Human cell‐based artificial antigen‐presenting cells for cancer immunotherapy

Adoptive T‐cell therapy, where anti‐tumor T cells are first prepared in vitro, is attractive since it facilitates the delivery of essential signals to selected subsets of anti‐tumor T cells without unfavorable immunoregulatory issues that exist in tumor‐bearing hosts. Recent clinical trials have demonstrated that anti‐tumor adoptive T‐cell therapy, i.e. infusion of tumor‐specific T cells, can induce clinically relevant and sustained responses in patients with advanced cancer. The goal of adoptive cell therapy is to establish anti‐tumor immunologic memory, which can result in life‐long rejection of tumor cells in patients. To achieve this goal, during the process of in vitro expansion, T‐cell grafts used in adoptive T‐cell therapy must be appropriately educated and equipped with the capacity to accomplish multiple, essential tasks. Adoptively transferred T cells must be endowed, prior to infusion, with the ability to efficiently engraft, expand, persist, and traffic to tumor in vivo. As a strategy to consistently generate T‐cell grafts with these capabilities, artificial antigen‐presenting cells have been developed to deliver the proper signals necessary to T cells to enable optimal adoptive cell therapy.

[1]  S. Olivares,et al.  Manufacture of Clinical-Grade CD19-Specific T Cells Stably Expressing Chimeric Antigen Receptor Using Sleeping Beauty System and Artificial Antigen Presenting Cells , 2013, PloS one.

[2]  S. Rosenberg,et al.  Treating B-cell cancer with T cells expressing anti-CD19 chimeric antigen receptors , 2013, Nature Reviews Clinical Oncology.

[3]  Bernd Hauck,et al.  Chimeric antigen receptor-modified T cells for acute lymphoid leukemia. , 2013, The New England journal of medicine.

[4]  Michel Sadelain,et al.  The basic principles of chimeric antigen receptor design. , 2013, Cancer discovery.

[5]  T. Welling,et al.  T cell anergy, exhaustion, senescence, and stemness in the tumor microenvironment. , 2013, Current opinion in immunology.

[6]  J. Rossjohn,et al.  Natural Killer T cell obsession with self-antigens. , 2013, Current opinion in immunology.

[7]  Qing He,et al.  CD19-Targeted T Cells Rapidly Induce Molecular Remissions in Adults with Chemotherapy-Refractory Acute Lymphoblastic Leukemia , 2013, Science Translational Medicine.

[8]  D. Powell,et al.  IL-21 promotes the expansion of CD27+CD28+ tumor infiltrating lymphocytes with high cytotoxic potential and low collateral expansion of regulatory T cells , 2013, Journal of Translational Medicine.

[9]  Pieter Wesseling,et al.  The immunosuppressive tumour network: myeloid‐derived suppressor cells, regulatory T cells and natural killer T cells , 2013, Immunology.

[10]  R. Sposto,et al.  Growth and Activation of Natural Killer Cells Ex Vivo from Children with Neuroblastoma for Adoptive Cell Therapy , 2013, Clinical Cancer Research.

[11]  A. Ferrante HLA‐DM: arbiter conformationis , 2013, Immunology.

[12]  E. Shpall,et al.  Clinical Application of Sleeping Beauty and Artificial Antigen Presenting Cells to Genetically Modify T Cells from Peripheral and Umbilical Cord Blood , 2013, Journal of visualized experiments : JoVE.

[13]  W. Leonard,et al.  Interleukin-2 at the crossroads of effector responses, tolerance, and immunotherapy. , 2013, Immunity.

[14]  P. Brennan,et al.  Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions , 2013, Nature Reviews Immunology.

[15]  P. Sharma,et al.  Harnessing the power of the immune system to target cancer. , 2013, Annual review of medicine.

[16]  M. Roederer,et al.  Identification, isolation and in vitro expansion of human and nonhuman primate T stem cell memory cells , 2012, Nature Protocols.

