1,869
Views
5
CrossRef citations to date
0
Altmetric
Original Research

Quantitative MRI cell tracking of immune cell recruitment to tumors and draining lymph nodes in response to anti-PD-1 and a DPX-based immunotherapy

, , , , , , ORCID Icon, ORCID Icon & ORCID Icon show all
Article: 1851539 | Received 31 Aug 2020, Accepted 11 Nov 2020, Published online: 29 Nov 2020

References

  • Weiss L, Huemer F, Mlineritsch B, Greil R. Immune checkpoint blockade in ovarian cancer. Memo Springer Vienna. 2016;9:82–10.
  • Ojalvo LS, Nichols PE, Jelovac D, Emens LA. Emerging immunotherapies in ovarian cancer. Discov Med. 2015;20:97–109.
  • Ferris RPD-1. targeting in cancer immunotherapy. Cancer. 2012;119:E1–E3. doi:10.1002/cncr.27832.
  • Baxevanis CN, Perez SA, Papamichail M. Combinatorial treatments including vaccines, chemotherapy and monoclonal antibodies for cancer therapy. Cancer Immunol Immunother. 2009;58(3):317–324. doi:10.1007/s00262-008-0576-4.
  • Sharma P, Allison JP. Immune checkpoint targeting in cancer therapy: toward combination strategies with curative potential. Cell. 2015;161(2):205–214. doi:10.1016/j.cell.2015.03.030.
  • Berinstein NL, Karkada M, Oza AM, Odunsi K, Villella JA, Nemunaitis JJ, Morse MA, Pejovic T, Bentley J, Buyse M, et al. Survivin-targeted immunotherapy drives robust polyfunctional T cell generation and differentiation in advanced ovarian cancer patients. Oncoimmunology. 2015;4(8):e1026529. doi:10.1080/2162402X.2015.1026529.
  • Garg H, Suri P, Gupta JC, Talwar GP, Dubey S. Survivin: a unique target for tumor therapy. Cancer Cell Int BioMed Central. 2016;16:49. doi:10.1186/s12935-016-0326-1.
  • Karkada M, Weir GM, Quinton T, Sammatur L, MacDonald LD, Grant A, Liwski R, Juskevicius R, Sinnathamby G, Philip R, et al. A novel breast/ovarian cancer peptide vaccine platform that promotes specific type-1 but not Treg/Tr1-type responses. J Immunother. 2010;33(3):250–261. doi:10.1097/CJI.0b013e3181c1f1e9.
  • Berinstein NL, Karkada M, Morse MA, Nemunaitis JJ, Chatta G, Kaufman H, Odunsi K, Nigam R, Sammatur L, MacDonald LD, et al. First-in-man application of a novel therapeutic cancer vaccine formulation with the capacity to induce multi-functional T cell responses in ovarian, breast and prostate cancer patients. J Transl Med BioMed Central. 2012;10:156. doi:10.1186/1479-5876-10-156.
  • Weir GM, Hrytsenko O, Stanford MM, Berinstein NL, Karkada M, Liwski RS, Mansour M. Metronomic cyclophosphamide enhances HPV16E7 peptide vaccine induced antigen-specific and cytotoxic T-cell mediated antitumor immune response. Oncoimmunology. 2014;3:e953407.
  • Medicines in development for cancer. Pharmaceutical research and manufacturers of America. 2015 Sep 1–4.
  • Ott PA, Hodi FS, Kaufman HL, Wigginton JM, Wolchok JD. Combination immunotherapy: a road map. J Immunother Cancer. 2017;5(1):16. doi:10.1186/s40425-017-0218-5.
  • Messenheimer DJ, Jensen SM, Afentoulis ME, Wegmann KW, Feng Z, Friedman DJ, Gough MJ, Urba WJ, Fox BA. Timing of PD-1 blockade is critical to effective combination immunotherapy with Anti-OX40. Clin Cancer Res. 2017;23(20):6165–6177. doi:10.1158/1078-0432.CCR-16-2677.
  • Zeelen C, Paus C, Draper D, Heskamp S, Signore A, Galli F, Griessinger C, Aarntzen EH. In-vivo imaging of tumor-infiltrating immune cells: implications for cancer immunotherapy. Q J Nucl Med Mol Imaging. 2018;62:56–77.
  • Ehlerding EB, England CG, McNeel DG, Cai W. Molecular imaging of immunotherapy targets in cancer. J Nucl Med. 2016;57(10):1487–1492. doi:10.2967/jnumed.116.177493.
  • Li A, Wu Y, Tang F, Li W, Feng X, Yao Z. In Vivo magnetic resonance imaging of CD8+ T lymphocytes recruiting to glioblastoma in mice. Cancer Biother Radiopharm. 2016;31(9):317–323. doi:10.1089/cbr.2016.2061.
  • Kikuchi M, Clump DA, Srivastava RM, Sun L, Zeng D, Diaz-Perez JA, Anderson CJ, Edwards WB, Ferris RL. Preclinical immunoPET/CT imaging using Zr-89-labeled anti-PD-L1 monoclonal antibody for assessing radiation-induced PD-L1 upregulation in head and neck cancer and melanoma. Oncoimmunology. 2017;6:e1329071. doi:10.1080/2162402X.2017.1329071.
  • Chatterjee S, Lesniak WG, Miller MS, Lisok A, Sikorska E, Wharram B, Kumar D, Gabrielson M, Pomper MG, Gabelli SB, et al. Rapid PD-L1 detection in tumors with PET using a highly specific peptide. Biochem Biophys Res Commun. 2017;483(1):258–263. doi:10.1016/j.bbrc.2016.12.156.
