Interferon-gamma-induced nitric oxide inhibits the proliferation of mu-rine renal cell carcinoma cells

International Journal of Biological Sciences

Volumn 8, Issue 8, 2012, Pages 1109-1120

  Tate, David J ^a   Patterson, John R ^a   Velasco Gonzalez, Cruz ^b   Carroll, Emily N ^c   Trinh, Janie ^a   Edwards, Daniel ^a   Aiyar, Ashok ^a   Finkel Jimenez, Beatriz ^a   Zea, Arnold H ^a  

^a LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^c OHIO STATE UNIVERSITY   (United States)

Author keywords

Arginase 2; Cell proliferation; Interferon gamma; L arginine; Nitric oxide; Nitric oxide synthase; Polyamines; Renal cell carcinoma

Indexed keywords

EID: 84867491526     PISSN: 14492288     EISSN: None     Source Type: Journal    
DOI: 10.7150/ijbs.4694     Document Type: Article

References (53)

1. Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 2011 Jul;61(4):212-36.
2. Staehler M, Rohrmann K, Bachmann A, Zaak D, Stief CG, Siebels M. Therapeutic approaches in metastatic renal cell carcinoma. BJU Int 2005 Jun;95(8):1153-61.
3. Bleumer I, Oosterwijk E, De MP, Mulders PF. Immunotherapy for renal cell carcinoma. Eur Urol 2003 Jul;44(1):65-75.
4. Atkins MB, Regan M, McDermott D. Update on the role of interleukin 2 and other cytokines in the treatment of patients with stage IV renal car-cinoma. Clin Cancer Res 2004 Sep 15;10(18 Pt 2):6342S-6S.
5. McDermott DF, Regan MM, Clark JI, Flaherty LE, Weiss GR, Logan TF, Kirkwood JM, Gordon MS, Sosman JA, Ernstoff MS, Tretter CP, Urba WJ, et al. Randomized phase III trial of high-dose interleukin-2 versus subcutaneous interleukin-2 and interferon in patients with metastatic renal cell carcinoma. J Clin Oncol 2005 Jan 1;23(1):133-41.
6. Atkins MB, Bukowski RM, Escudier BJ, Figlin RA, Hudes GH, Kaelin WG, Jr., Linehan WM, McDermott DF, Mier JW, Pedrosa I, Rini BI, Si-gnoretti S, et al. Innovations and challenges in renal cancer: summary statement from the Third Cambridge Conference. Cancer 2009 May 15;115(10 Suppl):2247-51.
7. Ko JS, Zea AH, Rini BI, Ireland JL, Elson P, Cohen P, Golshayan A, Rayman PA, Wood L, Garcia J, Dreicer R, Bukowski R, et al. Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin Cancer Res 2009 Mar 15;15(6):2148-57.
8. De Mulder PH. Targeted therapy in metastatic renal cell carcinoma. Ann Oncol 2007 Jul;18 Suppl 9:ix98-102.
9. Sosman JA, Puzanov I, Atkins MB. Opportunities and obstacles to com-bination targeted therapy in renal cell cancer. Clin Cancer Res 2007 Jan 15;13(2 Pt 2):764s-9s.
10. Morris SM, Jr. Recent advances in arginine metabolism: roles and regu-lation of the arginases. Br J Pharmacol 2009 Jul;157(6):922-30.
11. Munder M. Arginase: an emerging key player in the mammalian im-mune system. Br J Pharmacol 2009 Oct;158(3):638-51.
12. Bronte V, Zanovello P. Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol 2005 Aug;5(8):641-54.
13. Viola A, Bronte V. Metabolic mechanisms of cancer-induced inhibition of immune responses. Semin Cancer Biol 2007 Aug;17(4):309-16.
14. Peranzoni E, Marigo I, Dolcetti L, Ugel S, Sonda N, Taschin E, Mantelli B, Bronte V, Zanovello P. Role of arginine metabolism in immunity and immunopathology. Immunobiology 2007;212(9-10):795-812.
