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Original research

Listeria-based vaccination against the pericyte antigen RGS5 elicits anti-vascular effects and colon cancer protection

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Article: 2260620 | Received 28 Jun 2023, Accepted 14 Sep 2023, Published online: 28 Sep 2023

References

  • Xi Y, Xu P. Global colorectal cancer burden in 2020 and projections to 2040. Transl Oncol. 2021;14(10):101174. doi:10.1016/j.tranon.2021.101174.
  • Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–14. doi:10.3322/caac.21660.
  • Turano M, Delrio P, Rega D, Cammarota F, Polverino A, Duraturo F, Izzo P, De Rosa M. Promising colorectal cancer biomarkers for precision prevention and therapy. Cancers Basel. 2019;11(12):1932. doi:10.3390/cancers11121932.
  • Van der Jeught K, Xu H-C, Li Y-J, Lu X-B, Ji G. Drug resistance and new therapies in colorectal cancer. World J Gastroenterol. 2018;24(34):3834–3848. doi:10.3748/wjg.v24.i34.3834.
  • Douillard JY, Cunningham D, Roth AD, Navarro M, James RD, Karasek P, Jandik P, Iveson T, Carmichael J, Alakl M, et al. Irinotecan combined with fluorouracil compared with fluorouracil alone as first-line treatment for metastatic colorectal cancer: a multicentre randomised trial. Lancet. 2000;355(9209):1041–1047. doi:10.1016/S0140-6736(00)02034-1.
  • Fan A, Wang B, Wang X, Nie Y, Fan D, Zhao X, Lu Y. Immunotherapy in colorectal cancer: current achievements and future perspective. Int J Biol Sci. 2021;17(14):3837–3849. doi:10.7150/ijbs.64077.
  • Jia W, Zhang T, Huang H, Feng H, Wang S, Guo Z, Luo Z, Ji X, Cheng X, Zhao R, et al. Colorectal cancer vaccines: the current scenario and future prospects. Front Immunol. 2022;13:942235. doi:10.3389/fimmu.2022.942235.
  • Berry J, Vreeland T, Trappey A, Hale D, Peace K, Tyler J, Walker A, Brown R, Herbert G, Yi F, et al. Cancer vaccines in colon and rectal cancer over the last decade: lessons learned and future directions. Expert Rev Clin Immunol. 2017;13(3):235–245. doi:10.1080/1744666X.2016.1226132.
  • Sanchez-Leon ML, Jiménez-Cortegana C, Cabrera G, Vermeulen EM, de la Cruz-Merino L, Sánchez-Margalet V. The effects of dendritic cell-based vaccines in the tumor microenvironment: impact on myeloid-derived suppressor cells. Front Immunol. 2022;13:1050484. doi:10.3389/fimmu.2022.1050484.
  • Jahangir A, Chandra D, Quispe-Tintaya W, Singh M, Selvanesan BC, Gravekamp C. Immunotherapy with Listeria reduces metastatic breast cancer in young and old mice through different mechanisms. Oncoimmunology. 2017;6(9):e1342025. doi:10.1080/2162402X.2017.1342025.
  • Oladejo M, Nguyen H-M, Seah H, Datta A, Wood LM. Tumoral CD105 promotes immunosuppression, metastasis, and angiogenesis in renal cell carcinoma. Cancer Immunol Immunother. 2023;72(6):1633–1646. doi:10.1007/s00262-022-03356-5.
  • Zhou S, Gravekamp C, Bermudes D, Liu K. Tumour-targeting bacteria engineered to fight cancer. Nat Rev Cancer. 2018;18(12):727–743. doi:10.1038/s41568-018-0070-z.
  • Oladejo M, Paterson Y, Wood LM. Clinical experience and recent advances in the development of Listeria-based tumor immunotherapies. Front Immunol. 2021;12:642316. doi:10.3389/fimmu.2021.642316.
  • Fabian KL, Storkus WJ. Immunotherapeutic targeting of tumor-associated blood vessels. Adv Exp Med Biol. 2017;1036:191–211.
  • Schaaf MB, Garg AD, Agostinis P. Defining the role of the tumor vasculature in antitumor immunity and immunotherapy. Cell Death Disease. 2018;9(2):115. doi:10.1038/s41419-017-0061-0.
  • Martin JD, Seano G, Jain RK. Normalizing function of tumor vessels: progress, opportunities, and challenges. Annu Rev Physiol. 2019;81(1):505–534. doi:10.1146/annurev-physiol-020518-114700.
  • Garza Trevino EN, González PD, Valencia Salgado CI, Martinez Garza A. Effects of pericytes and colon cancer stem cells in the tumor microenvironment. Cancer Cell Int. 2019;19(1):173. doi:10.1186/s12935-019-0888-9.