[17]  J. Rossjohn,et al.  Recognition of CD1d-restricted antigens by natural killer T cells , 2012, Nature Reviews Immunology.

[18]  C. Klebanoff,et al.  Sorting Through Subsets: Which T-Cell Populations Mediate Highly Effective Adoptive Immunotherapy? , 2012, Journal of immunotherapy.

[19]  S. Walsh Structural insights into the common γ‐chain family of cytokines and receptors from the interleukin‐7 pathway , 2012, Immunological reviews.

[20]  C. Klebanoff,et al.  Paths to stemness: building the ultimate antitumour T cell , 2012, Nature Reviews Cancer.

[21]  V. Pascual,et al.  From IL-2 to IL-37: the expanding spectrum of anti-inflammatory cytokines , 2012, Nature Immunology.

[22]  Elaine Coustan-Smith,et al.  Large-scale ex vivo expansion and characterization of natural killer cells for clinical applications. , 2012, Cytotherapy.

[23]  O. Finn,et al.  Immuno-oncology: understanding the function and dysfunction of the immune system in cancer. , 2012, Annals of oncology : official journal of the European Society for Medical Oncology.

[24]  Jacques Thibodeau,et al.  Targeting the MHC Class II antigen presentation pathway in cancer immunotherapy , 2012, Oncoimmunology.

[25]  Luigi Naldini,et al.  A foundation for universal T-cell based immunotherapy: T cells engineered to express a CD19-specific chimeric-antigen-receptor and eliminate expression of endogenous TCR. , 2012, Blood.

[26]  F. Carrette,et al.  IL-7 signaling and CD127 receptor regulation in the control of T cell homeostasis. , 2012, Seminars in immunology.

[27]  E. Shpall,et al.  Infusing CD19-directed T cells to augment disease control in patients undergoing autologous hematopoietic stem-cell transplantation for advanced B-lymphoid malignancies. , 2012, Human gene therapy.

[28]  J. Schlom,et al.  Therapeutic cancer vaccines: current status and moving forward. , 2012, Journal of the National Cancer Institute.

[29]  T. Gajewski,et al.  Cancer immunotherapy , 2012, Molecular oncology.

[30]  R. Steinman Decisions about dendritic cells: past, present, and future. , 2012, Annual review of immunology.

[31]  S. Rosenberg,et al.  B-cell depletion and remissions of malignancy along with cytokine-associated toxicity in a clinical trial of anti-CD19 chimeric-antigen-receptor-transduced T cells. , 2012, Blood.

[32]  J. Banchereau,et al.  Cancer immunotherapy via dendritic cells , 2012, Nature Reviews Cancer.

[33]  Steven A. Rosenberg,et al.  Adoptive immunotherapy for cancer: harnessing the T cell response , 2012, Nature Reviews Immunology.

[34]  Eric Vivier,et al.  Targeting natural killer cells and natural killer T cells in cancer , 2012, Nature Reviews Immunology.

[35]  K. Wucherpfennig,et al.  The mechanism of HLA-DM induced peptide exchange in the MHC class II antigen presentation pathway. , 2012, Current opinion in immunology.

[36]  L. Hurton,et al.  Membrane-Bound IL-21 Promotes Sustained Ex Vivo Proliferation of Human Natural Killer Cells , 2012, PloS one.

[37]  Y. Yamashita,et al.  Ex Vivo Expansion of Human CD8+ T Cells Using Autologous CD4+ T Cell Help , 2012, PloS one.

[38]  George Coukos,et al.  Cancer immunotherapy comes of age , 2011, Nature.

[39]  L. Nadler,et al.  Endogenous Ligands Selectively Stimulate Highly Avid Autoreactive Human Invariant Natural Killer T Cells with Distinctive T-Cell Receptor Vβ11 CDR3 Sequence Motifs , 2011 .

