Cancer immunotherapy: accomplishments to date and future promise

Papers of special note have been highlighted as: ▪ of interest

References

• 1  Finn OJ. Immuno-oncology: understanding the function and dysfunction of the immune system in cancer. Ann. Oncol.23,viii6–viii9 (2012).
  MedlineGoogle Scholar
• 2  Hanahan D, Weinberg R. Hallmarks of cancer: the next generation. Cell144,646–674 (2011).▪ Updated version of the classic review article discussing the hallmark features of malignant cells. The key additions to this update include immune evasion and reprogramming energy metabolism.
  Medline CASGoogle Scholar
• 3  Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity‘s roles in cancer suppression and promotion. Science331,1565–1570 (2011).▪ Excellent review article discussing the key experiments supporting the concept of cancer immunoediting and how the immune system functions initially as a barrier to tumor growth, and later as a selective force driving the outgrowth of immune-resistant tumor cells.
  Medline CASGoogle Scholar
• 4  Burnet M. Cancer: a biological approach. I. The processes of control. Br. Med. J.1,779–786 (1957).▪ Seminal paper first discussing the concept of immunosurveillance.
  Medline CASGoogle Scholar
• 5  Roithmaier S, Haydon AM, Loi S et al. Incidence of malignancies in heart and/or lung transplant recipients: a single-institution experience. J. Heart Lung Transpl.26,845–849 (2007).
  MedlineGoogle Scholar
• 6  Vajdic CM, van Leeuwen MT. Cancer incidence and risk factors after solid organ transplantation. Int. J. Cancer125,1747–1754 (2009).
  Medline CASGoogle Scholar
• 7  Restifo NP, Esquivel F, Kawakami Y et al. Identification of human cancers deficient in antigen processing. J. Exp. Med.177,265–272 (1993).
  Medline CASGoogle Scholar
• 8  Vivier E, Ugolini S, Blaise D, Chabannon C, Brossay L. Targeting natural killer cells and natural killer T cells in cancer. Nat. Rev. Immunol.12,239–252 (2012).▪ Comprehensive recent review article describing the role of natural cells and natural killer T cells in cancer and how they may be exploited for therapy.
  Medline CASGoogle Scholar
• 9  Karre K, Ljunggren HG, Piontek G, Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature319,675–678 (1986).▪ Describes the concept of ‘missing self‘ in which NK cells are able to recognize and eliminate tumor cells that downregulate MHC class I molecules to avoid foreign antigen presentation.
  Medline CASGoogle Scholar
• 10  Prehn RT, Main JM. Immunity to methylcholanthrene-induced sarcomas. J. Natl Cancer Inst.18,769–778 (1957).
  Medline CASGoogle Scholar
• 11  van der Bruggen P, Traversari C, Chomez P et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science254,1643–1647 (1991).
  Medline CASGoogle Scholar
• 12  Graziano DF, Finn OJ. Tumor antigens and tumor antigen discovery. Cancer Treat. Res.123,89–111 (2005).
  Medline CASGoogle Scholar
• 13  Rabinovich GA, Gabrilovich D, Sotomayor EM. Immunosuppressive strategies that are mediated by tumor cells. Annu. Rev. Immunol.25,267–296 (2007).
  Medline CASGoogle Scholar
• 14  Houston A, Bennett MW, O‘Sullivan GC, Shanahan F, O‘Connell J. Fas ligand mediates immune privilege and not inflammation in human colon cancer, irrespective of TGF-beta expression. Br. J. Cancer89,1345–1351 (2003).
  Medline CASGoogle Scholar
• 15  Teicher BA. Transforming growth factor-β and the immune response to malignant disease. Clin. Cancer Res.13,6247–6251 (2007).
  Medline CASGoogle Scholar
• 16  Uyttenhove C, Pilotte L, Theate I et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat. Med.9,1269–1274 (2003).
  Medline CASGoogle Scholar
• 17  Muller AJ, Prendergast GC. Indoleamine 2,3-dioxygenase in immune suppression and cancer. Curr. Cancer Drug Targets7,31–40 (2007).
  Medline CASGoogle Scholar
• 18  Munn DH, Zhou M, Attwood JT et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science281,1191–1193 (1998).
