Gene expression analysis of TIL rich HPV-driven head and neck tumors reveals a distinct B-cell signature when compared to HPV independent tumors

Oncotarget

Volumn 7, Issue 35, 2016, Pages 56781-56797

  Wood, Oliver ^a   Woo, Jeongmin ^a   Seumois, Gregory ^c   Savelyeva, Natalia ^a   McCann, Katy J ^a   Singh, Divya ^c   Jones, Terry ^b   Peel, Lailah ^a   Breen, Michael S ^a   Ward, Matthew ^a   Martin, Eva Garrido ^a   Sanchez Elsner, Tilman ^a   Thomas, Gareth ^a   Vijayanand, Pandurangan ^a,c   Woelk, Christopher H ^a   King, Emma ^a   Ottensmeier, Christian ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Head and neck squamous cell carcinoma; Human papilloma virus; RNA sequencing; Transcriptome; Tumor infiltrating lymphocyte

Indexed keywords

CD200 ANTIGEN; PROTEIN BCL 2; TRANSCRIPTOME; VASCULAR CELL ADHESION MOLECULE 1;

ADAM28 GENE; ADAPTIVE IMMUNITY; ADULT; ARTICLE; B LYMPHOCYTE; BCL2 GENE; CANCER PROGNOSIS; CD200 GENE; CELL DENSITY; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION; GGA2 GENE; HEAD AND NECK CANCER; HUMAN; HUMAN TISSUE; ICOSLG GENE; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE COUNT; MALE; MIDDLE AGED; PAPILLOMAVIRUS INFECTION; QUALITATIVE ANALYSIS; RNA SEQUENCE; SEQUENCE ANALYSIS; SPIB GENE; STAG3 GENE; T LYMPHOCYTE; TUMOR ASSOCIATED LEUKOCYTE; VCAM1 GENE; AGED; CLUSTER ANALYSIS; COMPLICATION; CYTOLOGY; GENE EXPRESSION PROFILING; HEAD AND NECK TUMOR; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNOLOGY; KAPLAN MEIER METHOD; METABOLISM; PROGNOSIS; SQUAMOUS CELL CARCINOMA; VIROLOGY;

AGED; B-LYMPHOCYTES; CARCINOMA, SQUAMOUS CELL; CLUSTER ANALYSIS; FEMALE; GENE EXPRESSION PROFILING; HEAD AND NECK NEOPLASMS; HUMAN PAPILLOMAVIRUS 16; HUMANS; IMMUNOHISTOCHEMISTRY; KAPLAN-MEIER ESTIMATE; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MIDDLE AGED; PAPILLOMAVIRUS INFECTIONS; PROGNOSIS; SEQUENCE ANALYSIS, RNA; TRANSCRIPTOME;

EID: 84984889382     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.10788     Document Type: Article

References (52)

