Chemokine nitration prevents intratumoral infiltration of antigen-specific T cells

Journal of Experimental Medicine

Volumn 208, Issue 10, 2011, Pages 1949-1962

  Molon, Barbara ^a   Ugel, Stefano ^a,b   Del Pozzo, Federica ^c   Soldani, Cristiana ^c   Zilio, Serena ^d   Avella, Debora ^c   De Palma, Antonella ^e   Mauri, PierLuigi ^e   Monegal, Ana ^f   Rescigno, Maria ^f   Savino, Benedetta ^c   Colombo, Piergiuseppe ^c   Jonjic, Nives ^g   Pecanic, Sanja ^g   Lazzarato, Loretta ^h   Fruttero, Roberta ^h   Gasco, Alberto ^h   Bronte, Vincenzo ^a,j   Viola, Antonella ^c,i  

^a VENETO INSTITUTE OF ONCOLOGY IOV IRCCS   (Italy)

^b VENETIAN INSTITUTE OF MOLECULAR MEDICINE   (Italy)

^c HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

^e INSTITUTE OF BIOMEDICAL TECHNOLOGIES   (Italy)

^f EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^g UNIVERSITY OF RIJEKA   (Croatia)

^h UNIVERSITY OF TURIN   (Italy)

ⁱ UNIVERSITY OF MILAN   (Italy)

^j UNIVERSITY HOSPITAL OF VERONA   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD14 ANTIGEN; CD3 ANTIGEN; CD8 ANTIGEN; CHEMOKINE; INDUCIBLE NITRIC OXIDE SYNTHASE; MONOCYTE CHEMOTACTIC PROTEIN 1; REACTIVE NITROGEN SPECIES; SECONDARY LYMPHOID TISSUE CHEMOKINE; STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN SPECIFICITY; ARTICLE; CANCER CELL; CANCER IMMUNOTHERAPY; CANCER INVASION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; LEUKOCYTE; MOUSE; NITRATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; STROMA; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT;

ADOPTIVE TRANSFER; ANIMALS; CELL LINE, TUMOR; CELL MOVEMENT; CHEMOKINE CCL2; CHEMOKINE CXCL12; COLORECTAL NEOPLASMS; HUMANS; IMMUNOTHERAPY; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; PROTEIN PROCESSING, POST-TRANSLATIONAL; REACTIVE NITROGEN SPECIES; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR MICROENVIRONMENT;

EID: 80054694464     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20101956     Document Type: Article

References (73)

