1,702
Views
20
CrossRef citations to date
0
Altmetric
Original Research

In situ delivery of allogeneic natural killer cell (NK) combined with Cetuximab in liver metastases of gastrointestinal carcinoma: A phase I clinical trial

, , , ORCID Icon, , , , , , , , , , , , , , , , & show all
Article: e1424673 | Received 29 Sep 2017, Accepted 03 Jan 2018, Published online: 19 Mar 2018

References

  • Vivier E, Tomasello E, Baratin M, Walzer T, Ugolini S. Functions of natural killer cells. Nat Immunol. 2008;9:503–10. doi:10.1038/ni1582.
  • Borg C, Jalil A, Laderach D, Maruyama K, Wakasugi H, Charrier S, Ryffel B, Cambi A, Figdor C, Vainchenker W, et al. NK cell activation by dendritic cells (DCs) requires the formation of a synapse leading to IL-12 polarization in DCs. Blood. 2004;104:3267–75. doi:10.1182/blood-2004-01-0380.
  • Martín-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, Sallusto F. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol. 2004;5:1260–5. doi:10.1038/ni1138.
  • Falco M, Moretta L, Moretta A, Bottino C. KIR and KIR ligand polymorphism: a new area for clinical applications? Tissue Antigens. 2013;82:363–73. doi:10.1111/tan.12262.
  • Bachanova V, Miller JS. NK cells in therapy of cancer. Crit Rev Oncog. 2014;19:133–41. doi:10.1615/CritRevOncog.2014011091.
  • Berraondo P, Labiano S, Minute L, Etxeberria I, Vasquez M, Sanchez-Arraez A, Teijeira A, Melero I. Cellular immunotherapies for cancer. Oncoimmunology. 2017;6:e1306619. doi:10.1080/2162402X.2017.1306619.
  • Ruggeri L, Capanni M, Urbani E, Perruccio K, Shlomchik WD, Tosti A, Posati S, Rogaia D, Frassoni F, Aversa F, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295:2097–100. doi:10.1126/science.1068440.
  • Passweg JR, Tichelli A, Meyer-Monard S, Heim D, Stern M, Kühne T, Favre G, Gratwohl A. Purified donor NK-lymphocyte infusion to consolidate engraftment after haploidentical stem cell transplantation. Leukemia. 2004;18:1835–8. doi:10.1038/sj.leu.2403524.
  • Miller JS, Soignier Y, Panoskaltsis-Mortari A, McNearney SA, Yun GH, Fautsch SK, McKenna D, Le C, Defor TE, Burns LJ, et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood. 2005;105:3051–7. doi:10.1182/blood-2004-07-2974.
  • Curti A, Ruggeri L, Parisi S, Bontadini A, Dan E, Motta MR, Rizzi S, Trabanelli S, Ocadlikova D, Lecciso M, et al. Larger size of donor alloreactive NK Cell repertoire correlates with better response to NK cell immunotherapy in elderly acute myeloid leukemia patients. Clin Cancer Res. 2016;22:1914–21. doi:10.1158/1078-0432.CCR-15-1604.
  • Curti A, Ruggeri L, D'Addio A, Bontadini A, Dan E, Motta MR, Trabanelli S, Giudice V, Urbani E, Martinelli G, et al. Successful transfer of alloreactive haploidentical KIR ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients. Blood. 2011;118:3273–9. doi:10.1182/blood-2011-01-329508.
  • Rubnitz JE, Inaba H, Ribeiro RC, Pounds S, Rooney B, Bell T, Pui C-H, Leung W. NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J Clin Oncol. 2010;28:955–9. doi:10.1200/JCO.2009.24.4590.
  • 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.
  • Frohn C, Doehn C, Durek C, Böhle A, Schlenke P, Jocham D, Kirchner H. Feasibility of the adoptive transfusion of allogenic human leukocyte antigen-matched natural killer cells in patients with renal cell carcinoma. J Immunother. 2000;23:499–504. doi:10.1097/00002371-200007000-00014.
  • Parkhurst MR, Riley JP, Dudley ME, Rosenberg SA. Adoptive transfer of autologous natural killer cells leads to high levels of circulating natural killer cells but does not mediate tumor regression. Clin Cancer Res. 2011;17:6287–97. doi:10.1158/1078-0432.CCR-11-1347.
  • Naramura M, Gillies SD, Mendelsohn J, Reisfeld RA, Mueller BM. Therapeutic potential of chimeric and murine anti-(epidermal growth factor receptor) antibodies in a metastasis model for human melanoma. Cancer Immunol Immunother. 37:343–9. doi:10.1007/BF01518458.
  • Sliwkowski MX, Mellman I. Antibody therapeutics in cancer. Science. 2013;341:1192–8. doi:10.1126/science.1241145.
