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Original Research

CD44v6 as innovative sarcoma target for CAR-redirected CIK cells

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Article: e1423167 | Received 01 Sep 2017, Accepted 22 Dec 2017, Published online: 15 Feb 2018

References

  • Maula S, Huuhtanen RL, Blomqvist CP, Wiklund TA, Laurila P, Ristamäki R. The adhesion molecule CD44v6 is associated with a high risk for local recurrence in adult soft tissue sarcomas. Br J Cancer. 2001;84:244–52. doi:10.1054/bjoc.2000.1590. PMID:11161384.
  • Manten-Horst E, Danen EH, Smit L, Snoek M, Le Poole IC, Van Muijen GN, Pals ST, Ruiter DJ. Expression of CD44 splice variants in human cutaneous melanoma and melanoma cell lines is related to tumor progression and metastatic potential. Int J Cancer 1995;64:182–8. doi:10.1002/ijc.2910640307. PMID:7542641.
  • Kahara N, Ozaki T, Doi T, Nishida K, Kawai A, Shibahara M, et al. CD44 expression in soft tissue sarcomas. Virchows Arch. 2000;436:574–8. doi:10.1007/s004289900159. PMID:10917171.
  • Andritsch E, Beishon M, Bielack S, Bonvalot S, Casali P, Crul M, Delgado Bolton R, Donati DM, Douis H, Haas R, et al. ECCO Essential Requirements for Quality Cancer Care: Soft Tissue Sarcoma in Adults and Bone Sarcoma. A critical review. Crit Rev Oncol Hematol. 2017;110:94–105. doi:10.1016/j.critrevonc.2016.12.002.
  • Rosenberg SA. Cell transfer immunotherapy for metastatic solid cancer-what clinicians need to know. Nat Rev Clin Oncol. 2011;8:577–85. doi:10.1038/nrclinonc.2011.116. PMID:21808266.
  • Robbins PF, Morgan RA, Feldman SA, Yang JC, Sherry RM, Dudley ME, Wunderlich JR, Nahvi AV, Helman LJ, Mackall CL, et al. Tumor regression in patients with metastatic synovial cell sarcoma and melanoma using genetically engineered lymphocytes reactive with NY-ESO-1. J Clin Oncol. 2011;29:917–24. doi:10.1200/JCO.2010.32.2537. PMID:21282551.
  • Robbins PF, Kassim SH, Tran TL, Crystal JS, Morgan RA, Feldman SA, Yang JC, Dudley ME, Wunderlich JR, Sherry RM, et al. A pilot trial using lymphocytes genetically engineered with an NY-ESO-1-reactive T-cell receptor: long-term follow-up and correlates with response. Clin Cancer Res. 2015;21:1019–27. doi:10.1158/1078-0432.CCR-14-2708. PMID:25538264.
  • Schmidt-Wolf IG, Lefterova P, Mehta BA, Fernandez LP, Huhn D, Blume KG, Weissman IL, Negrin RS. Phenotypic characterization and identification of effector cells involved in tumor cell recognition of cytokine-induced killer cells. Exp Hematol 1993;21:1673–9. PMID:7694868.
  • Schmidt-Wolf IG, Finke S, Trojaneck B, Denkena A, Lefterova P, Schwella N, Heuft HG, Prange G, Korte M, Takeya M, et al. Phase I clinical study applying autologous immunological effector cells transfected with the interleukin-2 gene in patients with metastatic renal cancer, colorectal cancer and lymphoma. Br J Cancer 1999;81:1009–16. doi:10.1038/sj.bjc.6690800. PMID:10576658.
  • Gammaitoni L, Giraudo L, Leuci V, Todorovic M, Mesiano G, Picciotto F, Pisacane A, Zaccagna A, Volpe MG, Gallo S, et al. Effective Activity of Cytokine Induced Killer Cells against Autologous Metastatic Melanoma including Cells with Stemness Features. Clin Cancer Res. 2013;19(16):4347–58. doi:10.1158/1078-0432.CCR-13-0061 PMID:23794732.
