BRAFV600Ein papillary thyroid carcinoma is associated with increased programmed death ligand 1 expression and suppressive immune cell infiltration

Thyroid

Volumn 24, Issue 9, 2014, Pages 1385-1393

  Angell, Trevor E ^a,b   Lechner, Melissa G ^b   Jang, Julie K ^b   Correa, Adrian J ^b   LoPresti, Jonathan S ^b   Epstein, Alan L ^b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARGINASE 1; B RAF KINASE; CD3 ANTIGEN; CD68 ANTIGEN; CD8 ANTIGEN; CHLORDANE; INDOLEAMINE 2,3 DIOXYGENASE; PROGRAMMED DEATH 1 LIGAND 1; TRANSCRIPTION FACTOR FOXP3; BRAF PROTEIN, HUMAN; CD274 PROTEIN, HUMAN; HLA G ANTIGEN;

ADULT; AGED; ARTICLE; CANCER STAGING; CELL INFILTRATION; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA SEQUENCE; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOSUPPRESSIVE TREATMENT; LYMPH NODE METASTASIS; MACROPHAGE; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; RETROSPECTIVE STUDY; T LYMPHOCYTE; THYROID CARCINOMA; TUMOR ASSOCIATED LEUKOCYTE; TUMOR INVASION; GENETICS; METABOLISM; MIDDLE AGED; MUTATION; PAPILLARY CARCINOMA; PATHOLOGY; THYROID TUMOR; YOUNG ADULT;

ADULT; AGED; ANTIGENS, CD274; CARCINOMA, PAPILLARY; FEMALE; HLA-G ANTIGENS; HUMANS; MALE; MIDDLE AGED; MUTATION; PROTO-ONCOGENE PROTEINS B-RAF; THYROID NEOPLASMS; YOUNG ADULT;

EID: 84907081836     PISSN: 10507256     EISSN: 15579077     Source Type: Journal    
DOI: 10.1089/thy.2014.0134     Document Type: Article

References (56)