  • Berger M, Bergers G, Arnold B, Hammerling GJ, Ganss R. Regulator of G-protein signaling-5 induction in pericytes coincides with active vessel remodeling during neovascularization. Blood. 2005;105(3):1094–1101. doi:10.1182/blood-2004-06-2315.
  • Dabravolski SA, Andreeva ER, Eremin II, Markin AM, Nadelyaeva II, Orekhov AN, Melnichenko AA. The role of pericytes in regulation of innate and adaptive immunity. Biomedicines. 2023;11(2):600. doi:10.3390/biomedicines11020600.
  • Raza A, Franklin MJ, Dudek AZ. Pericytes and vessel maturation during tumor angiogenesis and metastasis. Am J Hematol. 2010;85(8):593–598. doi:10.1002/ajh.21745.
  • Zhao X, Bose A, Komita H, Taylor JL, Chi N, Lowe DB, Okada H, Cao Y, Mukhopadhyay D, Cohen PA, et al. Vaccines targeting tumor blood vessel antigens promote CD8(+) T cell-dependent tumor eradication or dormancy in HLA-A2 transgenic mice. J Immunol. 2012;188(4):1782–1788. doi:10.4049/jimmunol.1101644.
  • Hamzah J, Jugold M, Kiessling F, Rigby P, Manzur M, Marti HH, Rabie T, Kaden S, Gröne H-J, Hämmerling GJ, et al. Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature. 2008;453(7193):410–414. doi:10.1038/nature06868.
  • Storkus WJ, Maurer D, Lin Y, Ding F, Bose A, Lowe D, Rose A, DeMark M, Karapetyan L, Taylor JL, et al. Dendritic cell vaccines targeting tumor blood vessel antigens in combination with dasatinib induce therapeutic immune responses in patients with checkpoint-refractory advanced melanoma. J Immunother Cancer. 2021;9(11):e003675. doi:10.1136/jitc-2021-003675.
  • Singh R, Dominiecki ME, Jaffee EM, Paterson Y. Fusion to listeriolysin O and delivery by Listeria monocytogenes enhances the immunogenicity of HER-2/neu and reveals subdominant epitopes in the FVB/N mouse. J Immunol. 2005;175(6):3663–3673. doi:10.4049/jimmunol.175.6.3663.
  • Kim SH, Castro F, Gonzalez D, Maciag PC, Paterson Y, Gravekamp C. Mage-b vaccine delivered by recombinant Listeria monocytogenes is highly effective against breast cancer metastases. Br J Cancer. 2008;99(5):741–749. doi:10.1038/sj.bjc.6604526.
  • Monk IR, Gahan CG, Hill C. Tools for functional postgenomic analysis of listeria monocytogenes. Appl Environ Microbiol. 2008;74(13):3921–3934. doi:10.1128/AEM.00314-08.
  • Jones GS, D’Orazio SEF. Listeria monocytogenes: cultivation and laboratory maintenance. Curr Protoc Microbiol. 2013;31(1):B9 2 1–B9 2 7. doi:10.1002/9780471729259.mc09b02s31.
  • Son YI, Egawa S-I, Tatsumi T, Redlinger RE, Kalinski P, Kanto T. A novel bulk-culture method for generating mature dendritic cells from mouse bone marrow cells. J Immunol Methods. 2002;262(1–2):145–157. doi:10.1016/S0022-1759(02)00013-3.
  • Mailliard RB, Wankowicz-Kalinska A, Cai Q, Wesa A, Hilkens CM, Kapsenberg ML, Kirkwood JM, Storkus WJ, Kalinski P. α-type-1 polarized dendritic cells. Cancer Res. 2004;64(17):5934–5937. doi:10.1158/0008-5472.CAN-04-1261.
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods. 2001;25(4):402–408. doi:10.1006/meth.2001.1262.
  • Andreatta M, Nielsen M. Gapped sequence alignment using artificial neural networks: application to the MHC class I system. Bioinformatics. 2016;32(4):511–517. doi:10.1093/bioinformatics/btv639.
  • Nielsen M, Lundegaard C, Worning P, Lauemøller SL, Lamberth K, Buus S, Brunak S, Lund O. Reliable prediction of T-cell epitopes using neural networks with novel sequence representations. Protein Sci. 2003;12(5):1007–1017. doi:10.1110/ps.0239403.
  • Lowe DB, Bose A, Taylor JL, Tawbi H, Lin Y, Kirkwood JM, Storkus WJ. Dasatinib promotes the expansion of a therapeutically superior T-cell repertoire in response to dendritic cell vaccination against melanoma. Oncoimmunology. 2014;3(2):e27589. doi:10.4161/onci.27589.
