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Original Research

Intramuscular vaccination targeting mucosal tumor draining lymph node enhances integrins-mediated CD8+ T cell infiltration to control mucosal tumor growth

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Article: e1463946 | Received 11 Jan 2018, Accepted 07 Apr 2018, Published online: 24 May 2018

References

  • Schatton T, Scolyer RA, Thompson JF, Mihm MC, Jr. Tumor-infiltrating lymphocytes and their significance in melanoma prognosis. Methods Mol Biol. 2014;1102:287–324.
  • Santoiemma PP, Powell DJ, Jr. Tumor infiltrating lymphocytes in ovarian cancer. Cancer Biol Ther. 2015;16:807–20.
  • Dushyanthen S, Beavis PA, Savas P, Teo ZL, Zhou C, Mansour M, Darcy PK, Loi S. Relevance of tumor-infiltrating lymphocytes in breast cancer. BMC Med. 2015;13:202. doi:10.1186/s12916-015-0431-3. PMID:26300242.
  • Fridman WH, Galon J, Pages F, Tartour E, Sautes-Fridman C, Kroemer G. Prognostic and predictive impact of intra- and peritumoral immune infiltrates. Cancer Res. 2011;71:5601–5. doi:10.1158/0008-5472.CAN-11-1316. PMID:21846822.
  • Kang TH, Mao CP, Lee SY, Chen A, Lee JH, Kim TW, Alvarez RD, Roden RB, Pardoll D, Hung CF. Chemotherapy acts as an adjuvant to convert the tumor microenvironment into a highly permissive state for vaccination-induced antitumor immunity. Cancer Res. 2013;73:2493–504. doi:10.1158/0008-5472.CAN-12-4241. PMID:23418322.
  • Jin C, Liu Y, Zhu J, Xia T, Zhang B, Fei Y, Ma B, Ye J, Chen W. Recombinant Salmonella-based CEACAM6 and 4-1BBL vaccine enhances T-cell immunity and inhibits the development of colorectal cancer in rats: In vivo effects of vaccine containing 4-1BBL and CEACAM6. Oncol Rep. 2015;33:2837–44. doi:10.3892/or.2015.3901. PMID:25872647.
  • Gordy JT, Luo K, Zhang H, Biragyn A, Markham RB. Fusion of the dendritic cell-targeting chemokine MIP3alpha to melanoma antigen Gp100 in a therapeutic DNA vaccine significantly enhances immunogenicity and survival in a mouse melanoma model. J Immunother Cancer. 2016;4:96.
  • Sandoval F, Terme M, Nizard M, Badoual C, Bureau MF, Freyburger L, Clement O, Marcheteau E, Gey A, Fraisse G. Mucosal imprinting of vaccine-induced CD8(+) T cells is crucial to inhibit the growth of mucosal tumors. Sci Transl Med. 2013;5:172ra20. doi:10.1126/scitranslmed.3004888. PMID:23408053.
  • Sun Y, Peng S, Qiu J, Miao J, Yang B, Jeang J, Hung CF, Wu TC. Intravaginal HPV DNA vaccination with electroporation induces local CD8+ T-cell immune responses and antitumor effects against cervicovaginal tumors. Gene Ther. 2015;22:528–35. doi:10.1038/gt.2015.17. PMID:25786869.
  • Sun YY, Peng S, Han L, Qiu J, Song L, Tsai Y, Yang B, Roden RB, Trimble CL, Hung CF. Local HPV recombinant Vaccinia Boost following priming with an HPV DNA Vaccine enhances Local HPV-Specific CD8+ T-cell-Mediated Tumor control in the Genital Tract. Clin Cancer Res. 2016;22:657–69. doi:10.1158/1078-0432.CCR-15-0234. PMID:26420854.
  • Pialoux G, Hocini H, Perusat S, Silberman B, Salmon-Ceron D, Slama L, Journot V, Mathieu E, Gaillard C, Petitprez K. Phase I study of a candidate vaccine based on recombinant HIV-1 gp160 (MN/LAI) administered by the mucosal route to HIV-seronegative volunteers: the ANRS VAC14 study. Vaccine. 2008;26:2657–66.
  • Meque I, Dube K, Bierhuizen L, Zango A, Veldhuijzen N, Cumbe F, Feldblum PJ, van de Wijgert J. Willingness to participate in future HIV prevention trials in Beira, Mozambique. Afr J AIDS Res. 2014;13:393–8. doi:10.2989/16085906.2014.985239. PMID:25555105.
  • Swartz MA. Immunomodulatory roles of lymphatic vessels in cancer progression. Cancer Immunol Res. 2014;2:701–7. doi:10.1158/2326-6066.CIR-14-0115. PMID:25092811.