1. Argiris A, Karamouzis MV, Raben D and Ferris RL. Head and neck cancer. Lancet. 2008; 371:1695-1709.
2. Parkin DM, Bray F, Ferlay J and Pisani P. Global cancer statistics, 2002. CA. 2005; 55:74-108.
3. Blot WJ, McLaughlin JK, Winn DM, Austin DF, Greenberg RS, Preston-Martin S, Bernstein L, Schoenberg JB, Stemhagen A and Fraumeni JF, Jr. Smoking and drinking in relation to oral and pharyngeal cancer. Cancer research. 1988; 48:3282-3287.
4. Chaturvedi AK, Engels EA, Anderson WF and Gillison ML. Incidence trends for human papillomavirus-related and-unrelated oral squamous cell carcinomas in the United States. Journal of clinical oncology. 2008; 26:612-619.
5. Chaturvedi AK, Engels EA, Pfeiffer RM, Hernandez BY, Xiao W, Kim E, Jiang B, Goodman MT, Sibug-Saber M, Cozen W, Liu L, Lynch CF, Wentzensen N, Jordan RC, Altekruse S, Anderson WF, et al. Human papillomavirus and rising oropharyngeal cancer incidence in the United States. Journal of clinical oncology. 2011; 29:4294-4301.
6. Attner P, Du J, Nasman A, Hammarstedt L, Ramqvist T, Lindholm J, Marklund L, Dalianis T and Munck-Wikland E. The role of human papillomavirus in the increased incidence of base of tongue cancer. International journal of cancer. 2010; 126:2879-2884.
7. Ward MJ, Thirdborough SM, Mellows T, Riley C, Harris S, Suchak K, Webb A, Hampton C, Patel NN, Randall CJ, Cox HJ, Jogai S, Primrose J, Piper K, Ottensmeier CH, King EV, et al. Tumour-infiltrating lymphocytes predict for outcome in HPV-positive oropharyngeal cancer. British journal of cancer. 2014; 110:489-500.
8. Ang KK, Harris J, Wheeler R, Weber R, Rosenthal DI, Nguyen-Tan PF, Westra WH, Chung CH, Jordan RC, Lu C, Kim H, Axelrod R, Silverman CC, Redmond KP and Gillison ML. Human papillomavirus and survival of patients with oropharyngeal cancer. The New England journal of medicine. 2010; 363:24-35.
9. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, Tosolini M, Camus M, Berger A, Wind P, Zinzindohoue F, Bruneval P, Cugnenc PH, Trajanoski Z, Fridman WH and Pages F. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science. 2006; 313:1960-1964.
10. Rooney MS, Shukla SA, Wu CJ, Getz G and Hacohen N. Molecular and genetic properties of tumors associated with local immune cytolytic activity. Cell. 2015; 160:48-61.
11. Cancer Genome Atlas N. Comprehensive genomic characterization of head and neck squamous cell carcinomas. Nature. 2015; 517:576-582.
12. Heusinkveld M, Goedemans R, Briet RJ, Gelderblom H, Nortier JW, Gorter A, Smit VT, Langeveld AP, Jansen JC and van der Burg SH. Systemic and local human papillomavirus 16-specific T-cell immunity in patients with head and neck cancer. International journal of cancer. 2012; 131:E74-85.
13. Stransky N, EgloffAM, Tward AD, Kostic AD, Cibulskis K, Sivachenko A, Kryukov GV, Lawrence MS, Sougnez C, McKenna A, Shefler E, Ramos AH, Stojanov P, Carter SL, Voet D, Cortes ML, et al. The mutational landscape of head and neck squamous cell carcinoma. Science. 2011; 333:1157-1160.
14. Jung AC, Briolat J, Millon R, de Reynies A, Rickman D, Thomas E, Abecassis J, Clavel C and Wasylyk B. Biological and clinical relevance of transcriptionally active human papillomavirus (HPV) infection in oropharynx squamous cell carcinoma. International journal of cancer. 2010; 126:1882-1894.
15. Pyeon D, Newton MA, Lambert PF, den Boon JA, Sengupta S, Marsit CJ, Woodworth CD, Connor JP, Haugen TH, Smith EM, Kelsey KT, Turek LP and Ahlquist P. Fundamental differences in cell cycle deregulation in human papillomavirus-positive and human papillomavirusnegative head/neck and cervical cancers. Cancer research. 2007; 67:4605-4619.
16. Slebos RJ, Yi Y, Ely K, Carter J, Evjen A, Zhang X, Shyr Y, Murphy BM, Cmelak AJ, Burkey BB, Netterville JL, Levy S, Yarbrough WG and Chung CH. Gene expression differences associated with human papillomavirus status in head and neck squamous cell carcinoma. Clinical cancer research. 2006; 12:701-709.
17. Russell S, Angell T, Lechner M, Liebertz D, Correa A, Sinha U, Kokot N and Epstein A. Immune cell infiltration patterns and survival in head and neck squamous cell carcinoma. Head & neck oncology. 2013; 5:24.