  • Sangiolo D, Mesiano G, Gammaitoni L, Leuci V, Todorovic M, Giraudo L, Cammarata C, Dell'Aglio C, D'Ambrosio L, Pisacane A, et al. Cytokine-induced killer cells eradicate bone and soft-tissue sarcomas. Cancer Res. 2014;74:119–29. doi:10.1158/0008-5472.CAN-13-1559. PMID:24356422.
  • Gammaitoni L, Giraudo L, Macagno M, Leuci V, Mesiano G, Rotolo R, Sassi F, Sanlorenzo M, Zaccagna A, Pisacane A, et al. Cytokine-Induced Killer Cells Kill Chemo-surviving Melanoma Cancer Stem Cells. Clin Cancer Res. 2017;23:2277–88. doi:10.1158/1078-0432.CCR-16-1524. PMID:27815354.
  • Cappuzzello E, Tosi A, Zanovello P, Sommaggio R, Rosato A. Retargeting cytokine-induced killer cell activity by CD16 engagement with clinical-grade antibodies. Oncoimmunology. 2016;5:e1199311. doi:10.1080/2162402X.2016.1199311. PMID:27622068.
  • Olioso P, Giancola R, Di Riti M, Contento A, Accorsi P, Iacone A. Immunotherapy with cytokine induced killer cells in solid and hematopoietic tumours: a pilot clinical trial. Hematol Oncol. 2009. doi:10.1002/hon.886. PMID:19294626.
  • Giraudo L, Gammaitoni L, Cangemi M, Rotolo R, Aglietta M, Sangiolo D. Cytokine-induced killer cells as immunotherapy for solid tumors: current evidences and perspectives. Immunotherapy. 2015;7(9):999–1010. doi:10.2217/imt.15.61. PMID:26310715.
  • Pan K, Guan XX, Li YQ, Zhao JJ, Li JJ, Qiu HJ, Weng DS, Wang QJ, Liu Q, Huang LX, et al. Clinical activity of adjuvant cytokine-induced killer cell immunotherapy in patients with post-mastectomy triple-negative breast cancer. Clin Cancer Res. 2014;20:3003–11. doi:10.1158/1078-0432.CCR-14-0082. PMID:24668644.
  • Schmeel LC, Schmeel FC, Coch C, Schmidt-Wolf IG. Cytokine-induced killer (CIK) cells in cancer immunotherapy: report of the international registry on CIK cells (IRCC). J Cancer Res Clin Oncol. 2015;141(5):839–49. doi:10.1007/s00432-014-1864-3. PMID:25381063.
  • Cosman D, Mullberg J, Sutherland CL, Chin W, Armitage R, Fanslow W, Kubin M, Chalupny NJ. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity. 2001;14:123–33. doi:10.1016/S1074-7613(01)00095-4. PMID:11239445.
  • Groh V, Rhinehart R, Secrist H, Bauer S, Grabstein KH, Spies T. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci U S A 1999;96:6879–84. doi:10.1073/pnas.96.12.6879. PMID:10359807.
  • Sangiolo D, Martinuzzi E, Todorovic M, Vitaggio K, Vallario A, Jordaney N, Carnevale-Schianca F, Capaldi A, Geuna M, Casorzo L, et al. Alloreactivity and anti-tumor activity segregate within two distinct subsets of cytokine-induced killer (CIK) cells: implications for their infusion across major HLA barriers. Int Immunol. 2008;20:841–8. doi:10.1093/intimm/dxn042. PMID:18469328.
  • Elia AR, Circosta P, Sangiolo D, Bonini C, Gammaitoni L, Mastaglio S, Genovese P, Geuna M, Avolio F, Inghirami G, et al. Cytokine-induced killer cells engineered with exogenous T-cell receptors directed against melanoma antigens: enhanced efficacy of effector cells endowed with a double mechanism of tumor recognition. Hum Gene Ther. 2015;26:220–31. doi:10.1089/hum.2014.112. PMID:25758764.