[40]  Michael J. Bevan,et al.  CD8+ T Cells: Foot Soldiers of the Immune System , 2011, Immunity.

[41]  A. Bagg,et al.  Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. , 2011, The New England journal of medicine.

[42]  David L. Porter,et al.  T Cells with Chimeric Antigen Receptors Have Potent Antitumor Effects and Can Establish Memory in Patients with Advanced Leukemia , 2011, Science Translational Medicine.

[43]  Qunrui Ye,et al.  Engineered artificial antigen presenting cells facilitate direct and efficient expansion of tumor infiltrating lymphocytes , 2011, Journal of Translational Medicine.

[44]  C. Punt,et al.  Cancer immunotherapy – revisited , 2011, Nature Reviews Drug Discovery.

[45]  R. Storb,et al.  Influence of immunosuppressive treatment on risk of recurrent malignancy after allogeneic hematopoietic cell transplantation. , 2011, Blood.

[46]  S. Ansén,et al.  Induction of HLA-DP4–Restricted Anti-Survivin Th1 and Th2 Responses Using an Artificial Antigen-Presenting Cell , 2011, Clinical Cancer Research.

[47]  J. Sprent,et al.  Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells , 2011, Nature Immunology.

[48]  Bruce R. Blazar,et al.  Massive ex Vivo Expansion of Human Natural Regulatory T Cells (Tregs) with Minimal Loss of in Vivo Functional Activity , 2011, Science Translational Medicine.

[49]  S. Olivares,et al.  Reprogramming CD19-specific T cells with IL-21 signaling can improve adoptive immunotherapy of B-lineage malignancies. , 2011, Cancer research.

[50]  T. Fry,et al.  Harnessing the biology of IL-7 for therapeutic application , 2011, Nature Reviews Immunology.

[51]  D. Neuberg,et al.  Establishment of Antitumor Memory in Humans Using in Vitro–Educated CD8+ T Cells , 2011, Science Translational Medicine.

[52]  C. Turtle,et al.  Genetically retargeting CD8+ lymphocyte subsets for cancer immunotherapy. , 2011, Current opinion in immunology.

[53]  S. Rosenberg,et al.  CARs on track in the clinic. , 2011, Molecular therapy : the journal of the American Society of Gene Therapy.

[54]  S. Rosenberg,et al.  In vitro generated anti-tumor T lymphocytes exhibit distinct subsets mimicking in vivo antigen-experienced cells , 2011, Cancer Immunology, Immunotherapy.

[55]  Dean Anthony Lee,et al.  Expansion, purification, and functional assessment of human peripheral blood NK cells. , 2011, Journal of visualized experiments : JoVE.

[56]  Genita Metzler,et al.  A panel of human cell-based artificial APC enables the expansion of long-lived antigen-specific CD4+ T cells restricted by prevalent HLA-DR alleles. , 2010, International immunology.

[57]  G. Dotti,et al.  Redirecting T-cell specificity by introducing a tumor-specific chimeric antigen receptor. , 2010, Blood.

[58]  D. Schadendorf,et al.  Improved survival with ipilimumab in patients with metastatic melanoma. , 2010, The New England journal of medicine.

[59]  A. Kimura,et al.  IL‐6: Regulator of Treg/Th17 balance , 2010, European journal of immunology.

[60]  C. Turtle,et al.  Artificial Antigen-Presenting Cells for Use in Adoptive Immunotherapy , 2010, Cancer journal.

[61]  A. Ribas,et al.  Current Experience With CTLA4-blocking Monoclonal Antibodies for the Treatment of Solid Tumors , 2010, Journal of immunotherapy.

[62]  H. Heslop,et al.  Adoptive T cell therapy of cancer. , 2010, Current opinion in immunology.

[63]  P. Muranski,et al.  Naive tumor-specific CD4+ T cells differentiated in vivo eradicate established melanoma , 2010, The Journal of experimental medicine.