  • Stachura J, Wachowska M, Kilarski WW, Guc E, Golab J, Muchowicz A. The dual role of tumor lymphatic vessels in dissemination of metastases and immune response development. Oncoimmunology. 2016;5:e1182278. doi:10.1080/2162402X.2016.1182278. PMID:27622039.
  • Mehta NK, Moynihan KD, Irvine DJ. Engineering new approaches to Cancer Vaccines. Cancer Immunol Res. 2015;3:836–43. doi:10.1158/2326-6066.CIR-15-0112. PMID:26156157.
  • Gardner A, Ruffell B. Dendritic cells and Cancer immunity. Trends Immunol. 2016;37:855–65. doi:10.1016/j.it.2016.09.006. PMID:27793569.
  • Jeanbart L, Ballester M, de Titta A, Corthesy P, Romero P, Hubbell JA, Swartz MA. Enhancing efficacy of anticancer vaccines by targeted delivery to tumor-draining lymph nodes. Cancer Immunol Res. 2014;2:436–47. doi:10.1158/2326-6066.CIR-14-0019-T. PMID:24795356.
  • Shirone N, Shinkai T, Yamane T, Uto F, Yoshimura H, Tamai H, Imai T, Inoue M, Kitano S, Kichikawa K. Axillary lymph node accumulation on FDG-PET/CT after influenza vaccination. Ann Nucl Med. 2012;26:248–52. doi:10.1007/s12149-011-0568-x. PMID:22271546.
  • Coates EE, Costner PJ, Nason MC, Herrin DM, Conant S, Herscovitch P, Sarwar UN, Holman L, Mitchell J, Yamshchikov G. Lymph Node activation by PET/CT following Vaccination with licensed Vaccines for Human Papillomaviruses. Clin Nucl Med. 2017;42:329–34. doi:10.1097/RLU.0000000000001603. PMID:28288041.
  • Yoshikawa H, Seebach S. Lymphotropic delivery of cyclosporin A by intramuscular injection of biodegradable microspheres in mice. Biol Pharm Bull. 1996;19:1527–9.
  • Cantisani R, Pezzicoli A, Cioncada R, Malzone C, De Gregorio E DU, Piccioli D. Vaccine adjuvant MF59 promotes retention of unprocessed antigen in lymph node macrophage compartments and follicular dendritic cells. J Immunol. 2015;194:1717–25.
  • Raj LSM, Boaz K, Natarajan S. Prognostic significance of Lymph Node pattern in Oral Squamous Cell Carcinoma (OSCC). J Clin Diagn Res. 2014;8:232–5. doi:10.7860/JCDR/2014/7365.3974. PMID:24596783.
  • Thakare E, Gawande M, Chaudhary M, Seralathan M, Kannan K. Detection of micrometastasis in lymph nodes of oral squamous cell carcinoma: A comparative study. J Oral Maxillofac Pathol. 2013;17:374–80. doi:10.4103/0973-029X.125202. PMID:24574655.
  • Li X, Yin Y, Sheng X, Han X, Sun L, Lu C, Wang X. Distribution pattern of lymph node metastases and its implication in individualized radiotherapeutic clinical target volume delineation of regional lymph nodes in patients with stage IA to IIA cervical cancer. Radiat Oncol. 2015;10:40. doi:10.1186/s13014-015-0352-5. PMID:25886535.
  • Cheng WF, Hung CF, Chai CY, Hsu KF, He L, Ling M, Wu TC. Tumor-specific immunity and antiangiogenesis generated by a DNA vaccine encoding calreticulin linked to a tumor antigen. J Clin Invest. 2001;108:669–78.
  • Best SR, Peng S, Juang CM, Hung CF, Hannaman D, Saunders JR, Wu TC, Pai SI. Administration of HPV DNA vaccine via electroporation elicits the strongest CD8+ T cell immune responses compared to intramuscular injection and intradermal gene gun delivery. Vaccine. 2009;27:5450–9. doi:10.1016/j.vaccine.2009.07.005. PMID:19622402.
  • Alvarez RD, Huh WK, Bae S, Lamb LS, Jr., Conner MG, Boyer J, et al. A pilot study of pNGVL4a-CRT/E7(detox) for the treatment of patients with HPV16+ cervical intraepithelial neoplasia 2/3 (CIN2/3). Gynecol Oncol. 2016;140:245–52.
  • Huang B, Mao CP, Peng S, He L, Hung CF, Wu TC. Intradermal administration of DNA vaccines combining a strategy to bypass antigen processing with a strategy to prolong dendritic cell survival enhances DNA vaccine potency. Vaccine. 2007;25:7824–31.