  • Leuci V, Mesiano G, Gammaitoni L, Aglietta M, Sangiolo D. Genetically Redirected T Lymphocytes for Adoptive Immunotherapy of Solid Tumors. Curr Gene Ther. 2013.
  • Gill S, June CH. Going viral: chimeric antigen receptor T-cell therapy for hematological malignancies. Immunol Rev. 2015;263:68–89. doi:10.1111/imr.12243. PMID:25510272.
  • Dotti G, Savoldo B, Brenner M. Fifteen years of gene therapy based on chimeric antigen receptors: “are we nearly there yet?”. Hum Gene Ther. 2009;20:1229–39. doi:10.1089/hum.2009.142. PMID:19702437.
  • Eshhar Z, Waks T, Gross G, Schindler DG. Specific activation and targeting of cytotoxic lymphocytes through chimeric single chains consisting of antibody-binding domains and the gamma or zeta subunits of the immunoglobulin and T-cell receptors. Proc Natl Acad Sci U S A 1993;90:720–4. doi:10.1073/pnas.90.2.720. PMID:8421711.
  • Ahmed N, Brawley VS, Hegde M, Robertson C, Ghazi A, Gerken C, Liu E, Dakhova O, Ashoori A, Corder A, et al. Human Epidermal Growth Factor Receptor 2 (HER2) -Specific Chimeric Antigen Receptor-Modified T Cells for the Immunotherapy of HER2-Positive Sarcoma. J Clin Oncol. 2015;33:1688–96. doi:10.1200/JCO.2014.58.0225. PMID:25800760.
  • Leemhuis T, Wells S, Scheffold C, Edinger M, Negrin RS. A phase I trial of autologous cytokine-induced killer cells for the treatment of relapsed Hodgkin disease and non-Hodgkin lymphoma. BiolBlood Marrow Transplant. 2005;11:181–7. doi:10.1016/j.bbmt.2004.11.019.
  • Li R, Wang C, Liu L, Du C, Cao S, Yu J, et al. Autologous cytokine-induced killer cell immunotherapy in lung cancer: a phase II clinical study. Cancer Immunol Immunother. 2012;61:2125–33. doi:10.1007/s00262-012-1260-2. PMID:22581306.
  • Olioso P, Giancola R, Di Riti M, Contento A, Accorsi P, Iacone A. Immunotherapy with cytokine induced killer cells in solid and hematopoietic tumours: a pilot clinical trial. Hematol Oncol. 2009;27:130–9. doi:10.1002/hon.886. PMID:19294626.
  • Nishimura R, Baker J, Beilhack A, Zeiser R, Olson JA, Sega EI, Karimi M, Negrin RS. In vivo trafficking and survival of cytokine-induced killer cells resulting in minimal GVHD with retention of antitumor activity. Blood. 2008;112:2563–74. doi:10.1182/blood-2007-06-092817. PMID:18565854.
  • Pizzitola I, Anjos-Afonso F, Rouault-Pierre K, Lassailly F, Tettamanti S, Spinelli O, Biondi A, Biagi E, Bonnet D. Chimeric antigen receptors against CD33/CD123 antigens efficiently target primary acute myeloid leukemia cells in vivo. Leukemia. 2014;28:1596–605. doi:10.1038/leu.2014.62. PMID:24504024.
  • Tettamanti S, Marin V, Pizzitola I, Magnani CF, Giordano Attianese GM, Cribioli E, Maltese F, Galimberti S, Lopez AF, Biondi A, et al. Targeting of acute myeloid leukaemia by cytokine-induced killer cells redirected with a novel CD123-specific chimeric antigen receptor. Br J Haematol. 2013;161:389–401. doi:10.1111/bjh.12282. PMID:23432359.
  • Hombach AA, Rappl G, Abken H. Arming cytokine-induced killer cells with chimeric antigen receptors: CD28 outperforms combined CD28-OX40 “super-stimulation”. Mol Ther. 2013;21:2268–77. doi:10.1038/mt.2013.192. PMID:23985696.