18. Chung CH, Parker JS, Karaca G, Wu J, Funkhouser WK, Moore D, Butterfoss D, Xiang D, Zanation A, Yin X, Shockley WW, Weissler MC, Dressler LG, Shores CG, Yarbrough WG and Perou CM. Molecular classification of head and neck squamous cell carcinomas using patterns of gene expression. Cancer cell. 2004; 5:489-500.
19. Thurlow JK, Pena Murillo CL, Hunter KD, Buffa FM, Patiar S, Betts G, West CM, Harris AL, Parkinson EK, Harrison PR, Ozanne BW, Partridge M and Kalna G. Spectral clustering of microarray data elucidates the roles of microenvironment remodeling and immune responses in survival of head and neck squamous cell carcinoma. Journal of clinical oncology. 2010; 28:2881-2888.
20. Kamburov A, Pentchev K, Galicka H, Wierling C, Lehrach H and Herwig R. ConsensusPathDB: toward a more complete picture of cell biology. Nucleic acids research. 2011; 39:D712-717.
21. Shoemaker JE, Lopes TJ, Ghosh S, Matsuoka Y, Kawaoka Y and Kitano H. CTen: a web-based platform for identifying enriched cell types from heterogeneous microarray data. BMC genomics. 2012; 13:460.
22. Abbas AR, Baldwin D, Ma Y, Ouyang W, Gurney A, Martin F, Fong S, van Lookeren Campagne M, Godowski P, Williams PM, Chan AC and Clark HF. Immune response in silico (IRIS): immune-specific genes identified from a compendium of microarray expression data. Genes Immun. 2005; 6:319-331.
23. Watkins NA, Gusnanto A, de Bono B, De S, Miranda-Saavedra D, Hardie DL, Angenent WG, Attwood AP, Ellis PD, Erber W, Foad NS, Garner SF, Isacke CM, Jolley J, Koch K, Macaulay IC, et al. A HaemAtlas: characterizing gene expression in differentiated human blood cells. Blood. 2009; 113:e1-9.
24. Palmer C, Diehn M, Alizadeh AA and Brown PO. Cell-type specific gene expression profiles of leukocytes in human peripheral blood. BMC genomics. 2006; 7:115.
25. Grigoryev YA, Kurian SM, Avnur Z, Borie D, Deng J, Campbell D, Sung J, Nikolcheva T, Quinn A, Schulman H, Peng SL, Schaffer R, Fisher J, Mondala T, Head S, Flechner SM, et al. Deconvoluting post-transplant immunity: cell subset-specific mapping reveals pathways for activation and expansion of memory T, monocytes and B cells. PloS one. 2010; 5:e13358.
26. Whitney AR, Diehn M, Popper SJ, Alizadeh AA, Boldrick JC, Relman DA and Brown PO. Individuality and variation in gene expression patterns in human blood. Proceedings of the National Academy of Sciences of the United States of America. 2003; 100:1896-1901.
27. Prieto I, Suja JA, Pezzi N, Kremer L, Martinez AC, Rufas JS and Barbero JL. Mammalian STAG3 is a cohesin specific to sister chromatid arms in meiosis I. Nature cell biology. 2001; 3:761-766.
28. Colmont CS, Benketah A, Reed SH, Hawk NV, Telford WG, Ohyama M, Udey MC, Yee CL, Vogel JC and Patel GK. CD200-expressing human basal cell carcinoma cells initiate tumor growth. Proceedings of the National Academy of Sciences of the United States of America. 2013; 110:1434-1439.
29. Moreno-Galindo C, Hermsen M, Garcia-Pedrero JM, Fresno MF, Suarez C and Rodrigo JP. p27 and BCL2 expression predicts response to chemotherapy in head and neck squamous cell carcinomas. Oral oncology. 2014; 50:128-134.
30. Ward MJ, Mellows T, Harris S, Webb A, Patel NN, Cox HJ, Piper K, Ottensmeier CH, Thomas GJ and King EV. Staging and treatment of oropharyngeal cancer in the human papillomavirus era. Head & neck. 2014.
31. Liu D, Xu H, Shih C, Wan Z, Ma X, Ma W, Luo D and Qi H. T-B-cell entanglement and ICOSL-driven feed-forward regulation of germinal centre reaction. Nature. 2014.
32. Kobayashi A, Darragh T, Herndier B, Anastos K, MinkoffH, Cohen M, Young M, Levine A, Grant LA, Hyun W, Weinberg V, Greenblatt R and Smith-McCune K. Lymphoid follicles are generated in high-grade cervical dysplasia and have differing characteristics depending on HIV status. The American journal of pathology. 2002; 160:151-164.
33. Nelson BH. CD20+ B cells: the other tumorinfiltrating lymphocytes. Journal of immunology. 2010; 185:4977-4982.
