol Chem. 1997 Feb 28;272(9):6078-86
pubmed: 9038233
Nat Cell Biol. 2008 May;10(5):619-24
pubmed: 18425114
J Clin Invest. 1997 Mar 15;99(6):1173-8
pubmed: 9077524
Front Immunol. 2022 Aug 04;13:993967
pubmed: 35990697
Neuro Oncol. 2021 Aug 2;23(8):1231-1251
pubmed: 34185076
Transl Res. 2019 Aug;210:80-98
pubmed: 30998903
Nature. 2008 Oct 23;455(7216):1061-8
pubmed: 18772890
Mediators Inflamm. 2017;2017:4708076
pubmed: 28163397
EMBO J. 2017 Oct 16;36(20):3012-3028
pubmed: 28923825
Cancer Cell. 2018 Jul 9;34(1):119-135.e10
pubmed: 29937354
Nat Commun. 2021 Apr 6;12(1):2041
pubmed: 33824314
Biology (Basel). 2020 Jan 20;9(1):
pubmed: 31968627
Acta Pharmacol Sin. 2018 Apr;39(4):514-533
pubmed: 28858295
Am J Pathol. 2012 Nov;181(5):1573-84
pubmed: 23022210
Qatar Med J. 2021 Feb 22;2021(1):5
pubmed: 34604008
J Extracell Vesicles. 2017 Feb 28;6(1):1294368
pubmed: 28326171
J Biol Chem. 2014 Aug 8;289(32):22258-67
pubmed: 24951588
J Biophotonics. 2022 Apr;15(4):e202100351
pubmed: 34936211
PLoS One. 2017 Jan 20;12(1):e0169932
pubmed: 28107450
Sci Adv. 2018 Mar 07;4(3):eaar2766
pubmed: 29532035
J Proteome Res. 2012 Feb 3;11(2):1144-51
pubmed: 22149170
Biomedicines. 2022 Mar 30;10(4):
pubmed: 35453557
Front Immunol. 2018 Mar 15;9:534
pubmed: 29599781
Int J Oncol. 2019 Feb;54(2):713-721
pubmed: 30483768
Front Microbiol. 2022 Nov 10;13:1050271
pubmed: 36439842
Blood. 1999 Jun 1;93(11):3956-63
pubmed: 10339505
Nutrients. 2022 Jan 14;14(2):
pubmed: 35057528
Cell Rep. 2022 Apr 12;39(2):110651
pubmed: 35417683
Annu Rev Cell Dev Biol. 2014;30:255-89
pubmed: 25288114
Sci Signal. 2016 Feb 16;9(415):ra19
pubmed: 26884601
Front Immunol. 2020 Jan 21;10:3137
pubmed: 32038644
Cell Rep. 2019 Sep 17;28(12):3105-3119.e7
pubmed: 31533034
Int J Mol Sci. 2021 Mar 24;22(7):
pubmed: 33804873
Front Cell Dev Biol. 2017 Apr 26;5:43
pubmed: 28491867
Int J Mol Sci. 2016 Feb 06;17(2):175
pubmed: 26861306
Brain Pathol. 1999 Jul;9(3):435-42; discussion 432-3
pubmed: 10416984
Nat Rev Cancer. 2017 May;17(5):302-317
pubmed: 28303905
Biochim Biophys Acta. 2016 Aug;1857(8):1027-1038
pubmed: 27150504
Mol Cancer. 2014 Mar 21;13:65
pubmed: 24650096
Cell Cycle. 2013 Nov 15;12(22):3526-36
pubmed: 24091630
Biochem Soc Trans. 2019 Apr 30;47(2):509-516
pubmed: 30952802
Cancer Microenviron. 2017 Dec;10(1-3):57-68
pubmed: 28822081
Adv Biosyst. 2020 Dec;4(12):e2000017
pubmed: 32383351
Proc Natl Acad Sci U S A. 2018 Dec 11;115(50):E11721-E11730
pubmed: 30463946
Expert Rev Mol Diagn. 2014 Sep;14(7):819-25
pubmed: 25136839
Lancet. 2013 Mar 9;381(9869):825-35
pubmed: 23324563
Front Oncol. 2021 May 28;11:682932
pubmed: 34123852
Nat Rev Immunol. 2015 Jun;15(6):375-87
pubmed: 25976515
Nat Rev Microbiol. 2008 Feb;6(2):111-20
pubmed: 18197168
Int J Mol Sci. 2022 Aug 26;23(17):
pubmed: 36077083
Nat Rev Immunol. 2013 Aug;13(8):551-65
pubmed: 23846113
Proc Natl Acad Sci U S A. 2019 Feb 26;116(9):3909-3918
pubmed: 30733294
Cancer Lett. 2014 Oct 1;352(2):137-44
pubmed: 24956175
Cancer Res. 2017 Apr 1;77(7):1564-1574
pubmed: 28202516
Neuro Oncol. 2017 Oct 19;19(11):1494-1502
pubmed: 28453784