Ikk4a/Arf inactivation with activation of the NF-κB/IL-6 pathway is sufficient to drive the development and growth of angiosarcoma

Cancer Research

Volumn 72, Issue 18, 2012, Pages 4682-4695

  Yang, Jinming ^a   Kantrow, Sara ^a   Sai, Jiqing ^a   Hawkins, Oriana E ^a   Boothby, Mark ^a   Gregory D, Ayers ^a   Young, Eric D ^b   Demicco, Elizabeth G ^b   Lazar, Alexander J ^b   Lev, Dina ^b   Richmond, Ann ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (2 AMINOETHYLAMINO) 1,8 DIMETHYLIMIDAZO[1,2 A]QUINOXALINE; ARF PROTEIN; GLYCOPROTEIN GP 130; I KAPPA B KINASE; I KAPPA B KINASE 4A; I KAPPA B KINASE INHIBITOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; INTERLEUKIN 6; INTERLEUKIN 6 ANTIBODY; INTERLEUKIN 6 RECEPTOR; JANUS KINASE 2; STAT3 PROTEIN; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG;

ANGIOSARCOMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARF GENE; ARTICLE; BONE MARROW CELL; CANCER GROWTH; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME INHIBITION; GENE FUNCTION; GENE INACTIVATION; GENETIC TRAIT; GENETIC TRANSCRIPTION; HUMAN; HUMAN TISSUE; IKK4A GENE; MAJOR CLINICAL STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TUMOR IMMUNITY; TUMOR SUPPRESSOR GENE;

ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HEMANGIOSARCOMA; HUMANS; I-KAPPA B KINASE; INTERLEUKIN-6; MICE; MICE, KNOCKOUT; NF-KAPPA B; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TISSUE ARRAY ANALYSIS; TRANSCRIPTION FACTOR RELA;

EID: 84866396345     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-0440     Document Type: Article

References (50)

