Abstract
The novel multitargeted tyrosine kinase inhibitor sunitinib is used as an antiangiogenic agent for the treatment of several types of cancer, including metastatic renal cell carcinoma (RCC). Sunitinib was shown to positively change the immunosuppressive phenotype in RCC patients. To improve its antitumor efficacy, and offer strategies for its combination with other approaches, it is critical to fully elucidate its mechanisms of action. We show that sunitinib induces tumor cell apoptosis and growth arrest in RCC tumor cells, which correlates with signal transducer and activator of transcription 3 (Stat3) activity inhibition. Sunitinib-mediated direct effects on tumor cells occur regardless of von Hippel-Lindau tumor suppressor gene status and hypoxia-inducible transcription factor-2alpha levels. Reduction of Stat3 activity enhances the antitumor effects of sunitinib, whereas expression of a constitutively activated Stat3 mutant rescues tumor cell death. Intravital multiphoton microscopy data show that sunitinib induces mouse Renca tumor cell apoptosis in vivo before tumor vasculature collapse. Sunitinib also inhibits Stat3 in Renca tumor-associated myeloid-derived suppressor cells (MDSC), down-regulates angiogenic gene expression, and reduces MDSCs and tumor T regulatory cells. These results suggest that Stat3 activity is important for RCC response to sunitinib, and Stat3 inhibition permits the direct proapoptotic activity of sunitinib on tumor cells and positive effects on tumor immunologic microenvironment.
MeSH Terms
Animals
Antineoplastic Agents/pharmacology
Apoptosis/drug effects
Basic Helix-Loop-Helix Transcription Factors/immunology,metabolism
Carcinoma, Renal Cell/blood supply,drug therapy,immunology,pathology
Cell Growth Processes/drug effects
Cell Line, Tumor
Female
Humans
Indoles/pharmacology
Kidney Neoplasms/blood supply,drug therapy,immunology,pathology
Mice
Neovascularization, Pathologic/genetics,pathology
Pyrroles/pharmacology
STAT3 Transcription Factor/antagonists & inhibitors,immunology
Signal Transduction
Sunitinib
Von Hippel-Lindau Tumor Suppressor Protein/genetics,immunology
Chemicals
Antineoplastic Agents
Basic Helix-Loop-Helix Transcription Factors
Indoles
Pyrroles
STAT3 Transcription Factor
STAT3 protein, human
endothelial PAS domain-containing protein 1
Von Hippel-Lindau Tumor Suppressor Protein
Sunitinib
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Xin Hong
Divisions of Cancer Immunotherapeutics and Tumor Immunology, Beckman Research Institute and City of Hope Comprehensive Cancer Center, Duarte, California, USA.
Zhang Chunyan
Herrmann Andreas
Du Yan
Figlin Robert
Yu Hua
References (27)
27 references, click to expand
-
Molecular basis for sunitinib efficacy and future clinical development.
Nat Rev Drug Discov. 2007 Sep;6(9):734-45
PMID: 17690708
-
Stat3 activation is required for cellular transformation by v-src.
Mol Cell Biol. 1998 May;18(5):2553-8
PMID: 9566875
-
Hypoxia-inducible factor linked to differential kidney cancer risk seen with type 2A and type 2B VHL mutations.
Mol Cell Biol. 2007 Aug;27(15):5381-92
PMID: 17526729
-
The von Hippel-Lindau tumor suppressor gene and kidney cancer.
Clin Cancer Res. 2004 Sep 15;10(18 Pt 2):6290S-5S
PMID: 15448019
-
Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment.
Nat Rev Immunol. 2007 Jan;7(1):41-51
PMID: 17186030
-
Stat3 activation regulates the expression of matrix metalloproteinase-2 and tumor invasion and metastasis.
Oncogene. 2004 Apr 29;23(20):3550-60
PMID: 15116091
-
The STATs of cancer--new molecular targets come of age.
Nat Rev Cancer. 2004 Feb;4(2):97-105
PMID: 14964307
-
Sunitinib: from rational design to clinical efficacy.
J Clin Oncol. 2007 Mar 1;25(7):884-96
PMID: 17327610
-
HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity.
Cancer Cell. 2007 Apr;11(4):335-47
PMID: 17418410
-
Activation of dendritic cells via inhibition of Jak2/STAT3 signaling.
J Immunol. 2005 Oct 1;175(7):4338-46
PMID: 16177074
-
The activity of sunitinib against gastrointestinal stromal tumor seems to be distinct from its antiangiogenic effects.
Clin Cancer Res. 2006 Oct 15;12(20 Pt 1):6203-4
PMID: 17062698
-
Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein.
J Exp Med. 2008 Sep 29;205(10):2235-49
PMID: 18809714
-
A phase 1 study of SU11248 in the treatment of patients with refractory or resistant acute myeloid leukemia (AML) or not amenable to conventional therapy for the disease.
Blood. 2005 Feb 1;105(3):986-93
PMID: 15459012
-
SU11248 maintenance therapy prevents tumor regrowth after fractionated irradiation of murine tumor models.
Cancer Res. 2003 Jul 15;63(14):4009-16
PMID: 12873999
-
Stat3 as an oncogene.
Cell. 1999 Aug 6;98(3):295-303
PMID: 10458605
-
Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell carcinoma patients.
Clin Cancer Res. 2008 Oct 15;14(20):6674-82
PMID: 18927310
-
Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients.
Clin Cancer Res. 2009 Mar 15;15(6):2148-57
PMID: 19276286
-
Mutations in the EGFR kinase domain mediate STAT3 activation via IL-6 production in human lung adenocarcinomas.
J Clin Invest. 2007 Dec;117(12):3846-56
PMID: 18060032
-
Evolving role of novel targeted agents in renal cell carcinoma.
Oncology (Williston Park). 2007 Sep;21(10):1175-80; discussion 1184, 1187, 1190
PMID: 17926797
-
Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity.
Nat Med. 2005 Dec;11(12):1314-21
PMID: 16288283
-
Sunitinib versus interferon alfa in metastatic renal-cell carcinoma.
N Engl J Med. 2007 Jan 11;356(2):115-24
PMID: 17215529
-
Antiangiogenic and anti-invasive effects of sunitinib on experimental human glioblastoma.
Neuro Oncol. 2007 Oct;9(4):412-23
PMID: 17622648
-
In vivo antitumor activity of SU11248, a novel tyrosine kinase inhibitor targeting vascular endothelial growth factor and platelet-derived growth factor receptors: determination of a pharmacokinetic/pharmacodynamic relationship.
Clin Cancer Res. 2003 Jan;9(1):327-37
PMID: 12538485
-
Activation of signal transducer and activator of transcription 3 in renal cell carcinoma: a study of incidence and its association with pathological features and clinical outcome.
J Urol. 2002 Aug;168(2):762-5
PMID: 12131365
-
Stat3 activation by Src induces specific gene regulation and is required for cell transformation.
Mol Cell Biol. 1998 May;18(5):2545-52
PMID: 9566874
-
Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells.
Nat Med. 2004 Jan;10(1):48-54
PMID: 14702634
-
Stat3 mediates myeloid cell-dependent tumor angiogenesis in mice.
J Clin Invest. 2008 Oct;118(10):3367-77
PMID: 18776941