Biological intratumoral therapy for the high-grade glioma part II: vector- and cell-based therapies and radioimmunotherapy

Management of high-grade gliomas (HGGs) remains a complex challenge with an overall poor prognosis despite aggressive multimodal treatment. New translational research has focused on maximizing tumor cell eradication through improved tumor cell targeting while minimizing collateral systemic side effects. In particular, biological intratumoral therapies have been the focus of novel translational research efforts due to their inherent potential to be both dynamically adaptive and target specific. This two part review will provide an overview of biological intratumoral therapies that have been evaluated in human clinical trials in HGGs, and summarize key advances and remaining challenges in the development of these therapies as a potential new paradigm in the management of HGGs. Part II discusses vector-based therapies, cell-based therapies and radioimmunotherapy.

[1]  John H. Sampson,et al.  Recurrent Glioblastoma Treated with Recombinant Poliovirus , 2018, The New England journal of medicine.

[2]  P. Sminia,et al.  The therapeutic potential of polymersomes loaded with 225Ac evaluated in 2D and 3D in vitro glioma models , 2018, European journal of pharmaceutics and biopharmaceutics : official journal of Arbeitsgemeinschaft fur Pharmazeutische Verfahrenstechnik e.V.

[3]  H. Wolterbeek,et al.  Improved 225Ac daughter retention in InPO4 containing polymersomes. , 2017, Applied radiation and isotopes : including data, instrumentation and methods for use in agriculture, industry and medicine.

[4]  B. Badie,et al.  247. Phase I Study of Second Generation Chimeric Antigen Receptor-Engineered T Cells Targeting IL13Rα2 for the Treatment of Glioblastoma , 2016 .

[5]  L. Liau,et al.  IMCT-10A PHASE I DOSE ESCALATION STUDY TO TEST THE SAFETY OF INTRATUMORAL ADOPTIVE IMMUNE THERAPY WITH AlloCTL IN RECURRENT GLIOMA PATIENTS. , 2015 .

[6]  J. Bading,et al.  Bioactivity and Safety of IL13Rα2-Redirected Chimeric Antigen Receptor CD8+ T Cells in Patients with Recurrent Glioblastoma , 2015, Clinical Cancer Research.

[7]  H. Wolterbeek,et al.  A Critical Review of Alpha Radionuclide Therapy—How to Deal with Recoiling Daughters? , 2015, Pharmaceuticals.

[8]  H. Brem,et al.  Delivery of local therapeutics to the brain: working toward advancing treatment for malignant gliomas. , 2015, Therapeutic delivery.

[9]  H. Vié,et al.  Human natural killer cells promote cross‐presentation of tumor cell‐derived antigens by dendritic cells , 2015, International journal of cancer.

[10]  K. Aldape,et al.  FIRST-IN-HUMAN PHASE I CLINICAL TRIAL OF ONCOLYTIC DELTA-24-RGD (DNX-2401) WITH BIOLOGICAL ENDPOINTS: IMPLICATIONS FOR VIRO- IMMUNOTHERAPY , 2014 .

[11]  John A. Dagata,et al.  A Nanoparticle Carrying the p53 Gene Targets Tumors Including Cancer Stem Cells, Sensitizes Glioblastoma to Chemotherapy and Improves Survival , 2014, ACS nano.

[12]  H. Wolterbeek,et al.  Retention studies of recoiling daughter nuclides of 225Ac in polymer vesicles. , 2014, Applied radiation and isotopes : including data, instrumentation and methods for use in agriculture, industry and medicine.

[13]  B. Becher,et al.  Intratumoral IL-12 combined with CTLA-4 blockade elicits T cell–mediated glioma rejection , 2013, The Journal of experimental medicine.

[14]  S. Kesari,et al.  Clinical trials of viral therapy for malignant gliomas , 2013, Expert review of anticancer therapy.

[15]  Z. Ram,et al.  Adenovirus-mediated gene therapy with sitimagene ceradenovec followed by intravenous ganciclovir for patients with operable high-grade glioma (ASPECT): a randomised, open-label, phase 3 trial. , 2013, The Lancet. Oncology.

[16]  P. De Bonis,et al.  Radioimmunotherapy for high-grade glioma. , 2013, Immunotherapy.

[17]  Rex A. Moats,et al.  Neural Stem Cell–Mediated Enzyme/Prodrug Therapy for Glioma: Preclinical Studies , 2013, Science Translational Medicine.

[18]  P. Lowenstein,et al.  Safety profile, efficacy, and biodistribution of a bicistronic high-capacity adenovirus vector encoding a combined immunostimulation and cytotoxic gene therapy as a prelude to a phase I clinical trial for glioblastoma. , 2013, Toxicology and applied pharmacology.