1. Mark RJ, Poen JC, Tran LM, Fu YS, Juillard GF. Angiosarcoma: A report of 67 patients and a review of the literature. Cancer 1996;77:2400-6.
2. Lahat G, Dhuka AR, Hallevi H, Xiao L, Zou C, Smith KD, et al. Angiosarcoma: clinical and molecular insights. Ann Surg;251:1098-106.
3. Naka N, Ohsawa M, Tomita Y, Kanno H, Uchida A, Aozasa K. Angiosarcoma in Japan. A review of 99 cases. Cancer 1995;75:989-96.
4. Naka N, Ohsawa M, Tomita Y, Kanno H, Uchida A, Myoui A, et al. Prognostic factors in angiosarcoma: a multivariate analysis of 55 cases. J Surg Oncol 1996;61:170-6.
5. Cohen SM, Storer RD, Criswell KA, Doerrer NG, Dellarco VL, Pegg DG, et al. Hemangiosarcoma in rodents: mode-of-action evaluation and human relevance. Toxicol Sci 2009;111:4-18.
6. Young RJ, Brown NJ, Reed MW, Hughes D, Woll PJ. Angiosarcoma. Lancet Oncol 2010;11:983-91.
7. Zietz C, Rossle M, Haas C, Sendelhofert A, Hirschmann A, Sturzl M, et al. MDM-2 oncoprotein overexpression, p53 gene mutation, and VEGF up-regulation in angiosarcomas. Am J Pathol 1998;153:1425-33.
8. Przygodzki RM, Finkelstein SD, Keohavong P, Zhu D, Bakker A, Swalsky PA, et al. Sporadic and Thorotrast-induced angiosarcomas of the liver manifest frequent and multiple point mutations in K-ras-2. Lab Invest 1997;76:153-9.
9. Manner J, Radlwimmer B, Hohenberger P, Mossinger K, Kuffer S, Sauer C, et al. MYC high level gene amplification is a distinctive feature of angiosarcomas after irradiation or chronic lymphedema. Am J Pathol;176:34-9.
10. Wong KF, So CC, Wong N, Siu LL, Kwong YL, Chan JK. Sinonasal angiosarcoma with marrow involvement at presentation mimicking malignant lymphoma: cytogenetic analysis using multiple techniques. Cancer Genet Cytogenet 2001;129:64-8.
11. Weihrauch M, Markwarth A, Lehnert G, Wittekind C, Wrbitzky R, Tannapfel A. Abnormalities of the ARF-p53 pathway in primary angiosarcomas of the liver. Hum Pathol 2002;33:884-92.
12. Tannapfel A, Weihrauch M, Benicke M, Uhlmann D, Hauss J, Wrbitzky R, et al. p16INK4A-alterations in primary angiosarcoma of the liver. J Hepatol 2001;35:62-7.
13. Reznikoff CA, Yeager TR, Belair CD, Savelieva E, Puthenveettil JA, Stadler WM. Elevated p16 at senescence and loss of p16 at immortalization in human papillomavirus 16 E6, but not E7, transformed human uroepithelial cells. Cancer Res 1996;56:2886-90.
14. Sharpless NE, Bardeesy N, Lee KH, Carrasco D, Castrillon DH, Aguirre AJ, et al. Loss of p16Ink4a with retention of p19Arf predisposes mice to tumorigenesis. Nature 2001;413:86-91.
15. Zhang Y, Xiong Y, Yarbrough WG. ARF promotes MDM2 degradation and stabilizes p53: ARF-INK4a locus deletion impairs both the Rb and p53 tumor suppression pathways. Cell 1998;92:725-34.
16. Rocha S, Campbell KJ, Perkins ND. p53- and Mdm2-independent repression of NF-kappa B transactivation by the ARF tumor suppressor. Mol Cell 2003;12:15-25.
17. Baldwin AS. Control of oncogenesis and cancer therapy resistance by the transcription factor NF-kappaB. J Clin Invest 2001;107:241-6.
18. Soo J, Arif S, Kidd BL, Jawad AS. Pyrexia, pelvic pain and thrombocytopenia in an Asian man with Paget's disease of bone. Rheumatology (Oxford) 2004;43:110-1.
19. ChenSY, Takeuchi S, Urabe K, Hayashida S, Kido M, Tomoeda H, et al. Overexpression of phosphorylated-ATF2 and STAT3 in cutaneous angiosarcoma and pyogenic granuloma. J Cutan Pathol 2008;35:722-30.
20. Grivennikov S, Karin E, Terzic J, Mucida D, Yu GY, Vallabhapurapu S, et al. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer. Cancer Cell 2009;15:103-13.
21. Yang J, Splittgerber R, Yull FE, Kantrow S, Ayers GD, Karin M, et al. Conditional ablation of Ikkb inhibits melanoma tumor development in mice. J Clin Invest 2010;120:2563-74.
22. Serrano M, Lee H, Chin L, Cordon-Cardo C, Beach D, DePinho RA. Role of the INK4a locus in tumor suppression and cell mortality. Cell 1996;85:27-37.
23. Sharpless NE, Ramsey MR, Balasubramanian P, Castrillon DH, DePinho RA. The differential impact of p16(INK4a) or p19(ARF) de ficiency on cell growth and tumorigenesis. Oncogene 2004;23:379-85.
24. Sharpless NE, Alson S, Chan S, Silver DP, Castrillon DH, DePinho RA. p16(INK4a) and p53 deficiency cooperate in tumorigenesis. Cancer Res 2002;62:2761-5.
25. Yang J, Luan J, Yu Y, Li C, DePinho RA, Chin L, et al. Induction of melanoma in murine macrophage inflammatory protein 2 transgenic mice heterozygous for inhibitor of kinase/alternate reading frame. Cancer Res 2001;61:8150-7.
