NF-κB hyperactivation in tumor tissues allows tumor-selective reprogramming of the chemokine microenvironment to enhance the recruitment of cytolytic T effector cells

Cancer Research

Volumn 72, Issue 15, 2012, Pages 3735-3743

  Muthuswamy, Ravikumar ^a   Berk, Erik ^a   Junecko, Beth Fallert ^b   Zeh, Herbert J ^a   Zureikat, Amer H ^a   Normolle, Daniel ^d   Luong, The Minh ^d   Reinhart, Todd A ^b,c   Bartlett, David L ^a   Kalinski, Pawel ^a,b,c  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b UNIVERSITY OF PITTSBURGH   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MACROPHAGE DERIVED CHEMOKINE; RANTES;

ADULT; ARTICLE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOTOXIC T LYMPHOCYTE; EFFECTOR CELL; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOCYTE MIGRATION; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT;

CACO-2 CELLS; CARCINOMA; CELLS, CULTURED; CHEMOKINES; CHEMOTAXIS, LEUKOCYTE; COLORECTAL NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HT29 CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MALE; MIDDLE AGED; NEOPLASMS; NF-KAPPA B; NUCLEAR REPROGRAMMING; ORGAN SPECIFICITY; T-LYMPHOCYTES, CYTOTOXIC; TUMOR MICROENVIRONMENT; UP-REGULATION;

EID: 84864834764     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-11-4136     Document Type: Article

References (40)

1. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313: 1960-4.
2. Naito Y, Saito K, Shiiba K, Ohuchi A, Saigenji K, Nagura H, et al. CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res 1998;58:3491-4.
3. Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 2005;353: 2654-66.
4. Ropponen KM, Eskelinen MJ, Lipponen PK, Alhava E, Kosma VM. Prognostic value of tumour-infiltrating lymphocytes (TILs) in colorectal cancer. J Pathol 1997;182:318-24.
5. Clarke SL, Betts GJ, Plant A, Wright KL, El-Shanawany TM, Harrop R, et al. CD4+CD25+FOXP3+ regulatory T cells suppress anti-tumor immune responses in patients with colorectal cancer. PLoS One 2006;1:e129.
6. Ling KL, Dulphy N, Bahl P, Salio M, Maskell K, Piris J, et al. Modulation of CD103 expression on human colon carcinoma-specific CTL. J Immunol 2007;178:2908-15.
7. Michel S, Benner A, Tariverdian M, Wentzensen N, Hoefler P, Pommerencke T, et al. High density of FOXP3-positive T cells infiltrating colorectal cancers with microsatellite instability. Br J Cancer 2008;99:1867-73.
8. Chaput N, Louafi S, Bardier A, Charlotte F, Vaillant JC, Ménégaux F, et al. Identification of CD8+CD25+Foxp3 +suppressive T cells in colorectal cancer tissue. Gut 2009;58:520-9.
9. Bonecchi R, Bianchi G, Bordignon PP, D'Ambrosio D, Lang R, Borsatti A, et al. Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J Exp Med 1998;187:129-34.
10. Hirai H, Tanaka K, Yoshie O, Ogawa K, Kenmotsu K, Takamori Y, et al. Prostaglandin D2 selectively induces chemotaxis in T helper type 2 cells, eosinophils, and basophils via seven-transmembrane receptor CRTH2. J Exp Med 2001;193:255-61.
11. Iellem A, Mariani M, Lang R, Recalde H, Panina-Bordignon P, Sinigaglia F, et al. Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+) CD25(+) regulatory T cells. J Exp Med 2001;194:847-53.
12. Loetscher P, Uguccioni M, Bordoli L, Baggiolini M, Moser B, Chizzolini C, et al. CCR5 is characteristic of Th1 lymphocytes. Nature 1998; 391:344-5.
13. Sallusto F, Lenig D, Mackay CR, Lanzavecchia A. Flexible programs of chemokine receptor expression on human polarized T helper 1 and 2 lymphocytes. J Exp Med 1998;187:875-83.
14. Sallusto F, Mackay CR, Lanzavecchia A. Selective expression of the eotaxin receptor CCR3 by human T helper 2 cells. Science 1997;277:2005-7.
15. Musha H, Ohtani H, Mizoi T, Kinouchi M, Nakayama T, Shiiba K, et al. Selective infiltration of CCR5(+)CXCR3(+) T lymphocytes in human colorectal carcinoma. Int J Cancer 2005;116:949-56.
16. Kunz M, Toksoy A, Goebeler M, Engelhardt E, Brocker E, Gillitzer R. Strong expression of the lymphoattractant C-X-C chemokine Mig is associated with heavy in filtration of T cells in human malignant melanoma. J Pathol 1999;189:552-8.
17. Ohtani H, Jin Z, Takegawa S, Nakayama T, Yoshie O. Abundant expression of CXCL9 (MIG) by stromal cells that include dendritic cells and accumulation of CXCR3 +T cells in lymphocyte-rich gastric carcinoma. J Pathol 2009;217:21-31.
18. Mlecnik B, Tosolini M, Charoentong P, Kirilovsky A, Bindea G, Berger A, et al. Biomolecular network reconstruction identifies T cell homing factors associated with survival in colorectal cancer. Gastroenterology 2009;138:1429-40.
19. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004; 10:942-9.
20. Soumaoro LT, Uetake H, Higuchi T, Takagi Y, Enomoto M, Sugihara K. Cyclooxygenase-2 expression: a significant prognostic indicator for patients with colorectal cancer. Clin Cancer Res 2004;10:8465-71.
21. Williams C, Shattuck-Brandt RL, DuBois RN. The role of COX-2 in intestinal cancer. Ann N Y Acad Sci 1999;889:72-83.
22. Muthuswamy R, Urban J, Lee JJ, Reinhart TA, Bartlett D, Kalinski P. Ability of mature dendritic cells to interact with regulatory T cells is imprinted during maturation. Cancer Res 2008;68:5972-8.
23. Lebre MC, Kalinski P, Das PK, Everts V. Inhibition of contact sensitizer-induced migration of human Langerhans cells by matrix metalloproteinase inhibitors. Arch Dermatol Res 1999;291:447-52.
24. Greten FR, Eckmann L, Greten TF, Park JM, Li ZW, Egan LJ, et al. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 2004;118:285-96.
25. Sakamoto K, Maeda S, Hikiba Y, Nakagawa H, Hayakawa Y, Shibata W, et al. Constitutive NF-kappaB activation in colorectal carcinoma plays a key role in angiogenesis, promoting tumor growth. Clin Cancer Res 2009;15:2248-58.
26. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 2006;441:431-6.
27. Pikarsky E, Porat RM, Stein I, Abramovitch R, Amit S, Kasem S, et al. NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 2004;431:461-6.
28. Hoffmann A, Levchenko A, Scott ML, Baltimore D. The IkappaB-NFkappaB signaling module: temporal control and selective gene activation. Science 2002;298:1241-5.
29. Clarke DL, Clifford RL, Jindarat S, Proud D, Pang L, Belvisi M, et al. TNFα and IFNγ synergistically enhance transcriptional activation of CXCL10 in human airway smooth muscle cells via STAT-1, NF-κB, and the transcriptional coactivator CREB-binding protein. J Biol Chem 2010;285:29101-10.
30. Liu LY, Bates ME, Jarjour NN, Busse WW, Bertics PJ, Kelly EA. Generation of Th1 and Th2 chemokines by human eosinophils: evidence for a critical role of TNF-alpha. J Immunol 2007;179:4840-8.
31. Dudley ME, Wunderlich JR, Shelton TE, Even J, Rosenberg SA. Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients. J Immunother 2003;26: 332-42.
32. Watchmaker PB, Berk E, Muthuswamy R, Mailliard RB, Urban JA, Kirkwood JM, et al. Independent regulation of chemokine responsiveness and cytolytic function versus CD8+ T cell expansion by dendritic cells. J Immunol 2010;184:591-7.
33. Fallert BA, Reinhart TA. Improved detection of simian immunodeficiency virus RNA by in situ hybridization in fixed tissue sections: combined effects of temperatures for tissue fixation and probe hybridization. J Virol Methods 2002;99:23-32.
34. Reinhart TA, Fallert BA, Pfeifer ME, Sanghavi S, Capuano S, Rajakumar P, et al. Increased expression of the inflammatory chemokine CXC chemokine ligand 9/monokine induced by interferon-gamma in lymphoid tissues of rhesus macaques during simian immunodeficiency virus infection and acquired immunodeficiency syndrome. Blood 2002;99:3119-28.
35. Ascierto ML, De Giorgi V, Liu Q, Bedognetti D, Spivey TL, Murtas D, et al. An immunologic portrait of cancer. J Transl Med 2011;9:146.
36. Spivey TL, Uccellini L, Ascierto ML, Zoppoli G, De Giorgi V, Delogu LG, et al. Gene expression profiling in acute allograft rejection: challenging the immunologic constant of rejection hypothesis. J Transl Med 2011;9:174.
37. Ugurel S, Schrama D, Keller G, Schadendorf D, Bröcker EB, Houben R, et al. Impact of the CCR5 gene polymorphism on the survival of metastatic melanoma patients receiving immunotherapy. Cancer Immunol Immunother 2008;57:685-91.
38. Inngjerdingen M, Damaj B, Maghazachi AA. Expression and regulation of chemokine receptors in human natural killer cells. Blood 2001; 97:367-75.
39. Martín-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, et al. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 2004;5:1260-5.
40. Mailliard RB, Wankowicz-Kalinska A, Cai Q, Wesa A, Hilkens CM, Kapsenberg ML, et al. alpha-type-1 polarized dendritic cells: a novel immunization tool with optimized CTL-inducing activity. Cancer Res 2004;64:5934-7.