  • Srivastava AK, Jaganathan S, Stephen L, Hollingshead MG, Layhee A, Damour E, Govindharajulu JP, Donohue J, Esposito D, Mapes JP, et al. Effect of a Smac Mimetic (TL32711, Birinapant) on the apoptotic program and apoptosis biomarkers examined with validated multiplex immunoassays fit for clinical use. Clin Cancer Res. 2016;22:1000–10. doi:10.1158/1078-0432.CCR-14-3156.
  • Trotta AM, Ottaiano A, Romano C, Nasti G, Nappi A, De Divitiis C, Napolitano M, Zanotta S, Casaretti R, D'Alterio C, et al. Prospective evaluation of cetuximab-mediated antibody-dependent cell cytotoxicity in metastatic colorectal cancer patients predicts treatment efficacy. Cancer Immunol Res. 2016;4:366–74. doi:10.1158/2326-6066.CIR-15-0184.
  • Shah NN, Baird K, Delbrook CP, Fleisher TA, Kohler ME, Rampertaap S, Lemberg K, Hurley CK, Kleiner DE, Merchant MS, et al. Acute GVHD in patients receiving IL-15/4-1BBL activated NK cells following T-cell-depleted stem cell transplantation. Blood. 2015;125:784–92. doi:10.1182/blood-2014-07-592881.
  • Marçais A, Cherfils-Vicini J, Viant C, Degouve S, Viel S, Fenis A, Rabilloud J, Mayol K, Tavares A, Bienvenu J, et al. The metabolic checkpoint kinase mTOR is essential for IL-15 signaling during the development and activation of NK cells. Nat Immunol. 2014;15:749–57. doi:10.1038/ni.2936.
  • Wherry EJ. T cell exhaustion. Nat Immunol. 2011;12:492–9. doi:10.1038/ni.2035.
  • Lin S-J, Peacock CD, Bahl K, Welsh RM. Programmed death-1 (PD-1) defines a transient and dysfunctional oligoclonal T cell population in acute homeostatic proliferation. J Exp Med. 2007;204:2321–33. doi:10.1084/jem.20062150.
  • Gros A, Parkhurst MR, Tran E, Pasetto A, Robbins PF, Ilyas S, Prickett TD, Gartner JJ, Crystal JS, Roberts IM, et al. Prospective identification of neoantigen-specific lymphocytes in the peripheral blood of melanoma patients. Nat Med. 2016;22:433–8. doi:10.1038/nm.4051.
  • Fourcade J, Sun Z, Benallaoua M, Guillaume P, Luescher IF, Sander C, Kirkwood JM, Kuchroo V, Zarour HM. Upregulation of Tim-3 and PD-1 expression is associated with tumor antigen-specific CD8+ T cell dysfunction in melanoma patients. J Exp Med. 2010;207:2175–86. doi:10.1084/jem.20100637.
  • Benyunes MC, Higuchi C, York A, Lindgren C, Thompson JA, Buckner CD, Fefer A. Immunotherapy with interleukin 2 with or without lymphokine-activated killer cells after autologous bone marrow transplantation for malignant lymphoma: a feasibility trial. Bone Marrow Transplant. 1995;16:283–8.
  • Rosenberg SA, Lotze MT, Muul LM, Leitman S, Chang AE, Ettinghausen SE, Matory YL, Skibber JM, Shiloni E, Vetto JT. Observations on the systemic administration of autologous lymphokine-activated killer cells and recombinant interleukin-2 to patients with metastatic cancer. N Engl J Med. 1985;313:1485–92. doi:10.1056/NEJM198512053132327.
  • Wallen H, Thompson JA, Reilly JZ, Rodmyre RM, Cao J, Yee C. Fludarabine modulates immune response and extends in vivo survival of adoptively transferred CD8T cells in patients with metastatic melanoma. PloS One. 2009;4:e4749. doi:10.1371/journal.pone.0004749.
  • Qin Z, Chen J, Zeng J, Niu L, Xie S, Wang X, Liang Y, Wu Z, Zhang M. Effect of NK cell immunotherapy on immune function in patients with hepatic carcinoma: A preliminary clinical study. Cancer Biol Ther. 2017;18:323–30.
  • Bachanova V, Burns LJ, McKenna DH, Curtsinger J, Panoskaltsis-Mortari A, Lindgren BR, Cooley S, Weisdorf D, Miller JS. Allogeneic natural killer cells for refractory lymphoma. Cancer Immunol Immunother CII. 2010;59:1739–44. doi:10.1007/s00262-010-0896-z.
  • Geller MA, Cooley S, Judson PL, Ghebre R, Carson LF, Argenta PA, Jonson AL, Panoskaltsis-Mortari A, Curtsinger J, McKenna D, et al. A phase II study of allogeneic natural killer cell therapy to treat patients with recurrent ovarian and breast cancer. Cytotherapy. 2011;13:98–107. doi:10.3109/14653249.2010.515582.
  • Miller JS. Therapeutic applications: natural killer cells in the clinic. Hematol Am Soc Hematol Educ Program. 2013;2013:247–53.