  • Keu KV, Witney TH, Yaghoubi S, Rosenberg J, Kurien A, Magnusson R, Williams J, Habte F, Wagner JR, Forman S, et al. Reporter gene imaging of targeted T cell immunotherapy in recurrent glioma. Sci Transl Med. 2017;9(373):eaag2196. doi:10.1126/scitranslmed.aag2196.
  • Kircher MF, Allport JR, Graves EE, Love V, Josephson L, Lichtman AH, Weissleder R. In vivo high resolution three-dimensional imaging of antigen-specific cytotoxic T-lymphocyte trafficking to tumors. Cancer Res. 2003;63:6838–6846.
  • Makela AV, Gaudet JM, Foster PJ. Quantifying tumor associated macrophages in breast cancer: a comparison of iron and fluorine-based MRI cell tracking. Sci Rep. 2017;7(1):1–9. doi:10.1038/srep42109.
  • Zhang X, de Chickera SN, Willert C, Economopoulos V, Noad J, Rohani R, Wang AY, Levings MK, Scheid E, Foley R, et al. Cellular magnetic resonance imaging of monocyte-derived dendritic cell migration from healthy donors and cancer patients as assessed in a scid mouse model. Cytotherapy. 2012;13:1234–1248. doi:10.3109/14653249.2011.605349.
  • Srinivas M, Aarntzen EHJG, Bulte JWM, Oyen WJ, Heerschap A, de Vries IJM, Figdor CG. Imaging of cellular therapies. Adv Drug Deliv Rev. 2010;62(11):1080–1093. doi:10.1016/j.addr.2010.08.009.
  • Smirnov P, Lavergne E, Gazeau F, Lewin M, Boissonnas A, Doan BT, Gillet B, Combadière C, Combadière B, Clément O, et al. In vivo cellular imaging of lymphocyte trafficking by MRI: A tumor model approach to cell‐based anticancer therapy. Magn Reson Med. 2006;56(3):498–508. doi:10.1002/mrm.20996.
  • Mallett CL, McFadden C, Chen Y, Foster PJ. Migration of iron-labeled KHYG-1 natural killer cells to subcutaneous tumors in nude mice, as detected by magnetic resonance imaging. Cytotherapy. 2012;14(6):743–751. doi:10.3109/14653249.2012.667874.
  • Korchinski DJ, Taha M, Yang R, Nathoo N, Dunn JF. Iron Oxide as an MRI Contrast Agent for Cell Tracking. Magn Reson Insights. 2015;8:15–29.
  • Tremblay M-L, Davis C, Bowen CV, Stanley O, Parsons C, Weir G, Karkada M, Stanford MM, Brewer KD. Using MRI cell tracking to monitor immune cell recruitment in response to a peptide-based cancer vaccine. Magn Reson Med. 2017;342:1432.
  • Rioux JA, Brewer KD, Beyea SD, Bowen CV. Quantification of superparamagnetic iron oxide with large dynamic range using TurboSPI. J Magn Reson. 2012;216:152–160. doi:10.1016/j.jmr.2012.01.017.
  • Rioux JA, Beyea SD, Bowen CV. 3D single point imaging with compressed sensing provides high temporal resolution R2* mapping for in vivo preclinical applications. MAGMA. 2017;30:41–55. doi:10.1007/s10334-016-0583-y.
  • Weir GM, Hrytsenko O, Quinton T, Berinstein NL, Stanford MM, Mansour M. Anti-PD-1 increases the clonality and activity of tumor infiltrating antigen specific T cells induced by a potent immune therapy consisting of vaccine and metronomic cyclophosphamide. J Immunother Cancer. 2016;4(1):68. doi:10.1186/s40425-016-0169-2.
  • Feltkamp MC, Smits HL, Vierboom MP, Minnaar RP, de Jongh BM, Drijfhout JW, Schegget JT, Melief CJM, Kast WM. Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur J Immunol. 1993;23(9):2242–2249. doi:10.1002/eji.1830230929.
  • Brewer KD, Weir GM, Dude I, Davis C, Parsons C, Penwell A, Rajagopalan R, Sammatur L, Bowen CV, Stanford MM, et al. Unique depot formed by an oil based vaccine facilitates active antigen uptake and provides effective tumour control. J Biomed Sci. 2018;25(1):7. doi:10.1186/s12929-018-0413-9.
  • Schindelin J, Rueden CT, Hiner MC, Eliceiri KW. The ImageJ ecosystem: an open platform for biomedical image analysis. Mol Reprod Dev. 2015;82(7–8):518–529. doi:10.1002/mrd.22489.
  • O’Brien-Moran Z, Bowen CV, Rioux JA, Brewer KD. Cell density quantification with TurboSPI: R2* mapping with compensation for off-resonance fat modulation. MAGMA. 2019;3:250.
  • Weir GM, Liwski RS, Mansour M. Immune Modulation by Chemotherapy or Immunotherapy to Enhance Cancer Vaccines. Cancers. 2011;3(3):3114–3142. doi:10.3390/cancers3033114.
  • Veglia F, Gabrilovich DI. Dendritic cells in cancer: the role revisited. Curr Opin Immunol. 2017;45:43–51. doi:10.1016/j.coi.2017.01.002.
  • Na YR, Jung D, Gu GJ, Seok SH. GM-CSF grown bone marrow derived cells are composed of phenotypically different dendritic cells and macrophages. Mol Cells. 2016;39:734–741.