  • Oelsner S, Wagner J, Friede ME, Pfirrmann V, Genßler S, Rettinger E, Buchholz CJ, Pfeifer H, Schubert R, Ottmann OG, et al. CAR-engineered cytokine-induced killer cells overcome treatment resistance of pre-B-ALL and enhance survival. Int J Cancer. 2016;139(8):1799–809. doi:10.1002/ijc.30217. PMID:27253354.
  • Zuo S, Wen Y, Panha H, Dai G, Wang L, Ren X, Fu K. Modification of cytokine-induced killer cells with folate receptor alpha (FRα)-specific chimeric antigen receptors enhances their antitumor immunity toward FRα-positive ovarian cancers. Mol Immunol. 2017;85:293–304. doi:10.1016/j.molimm.2017.03.017. PMID:28360017.
  • Guo X, Zheng H, Luo W, Zhang Q, Liu J, Yao K. 5T4-specific chimeric antigen receptor modification promotes the immune efficacy of cytokine-induced killer cells against nasopharyngeal carcinoma stem cell-like cells. Sci Rep. 2017;7:4859. doi:10.1038/s41598-017-04756-9. PMID:28687750.
  • Zöller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule? Nat Rev Cancer. 2011;11:254–67. doi:10.1038/nrc3023. PMID:21390059.
  • Casucci M, Nicolis di Robilant B, Falcone L, Camisa B, Norelli M, Genovese P, Gentner B, Gullotta F, Ponzoni M, Bernardi M, et al. CD44v6-targeted T cells mediate potent antitumor effects against acute myeloid leukemia and multiple myeloma. Blood. 2013;122:3461–72. doi:10.1182/blood-2013-04-493361. PMID:24016461.
  • Kuryu M, Ozaki T, Nishida K, Shibahara M, Kawai A, Inoue H. Expression of CD44 variants in osteosarcoma. J Cancer Res Clin Oncol 1999;125:646–52. doi:10.1007/s004320050329. PMID:10541973.
  • Gammaitoni L, Giraudo L, Macagno M, Leuci V, Mesiano G, Rotolo R, Sassi F, Sanlorenzo M, Zaccagna A, Pisacane A, et al. Cytokine-Induced Killer Cells Kill Chemo-surviving Melanoma Cancer Stem Cells. Clin Cancer Res. 2017;23(9):2277–88. doi:10.1158/1078-0432.CCR-16-1524. PMID:27815354.
  • Marin V, Kakuda H, Dander E, Imai C, Campana D, Biondi A, D'Amico G. Enhancement of the anti-leukemic activity of cytokine induced killer cells with an anti-CD19 chimeric receptor delivering a 4-1BB-zeta activating signal. Exp Hematol. 2007;35:1388–97. doi:10.1016/j.exphem.2007.05.018. PMID:17656004.
  • Ren X, Ma W, Lu H, Yuan L, An L, Wang X, Cheng G, Zuo S. Modification of cytokine-induced killer cells with chimeric antigen receptors (CARs) enhances antitumor immunity to epidermal growth factor receptor (EGFR)-positive malignancies. Cancer Immunol Immunother. 2015;64:1517–29. doi:10.1007/s00262-015-1757-6. PMID:26386966.
  • Huang X, Park H, Greene J, Pao J, Mulvey E, Zhou SX, Albert CM, Moy F, Sachdev D, Yee D, et al. IGF1R- and ROR1-Specific CAR T Cells as a Potential Therapy for High Risk Sarcomas. PLoS One. 2015;10:e0133152. doi:10.1371/journal.pone.0133152. PMID:26173023.
  • Schönfeld K, Sahm C, Zhang C, Naundorf S, Brendel C, Odendahl M, Nowakowska P, Bönig H, Köhl U, Kloess S, et al. Selective inhibition of tumor growth by clonal NK cells expressing an ErbB2/HER2-specific chimeric antigen receptor. Mol Ther. 2015;23:330–8. doi:10.1038/mt.2014.219. PMID:25373520.