[19]  M. Andreou,et al.  Rhenium-188 Production in Hospitals, by W-188/Re-188 Generator, for Easy Use in Radionuclide Therapy , 2013, International journal of molecular imaging.

[20]  D. Casciano,et al.  Reversing chemoresistance of malignant glioma stem cells using gold nanoparticles , 2013, International journal of nanomedicine.

[21]  Vittorio Cristini,et al.  A Computational Model for Predicting Nanoparticle Accumulation in Tumor Vasculature , 2013, PloS one.

[22]  Weiwu Wang,et al.  Suppression of Autophagy Enhanced Growth Inhibition and Apoptosis of Interferon-β in Human Glioma Cells , 2013, Molecular Neurobiology.

[23]  S. Phuphanich,et al.  Phase I trial of a multi-epitope-pulsed dendritic cell vaccine for patients with newly diagnosed glioblastoma , 2012, Cancer Immunology, Immunotherapy.

[24]  Harry E. Gruber,et al.  Brain tumor eradication and prolonged survival from intratumoral conversion of 5-fluorocytosine to 5-fluorouracil using a nonlytic retroviral replicating vector , 2011, Neuro-oncology.

[25]  L. Liau,et al.  Implementing preclinical study findings to protocol design: translational studies with alloreactive CTL for gliomas. , 2012, American journal of translational research.

[26]  P. Lowenstein,et al.  Combined Flt3L/TK Gene Therapy Induces Immunological Surveillance Which Mediates an Immune Response Against a Surrogate Brain Tumor Neoantigen. , 2011, Molecular therapy : the journal of the American Society of Gene Therapy.

[27]  R. Grossman,et al.  Phase IB study of gene-mediated cytotoxic immunotherapy adjuvant to up-front surgery and intensive timing radiation for malignant glioma. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[28]  P. Lowenstein,et al.  Gene therapy and targeted toxins for glioma. , 2005, Current gene therapy.

[29]  A. Heimberger,et al.  Immunotherapy coming of age: what will it take to make it standard of care for glioblastoma? , 2011, Neuro-oncology.

[30]  Yang Xu,et al.  Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived PC12 cells. , 2010, ACS nano.

[31]  P. De Bonis,et al.  Glioblastoma therapy: going beyond Hercules Columns , 2010, Expert review of neurotherapeutics.

[32]  M. Gromeier,et al.  Preparing an oncolytic poliovirus recombinant for clinical application against glioblastoma multiforme. , 2010, Cytokine & growth factor reviews.

[33]  K. Harrington,et al.  Phase II clinical trial of a granulocyte-macrophage colony-stimulating factor-encoding, second-generation oncolytic herpesvirus in patients with unresectable metastatic melanoma. , 2009, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[34]  R. Dillman,et al.  Intralesional Lymphokine-activated Killer Cells as Adjuvant Therapy for Primary Glioblastoma , 2009, Journal of immunotherapy.

[35]  D. Bigner,et al.  Glioblastoma multiforme: a review of where we have been and where we are going , 2009, Expert opinion on investigational drugs.

[36]  Y. Tabata,et al.  Selective and sustained delivery of basic fibroblast growth factor (bFGF) for treatment of peripheral arterial disease: results of a phase I trial. , 2009, European journal of vascular and endovascular surgery : the official journal of the European Society for Vascular Surgery.

[37]  A. Haseley,et al.  Advances in oncolytic virus therapy for glioma. , 2009, Recent patents on CNS drug discovery.

[38]  W. Fellows-Mayle,et al.  Therapeutic efficacy of a herpes simplex virus with radiation or temozolomide for intracranial glioblastoma after convection-enhanced delivery. , 2008, Molecular therapy : the journal of the American Society of Gene Therapy.

[39]  Jun Yoshida,et al.  A phase I clinical trial of interferon‐beta gene therapy for high‐grade glioma: novel findings from gene expression profiling and autopsy , 2008, The journal of gene medicine.

[40]  S. Rosenfeld,et al.  A Phase I Trial of Ad.hIFN-β Gene Therapy for Glioma. , 2008, Molecular therapy : the journal of the American Society of Gene Therapy.

[41]  B. Thompson,et al.  A phase I trial of intratumoral administration of reovirus in patients with histologically confirmed recurrent malignant gliomas. , 2008, Molecular therapy : the journal of the American Society of Gene Therapy.

[42]  E. Galanis,et al.  Oncolytic measles virus strains in the treatment of gliomas , 2008, Expert opinion on biological therapy.