  • Yang A, Jeang J, Cheng K, Cheng T, Yang B, Wu TC, et al. Current state in the development of candidate therapeutic HPV vaccines. Expert Rev Vaccines. 2016;15:989–1007.
  • Badoual C, Sandoval F, Pere H, Hans S, Gey A, Merillon N, Van Ryswick C Q-CF, Bruneval P, Brasnu D. Better understanding tumor-host interaction in head and neck cancer to improve the design and development of immunotherapeutic strategies. Head Neck. 2010;32:946–58.
  • Cuburu N, Graham BS, Buck CB, Kines RC, Pang YY, Day PM, Lowy DR, Schiller JT. Intravaginal immunization with HPV vectors induces tissue-resident CD8+ T cell responses. J Clin Invest. 2012;122:4606–20. doi:10.1172/JCI63287. PMID:23143305.
  • Macedo R, Rochefort J, Guillot-Delost M, Tanaka K, Le Moignic A NC, Baillou C, Mateo V, Carpentier AF, Tartour E. Intra-cheek immunization as a novel vaccination route for therapeutic vaccines of head and neck squamous cell carcinomas using plasmo virus-like particles. Oncoimmunology. 2016;5:e1164363.
  • Liu J, O'Brien KL, Lynch DM, Simmons NL, La Porte A, Riggs AM, Abbink P, Coffey RT, Grandpre LE, Seaman MS. Immune control of an SIV challenge by a T-cell-based vaccine in rhesus monkeys. Nature. 2009;457:87–91. doi:10.1038/nature07469. PMID:18997770.
  • Masopust D, Choo D, Vezys V, Wherry EJ, Duraiswamy J, Akondy R, Wang J, Casey KA, Barber DL, Kawamura KS. Dynamic T cell migration program provides resident memory within intestinal epithelium. J Exp Med. 2010;207:553–64. doi:10.1084/jem.20090858. PMID:20156972.
  • Maldonado L, Teague JE, Morrow MP, Jotova I, Wu TC, Wang C, Desmarais C, Boyer JD, Tycko B, Robins HS. Intramuscular therapeutic vaccination targeting HPV16 induces T cell responses that localize in mucosal lesions. Sci Transl Med. 2014;6:221ra13. doi:10.1126/scitranslmed.3007323. PMID:24477000.
  • Belyakov IM, Ahlers JD, Brandwein BY, Earl P, Kelsall BL, Moss B, Strober W, Berzofsky JA. The importance of local mucosal HIV-specific CD8(+) cytotoxic T lymphocytes for resistance to mucosal viral transmission in mice and enhancement of resistance by local administration of IL-12. J Clin Invest. 1998;102:2072–81. doi:10.1172/JCI5102. PMID:9854042.
  • Trimble CL, Peng S, Thoburn C, Kos F, Wu TC. Naturally occurring systemic immune responses to HPV antigens do not predict regression of CIN2/3. Cancer Immunol Immunother. 2010;59:799–803.
  • Roberts EW, Broz ML, Binnewies M, Headley MB, Nelson AE, Wolf DM, Kaisho T, Bogunovic D, Bhardwaj N, Krummel MF. Critical role for CD103(+)/CD141(+) Dendritic cells bearing CCR7 for Tumor Antigen Trafficking and Priming of T Cell immunity in Melanoma. Cancer Cell. 2016;30:324–36. doi:10.1016/j.ccell.2016.06.003. PMID:27424807.
  • Mora JR, von Andrian UH. T-cell homing specificity and plasticity: new concepts and future challenges. Trends Immunol. 2006;27:235–43. doi:10.1016/j.it.2006.03.007. PMID:16580261.
  • Zammit DJ, Turner DL, Klonowski KD, Lefrancois L, Cauley LS. Residual antigen presentation after influenza virus infection affects CD8 T cell activation and migration. Immunity. 2006;24:439–49. doi:10.1016/j.immuni.2006.01.015. PMID:16618602.
  • Calzascia T, Masson F, Di Berardino-Besson W, Contassot E, Wilmotte R, Aurrand-Lions M, Rüegg C, Dietrich PY, Walker PR. Homing phenotypes of tumor-specific CD8 T cells are predetermined at the tumor site by crosspresenting APCs. Immunity. 2005;22:175–84. doi:10.1016/j.immuni.2004.12.008. PMID:15723806.
  • Brinkman CC, Peske JD, Engelhard VH. Peripheral tissue homing receptor control of naive, effector, and memory CD8 T cell localization in lymphoid and non-lymphoid tissues. Front Immunol. 2013;4:241. doi:10.3389/fimmu.2013.00241. PMID:23966998.