  Medline CASGoogle Scholar
• 19  Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat. Rev. Immunol.6,295–307 (2006).
  Medline CASGoogle Scholar
• 20  Woo EY, Chu CS, Goletz TJ et al. Regulatory CD4⁺CD25⁺ T cells in tumors from patients with early-stage non-small cell lung cancer and late-stage ovarian cancer. Cancer Res.61,4766–4772 (2001).
  Medline CASGoogle Scholar
• 21  Bergmann C, Strauss L, Zeidler R, Lang S, Whiteside TL. Expansion of human T regulatory type 1 cells in the microenvironment of cyclooxygenase 2 overexpressing head and neck squamous cell carcinoma. Cancer Res.67,8865–8873 (2007).
  Medline CASGoogle Scholar
• 22  Bergmann C, Strauss L, Zeidler R, Lang S, Whiteside T. Expansion and characteristics of human T regulatory type 1 cells in co-cultures simulating tumor microenvironment. Cancer Immunol. Immunother.56,1429–1442 (2007).
  MedlineGoogle Scholar
• 23  Fecci PE, Mitchell DA, Whitesides JF et al. Increased regulatory T-cell fraction amidst a diminished CD4 compartment explains cellular immune defects in patients with malignant glioma. Cancer Res.66,3294–3302 (2006).
  Medline CASGoogle Scholar
• 24  Nagaraj S, Gabrilovich DI. Myeloid-derived suppressor cells. Adv. Exp. Med. Biol.601,213–223 (2007).
  MedlineGoogle Scholar
• 25  Old LJ. Immunotherapy for cancer. Sci. Am.275,136–143 (1996).
  Medline CASGoogle Scholar
• 26  Coley WB. The treatment of malignant tumors by repeated inoculations of erysipelas. With a report of ten original cases. 1893. Clin. Orthop. Relat. Res.262,3–11 (1991).
  MedlineGoogle Scholar
• 27  Eggermont AMM. Can immuno-oncology offer a truly pan-tumour approach to therapy? Annals Oncol.23,viii53–viii57 (2012).
  MedlineGoogle Scholar
• 28  Challis GB, Stam HJ. The spontaneous regression of cancer. A review of cases from 1900 to 1987. Acta Oncol.29,545–550 (1990).
  Medline CASGoogle Scholar
• 29  Finn OJ. Cancer immunology. N. Engl. J. Med.358,2704–2715 (2008).
  Medline CASGoogle Scholar
• 30  Rosenberg AA, Yang JC, Topalian SL et al. Treatment of 283 consecutive patients with metastatic melanoma or renal cell cancer using high-dose bolus interleukin 2. JAMA271,907–913 (1994).
  Medline CASGoogle Scholar
• 31  Olsen E, Duvic M, Frankel A et al. Pivotal Phase III trial of two dose levels of denileukin diftitox for the treatment of cutaneous T-cell lymphoma. J. Clin. Oncol.19,376–388 (2001).
  Medline CASGoogle Scholar
• 32  Manoukian G, Hagemeister F. Denileukin diftitox: a novel immunotoxin. Expert Opin. Biol. Ther.9,1445–1451 (2009).
  Medline CASGoogle Scholar
• 33  Mahnke K, Schönfeld K, Fondel S et al. Depletion of CD4⁺CD25⁺ human regulatory T cells in vivo: kinetics of Treg depletion and alterations in immune functions in vivo and in vitro. Int. J. Cancer120,2723–2733 (2007).
  Medline CASGoogle Scholar
• 34  Waldmann TA. Immunotherapy: past, present and future. Nat. Med.9,269–277 (2003).
  Medline CASGoogle Scholar
• 35  Weiner L, Murray J, Shuptrine C. Antibody-based immunotherapy of cancer. Cell148,1081–1084 (2012).▪ Excellent review article discussing innovative strategies to manipulate antibody structure and function to target cancer.
  Medline CASGoogle Scholar
• 36  Steiner M, Neri D. Antibody-radionuclide conjugates for cancer therapy: historical considerations and new trends. Clin. Cancer Res.17,6406–6416 (2011).
  Medline CASGoogle Scholar
• 37  Sauter B, Albert ML, Francisco L, Larsson M, Somersan S, Bhardwaj N. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med.191,423–434 (2000).