  • Arai S, Meagher R, Swearingen M, Myint H, Rich E, Martinson J, et al. Infusion of the allogeneic cell line NK-92 in patients with advanced renal cell cancer or melanoma: a phase I trial. Cytotherapy. 2008;10:625–32. doi:10.1080/14653240802301872. PMID:18836917.
  • Tonn T, Schwabe D, Klingemann HG, Becker S, Esser R, Koehl U, et al. Treatment of patients with advanced cancer with the natural killer cell line NK-92. Cytotherapy. 2013;15:1563–70. doi:10.1016/j.jcyt.2013.06.017. PMID:24094496.
  • Gauthier J, Yakoub-Agha I. Chimeric antigen-receptor T-cell therapy for hematological malignancies and solid tumors: Clinical data to date, current limitations and perspectives. Curr Res Transl Med. 2017;65:93–102. doi:10.1016/j.retram.2017.08.003. PMID:28988742.
  • Maus MV, Levine BL. Chimeric Antigen Receptor T-Cell Therapy for the Community Oncologist. Oncologist. 2016;21:608–17. doi:10.1634/theoncologist.2015-0421. PMID:27009942.
  • Suzuki A, Leland P, Joshi BH, Puri RK. Targeting of IL-4 and IL-13 receptors for cancer therapy. Cytokine. 2015;75:79–88. doi:10.1016/j.cyto.2015.05.026. PMID:26088753.
  • Spear P, Barber A, Rynda-Apple A, Sentman CL. Chimeric antigen receptor T cells shape myeloid cell function within the tumor microenvironment through IFN-γ and GM-CSF. J Immunol. 2012;188:6389–98. doi:10.4049/jimmunol.1103019. PMID:22586039.
  • Toi M, Bicknell R, Harris AL. Inhibition of colon and breast carcinoma cell growth by interleukin-4. Cancer Res 1992;52:275–9. PMID:1728401.
  • Börjesson PK, Postema EJ, Roos JC, Colnot DR, Marres HA, van Schie MH, Stehle G, de Bree R, Snow GB, Oyen WJ, et al. Phase I therapy study with (186)Re-labeled humanized monoclonal antibody BIWA 4 (bivatuzumab) in patients with head and neck squamous cell carcinoma. Clin Cancer Res. 2003;9:3961. S-72S.
  • Tijink BM, Buter J, de Bree R, Giaccone G, Lang MS, Staab A, et al. A phase I dose escalation study with anti-CD44v6 bivatuzumab mertansine in patients with incurable squamous cell carcinoma of the head and neck or esophagus. Clin Cancer Res. 2006;12:6064–72. doi:10.1158/1078-0432.CCR-06-0910. PMID:17062682.
  • Zhang Y, Ding C, Wang J, Sun G, Cao Y, Xu L, Zhou L, Chen X. Prognostic significance of CD44V6 expression in osteosarcoma: a meta-analysis. J Orthop Surg Res. 2015;10:187. doi:10.1186/s13018-015-0328-z. PMID:26697855.
  • Irsan I, Akisue T, Hara H, Fujimoto T, Imabori M, Doita M, Kuroda R, Fujioka H, Kawamoto T, Yamamoto T, et al. Imatinib mesylate inhibits tumorigenicity of malignant fibrous histiocytoma cells in vivo. Anticancer Res. 2007;27:423–9. PMID:17352263.
  • Germano G, Frapolli R, Simone M, Tavecchio M, Erba E, Pesce S, Pasqualini F, Grosso F, Sanfilippo R, Casali PG, et al. Antitumor and anti-inflammatory effects of trabectedin on human myxoid liposarcoma cells. Cancer Res. 2010;70:2235–44. doi:10.1158/0008-5472.CAN-09-2335. PMID:20215499.
  • Fernández L, Metais JY, Escudero A, Vela M, Valentín J, Vallcorba I, Leivas A, Torres J, Valeri A, Patiño-García A, et al. MEMORY T CELLS EXPRESSING AN NKG2D-CAR EFFICIENTLY TARGET OSTEOSARCOMA CELLS. Clin Cancer Res. 2017;23(19):5824–35. doi:10.1158/1078-0432.CCR-17-0075.