  • Ray SJ, Franki SN, Pierce RH, Dimitrova S, Koteliansky V, Sprague AG, Doherty PC, de Fougerolles AR, Topham DJ. The collagen binding alpha1beta1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity. 2004;20:167–79. PMID:14975239.
  • Cheuk S, Schlums H, Gallais Serezal I, Martini E, Chiang SC, Marquardt N, Gibbs A, Detlofsson E, Introini A, Forkel M. CD49a expression defines Tissue-Resident CD8+ T Cells Poised for Cytotoxic function in Human skin. Immunity. 2017;46:287–300. doi:10.1016/j.immuni.2017.01.009. PMID:28214226.
  • De Calisto J, Villablanca EJ, Wang S, Bono MR, Rosemblatt M, Mora JR. T-cell homing to the gut mucosa: general concepts and methodological considerations. Methods Mol Biol. 2012;757:411–34. doi:10.1007/978-1-61779-166-6_24. PMID:21909925.
  • Trimble CL, Clark RA, Thoburn C, Hanson NC, Tassello J, Frosina D, Kos F, Teague J, Jiang Y, Barat NC. Human papillomavirus 16-associated cervical intraepithelial neoplasia in humans excludes CD8 T cells from dysplastic epithelium. J Immunol. 2010;185:7107–14. doi:10.4049/jimmunol.1002756. PMID:21037100.
  • Ahlen G, Soderholm J, Tjelle T, Kjeken R, Frelin L, Hoglund U, Blomberg P, Fons M, Mathiesen I, Sällberg M. In vivo electroporation enhances the immunogenicity of hepatitis C virus nonstructural 3/4A DNA by increased local DNA uptake, protein expression, inflammation, and infiltration of CD3+ T cells. J Immunol. 2007;179:4741–53. PMID:17878373.
  • Liu J, Kjeken R, Mathiesen I, Barouch DH. Recruitment of antigen-presenting cells to the site of inoculation and augmentation of human immunodeficiency virus type 1 DNA vaccine immunogenicity by in vivo electroporation. J Virol. 2008;82:5643–9. doi:10.1128/JVI.02564-07. PMID:18353952.
  • Sun Y, Peng S, Yang A, Farmer E, Wu TC, Hung CF. Coinjection of IL2 DNA enhances E7-specific antitumor immunity elicited by intravaginal therapeutic HPV DNA vaccination with electroporation. Gene Ther. 2017;24:408–15. doi:10.1038/gt.2017.38. PMID:28492521.
  • Neville BW, Day TA. Oral cancer and precancerous lesions. CA Cancer J Clin. 2002;52:195–215. PMID:12139232.
  • Rayatt SS, Dancey AL, Fagan J, Srivastava S. Axillary metastases from recurrent oral carcinoma. Br J Oral Maxillofac Surg. 2004;42:264–6. doi:10.1016/j.bjoms.2003.12.004. PMID:15121278.
  • Koga-Yamakawa E, Dovedi SJ, Murata M, Matsui H, Leishman AJ, Bell J, Ferguson D, Heaton SP, Oki T, Tomizawa H. Intratracheal and oral administration of SM-276001: a selective TLR7 agonist, leads to antitumor efficacy in primary and metastatic models of cancer. Int J Cancer. 2013;132:580–90. doi:10.1002/ijc.27691. PMID:22733292.
  • Trosman SJ, Koyfman SA, Ward MC, Al-Khudari S, Nwizu T, Greskovich JF, Lamarre ED, Scharpf J, Khan MJ, Lorenz RR. Effect of human papillomavirus on patterns of distant metastatic failure in oropharyngeal squamous cell carcinoma treated with chemoradiotherapy. JAMA Otolaryngol Head Neck Surg. 2015;141:457–62. doi:10.1001/jamaoto.2015.136. PMID:25742025.
  • Kang S. Unsuspected axillary lymph node metastasis of nasopharyngeal and cervical cancer on 18FDG PET/CT: a case report. Nucl Med Rev Cent East Eur. 2016;19:20–1. doi:10.5603/NMR.2016.0032. PMID:27900757.
  • Kim TW, Hung CF, Ling M, Juang J, He L, Hardwick JM, Kumar S, Wu TC. Enhancing DNA vaccine potency by coadministration of DNA encoding antiapoptotic proteins. J Clin Invest. 2003;112:109–17. doi:10.1172/JCI17293. PMID:12840065.
  • Huang B, Mao CP, Peng S, Hung CF, Wu TC. RNA interference-mediated in vivo silencing of fas ligand as a strategy for the enhancement of DNA vaccine potency. Hum Gene Ther. 2008;19:763–73. doi:10.1089/hum.2007.059. PMID:18627219.

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