  Medline CASGoogle Scholar
• 38  Dhodapkar KM, Krasovsky J, Williamson B, Dhodapkar MV. Antitumor monoclonal antibodies enhance cross-presentation of cellular antigens and the generation of myeloma-specific killer T cells by dendritic cells. J. Exp. Med.195,125–133 (2002).
  Medline CASGoogle Scholar
• 39  Hilchey SP, Hyrien O, Mosmann TR et al. Rituximab immunotherapy results in the induction of a lymphoma idiotype-specific T-cell response in patients with follicular lymphoma: support for a “vaccinal effect” of rituximab. Blood113,3809–3812 (2009).
  Medline CASGoogle Scholar
• 40  Scott AM, Wolchok JD, Old LJ. Antibody therapy of cancer. Nat. Rev. Cancer12,278–287 (2012).▪ Excellent article reviewing US FDA-approved monoclonal antibody therapies for cancer.
  Medline CASGoogle Scholar
• 41  Galon J, Costes A, Sanchez-Cabo F et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science313,1960–1964 (2006).
  Medline CASGoogle Scholar
• 42  Pages F, Berger A, Camus M et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med.353,2654–2666 (2005).
  Medline CASGoogle Scholar
• 43  Mlecnik B, Tosolini M, Kirilovsky A et al. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J. Clin. Oncol.29,610–618 (2011).
  MedlineGoogle Scholar
• 44  Hodi FS, O‘Day SJ, McDermott DF et al. Improved survival with ipilimumab in patients with metastatic melanoma. N. Engl. J. Med.363,711–723 (2010).▪ Describes the Phase III trial that led to the approval of the immunomodulatory CTLA-4 antagonist monoclonal antibody ipilimumab for metastatic melanoma.
  Medline CASGoogle Scholar
• 45  Schwartzentruber DJ, Lawson DH, Richards JM et al. gp100 peptide vaccine and interleukin-2 in patients with advanced melanoma. N. Engl. J. Med.364,2119–2127 (2011).
  Medline CASGoogle Scholar
• 46  Wang E, Bedognetti D, Marincola FM. Prediction of response to anticancer immunotherapy using gene signatures. J. Clin. Oncol.31,2369–2371 (2013).
  Medline CASGoogle Scholar
• 47  Kruit WHJ, Suciu S, Dreno B et al. Selection of immunostimulant AS15 for active immunization with MAGE-A3 protein: results of a randomized Phase II study of the European Organisation for Research and Treatment of Cancer Melanoma Group in Metastatic Melanoma. J. Clin. Oncol.31,2413–2420 (2013).
  Medline CASGoogle Scholar
• 48  Vansteenkiste J, Zielinski M, Linder A et al. Adjuvant MAGE-A3 immunotherapy in resected non-small-cell lung cancer: Phase II randomized study results. J. Clin. Oncol.31,2396–2403 (2013).
  Medline CASGoogle Scholar
• 49  Ulloa-Montoya F, Louahed J, Dizier B et al. Predictive gene signature in MAGE-A3 antigen-specific cancer immunotherapy. J. Clin. Oncol.31,2388–2395 (2013).
  Medline CASGoogle Scholar
• 50  Brahmer JR, Drake CG, Wollner I et al. Phase I study of single-agent anti-programmed death-1 (MDX-1106) in refractory solid tumors: safety, clinical activity, pharmacodynamics, and immunologic correlates. J. Clin. Oncol.28,3167–3175 (2010).
  Medline CASGoogle Scholar
• 51  Beatty GL, Chiorean EG, Fishman MP et al. CD40 agonists alter tumor stroma and show efficacy against pancreatic carcinoma in mice and humans. Science331,1612–1616 (2011).
  Medline CASGoogle Scholar
• 52  Kirkwood JM, Tarhini AA, Panelli MC et al. Next generation of immunotherapy for melanoma. J. Clin. Oncol.26,3445–3455 (2008).
  Medline CASGoogle Scholar
• 53  Wolchok JD, Kluger H, Callahan MK et al. Nivolumab plus ipilimumab in advanced melanoma. N. Engl. J. Med.369,122–133 (2013).