[64]  R. Blasberg,et al.  Tumor-reactive CD4+ T cells develop cytotoxic activity and eradicate large established melanoma after transfer into lymphopenic hosts , 2010, The Journal of experimental medicine.

[65]  P. Hwu,et al.  MART-1–Specific Melanoma Tumor-Infiltrating Lymphocytes Maintaining CD28 Expression Have Improved Survival and Expansion Capability Following Antigenic Restimulation In Vitro , 2009, The Journal of Immunology.

[66]  Kensuke Takada,et al.  Naive T cell homeostasis: from awareness of space to a sense of place , 2009, Nature Reviews Immunology.

[67]  Axel Hoos,et al.  Guidelines for the Evaluation of Immune Therapy Activity in Solid Tumors: Immune-Related Response Criteria , 2009, Clinical Cancer Research.

[68]  Yun Ji,et al.  Adoptively transferred effector cells derived from naïve rather than central memory CD8+ T cells mediate superior antitumor immunity , 2009, Proceedings of the National Academy of Sciences.

[69]  Michael J. Bevan,et al.  The precursors of memory: models and controversies , 2009, Nature Reviews Immunology.

[70]  W. Leonard,et al.  New insights into the regulation of T cells by γc family cytokines , 2009, Nature Reviews Immunology.

[71]  A. Zajac,et al.  A Vital Role for Interleukin-21 in the Control of a Chronic Viral Infection , 2009, Science.

[72]  K. Sauer,et al.  IL-21 Is Required to Control Chronic Viral Infection , 2009, Science.

[73]  J. Weber,et al.  IL-21R on T Cells Is Critical for Sustained Functionality and Control of Chronic Viral Infection , 2009, Science.

[74]  P. Muranski,et al.  Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells , 2009, Nature Medicine.

[75]  D. Campana,et al.  Expansion of highly cytotoxic human natural killer cells for cancer cell therapy. , 2009, Cancer research.

[76]  Christian Stemberger,et al.  Stem cell-like plasticity of naïve and distinct memory CD8+ T cell subsets. , 2009, Seminars in immunology.

[77]  A. Livingstone,et al.  Cutting Edge: CD4+ T Cell-Derived IL-2 Is Essential for Help-Dependent Primary CD8+ T Cell Responses1 , 2008, The Journal of Immunology.

[78]  S. Rosenberg,et al.  Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens. , 2008, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[79]  Hao Liu,et al.  Virus-specific T cells engineered to coexpress tumor-specific receptors: persistence and antitumor activity in individuals with neuroblastoma , 2008, Nature Medicine.

[80]  K. Stevenson,et al.  Dissociation of Its Opposing Immunologic Effects Is Critical for the Optimization of Antitumor CD8+ T-Cell Responses Induced by Interleukin 21 , 2008, Clinical Cancer Research.

[81]  Chen Dong,et al.  Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. , 2008, Immunity.

[82]  Jianhong Cao,et al.  Treatment of metastatic melanoma with autologous CD4+ T cells against NY-ESO-1. , 2008, The New England journal of medicine.

[83]  W. Leonard,et al.  IL-2 and IL-21 confer opposing differentiation programs to CD8+ T cells for adoptive immunotherapy. , 2008, Blood.

[84]  R. Kennedy,et al.  Multiple roles for CD4+ T cells in anti‐tumor immune responses , 2008, Immunological reviews.

[85]  W. Leonard,et al.  Interleukin-21: basic biology and implications for cancer and autoimmunity. , 2008, Annual review of immunology.

[86]  Mike Gough,et al.  Adoptive transfer of effector CD8+ T cells derived from central memory cells establishes persistent T cell memory in primates. , 2008, The Journal of clinical investigation.

[87]  Chung-Che Chang,et al.  Complete responses of relapsed lymphoma following genetic modification of tumor-antigen presenting cells and T-lymphocyte transfer. , 2007, Blood.