  • Liu Y, Niu L, Li N, Wang Y, Liu M, Su X, Bao X, Yin B, Shen S. Bacterial-mediated tumor therapy: old treatment in a New context. Adv Sci. 2023;10(12):e2205641. doi:10.1002/advs.202205641.
  • Wood LM, Pan Z-K, Guirnalda P, Tsai P, Seavey M, Paterson Y. Targeting tumor vasculature with novel Listeria-based vaccines directed against CD105. Cancer Immunol Immunother. 2011;60(7):931–942. doi:10.1007/s00262-011-1002-x.
  • Gunn GR, Zubair A, Peters C, Pan ZK, Wu TC, Paterson Y. Two Listeria monocytogenes vaccine vectors that express different molecular forms of human papilloma virus-16 (HPV-16) E7 induce qualitatively different T cell immunity that correlates with their ability to induce regression of established tumors immortalized by HPV-16. J Immunol. 2001;167(11):6471–6479. doi:10.4049/jimmunol.167.11.6471.
  • Chandra D, Jahangir A, Quispe-Tintaya W, Einstein MH, Gravekamp C. Myeloid-derived suppressor cells have a central role in attenuated Listeria monocytogenes-based immunotherapy against metastatic breast cancer in young and old mice. Br J Cancer. 2013;108(11):2281–2290. doi:10.1038/bjc.2013.206.
  • Kheirolomoom A, Kare AJ, Ingham ES, Paulmurugan R, Robinson ER, Baikoghli M, Inayathullah M, Seo JW, Wang J, Fite BZ, et al. In situ T-cell transfection by anti-CD3-conjugated lipid nanoparticles leads to T-cell activation, migration, and phenotypic shift. Biomaterials. 2022;281:121339. doi:10.1016/j.biomaterials.2021.121339.
  • Ghanekar SA, Nomura LE, Suni MA, Picker LJ, Maecker HT, Maino VC. Gamma interferon expression in CD8+T cells is a marker for circulating cytotoxic T lymphocytes that recognize an HLA A2-restricted epitope of human cytomegalovirus phosphoprotein pp65. Clin Diagn Lab Immunol. 2001;8(3):628–631. doi:10.1128/CDLI.8.3.628-631.2001.
  • Horton H, Russell N, Moore E, Frank I, Baydo R, Havenar‐Daughton C, Lee D, Deers M, Hudgens M, Weinhold K, et al. Correlation between Interferon-γ secretion and cytotoxicity, in Virus-specific Memory T cells. J Infect Dis. 2004;190(9):1692–1696. doi:10.1086/424490.
  • Simon S, Labarriere N. PD-1 expression on tumor-specific T cells: friend or foe for immunotherapy? Oncoimmunology. 2017;7(1):e1364828. doi:10.1080/2162402X.2017.1364828.
  • Montfort A, Colacios C, Levade T, Andrieu-Abadie N, Meyer N, Ségui B. The TNF paradox in cancer progression and immunotherapy. Front Immunol. 2019;10:1818. doi:10.3389/fimmu.2019.01818.
  • Oladejo M, Nguyen H-M, Silwal A, Reese B, Paulishak W, Markiewski MM, Wood LM. Listeria-based immunotherapy directed against CD105 exerts anti-angiogenic and anti-tumor efficacy in renal cell carcinoma. Front Immunol. 2022;13:1038807. doi:10.3389/fimmu.2022.1038807.
  • Lechner MG, Karimi SS, Barry-Holson K, Angell TE, Murphy KA, Church CH, Ohlfest JR, Hu P, Epstein AL. Immunogenicity of murine solid tumor models as a defining feature of in vivo behavior and response to immunotherapy. J Immunother (1991). 2013;36(9):477–489. doi:10.1097/01.cji.0000436722.46675.4a.
  • Lau J, Cheung J, Navarro A, Lianoglou S, Haley B, Totpal K, Sanders L, Koeppen H, Caplazi P, McBride J, et al. Tumour and host cell PD-L1 is required to mediate suppression of anti-tumour immunity in mice. Nat Commun. 2017;8(1):14572. doi:10.1038/ncomms14572.
  • 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. 2017;5(9):767–777. doi:10.1158/2326-6066.CIR-16-0365.
  • Ganesh K, Stadler ZK, Cercek A, Mendelsohn RB, Shia J, Segal NH, Diaz LA. Immunotherapy in colorectal cancer: rationale, challenges and potential. Nat Rev Gastroenterol Hepatol. 2019;16(6):361–375. doi:10.1038/s41575-019-0126-x.
  • Goel S, Duda DG, Xu L, Munn LL, Boucher Y, Fukumura D, Jain RK. Normalization of the vasculature for treatment of cancer and other diseases. Physiol Rev. 2011;91(3):1071–1121. doi:10.1152/physrev.00038.2010.