[43]  J. Karp,et al.  Nanocarriers as an Emerging Platform for Cancer Therapy , 2022 .

[44]  P. Lehenkari,et al.  Human mesenchymal stem cells lack tumor tropism but enhance the antitumor activity of oncolytic adenoviruses in orthotopic lung and breast tumors. , 2007, Human gene therapy.

[45]  D. Bigner,et al.  Antitenascin-C monoclonal antibody radioimmunotherapy for malignant glioma patients , 2007, Expert review of anticancer therapy.

[46]  S. Russell,et al.  History of oncolytic viruses: genesis to genetic engineering. , 2007, Molecular therapy : the journal of the American Society of Gene Therapy.

[47]  J. Nicholas,et al.  Convection-enhanced delivery of immunotoxins and radioisotopes for treatment of malignant gliomas. , 2006, Neurosurgical focus.

[48]  M. Berger,et al.  Comparison of intratumoral bolus injection and convection-enhanced delivery of radiolabeled antitenascin monoclonal antibodies. , 2006, Neurosurgical focus.

[49]  J. Gomori,et al.  Phase I/II trial of intravenous NDV-HUJ oncolytic virus in recurrent glioblastoma multiforme. , 2006, Molecular therapy : the journal of the American Society of Gene Therapy.

[50]  L. Coussens,et al.  Paradoxical roles of the immune system during cancer development , 2006, Nature Reviews Cancer.

[51]  E. Oldfield,et al.  Surface properties, more than size, limiting convective distribution of virus-sized particles and viruses in the central nervous system. , 2005, Journal of neurosurgery.

[52]  Timothy F. Cloughesy,et al.  Dendritic Cell Vaccination in Glioblastoma Patients Induces Systemic and Intracranial T-cell Responses Modulated by the Local Central Nervous System Tumor Microenvironment , 2005, Clinical Cancer Research.

[53]  Barry W Wessels,et al.  Safety and Feasibility of Convection-enhanced Delivery of Cotara for the Treatment of Malignant Glioma: Initial Experience in 51 Patients , 2005, Neurosurgery.

[54]  Naoto Tsuchiya,et al.  Clinical evaluation of dendritic cell vaccination for patients with recurrent glioma: results of a clinical phase I/II trial. , 2005, Clinical cancer research : an official journal of the American Association for Cancer Research.

[55]  P. Lowenstein,et al.  Gene therapy and targeted toxins for glioma. , 2005, Current gene therapy.

[56]  J. Olson,et al.  A phase I open-label, dose-escalation, multi-institutional trial of injection with an E1B-Attenuated adenovirus, ONYX-015, into the peritumoral region of recurrent malignant gliomas, in the adjuvant setting. , 2004, Molecular therapy : the journal of the American Society of Gene Therapy.

[57]  M. Zalutsky,et al.  Targeted radiotherapy of brain tumours , 2004, British Journal of Cancer.

[58]  C. Herold-Mende,et al.  Parvovirus H‐1 infection of human glioma cells leads to complete viral replication and efficient cell killing , 2004, International journal of cancer.

[59]  Brian M. Suzuki,et al.  Striatal delivery of rAAV-hAADC to rats with preexisting immunity to AAV. , 2004, Molecular therapy : the journal of the American Society of Gene Therapy.

[60]  B. Bodey,et al.  MTH-68/H Oncolytic Viral Treatment in Human High-Grade Gliomas , 2004, Journal of Neuro-Oncology.

[61]  M. Mizuno,et al.  IFN-β Gene Therapy Induces Systemic Antitumor Immunity Against Malignant Glioma , 2000, Journal of Neuro-Oncology.

[62]  Volker Sturm,et al.  Imaging‐guided convection‐enhanced delivery and gene therapy of glioblastoma , 2003, Annals of neurology.

[63]  R. Tanaka,et al.  Vaccination of recurrent glioma patients with tumour lysate-pulsed dendritic cells elicits immune responses: results of a clinical phase I/II trial , 2003, British Journal of Cancer.

[64]  D. B. Paul,et al.  Human Alloreactive CTL Interactions with Gliomas and with Those Having Upregulated HLA Expression from Exogenous IFN-γ or IFN-γ Gene Modification , 2003 .

[65]  Susan M. Chang,et al.  Phase I trial of adenovirus-mediated p53 gene therapy for recurrent glioma: biological and clinical results. , 2003, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[66]  G. Fuller,et al.  Preclinical characterization of the antiglioma activity of a tropism-enhanced adenovirus targeted to the retinoblastoma pathway. , 2003, Journal of the National Cancer Institute.

