CTLA-4 blockade and interferon-α induce proinflammatory transcriptional changes in the tumor immune landscape that correlate with pathologic response in melanoma

PLoS One. 2021 Jan 11;16(1):e0245287. doi: 10.1371/journal.pone.0245287. eCollection 2021.

Abstract

Patients with locally/regionally advanced melanoma were treated with neoadjuvant combination immunotherapy with high-dose interferon α-2b (HDI) and ipilimumab in a phase I clinical trial. Tumor specimens were obtained prior to the initiation of neoadjuvant therapy, at the time of surgery and progression if available. In this study, gene expression profiles of tumor specimens (N = 27) were investigated using the NanoString nCounter® platform to evaluate associations with clinical outcomes (pathologic response, radiologic response, relapse-free survival (RFS), and overall survival (OS)) and define biomarkers associated with tumor response. The Tumor Inflammation Signature (TIS), an 18-gene signature that enriches for response to Programmed cell death protein 1 (PD-1) checkpoint blockade, was also evaluated for association with clinical response and survival. It was observed that neoadjuvant ipilimumab-HDI therapy demonstrated an upregulation of immune-related genes, chemokines, and transcription regulator genes involved in immune cell activation, function, or cell proliferation. Importantly, increased expression of baseline pro-inflammatory genes CCL19, CD3D, CD8A, CD22, LY9, IL12RB1, C1S, C7, AMICA1, TIAM1, TIGIT, THY1 was associated with longer OS (p < 0.05). In addition, multiple genes that encode a component or a regulator of the extracellular matrix such as MMP2 and COL1A2 were identified post-treatment as being associated with longer RFS and OS. In all baseline tissues, high TIS scores were associated with longer OS (p = 0.0166). Also, downregulated expression of cell proliferation-related genes such as CUL1, CCND1 and AAMP at baseline was associated with pathological and radiological response (unadjusted p < 0.01). In conclusion, we identified numerous genes that play roles in multiple biological pathways involved in immune activation, immune suppression and cell proliferation correlating with pathological/radiological responses following neoadjuvant immunotherapy highlighting the complexity of immune responses modulated by immunotherapy. Our observations suggest that TIS may be a useful biomarker for predicting survival outcomes with combination immunotherapy.

Publication types

  • Clinical Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • CTLA-4 Antigen / antagonists & inhibitors*
  • CTLA-4 Antigen / metabolism
  • Combined Modality Therapy
  • Disease-Free Survival
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic / drug effects
  • Immunotherapy
  • Inflammation / genetics*
  • Interferon-alpha / pharmacology
  • Interferon-alpha / therapeutic use*
  • Ipilimumab / therapeutic use
  • Melanoma / drug therapy
  • Melanoma / genetics
  • Melanoma / immunology*
  • Melanoma / pathology*
  • Neoadjuvant Therapy
  • Neoplasm Recurrence, Local / genetics
  • Neoplasm Recurrence, Local / pathology
  • Skin Neoplasms / drug therapy
  • Skin Neoplasms / genetics
  • Skin Neoplasms / immunology*
  • Skin Neoplasms / pathology*
  • Survival Analysis
  • Transcription, Genetic* / drug effects
  • Treatment Outcome

Substances

  • CTLA-4 Antigen
  • Interferon-alpha
  • Ipilimumab

Grants and funding

The study received research grant support from Bristol-Myers Squibb, Merck and NanoString Technologies. The funder provided support in the form of salaries for authors [EP, SW, THS, XR, AW, NE, AC, JB], but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section