15. Wu G, Morris SM, Jr. Arginine metabolism: nitric oxide and beyond. Biochem J 1998 Nov 15;336 (Pt 1):1-17.
16. Li H, Meininger CJ, Kelly KA, Hawker JR, Jr., Morris SM, Jr., Wu G. Activities of arginase I and II are limiting for endothelial cell prolifera-tion. Am J Physiol Regul Integr Comp Physiol 2002 Jan;282(1):R64-R69.
17. Buga GM, Wei LH, Bauer PM, Fukuto JM, Ignarro LJ. NG-hydroxy-L-arginine and nitric oxide inhibit Caco-2 tumor cell pro-liferation by distinct mechanisms. Am J Physiol 1998 Oct;275(4 Pt 2):R1256-R1264.
18. Zea AH, Rodriguez PC, Culotta KS, Hernandez CP, DeSalvo J, Ochoa JB, Park HJ, Zabaleta J, Ochoa AC. L-Arginine modulates CD3zeta expres-sion and T cell function in activated human T lymphocytes. Cell Immu-nol 2004 Nov;232(1-2):21-31.
19. Munder M, Eichmann K, Moran JM, Centeno F, Soler G, Modolell M. Th1/Th2-regulated expression of arginase isoforms in murine macro-phages and dendritic cells. J Immunol 1999 Oct 1;163(7):3771-7.
20. Finke JH, Rini B, Ireland J, Rayman P, Richmond A, Golshayan A, Wood L, Elson P, Garcia J, Dreicer R, Bukowski R. Sunitinib reverses type-1 immune suppression and decreases T-regulatory cells in renal cell car-cinoma patients. Clin Cancer Res 2008 Oct 15;14(20):6674-82.
21. Tatsumi T, Kierstead LS, Ranieri E, Gesualdo L, Schena FP, Finke JH, Bukowski RM, Mueller-Berghaus J, Kirkwood JM, Kwok WW, Storkus WJ. Disease-associated bias in T helper type 1 (Th1)/Th2 CD4(+) T cell responses against MAGE-6 in HLA-DRB10401(+) patients with renal cell carcinoma or melanoma. J Exp Med 2002 Sep 2;196(5):619-28.
22. Onishi T, Ohishi Y, Imagawa K, Ohmoto Y, Murata K. An assessment of the immunological environment based on intratumoral cytokine pro-duction in renal cell carcinoma. BJU Int 1999 Mar;83(4):488-92.
23. Tate DJ, Jr., Vonderhaar DJ, Caldas YA, Metoyer T, Patterson JR, Aviles DH, Zea AH. Effect of arginase II on L-arginine depletion and cell growth in murine cell lines of renal cell carcinoma. J Hematol Oncol 2008;1:14.
24. Dutcher JP, Fine JP, Krigel RL, Murphy BA, Schaefer PL, Ernstoff MS, Loehrer PJ. Stratification by risk factors predicts survival on the active treatment arm in a randomized phase II study of interferon-gamma plus/minus interferon-alpha in advanced renal cell carcinoma (E6890). Med Oncol 2003;20(3):271-81.
25. Kirkwood JM, Bryant J, Schiller JH, Oken MM, Borden EC, Whiteside TL. Immunomodulatory function of interferon-gamma in patients with metastatic melanoma: results of a phase II-B trial in subjects with meta-static melanoma, ECOG study E 4987. Eastern Cooperative Oncology Group. J Immunother 1997 Mar;20(2):146-57.
26. Berner V, Liu H, Zhou Q, Alderson KL, Sun K, Weiss JM, Back TC, Longo DL, Blazar BR, Wiltrout RH, Welniak LA, Redelman D, et al. IFN-gamma mediates CD4+ T-cell loss and impairs secondary antitumor responses after successful initial immunotherapy. Nat Med 2007 Mar;13(3):354-60.
27. Hillman GG, Younes E, Visscher D, Hamzavi F, Kim S, Lam JS, Mon-tecillo EJ, Ali E, Pontes JE, Puri RK, Haas GP. Inhibition of murine renal carcinoma pulmonary metastases by systemic administration of inter-feron gamma: mechanism of action and potential for combination with interleukin 4. Clin Cancer Res 1997 Oct;3(10):1799-806.