  Medline CASGoogle Scholar
• 54  Geary SM, Salem AK. Prostate cancer vaccines: update on clinical development. Oncoimmunology2(5) e24523 (2013).
  MedlineGoogle Scholar
• 55  Lubaroff DM. Prostate cancer vaccines in clinical trials. Expert Rev. Vaccines11,857–868 (2012).
  Medline CASGoogle Scholar
• 56  Sims RB. Development of sipuleucel-T: autologous cellular immunotherapy for the treatment of metastatic castrate resistant prostate cancer. Vaccine30,4394–4397 (2012).
  Medline CASGoogle Scholar
• 57  Valone FH, Small E, MacKenzie M, et al. Dendritic cell-based treatment of cancer: closing in on a cellular therapy. Cancer J.7(Suppl. 2),S53–S61 (2001).
  MedlineGoogle Scholar
• 58  Ji RR, Chasalow S, Wang L et al. An immune-active tumor microenvironment favors clinical response to ipilimumab. Cancer Immunol. Immunother.61,1019–1031 (2012).
  Medline CASGoogle Scholar
• 59  Hamid O, Schmidt H, Nissan A et al. A prospective Phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma. J. Transl. Med.9,204 (2011).
  Medline CASGoogle Scholar
• 60  Chao MP, Majeti R, Weissman IL. Programmed cell removal: a new obstacle in the road to developing cancer. Nat. Rev. Cancer12,58–67 (2012).
  CASGoogle Scholar
• 61  Majeti R, Chao MP, Alizadeh AA et al. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell138,286–299 (2009).▪ Demonstrates that blocking the CD47 ‘don‘t eat me‘ signal on acute myeloid leukemia cells restores program cell removal immune processes, leading to regression of disease.
  Medline CASGoogle Scholar
• 62  Heiss MM, Murawa P, Koralewski P et al. The trifunctional antibody catumaxomab for the treatment of malignant ascites due to epithelial cancer: Results of a prospective randomized Phase II/III trial. Int. J. Cancer127,2209–2221 (2010).
  Medline CASGoogle Scholar
• 63  Kolb HJ. Graft-versus-leukemia effects of transplantation and donor lymphocytes. Blood112,4371–4383 (2008).
  Medline CASGoogle Scholar
• 64  Weiden PL, Flournoy N, Thomas ED et al. Antileukemic effect of graft-versus-host disease in human recipients of allogeneic-marrow grafts. N. Engl. J. Med.300,1068–1073 (1979).
  Medline CASGoogle Scholar
• 65  Rosenberg SA, Yang JC, Sherry RM et al. Durable complete responses in heavily pretreated patients with metastatic melanoma using T-cell transfer immunotherapy. Clin. Cancer Res.17,4550–4557 (2011).▪ Clinical study demonstrates that adoptive cell transfer of tumor-infiltrating lymphocytes in patients following a condition regimen can induce a durable complete response in patients with metastatic melanoma.
  Medline CASGoogle Scholar
• 66  Itzhaki O, Hovav E, Ziporen Y et al. Establishment and large-scale expansion of minimally cultured ‘young‘ tumor infiltrating lymphocytes for adoptive transfer therapy. J. Immunother.34,212–220 (2011).
  MedlineGoogle Scholar
• 67  Besser MJ, Shapira-Frommer R, Treves AJ et al. Clinical responses in a Phase II study using adoptive transfer of short-term cultured tumor infiltration lymphocytes in metastatic melanoma patients. Clin. Cancer Res.16,2646–2655 (2010).
  Medline CASGoogle Scholar
• 68  Galluzzi L, Vacchelli E, Eggermont A et al. Trial watch. Adoptive cell transfer immunotherapy. Oncoimmunology1,306–315 (2012).
  MedlineGoogle Scholar
• 69  Chang AE, Li Q, Jiang G, Sayre DM, Braun TM, Redman BG. Phase II trial of autologous tumor vaccination, anti-CD3-activated vaccine-primed lymphocytes, and interleukin-2 in stage IV renal cell cancer. J. Clin. Oncol.21,884–890 (2003).