  • Tian L, Goldstein A, Wang H, Ching Lo H, Sun Kim I, Welte T, Sheng K, Dobrolecki LE, Zhang X, Putluri N, et al. Mutual regulation of tumour vessel normalization and immunostimulatory reprogramming. Nature. 2017;544(7649):250–254. doi:10.1038/nature21724.
  • Liu Z, Wang Y, Huang Y, Kim BYS, Shan H, Wu D, Jiang W. Tumor vasculatures: a New target for cancer immunotherapy. Trends Pharmacol Sci. 2019;40(9):613–623. doi:10.1016/j.tips.2019.07.001.
  • Yang S, Fei W, Zhao Y, Wang F, Ye Y, Wang F. Combat against gynecological cancers with blood vessels as entry point: Anti-angiogenic drugs, clinical trials and pre-clinical nano-delivery platforms. Int J Nanomedicine. 2023;18:3035–3046. doi:10.2147/IJN.S411761.
  • Baar J, Storkus WJ, Finke J, Butterfield L, Lazarus H, Reese J, Downes K, Budd T, Brufsky A, Fu P. Pilot trial of a type I - polarized autologous dendritic cell vaccine incorporating tumor blood vessel antigen-derived peptides in patients with metastatic breast cancer. J Immunother Cancer. 2015;33(S1):P3. doi:10.1186/2051-1426-3-S1-P3.
  • Stapor PC, Sweat RS, Dashti DC, Betancourt AM, Murfee WL. Pericyte dynamics during angiogenesis: new insights from new identities. J Vasc Res. 2014;51(3):163–174. doi:10.1159/000362276.
  • Meng MB, Zaorsky NG, Deng L, Wang H-H, Chao J, Zhao L-J, Yuan Z-Y, Ping W. Pericytes: a double-edged sword in cancer therapy. Future Oncol. 2015;11(1):169–179. doi:10.2217/fon.14.123.
  • Firat H, Garcia-Pons F, Tourdot S, Pascolo S, Scardino A, Garcia Z, Michel M-L, Jack RW, Jung G, Kosmatopoulos K, et al. H-2 class I knockout, HLA-A2.1-transgenic mice: a versatile animal model for preclinical evaluation of antitumor immunotherapeutic strategies. Eur J Immunol. 1999;29(10):3112–3121. doi:10.1002/(SICI)1521-4141(199910)29:10<3112:AID-IMMU3112>3.0.CO;2-Q.
  • Street MD, Doan T, Herd KA, Tindle RW. Limitations of HLA-transgenic mice in presentation of HLA-restricted cytotoxic T-cell epitopes from endogenously processed human papillomavirus type 16 E7 protein. Immunology. 2002;106(4):526–536. doi:10.1046/j.1365-2567.2002.01442.x.
  • Angelakopoulos H, Loock K, Sisul DM, Jensen ER, Miller JF, Hohmann EL. Safety and shedding of an attenuated strain of Listeria monocytogenes with a deletion of actA/plcb in adult volunteers: a dose escalation study of oral inoculation. Infect Immun. 2002;70(7):3592–3601. doi:10.1128/IAI.70.7.3592-3601.2002.
  • Maciag PC, Radulovic S, Rothman J. The first clinical use of a live-attenuated Listeria monocytogenes vaccine: a phase I safety study of Lm-LLO-E7 in patients with advanced carcinoma of the cervix. Vaccine. 2009;27(30):3975–3983. doi:10.1016/j.vaccine.2009.04.041.
  • Tsujikawa T, Crocenzi T, Durham JN, Sugar EA, Wu AA, Onners B, Nauroth JM, Anders RA, Fertig EJ, Laheru DA, et al. Evaluation of cyclophosphamide/GVAX pancreas followed by Listeria-mesothelin (CRS-207) with or without nivolumab in patients with pancreatic cancer. Clin Cancer Res. 2020;26(14):3578–3588. doi:10.1158/1078-0432.CCR-19-3978.
  • Mason NJ, Gnanandarajah JS, Engiles JB, Gray F, Laughlin D, Gaurnier-Hausser A, Wallecha A, Huebner M, Paterson Y. Immunotherapy with a HER2-targeting Listeria induces HER2-specific immunity and demonstrates potential therapeutic effects in a phase I trial in canine osteosarcoma. Clin Cancer Res. 2016;22(17):4380–4390. doi:10.1158/1078-0432.CCR-16-0088.
  • Wallecha A, Malinina I, Molli P. Listeria monocytogenes (Lm)-LLO immunotherapies reduce the immunosuppressive activity of myeloid-derived suppressor cells and regulatory T cells in the tumor microenvironment. J Immunother Cancer. 2013;1(S1):468–476. doi:10.1186/2051-1426-1-S1-O18.