1. Abello, N., H.A. Kerstjens, D.S. Postma, and R. Bischoff. 2009. Protein tyrosine nitration: selectivity, physicochemical and biological consequences, denitration, and proteomics methods for the identification of tyrosine-nitrated proteins. J. Proteome Res. 8:3222-3238. http://dx.doi.org/10.1021/pr900039c
2. Allavena, P., G. Bianchi, D. Zhou, J. van Damme, P. Jílek, S. Sozzani, and A. Mantovani. 1994. Induction of natural killer cell migration by monocyte chemotactic protein-1, -2 and -3. Eur. J. Immunol. 24:3233-3236. http://dx.doi.org/10.1002/eji.1830241249
3. Andrew, P.J., and B. Mayer. 1999. Enzymatic function of nitric oxide synthases. Cardiovasc. Res. 43:521-531. http://dx.doi.org/10.1016/S0008-6363(99)00115-7
4. Apolloni, E., V. Bronte, A. Mazzoni, P. Serafini, A. Cabrelle, D.M. Segal, H.A. Young, and P. Zanovello. 2000. Immortalized myeloid suppressor cells trigger apoptosis in antigen-activated T lymphocytes. J. Immunol. 165:6723-6730.
5. Balkwill, F., and A. Mantovani. 2001. Inflammation and cancer: back to Virchow? Lancet. 357:539-545. http://dx.doi.org/10.1016/S0140-6736(00)04046-0
6. Boissonnas, A., L. Fetler, I.S. Zeelenberg, S. Hugues, and S. Amigorena. 2007. In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J. Exp. Med. 204:345-356. http://dx.doi.org/10.1084/jem.20061890
7. Bottazzi, B., S. Walter, D. Govoni, F. Colotta, and A. Mantovani. 1992. Monocyte chemotactic cytokine gene transfer modulates macrophage infiltration, growth, and susceptibility to IL-2 therapy of a murine melanoma. J. Immunol. 148:1280-1285.
8. Breart, B., F. Lemaître, S. Celli, and P. Bousso. 2008. Two-photon imaging of intratumoral CD8+ T cell cytotoxic activity during adoptive T cell therapy in mice. J. Clin. Invest. 118:1390-1397. http://dx.doi.org/10.1172/JCI34388
9. Bronte, V., and P. Zanovello. 2005. Regulation of immune responses by L-arginine metabolism. Nat. Rev. Immunol. 5:641-654. http://dx.doi.org/10.1038/nri1668
10. Bronte, V., P. Serafini, C. De Santo, I. Marigo, V. Tosello, A. Mazzoni, D.M. Segal, C. Staib, M. Lowel, G. Sutter, et al. 2003. IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice. J. Immunol. 170:270-278.
11. Bronte, V., T. Kasic, G. Gri, K. Gallana, G. Borsellino, I. Marigo, L. Battistini, M. Iafrate, T. Prayer-Galetti, F. Pagano, and A. Viola. 2005. Boosting antitumor responses of T lymphocytes infiltrating human prostate cancers. J. Exp. Med. 201:1257-1268. http://dx.doi.org/10.1084/jem.20042028
12. Brown, C.E., R.P. Vishwanath, B. Aguilar, R. Starr, J. Najbauer, K.S. Aboody, and M.C. Jensen. 2007. Tumor-derived chemokine MCP-1/CCL2 is sufficient for mediating tumor tropism of adoptively transferred T cells. J. Immunol. 179:3332-3341.
13. Buckanovich, R.J., A. Facciabene, S. Kim, F. Benencia, D. Sasaroli, K. Balint, D. Katsaros, A. O'Brien-Jenkins, P.A. Gimotty, and G. Coukos. 2008. Endothelin B receptor mediates the endothelial barrier to T cell homing to tumors and disables immune therapy. Nat. Med. 14:28-36. http://dx.doi.org/10.1038/nm1699
14. Butcher, E.C., and L.J. Picker. 1996. Lymphocyte homing and homeostasis. Science. 272:60-66. http://dx.doi.org/10.1126/science.272.5258.60
15. Carr, M.W., S.J. Roth, E. Luther, S.S. Rose, and T.A. Springer. 1994. Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc. Natl. Acad. Sci. USA. 91:3652-3656. http://dx.doi.org/10.1073/pnas.91.9.3652
16. Colombo, M.P., and S. Piconese. 2007. Regulatory-T-cell inhibition versus depletion: the right choice in cancer immunotherapy. Nat. Rev. Cancer. 7:880-887. http://dx.doi.org/10.1038/nrc2250