  Medline CASGoogle Scholar
• 70  Thompson JA, Figlin RA, Sifri-Steele C, Berenson RJ, Frohlich MW. A Phase I trial of CD3/CD28-activated T cells (Xcellerated T cells) and interleukin-2 in patients with metastatic renal cell carcinoma. Clin. Cancer Res.9,3562–3570 (2003).
  Medline CASGoogle Scholar
• 71  Hinrichs CS, Borman ZA, Gattinoni L et al. Human effector CD8⁺ T cells derived from naive rather than memory subsets possess superior traits for adoptive immunotherapy. Blood117,808–814 (2011).
  Medline CASGoogle Scholar
• 72  Liu K, Rosenberg SA. Transduction of an IL-2 gene into human melanoma-reactive lymphocytes results in their continued growth in the absence of exogenous IL-2 and maintenance of specific antitumor activity. J. Immunol.167,6356–6365 (2001).
  Medline CASGoogle Scholar
• 73  Zhang Q, Yang X, Pins M et al. Adoptive transfer of tumor-reactive transforming growth factor-beta-insensitive CD8⁺ T cells: eradication of autologous mouse prostate cancer. Cancer Res.65,1761–1769 (2005).
  Medline CASGoogle Scholar
• 74  Zhou J, Shen X, Huang J, Hodes RJ, Rosenberg SA, Robbins PF. Telomere length of transferred lymphocytes correlates with in vivo persistence and tumor regression in melanoma patients receiving cell transfer therapy. J. Immunol.175,7046–7052 (2005).
  Medline CASGoogle Scholar
• 75  Kalbasi A, Shrimali RK, Chinnasamy D, Rosenberg SA. Prevention of interleukin-2 withdrawal-induced apoptosis in lymphocytes retrovirally cotransduced with genes encoding an antitumor T-cell receptor and an antiapoptotic protein. J. Immunother.33,672–683 (2010).
  Medline CASGoogle Scholar
• 76  Di Stasi A, Tey SK, Dotti G et al. Inducible apoptosis as a safety switch for adoptive cell therapy. N. Engl. J. Med.365,1673–1683 (2011).
  Medline CASGoogle Scholar
• 77  Johnson LA, Morgan RA, Dudley ME et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood114,535–546 (2009).
  Medline CASGoogle Scholar
• 78  Clay TM, Custer MC, Sachs J, Hwu P, Rosenberg SA, Nishimura MI. Efficient transfer of a tumor antigen-reactive TCR to human peripheral blood lymphocytes confers anti-tumor reactivity. J. Immunol.163,507–513 (1999).
  Medline CASGoogle Scholar
• 79  Morgan RA, Dudley ME, Wunderlich JR et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science314,126–129 (2006).
  Medline CASGoogle Scholar
• 80  Essand M, Loskog ASI. Genetically engineered T cells for the treatment of cancer. J. Intern. Med.273,166–181 (2013).
  Medline CASGoogle Scholar
• 81  Restifo NP, Dudley ME, Rosenberg SA. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol.12,269–281 (2012).▪ Excellent review article discussing T-cell immunotherapies.
  Medline CASGoogle Scholar
• 82  Parkhurst MR, Yang JC, Langan RC et al. T cells targeting carcinoembryonic antigen can mediate regression of metastatic colorectal cancer but induce severe transient colitis. Mol. Ther.19,620–626 (2011).
  Medline CASGoogle Scholar
• 83  Sadelain M, Brentjens R, Riviere I. The promise and potential pitfalls of chimeric antigen receptors. Curr. Opin. Immunol.21,215–223 (2009).
  Medline CASGoogle Scholar
• 84  Gross G, Waks T, Eshhar Z. Expression of immunoglobulin-T-cell receptor chimeric molecules as functional receptors with antibody-type specificity. Proc. Natl Acad. Sci. USA86,10024–10028 (1989).
  Medline CASGoogle Scholar
• 85  Lamers CHJ, Sleijfer S, Vulto AG et al. Treatment of metastatic renal cell carcinoma with autologous T-lymphocytes genetically retargeted against carbonic anhydrase IX: first clinical experience. J. Clin. Oncol.24,e20–e22 (2006).