26. Meis-Kindblom JM, Kindblom LG. Angiosarcoma of soft tissue: a study of 80 cases. Am J Surg Pathol 1998;22:683-97.
27. Maddox JC, Evans HL. Angiosarcoma of skin and soft tissue: a study of forty-four cases. Cancer 1981;48:1907-21.
28. Fan Y, Ye J, Shen F, Zhu Y, Yeghiazarians Y, Zhu W, et al. Interleukin-6 stimulates circulating blood-derived endothelial progenitor cell angiogenesis in vitro. J Cereb Blood Flow Metab 2008;28:90-8.
29. McClintock JY, Wagner EM. Role of IL-6 in systemic angiogenesis of the lung. J Appl Physiol 2005;99:861-6.
30. Gregory MS, Faunce DE, Duffner LA, Kovacs EJ. Gender difference in cell-mediated immunity after thermal injury is mediated, in part, by elevated levels of interleukin-6. J Leukoc Biol 2000;67:319-26.
31. Poutahidis T, Haigis KM, Rao VP, Nambiar PR, Taylor CL, Ge Z, et al. Rapid reversal of interleukin-6-dependent epithelial invasion in a mouse model of microbially induced colon carcinoma. Carcinogenesis 2007;28:2614-23.
32. Becker TM, Rizos H, de la Pena A, Leclercq IA, Woodruff S, Kefford RF, et al. Impaired inhibition of NF-kappaB activity by melanoma-associated p16INK4a mutations. Biochem Biophys Res Commun 2005;332:873-9.
33. Serrano M, Hannon GJ, Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 1993;366:704-7.
34. Hagemann T, Lawrence T, McNeish I, Charles KA, Kulbe H, Thompson RG, et al. "Re-educating" tumor-associated macrophages by targeting NF-kappaB. J Exp Med 2008;205:1261-8.
35. Silva MT. Neutrophils and macrophages work in concert as inducers and effectors of adaptive immunity against extracellular and intracellular microbial pathogens. J Leukoc Biol 2010;87:805-13.
36. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 1999;8:265-77.
37. Muzumdar MD, Tasic B, Miyamichi K, Li L, Luo L. A global double-fluorescent Cre reporter mouse. Genesis 2007;45:593-605.
38. Ray A, Tatter SB, May LT, Sehgal PB. Activation of the human "beta 2-interferon/hepatocyte-stimulating factor/interleukin 6" promoter by cytokines, viruses, and second messenger agonists. Proc Natl Acad Sci U S A 1988;85:6701- 5.
39. Karin M, Lin A. NF-kappaB at the crossroads of life and death. Nat Immunol 2002;3:221-7.
40. Basseres DS, Baldwin AS. Nuclear factor-kappaB and inhibitor of kappaB kinase pathways in oncogenic initiation and progression. Oncogene 2006;25:6817-30.
41. Squarize CH, Castilho RM, Sriuranpong V, Pinto DS Jr, Gutkind JS. Molecular cross-talk between the NFkappaB and STAT3 signaling pathways in head and neck squamous cell carcinoma. Neoplasia 2006;8:733-46.
42. Zerbini LF, Wang Y, Cho JY, Libermann TA. Constitutive activation of nuclear factor kappaB p50/p65 and Fra-1 and JunD is essential for deregulated interleukin 6 expression in prostate cancer. Cancer Res 2003;63:2206-15.
43. Maeda S, Hikiba Y, Sakamoto K, Nakagawa H, Hirata Y, Hayakawa Y, et al. Ikappa B kinasebeta/nuclear factor-kappaB activation controls the development of liver metastasis by way of interleukin-6 expression. Hepatology 2009;50:1851-60.
44. Li N, Grivennikov SI, Karin M. The unholy trinity: inflammation, cytokines, and STAT3 shape the cancer microenvironment. Cancer Cell 2011;19:429-31.
45. Yu H, Kortylewski M, Pardoll D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol 2007;7:41-51.
46. Maki RG, D'Adamo DR, Keohan ML, Saulle M, Schuetze SM, Undevia SD, et al. Phase II study of sorafenib in patients with metastatic or recurrent sarcomas. J Clin Oncol 2009;27:3133-40.
47. Chugh R, Wathen JK, Maki RG, Benjamin RS, Patel SR, Meyers PA, et al. Phase II multicenter trial of imatinib in 10 histologic subtypes of sarcoma using a bayesian hierarchical statistical model. J Clin Oncol 2009;27:3148-53.
48. Fayette J, Martin E, Piperno-Neumann S, Le Cesne A, Robert C, Bonvalot S, et al. Angiosarcomas, a heterogeneous group of sarcomas with specific behavior depending on primary site: a retrospective study of 161 cases. Ann Oncol 2007;18:2030-6.
49. Penel N, Marreaud S, Robin YM, Hohenberger P. Angiosarcoma: state of the art and perspectives. Crit Rev Oncol Hematol 2011;80:257-63.
50. Anglesio MS, George J, Kulbe H, Friedlander M, Rischin D, Lemech C, et al. IL6-STAT3-HIF signaling and therapeutic response to the angiogenesis inhibitor sunitinib in ovarian clear cell cancer. Clin Cancer Res 2011;17:2538-48.