17. Corzo, C.A., T. Condamine, L. Lu, M.J. Cotter, J.I. Youn, P. Cheng, H.I. Cho, E. Celis, D.G. Quiceno, T. Padhya, et al. 2010. HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 207:2439-2453. http://dx.doi.org/10.1084/jem.20100587
18. De Palma, R., I. Marigo, F. Del Galdo, C. De Santo, P. Serafini, S. Cingarlini, T. Tüting, J. Lenz, G. Basso, G. Milan, et al. 2004. Therapeutic effectiveness of recombinant cancer vaccines is associated with a prevalent T-cell receptor alpha usage by melanoma-specific CD8+ T lymphocytes. Cancer Res. 64:8068-8076. http://dx.doi.org/10.1158/0008-5472.CAN-04-0067
19. De Santo, C., P. Serafini, I. Marigo, L. Dolcetti, M. Bolla, P. Del Soldato, C. Melani, C. Guiducci, M.P. Colombo, M. Iezzi, et al. 2005. Nitroaspirin corrects immune dysfunction in tumor-bearing hosts and promotes tumor eradication by cancer vaccination. Proc. Natl. Acad. Sci. USA. 102: 4185-4190. http://dx.doi.org/10.1073/pnas.0409783102
20. Doedens, A.L., C. Stockmann, M.P. Rubinstein, D. Liao, N. Zhang, D.G. DeNardo, L.M. Coussens, M. Karin, A.W. Goldrath, and R.S. Johnson. 2010. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 70:7465-7475. http://dx.doi.org/10.1158/0008-5472.CAN-10-1439
21. Frederick, M.J., and G.L. Clayman. 2001. Chemokines in cancer. Expert Rev. Mol. Med. 3:1-18. http://dx.doi.org/10.1017/S1462399401003301
22. Fridlender, Z.G., G. Buchlis, V. Kapoor, G. Cheng, J. Sun, S. Singhal, M.C. Crisanti, L.C. Wang, D. Heitjan, L.A. Snyder, and S.M. Albelda. 2010. CCL2 blockade augments cancer immunotherapy. Cancer Res. 70:109- 118. http://dx.doi.org/10.1158/0008-5472.CAN-09-2326
23. Gabrilovich, D.I., and S. Nagaraj. 2009. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol. 9:162-174. http://dx.doi.org/10.1038/nri2506
24. Galon, J., A. Costes, F. Sanchez-Cabo, A. Kirilovsky, B. Mlecnik, C. Lagorce-Pagès, M. Tosolini, M. Camus, A. Berger, P. Wind, et al. 2006. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 313:1960-1964. http://dx.doi.org/10.1126/science.1129139
25. Gattinoni, L., D.J. Powell Jr., S.A. Rosenberg, and N.P. Restifo. 2006. Adoptive immunotherapy for cancer: building on success. Nat. Rev. Immunol. 6:383-393. http://dx.doi.org/10.1038/nri1842
26. Griscavage, J.M., A.J. Hobbs, and L.J. Ignarro. 1995. Negative modulation of nitric oxide synthase by nitric oxide and nitroso compounds. Adv. Pharmacol. 34:215-234. http://dx.doi.org/10.1016/S1054-3589(08)61088-1
27. Grohmann, U., and V. Bronte. 2010. Control of immune response by amino acid metabolism. Immunol. Rev. 236:243-264. http://dx.doi.org/10.1111/j.1600-065X.2010.00915.x
28. Hamzah, J., M. Jugold, F. Kiessling, P. Rigby, M. Manzur, H.H. Marti, T. Rabie, S. Kaden, H.J. Gröne, G.J. Hämmerling, et al. 2008. Vascular normalization in Rgs5-deficient tumours promotes immune destruction. Nature. 453:410-414. http://dx.doi.org/10.1038/nature06868
29. Harlin, H., Y. Meng, A.C. Peterson, Y. Zha, M. Tretiakova, C. Slingluff, M. McKee, and T.F. Gajewski. 2009. Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment. Cancer Res. 69:3077-3085. http://dx.doi.org/10.1158/0008-5472.CAN-08-2281
30. Homey, B., A. Müller, and A. Zlotnik. 2002. Chemokines: agents for the immunotherapy of cancer? Nat. Rev. Immunol. 2:175-184. http://dx.doi.org/10.1038/nri748
