OX40 expression enhances the prognostic significance of CD8 positive lymphocyte infiltration in colorectal cancer

Oncotarget

Volumn 6, Issue 35, 2015, Pages 37588-37599

  Weixler, Benjamin ^a   Cremonesi, Eleonora ^a   Sorge, Roberto ^b   Muraro, Manuele Giuseppe ^a   Delko, Tarik ^a   Nebiker, Christian A ^a   Däster, Silvio ^a   Governa, Valeria ^a   Amicarella, Francesca ^a   Soysal, Savas D ^a   Kettelhack, Christoph ^a   von Holzen, Urs W ^a,c   Eppenberger Castori, Serenella ^d   Spagnoli, Giulio C ^a   Oertli, Daniel ^a   Iezzi, Giandomenica ^a   Terracciano, Luigi ^d   Tornillo, Luigi ^d   Sconocchia, Giuseppe ^e   Droeser, Raoul A ^a  

^a UNIVERSITY HOSPITAL BASEL   (Switzerland)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c IU Health Goshen Center for Cancer Care   (United States)

^d UNIVERSITY HOSPITAL BASEL   (Switzerland)

^e INSTITUTE OF TRANSLATIONAL PHARMACOLOGY   (Italy)

Author keywords

CD8; Colorectal cancer; Microenvironment; OX40; Prognosis

Indexed keywords

CD134 ANTIGEN; CD8 ANTIGEN; TRANSCRIPTION FACTOR FOXP3; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; MESSENGER RNA; TNFRSF4 PROTEIN, HUMAN; TUMOR MARKER;

ADULT; AGED; ARTICLE; CANCER PROGNOSIS; COHORT ANALYSIS; COLORECTAL CANCER; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE COURSE; FEMALE; GENE EXPRESSION REGULATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; MALE; ONCOGENE; OVERALL SURVIVAL; OX40 GENE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REGRESSION ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL RATE; TISSUE MICROARRAY; TUMOR VOLUME; VALIDATION PROCESS; CANCER GRADING; CANCER STAGING; CD8+ T LYMPHOCYTE; COLORECTAL TUMOR; ENZYME IMMUNOASSAY; FOLLOW UP; GENETICS; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MORTALITY; PROGNOSIS; REAL TIME POLYMERASE CHAIN REACTION; TUMOR ASSOCIATED LEUKOCYTE; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ANTIGENS, CD8; BIOMARKERS, TUMOR; CD8-POSITIVE T-LYMPHOCYTES; COLORECTAL NEOPLASMS; FEMALE; FOLLOW-UP STUDIES; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; IMMUNOENZYME TECHNIQUES; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM STAGING; PROGNOSIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, OX40; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SURVIVAL RATE; TISSUE ARRAY ANALYSIS;

EID: 84947765628     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.5940     Document Type: Article

References (43)