[88]  M. Fujimoto,et al.  CD83 Expression Is a Sensitive Marker of Activation Required for B Cell and CD4+ T Cell Longevity In Vivo1 , 2007, The Journal of Immunology.

[89]  S. Forman,et al.  Antigen-independent and antigen-dependent methods to numerically expand CD19-specific CD8+ T cells. , 2007, Experimental hematology.

[90]  K. Schwarz,et al.  Differential role of IL‐2R signaling for CD8+ T cell responses in acute and chronic viral infections , 2007, European journal of immunology.

[91]  G. Zhu,et al.  CD137 stimulation delivers an antigen-independent growth signal for T lymphocytes with memory phenotype. , 2007, Blood.

[92]  C. June,et al.  Engineering artificial antigen-presenting cells to express a diverse array of co-stimulatory molecules. , 2007, Molecular therapy : the journal of the American Society of Gene Therapy.

[93]  D. Neuberg,et al.  Long-Lived Antitumor CD8+ Lymphocytes for Adoptive Therapy Generated Using an Artificial Antigen-Presenting Cell , 2007, Clinical Cancer Research.

[94]  A. Mackensen,et al.  Phase I study of adoptive T-cell therapy using antigen-specific CD8+ T cells for the treatment of patients with metastatic melanoma. , 2006, Journal of Clinical Oncology.

[95]  S. Rosenberg,et al.  Cancer Regression in Patients After Transfer of Genetically Engineered Lymphocytes , 2006, Science.

[96]  T. Waldmann The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design , 2006, Nature Reviews Immunology.

[97]  S. Rosenberg,et al.  Modulation by IL-2 of CD70 and CD27 Expression on CD8+ T Cells: Importance for the Therapeutic Effectiveness of Cell Transfer Immunotherapy1 , 2006, The Journal of Immunology.

[98]  A. Tyznik,et al.  Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells , 2006, Nature.

[99]  L. Nadler,et al.  Efficient Presentation of Naturally Processed HLA Class I Peptides by Artificial Antigen-Presenting Cells for the Generation of Effective Antitumor Responses , 2006, Clinical Cancer Research.

[100]  P. Burkett,et al.  Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. , 2006, Annual review of immunology.

[101]  D. Neuberg,et al.  Engagement of CD83 ligand induces prolonged expansion of CD8+ T cells and preferential enrichment for antigen specificity. , 2006, Blood.

[102]  S. Rosenberg,et al.  Telomere Length of Transferred Lymphocytes Correlates with In Vivo Persistence and Tumor Regression in Melanoma Patients Receiving Cell Transfer Therapy1 , 2005, The Journal of Immunology.

[103]  K. Echasserieau,et al.  Adoptive Transfer of Tumor-Reactive Melan-A-Specific CTL Clones in Melanoma Patients Is Followed by Increased Frequencies of Additional Melan-A-Specific T Cells1 , 2005, The Journal of Immunology.

[104]  J. Harding,et al.  Achieving stability through editing and chaperoning: regulation of MHC class II peptide binding and expression , 2005, Immunological reviews.

[105]  D. Campana,et al.  Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells. , 2005, Blood.

[106]  S. Rosenberg,et al.  Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. , 2005, The Journal of clinical investigation.

[107]  L. Nadler,et al.  4-1BB (CD137) or CD40 Signaling Fails To Improve the Expansion of Antigen Specific T Cells Demonstrated with Engagement of TCR, CD28 and CD83 Ligand. , 2004 .

[108]  S. Rosenberg,et al.  Cancer immunotherapy: moving beyond current vaccines , 2004, Nature Medicine.

[109]  M. Bevan Helping the CD8+ T-cell response , 2004, Nature Reviews Immunology.

[110]  Qingsheng Li,et al.  IL-21 Enhances and Sustains CD8+ T Cell Responses to Achieve Durable Tumor Immunity: Comparative Evaluation of IL-2, IL-15, and IL-211 , 2004, The Journal of Immunology.

