Oncolytic adenovirus with temozolomide induces autophagy and antitumor immune responses in cancer patients

Mol Ther. 2013 Jun;21(6):1212-23. doi: 10.1038/mt.2013.51. Epub 2013 Apr 2.

Abstract

Oncolytic adenoviruses and certain chemotherapeutics can induce autophagy and immunogenic cancer cell death. We hypothesized that the combination of oncolytic adenovirus with low-dose temozolomide (TMZ) is safe, effective, and capable of inducing antitumor immune responses. Metronomic low-dose cyclophosphamide (CP) was added to selectively reduce regulatory T-cells. Preclinically, combination therapy inhibited tumor growth, increased autophagy, and triggered immunogenic cell death as indicated by elevated calreticulin, adenosine triphosphate (ATP) release, and nuclear protein high-mobility group box-1 (HMGB1) secretion. A total of 41 combination treatments given to 17 chemotherapy-refractory cancer patients were well tolerated. We observed anti- and proinflammatory cytokine release, evidence of virus replication, and induction of neutralizing antibodies. Tumor cells showed increased autophagy post-treatment. Release of HMGB1 into serum--a possible indicator of immune response--increased in 60% of treatments, and seemed to correlate with tumor-specific T-cell responses, observed in 10/15 cases overall (P = 0.0833). Evidence of antitumor efficacy was seen in 67% of evaluable treatments with a trend for increased survival over matched controls treated with virus only. In summary, the combination of oncolytic adenovirus with low-dose TMZ and metronomic CP increased tumor cell autophagy, elicited antitumor immune responses, and showed promising safety and efficacy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Adenoviridae / genetics*
  • Adenoviridae / physiology
  • Adolescent
  • Adult
  • Aged
  • Animals
  • Antibodies, Neutralizing / blood
  • Antineoplastic Agents / pharmacology*
  • Autophagy / drug effects*
  • Calreticulin / metabolism
  • Cell Death / drug effects
  • Cell Line, Tumor
  • Child
  • Combined Modality Therapy / methods
  • Cyclophosphamide / pharmacology
  • Cytokines / blood
  • DNA, Viral / blood
  • Dacarbazine / analogs & derivatives*
  • Dacarbazine / pharmacology
  • Dose-Response Relationship, Drug
  • Female
  • HMGB1 Protein / blood
  • HMGB1 Protein / metabolism
  • Humans
  • Immunohistochemistry
  • Male
  • Mice
  • Mice, Nude
  • Microscopy, Electron
  • Middle Aged
  • Neoplasms / therapy*
  • Oncolytic Virotherapy / methods*
  • Oncolytic Viruses / genetics
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism
  • Temozolomide
  • Virus Replication
  • Xenograft Model Antitumor Assays
  • Young Adult

Substances

  • Antibodies, Neutralizing
  • Antineoplastic Agents
  • Calreticulin
  • Cytokines
  • DNA, Viral
  • HMGB1 Protein
  • HMGB1 protein, human
  • Dacarbazine
  • Adenosine Triphosphate
  • Cyclophosphamide
  • Temozolomide