34. Martin-Orozco N, Li Y, Wang Y, Liu S, Hwu P, Liu YJ, Dong C and Radvanyi L. Melanoma cells express ICOS ligand to promote the activation and expansion of T-regulatory cells. Cancer research. 2010; 70:9581-9590.
35. Fan X, Quezada SA, Sepulveda MA, Sharma P and Allison JP. Engagement of the ICOS pathway markedly enhances efficacy of CTLA-4 blockade in cancer immunotherapy. The Journal of experimental medicine. 2014; 211:715-725.
36. Su GH, Ip HS, Cobb BS, Lu MM, Chen HM and Simon MC. The Ets protein Spi-B is expressed exclusively in B cells and T cells during development. The Journal of experimental medicine. 1996; 184:203-214.
37. Liang C, Marsit CJ, McClean MD, Nelson HH, Christensen BC, Haddad RI, Clark JR, Wein RO, Grillone GA, Houseman EA, Halec G, Waterboer T, Pawlita M, Krane JF and Kelsey KT. Biomarkers of HPV in head and neck squamous cell carcinoma. Cancer research. 2012; 72:5004-5013.
38. Barclay AN, Wright GJ, Brooke G and Brown MH. CD200 and membrane protein interactions in the control of myeloid cells. Trends in immunology. 2002; 23:285-290.
39. Holmannova D, Kolackova M, Kondelkova K, Kunes P, Krejsek J and Andrys C. CD200/CD200R paired potent inhibitory molecules regulating immune and inflammatory responses; Part I: CD200/CD200R structure, activation, and function. Acta Medica (Hradec Kralove). 2012; 55:12-17.
40. Badoual C, Hans S, Rodriguez J, Peyrard S, Klein C, Agueznay Nel H, Mosseri V, Laccourreye O, Bruneval P, Fridman WH, Brasnu DF and Tartour E. Prognostic value of tumor-infiltrating CD4+ T-cell subpopulations in head and neck cancers. Clinical cancer research: an official journal of the American Association for Cancer Research. 2006; 12:465-472.
41. Lindner S, Dahlke K, Sontheimer K, Hagn M, Kaltenmeier C, Barth TF, Beyer T, Reister F, Fabricius D, LotfiR, Lunov O, Nienhaus GU, Simmet T, Kreienberg R, Moller P, Schrezenmeier H, et al. Interleukin 21-induced granzyme B-expressing B cells infiltrate tumors and regulate T cells. Cancer research. 2013; 73:2468-2479.
42. Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, Venturi GM, Szabolcs PM, Bernstein SH, Magro CM, Williams AD, Hall RP, St Clair EW and Tedder TF. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011; 117:530-541.
43. Rygiel TP and Meyaard L. CD200R signaling in tumor tolerance and inflammation: A tricky balance. Current opinion in immunology. 2012; 24:233-238.
44. Wang L, Liu JQ, Talebian F, El-Omrani HY, Khattabi M, Yu L and Bai XF. Tumor expression of CD200 inhibits IL-10 production by tumor-associated myeloid cells and prevents tumor immune evasion of CTL therapy. European journal of immunology. 2010; 40:2569-2579.
45. Affara NI, Ruffell B, Medler TR, Gunderson AJ, Johansson M, Bornstein S, Bergsland E, SteinhoffM, Li Y, Gong Q, Ma Y, Wiesen JF, Wong MH, Kulesz-Martin M, Irving B and Coussens LM. B cells regulate macrophage phenotype and response to chemotherapy in squamous carcinomas. Cancer cell. 2014; 25:809-821.
46. Woyach JA, Johnson AJ and Byrd JC. The B-cell receptor signaling pathway as a therapeutic target in CLL. Blood. 2012; 120:1175-1184.
47. Anders S, Pyl PT and Huber W. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinformatics. 2014.
48. Nikolayeva O and Robinson MD. edgeR for differential RNA-seq and ChIP-seq analysis: an application to stem cell biology. Methods in molecular biology. 2014; 1150:45-79.
49. Robinson MD, McCarthy DJ and Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010; 26:139-140.
50. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, PfafflMW, Shipley GL, Vandesompele J and Wittwer CT. The MIQE guidelines: minimum information for publication of quantitative realtime PCR experiments. Clinical chemistry. 2009; 55:611-622.
51. Livak KJ and Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001; 25:402-408.
52. Yang X, Regan K, Huang Y, Zhang Q, Li J, Seiwert TY, Cohen EE, Xing HR and Lussier YA. Single sample expression-anchored mechanisms predict survival in head and neck cancer. PLoS computational biology. 2012; 8:e1002350.