28. Gruys ME, Back TC, Subleski J, Wiltrout TA, Lee JK, Schmidt L, Watanabe M, Stanyon R, Ward JM, Wigginton JM, Wiltrout RH. Induc-tion of transplantable mouse renal cell cancers by streptozotocin: in vivo growth, metastases, and angiogenic phenotype. Cancer Res 2001 Aug 15;61(16):6255-63.
29. Zea AH, Culotta KS, Ali J, Mason C, Park HJ, Zabaleta J, Garcia LF, Ochoa AC. Decreased expression of CD3zeta and nuclear transcription factor kappa B in patients with pulmonary tuberculosis: potential mechanisms and reversibility with treatment. J Infect Dis 2006 Nov 15;194(10):1385-93.
30. Cory AH, Owen TC, Barltrop JA, Cory JG. Use of an aqueous soluble tetrazolium/formazan assay for cell growth assays in culture. Cancer Commun 1991 Jul;3(7):207-12.
31. Zea AH, Rodriguez PC, Atkins MB, Hernandez C, Signoretti S, Zabaleta J, McDermott D, Quiceno D, Youmans A, O'Neill A, Mier J, Ochoa AC. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res 2005 Apr 15;65(8):3044-8.
32. Haas GP, Hillman GG. Update on the Role of Immunotherapy in the Management of Kidney Cancer. Cancer Control 1996 Nov;3(6):536-41.
33. Hillman GG, Younes E, Visscher D, Hamzavi F, Kim S, Lam JS, Mon-tecillo EJ, Ali E, Pontes JE, Puri RK, Haas GP. Inhibition of murine renal carcinoma pulmonary metastases by systemic administration of inter-feron gamma: mechanism of action and potential for combination with interleukin 4. Clin Cancer Res 1997 Oct;3(10):1799-806.
34. Negrier S, Escudier B, Lasset C, Douillard JY, Savary J, Chevreau C, Ravaud A, Mercatello A, Peny J, Mousseau M, Philip T, Tursz T. Re-combinant human interleukin-2, recombinant human interferon alfa-2a, or both in metastatic renal-cell carcinoma. Groupe Francais d'Immuno-therapie. N Engl J Med 1998 Apr 30;338(18):1272-8.
35. Motzer RJ, Bacik J, Murphy BA, Russo P, Mazumdar M. Interferon-alfa as a comparative treatment for clinical trials of new therapies against advanced renal cell carcinoma. J Clin Oncol 2002 Jan 1;20(1):289-96.
36. Rosenberg SA, Lotze MT, Yang JC, Linehan WM, Seipp C, Calabro S, Karp SE, Sherry RM, Steinberg S, White DE. Combination therapy with interleukin-2 and alpha-interferon for the treatment of patients with advanced cancer. J Clin Oncol 1989 Dec;7(12):1863-74.
37. Spencer WF, Linehan WM, Walther MM, Haas GP, Lotze MT, Topalian SL, Yang JC, Merino MJ, Lange JR, Pockaj BA,. Immunotherapy with interleukin-2 and alpha-interferon in patients with metastatic renal cell cancer with in situ primary cancers: a pilot study. J Urol 1992 Jan;147(1):24-30.
38. Ellerhorst JA, Kilbourn RG, Amato RJ, Zukiwski AA, Jones E, Logothetis CJ. Phase II trial of low dose gamma-interferon in metastatic renal cell carcinoma. J Urol 1994 Sep;152(3):841-5.
39. Ernstoff MS, Nair S, Bahnson RR, Miketic LM, Banner B, Gooding W, Day R, Whiteside T, Hakala T, Kirkwood JM. A phase IA trial of se-quential administration recombinant DNA-produced interferons: com-bination recombinant interferon gamma and recombinant interferon alfa in patients with metastatic renal cell carcinoma. J Clin Oncol 1990 Oct;8(10):1637-49.