  MedlineGoogle Scholar
• 86  Till BG, Jensen MC, Wang J et al. Adoptive immunotherapy for indolent non-Hodgkin lymphoma and mantle cell lymphoma using genetically modified autologous CD20-specific T cells. Blood112,2261–2271 (2008).
  Medline CASGoogle Scholar
• 87  Park JR, DiGiusto DL, Slovak M et al. Adoptive transfer of chimeric antigen receptor re-directed cytolytic T lymphocyte clones in patients with neuroblastoma. Mol. Ther.15,825–833 (2007).
  Medline CASGoogle Scholar
• 88  Kershaw MH, Westwood JA, Parker LL et al. A Phase I study on adoptive immunotherapy using gene-modified T cells for ovarian cancer. Clin. Cancer Res.12,6106–6115 (2006).
  Medline CASGoogle Scholar
• 89  Finney HM, Akbar AN, Lawson ADG. Activation of resting human primary T cells with chimeric receptors: costimulation from CD28, inducible costimulator, CD134, and CD137 in series with signals from the TCRζ chain. J. Immunol.172,104–113 (2004).
  Medline CASGoogle Scholar
• 90  Loskog A, Giandomenico V, Rossig C, Pule M, Dotti G, Brenner MK. Addition of the CD28 signaling domain to chimeric T-cell receptors enhances chimeric T-cell resistance to T regulatory cells. Leukemia20,1819–1828 (2006).
  Medline CASGoogle Scholar
• 91  Song DG, Ye Q, Carpenito C et al.In vivo persistence, tumor localization, and antitumor activity of CAR-engineered T cells is enhanced by costimulatory signaling through CD137 (4–1BB). Cancer Res.71,4617–4627 (2011).
  Medline CASGoogle Scholar
• 92  Kalos M, Levine BL, Porter DL et al. T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia. Sci. Transl. Med.3(95) 95ra73 (2011).
  Medline CASGoogle Scholar
• 93  Porter DL, Levine BL, Kalos M, Bagg A, June CH. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med.365,725–733 (2011).▪ Clinical study describing a complete durable remission of chronic lymphoid leukemia in a patient receiving CD19 chimeric antigen receptor T-cell adoptive cell transfer.
  Medline CASGoogle Scholar
• 94  Grupp SA, Kalos M, Barrett D et al. Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. N. Engl. J. Med.368,1509–1518 (2013).▪ Clinical study describing CD19 chimeric antigen receptor T-cell adoptive cell transfer for acute lymphoid leukemia in which one patient achieves a durable remission and the second patient relapses with CD19-negative leukemic cells.
  Medline CASGoogle Scholar
• 95  June C, Rosenberg SA, Sadelain M, Weber JS. T-cell therapy at the threshold. Nat. Biotech.30,611–614 (2012).▪ Thoughtful discussion about the challenges and promise of T-cell adoptive cell transfer therapy for cancer by pioneers in the field.
  Medline CASGoogle Scholar
• 96  Gattinoni L, Klebanoff CA, Restifo NP. Paths to stemness: building the ultimate antitumour T cell. Nat. Rev. Cancer12,671–684 (2012).
  Medline CASGoogle Scholar
• 97  Li Q, Lao X, Pan Q et al. Adoptive transfer of tumor reactive B cells confers host T-cell immunity and tumor regression. Clin. Cancer Res.17,4987–4995 (2011).
  Medline CASGoogle Scholar
• 98  Oldham RK, Herberman RB. Evaluation of cell-mediated cytotoxic reactivity against tumor associated antigens with ¹²⁵I-iododeoxyuridine labeled target cells. J. Immunol.111,862–871 (1973).
  Medline CASGoogle Scholar
• 99  Herberman RB, Nunn ME, Holden HT, Lavrin DH. Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. II. Characterization of effector cells. Int. J. Cancer16,230–239 (1975).
  Medline CASGoogle Scholar
• 100  Kiessling R, Klein E, Wigzell H. ‘Natural‘ killer cells in the mouse. I. Cytotoxic cells with specificity for mouse Moloney leukemia cells. Specificity and distribution according to genotype. Eur. J. Immunol.5,112–117 (1975).
  Medline CASGoogle Scholar
• 101  Dong Z, Cruz-Munoz ME, Zhong MC, Chen R, Latour S, Veillette A. Essential function for SAP family adaptors in the surveillance of hematopoietic cells by natural killer cells. Nat. Immunol.10,973–980 (2009).