[67]  D. B. Paul,et al.  Human alloreactive CTL interactions with gliomas and with those having upregulated HLA expression from exogenous IFN-gamma or IFN-gamma gene modification. , 2003, Journal of interferon & cytokine research : the official journal of the International Society for Interferon and Cytokine Research.

[68]  Margareta M. Mueller,et al.  Clinical impact and functional aspects of tenascin‐C expression during glioma progression , 2002, International journal of cancer.

[69]  R. Coleman,et al.  Phase II trial of murine (131)I-labeled antitenascin monoclonal antibody 81C6 administered into surgically created resection cavities of patients with newly diagnosed malignant gliomas. , 2002, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[70]  K. Black,et al.  Vaccination of malignant glioma patients with peptide-pulsed dendritic cells elicits systemic cytotoxicity and intracranial T-cell infiltration. , 2001, Cancer research.

[71]  N. Rainov A phase III clinical evaluation of herpes simplex virus type 1 thymidine kinase and ganciclovir gene therapy as an adjuvant to surgical resection and radiation in adults with previously untreated glioblastoma multiforme. , 2000, Human gene therapy.

[72]  P. Black,et al.  Neural stem cells display extensive tropism for pathology in adult brain: evidence from intracranial gliomas. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[73]  M. Zalutsky,et al.  Astatine-211-labeled radiotherapeutics: an emerging approach to targeted alpha-particle radiotherapy. , 2000, Current pharmaceutical design.

[74]  R. Martuza,et al.  Conditionally replicating herpes simplex virus mutant, G207 for the treatment of malignant glioma: results of a phase I trial , 2000, Gene Therapy.

[75]  A. Maclean,et al.  Toxicity evaluation of replication-competent herpes simplex virus (ICP 34.5 null mutant 1716) in patients with recurrent malignant glioma , 2000, Gene Therapy.

[76]  R. Grossman,et al.  Phase I study of adenoviral delivery of the HSV-tk gene and ganciclovir administration in patients with current malignant brain tumors. , 2000, Molecular therapy : the journal of the American Society of Gene Therapy.

[77]  M. Mizuno,et al.  IFN-beta gene therapy induces systemic antitumor immunity against malignant glioma. , 2000, Journal of neuro-oncology.

[78]  D. Louis,et al.  Oncolytic virus therapy of multiple tumors in the brain requires suppression of innate and elicited antiviral responses , 1999, Nature Medicine.

[79]  A. Merlo,et al.  Frequent Co‐Alterations of TP53, p16/CDKN2A, p14ARF, PTEN Tumor Suppressor Genes in Human Glioma Cell Lines. , 1999, Brain pathology.

[80]  S. Ylä-Herttuala,et al.  Beta-galactosidase gene transfer to human malignant glioma in vivo using replication-deficient retroviruses and adenoviruses. , 1998, Human gene therapy.

[81]  C. Janeway,et al.  Innate immunity: impact on the adaptive immune response. , 1997, Current opinion in immunology.

[82]  R. Martuza,et al.  Attenuated multi–mutated herpes simplex virus–1 for the treatment of malignant gliomas , 1995, Nature Medicine.

[83]  P F Morrison,et al.  Convection-enhanced distribution of large molecules in gray matter during interstitial drug infusion. , 1995, Journal of neurosurgery.

[84]  B. Badie,et al.  Adenovirus-mediated p53 gene delivery inhibits 9L glioma growth in rats. , 1995, Neurological research.

[85]  W. Paulus,et al.  Messenger RNA expression of the immunosuppressive cytokine IL-10 in human gliomas. , 1995, The American journal of pathology.

[86]  K. Hopkins,et al.  A pilot study of the treatment of patients with recurrent malignant gliomas with intratumoral yttrium-90 radioimmunoconjugates. , 1995, Radiotherapy and oncology : journal of the European Society for Therapeutic Radiology and Oncology.

[87]  D. Constam,et al.  Differential expression of transforming growth factor-beta 1, -beta 2, and -beta 3 by glioblastoma cells, astrocytes, and microglia. , 1992, Journal of immunology.

[88]  D M Coen,et al.  Experimental therapy of human glioma by means of a genetically engineered virus mutant , 1991, Science.

[89]  R. Merchant,et al.  Adoptive immunotherapy for recurrent glioblastoma multiforme using lymphokine activated killer cells and recombinant interleukin‐2 , 1988, Cancer.

[90]  T. Friedmann,et al.  Gene Therapy for Human Genetic Disease? , 1972, Science.

[91]  P. Medawar Immunity to homologous grafted skin; the fate of skin homografts transplanted to the brain, to subcutaneous tissue, and to the anterior chamber of the eye. , 1948, British journal of experimental pathology.