31. Hu, H., L. Sun, C. Guo, Q. Liu, Z. Zhou, L. Peng, J. Pan, L. Yu, J. Lou, Z. Yang, et al. 2009. Tumor cell-microenvironment interaction models coupled with clinical validation reveal CCL2 and SNCG as two predictors of colorectal cancer hepatic metastasis. Clin. Cancer Res. 15:5485- 5493. http://dx.doi.org/10.1158/1078-0432.CCR-08-2491
32. Huang, B., Z. Lei, J. Zhao, W. Gong, J. Liu, Z. Chen, Y. Liu, D. Li, Y. Yuan, G.M. Zhang, and Z.H. Feng. 2007. CCL2/CCR2 pathway mediates recruitment of myeloid suppressor cells to cancers. Cancer Lett. 252:86-92. http://dx.doi.org/10.1016/j.canlet.2006.12.012
33. Izhak, L., G. Wildbaum, U. Weinberg, Y. Shaked, J. Alami, D. Dumont, B. Friedman, A. Stein, and N. Karin. 2010. Predominant expression of CCL2 at the tumor site of prostate cancer patients directs a selective loss of immunological tolerance to CCL2 that could be amplified in a beneficial manner. J. Immunol. 184:1092-1101. http://dx.doi.org/10.4049/jimmunol.0902725
34. Johnson, L.A., R.A. Morgan, M.E. Dudley, L. Cassard, J.C. Yang, M.S. Hughes, U.S. Kammula, R.E. Royal, R.M. Sherry, J.R. Wunderlich, et al. 2009. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood. 114:535-546. http://dx.doi.org/10.1182/blood-2009-03-211714
35. June, C.H. 2007. Adoptive T cell therapy for cancer in the clinic. J. Clin. Invest. 117:1466-1476. http://dx.doi.org/10.1172/JCI32446
36. Kaplan-Lefko, P.J., T.M. Chen, M.M. Ittmann, R.J. Barrios, G.E. Ayala, W.J. Huss, L.A. Maddison, B.A. Foster, and N.M. Greenberg. 2003. Pathobiology of autochthonous prostate cancer in a pre-clinical transgenic mouse model. Prostate. 55:219-237. http://dx.doi.org/10.1002/pros.10215
37. Kasic, T., P. Colombo, C. Soldani, C.M. Wang, E. Miranda, M. Roncalli, V. Bronte, and A. Viola. 2011. Modulation of human T-cell functions by reactive nitrogen species. Eur. J. Immunol. 41:1843-1849. http://dx.doi.org/10.1002/eji.201040868
38. Kurata, S., M. Matsumoto, and U. Yamashita. 1996. Concomitant transcriptional activation of nitric oxide synthase and heme oxygenase genes during nitric oxide-mediated macrophage cytostasis. J. Biochem. 120:49-52.
39. Loetscher, P., M. Seitz, I. Clark-Lewis, M. Baggiolini, and B. Moser. 1996. Activation of NK cells by CC chemokines. Chemotaxis, Ca2+ mobilization, and enzyme release. J. Immunol. 156:322-327.
40. Loos, T., A. Mortier, and P. Proost. 2009. Chapter 1. Isolation, identification, and production of posttranslationally modified chemokines. Methods Enzymol. 461:3-29. http://dx.doi.org/10.1016/S0076-6879(09)05401-9
41. Marigo, I., E. Bosio, S. Solito, C. Mesa, A. Fernandez, L. Dolcetti, S. Ugel, N. Sonda, S. Bicciato, E. Falisi, et al. 2010. Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor. Immunity. 32:790-802. http://dx.doi.org/10.1016/j.immuni.2010.05.010
42. Mariotto, S., L. Cuzzolin, A. Adami, P. Del Soldato, H. Suzuki, and G. Benoni. 1995. Effect of a new non-steroidal anti-inflammatory drug, nitroflurbiprofen, on the expression of inducible nitric oxide synthase in rat neutrophils. Br. J. Pharmacol. 115:225-226.
43. Melillo, G., T. Musso, A. Sica, L.S. Taylor, G.W. Cox, and L. Varesio. 1995. A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J. Exp. Med. 182:1683-1693. http://dx.doi.org/10.1084/jem.182.6.1683
44. Mennuni, C., S. Ugel, F. Mori, B. Cipriani, M. Iezzi, T. Pannellini, D. Lazzaro, G. Ciliberto, N. La Monica, P. Zanovello, et al. 2008. Preventive vaccination with telomerase controls tumor growth in genetically engineered and carcinogen-induced mouse models of cancer. Cancer Res. 68:9865-9874. http://dx.doi.org/10.1158/0008-5472.CAN-08-1603