[111]  M. Sadelain,et al.  The ABCs of artificial antigen presentation , 2004, Nature Biotechnology.

[112]  Antonio Lanzavecchia,et al.  Central memory and effector memory T cell subsets: function, generation, and maintenance. , 2004, Annual review of immunology.

[113]  Rustom Antia,et al.  Lineage relationship and protective immunity of memory CD8 T cell subsets , 2003, Nature Immunology.

[114]  S. Larson,et al.  Eradication of systemic B-cell tumors by genetically targeted human T lymphocytes co-stimulated by CD80 and interleukin-15 , 2003, Nature Medicine.

[115]  J. Thompson,et al.  Adoptive T cell therapy using antigen-specific CD8+ T cell clones for the treatment of patients with metastatic melanoma: In vivo persistence, migration, and antitumor effect of transferred T cells , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[116]  David Allman,et al.  Ex vivo expansion of polyclonal and antigen-specific cytotoxic T lymphocytes by artificial APCs expressing ligands for the T-cell receptor, CD28 and 4-1BB , 2002, Nature Biotechnology.

[117]  F. Marincola,et al.  Adoptive Transfer of Cloned Melanoma-Reactive T Lymphocytes for the Treatment of Patients with Metastatic Melanoma , 2001, Journal of immunotherapy.

[118]  F. Sallusto,et al.  Dynamics of T lymphocyte responses: intermediates, effectors, and memory cells. , 2000, Science.

[119]  F. Sallusto,et al.  Two subsets of memory T lymphocytes with distinct homing potentials and effector functions , 1999, Nature.

[120]  M. Connors,et al.  Effects of CD28 costimulation on long-term proliferation of CD4+ T cells in the absence of exogenous feeder cells. , 1997, Journal of immunology.

[121]  Y. Yazaki,et al.  Expression of costimulatory molecules in human leukemias. , 1996, Leukemia.

[122]  Liangji Zhou,et al.  Human blood dendritic cells selectively express CD83, a member of the immunoglobulin superfamily. , 1995, Journal of immunology.

[123]  Catia,et al.  A nonapeptide encoded by human gene MAGE-1 is recognized on HLA-A1 by cytolytic T lymphocytes directed against tumor antigen MZ2-E , 1992, The Journal of experimental medicine.

[124]  Liangji Zhou,et al.  A novel cell-surface molecule expressed by human interdigitating reticulum cells, Langerhans cells, and activated lymphocytes is a new member of the Ig superfamily. , 1992, Journal of immunology.

[125]  P. Chomez,et al.  A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. , 1991, Science.

[126]  C. Anderson,et al.  Human monocytes and U937 cells bear two distinct Fc receptors for IgG. , 1986, Journal of immunology.

[127]  F. Ruscetti Biology of interleukin-2 , 1984, Survey of immunologic research.

[128]  C. Lozzio,et al.  Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. , 1975, Blood.

[129]  S. Riddell,et al.  Engraftment of human central memory-derived effector CD8+ T cells in immunodeficient mice. , 2011, Blood.

[130]  S. Forman,et al.  Characterization of an artificial antigen-presenting cell to propagate cytolytic CD19-specific T cells , 2006, Leukemia.

[131]  C. Fox,et al.  Subtractive cDNA cloning of a novel member of the Ig gene superfamily expressed at high levels in activated B lymphocytes. , 1993, Blood.

[132]  W. Fiers,et al.  Modulation of expression of class II histocompatibility antigens by secretion of a cellular inhibitor in K562 leukemic cells , 1987, European journal of immunology.

[133]  C. Lozzio,et al.  Properties of the K562 cell line derived from a patient with chronic myeloid leukemia. , 1977, International journal of cancer.

[134]  Lozzio Bb,et al.  Properties of the K562 cell line derived from a patient with chronic myeloid leukemia. , 1977 .