  • Sim GC, Martin-Orozco N, Jin L, Yang Y, Wu S, Washington E, Sanders D, Lacey C, Wang Y, Vence L, et al. IL-2 therapy promotes suppressive ICOS+ Treg expansion in melanoma patients. J Clin Invest. 2014;124:99–110. doi:10.1172/JCI46266.
  • Yao X, Ahmadzadeh M, Lu Y-C, Liewehr DJ, Dudley ME, Liu F, Schrump DS, Steinberg SM, Rosenberg SA, Robbins PF. Levels of peripheral CD4(+)FoxP3(+) regulatory T cells are negatively associated with clinical response to adoptive immunotherapy of human cancer. Blood. 2012;119:5688–96. doi:10.1182/blood-2011-10-386482.
  • Bachanova V, Cooley S, Defor TE, Verneris MR, Zhang B, McKenna DH, Curtsinger J, Panoskaltsis-Mortari A, Lewis D, Hippen K, et al. Clearance of acute myeloid leukemia by haploidentical natural killer cells is improved using IL-2 diphtheria toxin fusion protein. Blood. 2014;123:3855–63. doi:10.1182/blood-2013-10-532531.
  • Barkholt L, Danielsson R, Calissendorff B, Svensson L, Malihi R, Remberger M, Uzunel M, Thörne A, Ringdén O. Indium-111-labelled donor-lymphocyte infusion by way of hepatic artery and radio-frequency ablation against liver metastases of renal and colon carcinoma after allogeneic hematopoietic stem-cell transplantation. Transplantation. 2004;78:697–703. doi:10.1097/01.TP.0000129807.53523.97.
  • Katz SC, Burga RA, McCormack E, Wang LJ, Mooring W, Point GR, Khare PD, Thorn M, Ma Q, Stainken BF, et al. Phase I Hepatic Immunotherapy for Metastases Study of Intra-Arterial Chimeric Antigen Receptor-Modified T-cell Therapy for CEA+ Liver Metastases. Clin Cancer Res. 2015;21:3149–59. doi:10.1158/1078-0432.CCR-14-1421.
  • Benson DM, Caligiuri MA. Killer immunoglobulin-like receptors and tumor immunity. Cancer Immunol Res. 2014;2:99–104. doi:10.1158/2326-6066.CIR-13-0219.
  • Koehl U, Kalberer C, Spanholtz J, Lee DA, Miller JS, Cooley S, Lowdell M, Uharek L, Klingemann H, Curti A, et al. Advances in clinical NK cell studies: Donor selection, manufacturing and quality control. Oncoimmunology. 2016;5:e1115178. doi:10.1080/2162402X.2015.1115178.
  • Taylor RJ, Saloura V, Jain A, Goloubeva O, Wong S, Kronsberg S, Nagilla M, Silpino L, de Souza J, Seiwert T, et al. Ex vivo antibody-dependent cellular cytotoxicity inducibility predicts efficacy of cetuximab. Cancer Immunol Res. 2015;3:567–74. doi:10.1158/2326-6066.CIR-14-0188.
  • Binyamin L, Alpaugh RK, Hughes TL, Lutz CT, Campbell KS, Weiner LM. Blocking NK cell inhibitory self-recognition promotes antibody-dependent cellular cytotoxicity in a model of anti-lymphoma therapy. J Immunol. 2008;180:6392–401. doi:10.4049/jimmunol.180.9.6392.
  • Roberti MP, Juliá EP, Rocca YS, Amat M, Bravo AI, Loza J, Coló F, Loza CM, Fabiano V, Maino M, et al. Overexpression of CD85j in TNBC patients inhibits Cetuximab-mediated NK-cell ADCC but can be restored with CD85j functional blockade. Eur J Immunol. 2015;45:1560–9. doi:10.1002/eji.201445353.
  • Kohrt HE, Thielens A, Marabelle A, Sagiv-Barfi I, Sola C, Chanuc F, Fuseri N, Bonnafous C, Czerwinski D, Rajapaksa A, et al. Anti-KIR antibody enhancement of anti-lymphoma activity of natural killer cells as monotherapy and in combination with anti-CD20 antibodies. Blood. 2014;123:678–86. doi:10.1182/blood-2013-08-519199.
  • Vey N, Bourhis J-H, Boissel N, Bordessoule D, Prebet T, Charbonnier A, Etienne A, Andre P, Romagne F, Benson D, et al. A phase 1 trial of the anti-inhibitory KIR mAb IPH2101 for AML in complete remission. Blood. 2012;120:4317–23. doi:10.1182/blood-2012-06-437558.
  • Oberschmidt O, Kloess S, Koehl U. Redirected primary human chimeric antigen receptor natural killer cells as an “Off-the-Shelf Immunotherapy” for improvement in cancer treatment. Front Immunol. 2017;8:654. doi:10.3389/fimmu.2017.00654.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.