  Medline CASGoogle Scholar
• 102  Ruggeri L, Capanni M, Urbani E et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science295,2097–2100 (2002).
  Medline CASGoogle Scholar
• 103  Aversa F, Tabilio A, Velardi A et al. Treatment of high-risk acute leukemia with T-cell-depleted stem cells from related donors with one fully mismatched HLA haplotype. N. Engl. J. Med.339,1186–1193 (1998).
  Medline CASGoogle Scholar
• 104  Miller JS, Soignier Y, Panoskaltsis-Mortari A et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood105,3051–3057 (2005).▪ Describes the first safe and successful adoptive transfer of NK cells for the treatment of acute myeloid leukemia.
  Medline CASGoogle Scholar
• 105  Curti A, Ruggeri L, D‘Addio A et al. Successful transfer of alloreactive haploidentical KIR ligand-mismatched natural killer cells after infusion in elderly high risk acute myeloid leukemia patients. Blood118,3273–3279 (2011).
  Medline CASGoogle Scholar
• 106  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.17,6287–6297 (2011).
  Medline CASGoogle Scholar
• 107  Schietinger A, Philip M, Schreiber H. Specificity in cancer immunotherapy. Sem. Immunol.20,276–285 (2008).
  Medline CASGoogle Scholar
• 108  Antonia SJ, Mirza N, Fricke I et al. Combination of p53 cancer vaccine with chemotherapy in patients with extensive stage small cell lung cancer. Clin. Cancer Res.12,878–887 (2006).
  Medline CASGoogle Scholar
• 109  Inoges S, Rodriguez-Calvillo M, Zabalegui N et al. Clinical benefit associated with idiotypic vaccination in patients with follicular lymphoma. J. Natl Cancer Inst.98,1292–1301 (2006).
  MedlineGoogle Scholar
• 110  Emens LA, Jaffee EM. Leveraging the activity of tumor vaccines with cytotoxic chemotherapy. Cancer Res.65,8059–8064 (2005).
  Medline CASGoogle Scholar
• 111  Prestwich RJ, Errington F, Harrington KJ, Pandha HS, Selby P, Melcher A. Oncolytic viruses: do they have a role in anti-cancer therapy? Clin. Med. Oncol.2,83–96 (2008).
  Medline CASGoogle Scholar
• 112  Tong AW, Senzer N, Cerullo V, Templeton NS, Hemminki A, Nemunaitis J. Oncolytic viruses for induction of anti-tumor immunity. Curr. Pharm. Biotechnol.13,1750–1760 (2012).
  Medline CASGoogle Scholar
• 113  Shirota T, Kasuya H, Kodera Y et al. Oncolytic herpes virus induces effective anti-cancer immunity against murine colon cancer. Hepatogastroenterology58,1482–1489 (2011).
  Medline CASGoogle Scholar
• 114  Heo J, Breitbach CJ, Moon A et al. Sequential therapy with JX-594, a targeted oncolytic poxvirus, followed by sorafenib in hepatocellular carcinoma: preclinical and clinical demonstration of combination efficacy. Mol. Ther.19,1170–1179 (2011).
  Medline CASGoogle Scholar
• 115  Stephenson KB, Barra NG, Davies E, Ashkar AA, Lichty BD. Expressing human interleukin-15 from oncolytic vesicular stomatitis virus improves survival in a murine metastatic colon adenocarcinoma model through the enhancement of anti-tumor immunity. Cancer Gene Ther.19,238–246 (2012).
  Medline CASGoogle Scholar
• 116  Hastie E, Grdzelishvili VZ. Vesicular stomatitis virus as a flexible platform for oncolytic virotherapy against cancer. J. General Virol.93,2529–2545 (2012).
  Medline CASGoogle Scholar
• 117  Dempe S, Lavie M, Struyf S et al. Antitumoral activity of parvovirus-mediated IL-2 and MCP-3/CCL7 delivery into human pancreatic cancer: implication of leucocyte recruitment. Cancer Immunol. Immunother.61,2113–2123 (2012).
  Medline CASGoogle Scholar