45. Monegal, A., D. Ami, C. Martinelli, H. Huang, M. Aliprandi, P. Capasso, C. Francavilla, G. Ossolengo, and A. de Marco. 2009. Immunological applications of single-domain llama recombinant antibodies isolated from a naïve library. Protein Eng. Des. Sel. 22:273-280. http://dx.doi.org/10.1093/protein/gzp002
46. Morgan, R.A., M.E. Dudley, J.R. Wunderlich, M.S. Hughes, J.C. Yang, R.M. Sherry, R.E. Royal, S.L. Topalian, U.S. Kammula, N.P. Restifo, et al. 2006. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science. 314:126-129. http://dx.doi.org/10.1126/science.1129003
47. Mukai, S., J. Kjaergaard, S. Shu, and G.E. Plautz. 1999. Infiltration of tumors by systemically transferred tumor-reactive T lymphocytes is required for antitumor efficacy. Cancer Res. 59:5245-5249.
48. Murphy, P.M. 2001. Chemokines and the molecular basis of cancer metastasis. N. Engl. J. Med. 345:833-835. http://dx.doi.org/10.1056/NEJM200109133451113
49. Muzaffar, S., N. Shukla, G. Angelini, and J.Y. Jeremy. 2004. Nitroaspirins and morpholinosydnonimine but not aspirin inhibit the formation of superoxide and the expression of gp91phox induced by endotoxin and cytokines in pig pulmonary artery vascular smooth muscle cells and endothelial cells. Circulation. 110:1140-1147. http://dx.doi.org/10.1161/01.CIR.0000139851.50067.E4
50. Nagaraj, S., K. Gupta, V. Pisarev, L. Kinarsky, S. Sherman, L. Kang, D.L. Herber, J. Schneck, and D.I. Gabrilovich. 2007. Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat. Med. 13:828-835. http://dx.doi.org/10.1038/nm1609
51. Nathan, C., and A. Ding. 2010. SnapShot: reactive oxygen intermediates (ROI). Cell. 140:951-951: e2. http://dx.doi.org/10.1016/j.cell.2010.03.008
52. Noda, S., S.A. Aguirre, A. Bitmansour, J.M. Brown, T.E. Sparer, J. Huang, and E.S. Mocarski. 2006. Cytomegalovirus MCK-2 controls mobilization and recruitment of myeloid progenitor cells to facilitate dissemination. Blood. 107:30-38. http://dx.doi.org/10.1182/blood-2005-05-1833
53. Pagès, F., A. Berger, M. Camus, F. Sanchez-Cabo, A. Costes, R. Molidor, B. Mlecnik, A. Kirilovsky, M. Nilsson, D. Damotte, et al. 2005. Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med. 353:2654-2666. http://dx.doi.org/10.1056/NEJMoa051424
54. Pfeiffer, S., A. Lass, K. Schmidt, and B. Mayer. 2001. Protein tyrosine nitration in cytokine-activated murine macrophages. Involvement of a peroxidase/nitrite pathway rather than peroxynitrite. J. Biol. Chem. 276: 34051-34058. http://dx.doi.org/10.1074/jbc.M100585200
55. Pivarcsi, A., A. Müller, A. Hippe, J. Rieker, A. van Lierop, M. Steinhoff, S. Seeliger, R. Kubitza, U. Pippirs, S. Meller, et al. 2007. Tumor immune escape by the loss of homeostatic chemokine expression. Proc. Natl. Acad. Sci. USA. 104:19055-19060. http://dx.doi.org/10.1073/pnas.0705673104
56. Quezada, S.A., K.S. Peggs, M.A. Curran, and J.P. Allison. 2006. CTLA4 blockade and GM-CSF combination immunotherapy alters the intratumor balance of effector and regulatory T cells. J. Clin. Invest. 116:1935-1945. http://dx.doi.org/10.1172/JCI27745
57. Rollins, B.J., and M.E. Sunday. 1991. Suppression of tumor formation in vivo by expression of the JE gene in malignant cells. Mol. Cell. Biol. 11:3125-3131.
58. Rosenberg, S.A., and M.E. Dudley. 2009. Adoptive cell therapy for the treatment of patients with metastatic melanoma. Curr. Opin. Immunol. 21:233-240. http://dx.doi.org/10.1016/j.coi.2009.03.002
59. Rosenberg, S.A., N.P. Restifo, J.C. Yang, R.A. Morgan, and M.E. Dudley. 2008. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat. Rev. Cancer. 8:299-308. http://dx.doi.org/10.1038/nrc2355