1. Ferlay J, Soerjomataram I I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin D M, Forman D D, Bray F. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 2014;136:E359-86.
2. Cunningham D, Atkin W, Lenz H-J, Lynch HT, Minsky B, Nordlinger B, Starling N. Colorectal cancer. Lancet (London, England) 2010;375:1030-47.
3. Zlobec I, Lugli A. Prognostic and predictive factors in colorectal cancer. Postgrad Med J 2008;84:403-11.
4. Fridman WH, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012;12:298-306.
5. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoué F, Bruneval P, Cugnenc PH, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313:1960-4.
6. Pagès F, Berger A, Camus M, Sanchez-Cabo F, Costes A, Molidor R, Mlecnik B, Kirilowsky A, Nilsson M, Damotte D, Meatchi T, Brunveal P, Cugnenc PH, et al. Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 2005;353:2654-66.
7. Lugli A, Karamitopoulou E, Panayiotides I, Karakitsos P, Rallis G, Peros G, Iezzi G, Spagnoli G, Bihl M, Terracciano L, Zlobec I. CD8+ lymphocytes/tumour-budding index: an independent prognostic factor representing a "pro-/anti-tumour" approach to tumour host interaction in colorectal cancer. Br J Cancer 2009;101:1382-92.
8. Zlobec I, Karamitopoulou E, Terracciano L, Piscuoglio S, Iezzi G, Muraro MG, Spagnoli G, Baker K, Tzankow A, Lugli A. TIA-1 cytotoxic granule-associated RNA binding protein improves the prognostic performance of CD8 in mismatch repair-proficient colorectal cancer. PLoS One 2010;5:e14282.
9. Reissfelder C, Stamova S, Gossmann C, Braun M, Bonertz A, Walliczek U, Grimm M, Rahbari N, Koch M, Saadati M, Benner A, Buechler MW, Jaeger D, et al. Tumor-specific cytotoxic T lymphocyte activity determines colorectal cancer patient prognosis. J Clin Invest 2015;125:739-51.
10. Frey DM, Droeser RA, Viehl CT, Zlobec I, Lugli A, Zingg U, Oerlti D, Kettelhack C, Terracciano L, Tornillo L. High frequency of tumor-infiltrating FOXP3(+) regulatory T cells predicts improved survival in mismatch repair-proficient colorectal cancer patients. Int J Cancer 2010;126:2635-43.
11. Salama P, Phillips M, Grieu F, Morris M, Zeps N, Joseph D, Platell C, Iacopetta B. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 2009;27:186-92.
12. Sconocchia G, Zlobec I, Lugli A, Calabrese D, Iezzi G, Karamitopoulou E, Patsouris E, Peros G, Horcic M, Tornillo L, Zuber M, Droeser R, Muraro MG, et al. Tumor infiltration by FcγRIII (CD16)+ myeloid cells is associated with improved survival in patients with colorectal carcinoma. Int J Cancer 2011;128:2663-72.
13. Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell 2006;124:263-6.
14. Curiel TJ. Tregs and rethinking cancer immunotherapy. J Clin Invest 2007;117:1167-74.
15. Gough MJ, Weinberg AD. OX40 (CD134) and OX40L. Adv Exp Med Biol 2009;647:94-107.
16. Taraban VY, Rowley TF, O'Brien L, Chan HTC, Haswell LE, Green MHA, Tutt AL, Glennie MJ, Al-Shamkhani A. Expression and costimulatory effects of the TNF receptor superfamily members CD134 (OX40) and CD137 (4-1BB), and their role in the generation of anti-tumor immune responses. Eur J Immunol 2002;32:3617-27.
17. Croft M. Control of immunity by the TNFR-related molecule OX40 (CD134). Annu Rev Immunol 2010;28:57-78.
18. Sugamura K, Ishii N, Weinberg AD. Therapeutic targeting of the effector T-cell co-stimulatory molecule OX40. Nat Rev Immunol 2004;4:420-31.
19. Weinberg AD, Evans DE, Thalhofer C, Shi T, Prell RA. The generation of T cell memory: a review describing the molecular and cellular events following OX40 ( CD134 ) engagement 2004;40.
20. Bansal-Pakala P, Halteman BS, Cheng MH-Y, Croft M. Costimulation of CD8 T cell responses by OX40. J Immunol 2004;172:4821-5.
21. De Smedt T, Smith J, Baum P, Fanslow W, Butz E, Maliszewski C. Ox40 costimulation enhances the development of T cell responses induced by dendritic cells in vivo. J Immunol 2002;168:661-70.
22. Maxwell JR, Weinberg A, Prell RA, Vella AT. Danger and OX40 receptor signaling synergize to enhance memory T cell survival by inhibiting peripheral deletion. J Immunol 2000;164:107-12.
23. Curti BD, Kovacsovics-Bankowski M, Morris N, Walker E, Chisholm L, Floyd K, Walker J, Gonzalez I, Meeuwsen T, Fox B, Moudgil T, Miller W, Haley D, et al. OX40 is a potent immune-stimulating target in late-stage cancer patients. Cancer Res 2013;73:7189-98.