40. Ikeda H, Old LJ, Schreiber RD. The roles of IFN gamma in protection against tumor development and cancer immunoediting. Cytokine Growth Factor Rev 2002 Apr;13(2):95-109.
41. Angiolillo AL, Sgadari C, Taub DD, Liao F, Farber JM, Maheshwari S, Kleinman HK, Reaman GH, Tosato G. Human interferon-inducible pro-tein 10 is a potent inhibitor of angiogenesis in vivo. J Exp Med 1995 Jul 1;182(1):155-62.
42. Ignarro LJ. The unique role of nitric oxide as a signaling molecule in the cardiovascular system. Ital Heart J 2000 Sep;1 Suppl 3:S28-S29.
43. Li H, Meininger CJ, Hawker JR, Jr., Haynes TE, Kepka-Lenhart D, Mistry SK, Morris SM, Jr., Wu G. Regulatory role of arginase I and II in nitric oxide, polyamine, and proline syntheses in endothelial cells. Am J Physiol Endocrinol Metab 2001 Jan;280(1):E75-E82.
44. Wang WW, Jenkinson CP, Griscavage JM, Kern RM, Arabolos NS, Byrns RE, Cederbaum SD, Ignarro LJ. Co-induction of arginase and nitric oxide synthase in murine macrophages activated by lipopolysaccharide. Bio-chem Biophys Res Commun 1995 May 25;210(3):1009-16.
45. Gotoh T, Mori M. Arginase II downregulates nitric oxide (NO) produc-tion and prevents NO-mediated apoptosis in murine macro-phage-derived RAW 264.7 cells. J Cell Biol 1999 Feb 8;144(3):427-34.
46. Sousa MS, Latini FR, Monteiro HP, Cerutti JM. Arginase 2 and nitric oxide synthase: Pathways associated with the pathogenesis of thyroid tumors. Free Radic Biol Med 2010 Sep 15;49(6):997-1007.
47. Hussain SP, Trivers GE, Hofseth LJ, He P, Shaikh I, Mechanic LE, Doja S, Jiang W, Subleski J, Shorts L, Haines D, Laubach VE, et al. Nitric oxide, a mediator of inflammation, suppresses tumorigenesis. Cancer Res 2004 Oct 1;64(19):6849-53.
48. Rodriguez PC, Quiceno DG, Ochoa AC. L-arginine availability regulates T-lymphocyte cell-cycle progression. Blood 2007 Feb 15;109(4):1568-73.
49. Singh R, Pervin S, Karimi A, Cederbaum S, Chaudhuri G. Arginase activity in human breast cancer cell lines: N(omega)-hydroxy-L-arginine selectively inhibits cell proliferation and induces apoptosis in MDA-MB-468 cells. Cancer Res 2000 Jun 15;60(12):3305-12.
50. Korkola JE, Blaveri E, DeVries S, Moore DH, Hwang ES, Chen YY, Estep AL, Chew KL, Jensen RH, Waldman FM. Identification of a robust gene signature that predicts breast cancer outcome in independent data sets. BMC Cancer 2007;7:61.
51. Brinckmann A, Axer S, Jakschies D, Dallmann I, Grosse J, Patzelt T, Bernier T, Emmendoerffer A, Atzpodien J. Interferon-alpha resistance in renal carcinoma cells is associated with defective induction of signal transducer and activator of transcription 1 which can be restored by a supernatant of phorbol 12-myristate 13-acetate stimulated peripheral blood mononuclear cells. Br J Cancer 2002 Feb 1;86(3):449-55.
52. Shang D, Liu Y, Ito N, Kamoto T, Ogawa O. Defective Jak-Stat activation in renal cell carcinoma is associated with interferon-alpha resistance. Cancer Sci 2007 Aug;98(8):1259-64.
53. Fukumura D, Kashiwagi S, Jain RK. The role of nitric oxide in tumour progression. Nat Rev Cancer 2006 Jul;6(7):521-34.