60. Rossi, C.A., M. Flaibani, B. Blaauw, M. Pozzobon, E. Figallo, C. Reggiani, L. Vitiello, N. Elvassore, and P. De Coppi. 2011. In vivo tissue engineering of functional skeletal muscle by freshly isolated satellite cells embedded in a photopolymerizable hydrogel. FASEB J. 25:2296-2304. http://dx.doi.org/10.1096/fj.10-174755
61. Sato, E., S.H. Olson, J. Ahn, B. Bundy, H. Nishikawa, F. Qian, A.A. Jungbluth, D. Frosina, S. Gnjatic, C. Ambrosone, et al. 2005. Intraepithelial CD8+ tumor-infiltrating lymphocytes and a high CD8+/ regulatory T cell ratio are associated with favorable prognosis in ovarian cancer. Proc. Natl. Acad. Sci. USA. 102:18538-18543. http://dx.doi.org/10.1073/pnas.0509182102
62. Serbina, N.V., T. Jia, T.M. Hohl, and E.G. Pamer. 2008. Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26:421-452. http://dx.doi.org/10.1146/annurev.immunol.26.021607.090326
63. Sozzani, S., M. Locati, D. Zhou, M. Rieppi, W. Luini, G. Lamorte, G. Bianchi, N. Polentarutti, P. Allavena, and A. Mantovani. 1995. Receptors, signal transduction, and spectrum of action of monocyte chemotactic protein-1 and related chemokines. J. Leukoc. Biol. 57:788-794.
64. Springer, T.A. 1994. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 76:301-314. http://dx.doi.org/10.1016/0092-8674(94)90337-9
65. Suzuki, M., M. Tabuchi, M. Ikeda, and T. Tomita. 2002. Concurrent formation of peroxynitrite with the expression of inducible nitric oxide synthase in the brain during middle cerebral artery occlusion and reperfusion in rats. Brain Res. 951:113-120. http://dx.doi.org/10.1016/S0006-8993(02)03145-1
66. Szabó, C., H. Ischiropoulos, and R. Radi. 2007. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat. Rev. Drug Discov. 6:662-680. http://dx.doi.org/10.1038/nrd2222
67. Ugel, S., E. Scarselli, M. Iezzi, C. Mennuni, T. Pannellini, F. Calvaruso, B. Cipriani, R. De Palma, L. Ricci-Vitiani, E. Peranzoni, et al. 2010. Autoimmune B-cell lymphopenia after successful adoptive therapy with telomerase-specific T lymphocytes. Blood. 115:1374-1384. http://dx.doi.org/10.1182/blood-2009-07-233270
68. Viola, A., and V. Bronte. 2007. Metabolic mechanisms of cancer-induced inhibition of immune responses. Semin. Cancer Biol. 17:309-316. http://dx.doi.org/10.1016/j.semcancer.2007.06.005
69. Viola, A., and A.D. Luster. 2008. Chemokines and their receptors: drug targets in immunity and inflammation. Annu. Rev. Pharmacol. Toxicol. 48:171- 197. http://dx.doi.org/10.1146/annurev.pharmtox.48.121806.154841
70. Weishaupt, C., K.N. Munoz, E. Buzney, T.S. Kupper, and R.C. Fuhlbrigge. 2007. T-cell distribution and adhesion receptor expression in metastatic melanoma. Clin. Cancer Res. 13:2549-2556. http://dx.doi.org/10.1158/1078-0432.CCR-06-2450
71. Xia, Y., and J.L. Zweier. 1997. Superoxide and peroxynitrite generation from inducible nitric oxide synthase in macrophages. Proc. Natl. Acad. Sci. USA. 94:6954-6958. http://dx.doi.org/10.1073/pnas.94.13.6954
72. Xia, Y., L.J. Roman, B.S. Masters, and J.L. Zweier. 1998. Inducible nitricoxide synthase generates superoxide from the reductase domain. J. Biol. Chem. 273:22635-22639. http://dx.doi.org/10.1074/jbc.273.35.22635
73. Zhang, B., Y. Zhang, N.A. Bowerman, A. Schietinger, Y.X. Fu, D.M. Kranz, D.A. Rowley, and H. Schreiber. 2008. Equilibrium between host and cancer caused by effector T cells killing tumor stroma. Cancer Res. 68:1563-1571. http://dx.doi.org/10.1158/0008-5472.CAN-07-5324