24. Gough MJ, Ruby CE, Redmond WL, Dhungel B, Brown A, Weinberg AD. OX40 agonist therapy enhances CD8 infiltration and decreases immune suppression in the tumor. Cancer Res 2008;68:5206-15.
25. Petty JK, He K, Corless CL, Ph D, Vetto JT, Weinberg AD. Survival in human colorectal cancer correlates with expression of the T-cell costimulatory molecule OX-40 ( CD134 ) 2002;183:512-8.
26. Nebiker CA, Han J, Eppenberger-Castori S, Iezzi G, Hirt C, Amicarella F, Cremonesi E, Huber X, Padovan E, Angrisani B, Droeser R, Rosso R, Bolli M, et al. GM-CSF Production by Tumor Cells Is Associated with Improved Survival in Colorectal Cancer. Clin Cancer Res 2014;20:3094-106.
27. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001;25:402-8.
28. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, Barrette T, Pandey A, Chinnaiyan AM. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 6:1-6.
29. Skrzypczak M, Goryca K, Rubel T, Paziewska A, Mikula M, Jarosz D, Pachlewski J, Oledzki J, Ostrowski J, Ostrowsk J, et al. Modeling oncogenic signaling in colon tumors by multidirectional analyses of microarray data directed for maximization of analytical reliability. PLoS One 2010;5.
30. Hong Y, Downey T, Eu KW, Koh PK, Cheah PY. A "metastasis-prone" signature for early-stage mismatch-repair proficient sporadic colorectal cancer patients and its implications for possible therapeutics. Clin Exp Metastasis 2010;27:83-90.
31. Kaiser S, Park Y-K, Franklin JL, Halberg RB, Yu M, Jessen WJ, Freudenberg J, Chen X, Haigis K, Jegga AG, Kong S, Sakthivel B, Xu H, Reichling T, et al. Transcriptional recapitulation and subversion of embryonic colon development by mouse colon tumor models and human colon cancer. Genome Biol 2007;8:R131.
32. Gaedcke J, Grade M, Jung K, Camps J, Jo P, Emons G, Gehoff A, Sax U, Schirmer M, Becker H, Beissbarth T, Ried T, Ghadimi BM. Mutated KRAS results in overexpression of DUSP4, a MAP-kinase phosphatase, and SMYD3, a histone methyltransferase, in rectal carcinomas. Genes Chromosomes Cancer 2010;49:1024-34.
33. Ki DH, Jeung H-C, Park CH, Kang SH, Lee GY, Lee WS, Kim NK, Chung HC, Rha SJ. Whole genome analysis for liver metastasis gene signatures in colorectal cancer. Int J Cancer 2007;121:2005-12.
34. Jass JR, Atkin WS, Cuzick J, Bussey HJ, Morson BC, Northover JM, Todd IP. The grading of rectal cancer: historical perspectives and a multivariate analysis of 447 cases. Histopathology 1986;10:437-59.
35. Blanche P, Dartigues J-F, Jacqmin-Gadda H. Estimating and comparing time-dependent areas under receiver operating characteristic curves for censored event times with competing risks. Stat Med 2013;32:5381-97.
36. Zlobec I, Steele R, Terracciano L, Jass JR, Lugli A. Selecting immunohistochemical cut-off scores for novel biomarkers of progression and survival in colorectal cancer. J Clin Pathol 2007;60:1112-6.
37. Tosolini M, Kirilovsky A, Mlecnik B, Fredriksen T, Mauger S, Bindea G, Berger A, Bruneval P, Fridman WH, Pages F, Galon J. Clinical Impact of Different Classes of Infiltrating T Cytotoxic and Helper Cells (Th1, Th2, Treg, Th17) in Patients with Colorectal Cancer. Cancer Res 2011;71:1263-71.
38. Hampel H, Stephens JA, Pukkala E, Sankila R, Aaltonen LA, Mecklin J-P, de la Chapelle A. Cancer risk in hereditary nonpolyposis colorectal cancer syndrome: later age of onset. Gastroenterology 2005;129:415-21.
39. Piconese S, Timperi E, Pacella I, Schinzari V, Tripodo C, Rossi M, Guglielmo N, Mennini G, Grazi GL, Di Filippo S, Brozzetti S, Fazzi K, Antonelli G, et al. Human OX40 tunes the function of regulatory T cells in tumor and nontumor areas of hepatitis C virus-infected liver tissue. Hepatology 2014;60:1494-507.
40. Ruby CE, Redmond WL, Haley D, Weinberg AD. Anti-OX40 stimulation in vivo enhances CD8 + memory T cell survival and significantly increases recall responses 2007:157-66.
41. Weinberga D, Rivera MM, Prell R, Morris a, Ramstad T, Vetto JT, Urba WJ, Alvord G, Bunce C, Shields J. Engagement of the OX-40 receptor in vivo enhances antitumor immunity. J Immunol 2000;164:2160-9.
42. Weinberg AD, Morris NP, Kovacsovics-Bankowski M, Urba WJ, Curti BD. Science gone translational: the OX40 agonist story. Immunol Rev 2011;244:218-31.
43. Abreu MT. Toll-like receptor signalling in the intestinal epithelium: how bacterial recognition shapes intestinal function. Nat Rev Immunol 2010;10:131-44.