1. Siegel R, Naishadham D, Jemal A 2013 Cancer statistics, 2013. CA Cancer J Clin 63:11-30.
2. Amphlett B, Lawson Z, Abdulrahman GO Jr, White C, Bailey R, Premawardhana LD, Okosieme OE 2013 Recent trends in the incidence, geographical distribution, and survival from thyroid cancer in Wales, 1985-2010. Thyroid 23: 1470-1478.
3. Chen AY, Jemal A, Ward EM 2009 Increasing incidence of differentiated thyroid cancer in the United States, 1988-2005. Cancer Aug 115:3801-3807.
4. Davies L, Welch HG 2006 Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA 295: 2164-2167.
5. Hay ID, Thompson GB, Grant CS, Bergstralh EJ, Dvorak CE, Gorman CA, Maurer MS, McIver B, Mullan BP, Oberg AL, Powell CC, van Heerden JA, Goellner JR 2003 Papillary thyroid carcinoma managed at the Mayo Clinic during six decades (1940-1999): temporal trends in initial therapy and long-term outcome in 2444 consecutively treated patients. World J Surg 26:879-885. (Pubitemid 36920280)
6. American Thyroid Association (ATA) Guidelines Taskforce on Thyroid Nodules and Differentiated Thyroid Cancer, Cooper DS, Doherty GM, Haugen BR, Kloos RT, Lee SL, Mandel SJ, Mazzaferri EL, McIver B, Pacini F, Schlumberger M, Sherman SI, Steward DL, Tuttle RM 2009 Revised American Thyroid Association management guidelines for patients with thyroid nodules and differentiated thyroid cancer. Thyroid 19:1167-1214.
7. Grebe SK, Hay ID 1996 Thyroid cancer nodal metastases: biologic significance and therapeutic considerations. Surg Oncol Clin N Am 5:43-63. (Pubitemid 26047382)
8. Howlader N, Noone AM, Krapcho M, Garshell J, Neyman N, Altekruse SF, Kosary CL, Yu M, Ruhl J, Tatalovich Z, Cho H, Mariotto A, Lewis DR, Chen HS, Feuer EJ, Cronin KA (eds) 2013 SEER Cancer Statistics Review, 1975-2010, National Cancer Institute. Bethesda, MD. http://seer.cancer.gov/csr/1975-2010/ (Last accesed July 2, 2014).
9. Xing M 2013 Molecular pathogenesis and mechanisms of thyroid cancer. Nat Rev Cancer 13:184-199.
10. Xing M, Alzahrani AS, Carson KA, Viola D, Elisei R, Bendlova B, Yip L, Mian C, Vianello F, Tuttle RM, Robenshtok E, Fagin JA, Puxeddu E, Fugazzola L, Czarniecka A, Jarzab B, O'Neill CJ, Sywak MS, Lam AK, Riesco-Eizaguirre G, Santisteban P, Nakayama H, Tufano RP, Pai SI, Zeiger MA, Westra WH, Clark DP, Clifton-Bligh R, Sidransky D, Ladenson PW, Sykorova V 2013 Association between BRAF V600E mutation and mortality in patients with papillary thyroid cancer. JAMA 309:1493-1501.
11. Nikiforov YE 2011 Molecular analysis of thyroid tumors. Mod Pathol 24(Suppl 2):S34-43.
12. O'Neill CJ, Bullock M, Chou A, Sidhu SB, Delbridge LW, Robinson BG, Gill AJ, Learoyd DL, Clifton-Bligh R, Sywak MS 2010 BRAF(V600E) mutation is associated with an increased risk of nodal recurrence requiring reoperative surgery in patients with papillary thyroid cancer. Surgery 148:1139-1145.
13. Li C, Lee KC, Schneider EB, Zeiger MA 2012 BRAF V600E mutation and its association with clinicopathological features of papillary thyroid cancer: a meta-analysis. J Clin Endocrinol Metab 97:4559-4570.
14. Liu RT, Chen YJ, Chou FF, Li CL, Wu WL, Tsai PC, Huang CC, Cheng JT 2005 No correlation between BRAFV600E mutation and clinicopathological features of papillary thyroid carcinomas in Taiwan. Clin Endocrinol (Oxf) 63:461-466.
15. Gouveia C, Can NT, Bostrom A, Grenert JP, van Zante A, Orloff LA 2013 Lack of association of BRAF mutation with negative prognostic indicators in papillary thyroid carcinoma: the University of California, San Francisco, experience. JAMA Otolaryngol Head Neck Surg 139:1164-1170.
16. Stewart TJ, Abrams SI 2008 How tumours escape mass destruction. Oncogene 27:5894-5903.
17. Gooden MJ, de Bock GH, Leffers N, Daemen T, Nijman HW 2011 The prognostic influence of tumour-infiltrating lymphocytes in cancer: a systematic review with metaanalysis. Br J Cancer 105:93-103.
18. Sadun RE, Sachsman SM, Chen X, Christenson KW, Morris WZ, Hu P, Epstein AL 2007 Immune signatures of murine and human cancers reveal unique mechanisms of tumor escape and new targets for cancer immunotherapy. Clin Cancer Res 13: 4016-4025. (Pubitemid 47037610)
19. Russell SM, Angell TE, Lechner MG, Liebertz DJ, Correa AJ, Sinha UK, Kokot N, Epstein AL 2013 Immune cell infiltration patterns and survival in head and neck squamous cell carcinoma. Head Neck Oncol 5: 24.
20. Lechner MG, Karimi SS, Barry-Holson K, Angell TE, Church CH, Murphy KA, Ohlfest JR, Hu P, Epstein AL 2012 Immunogenicity of murine solid tumor models as a defining feature of in vivo behavior and response to immunotherapy. J Immunother Clin Cancer Res 18:4549-4559.
21. Camus M, Tosolini M, Mlecnik B, Pagès F, Kirilovsky A, Berger A, Costes A, Bindea G, Charoentong P, Bruneval P, Trajanoski Z, Fridman WH, Galon J 2008 Coordination of intratumoral immune reaction and human colorectal cancer recurrence. Cancer Res 69:2685-2693.
22. Galon J, Pagès F, Marincola FM, Thurin M, Trinchieri G, Fox BA, Gajewski TF, Ascierto PA 2012 The immune score as a new possible approach for the classification of cancer. J Transl Med 10:1.
23. Moretti S1, Menicali E, Voce P, Morelli S, Cantarelli S, Sponziello M, Colella R, Fallarino F, Orabona C, Alunno A, de Biase D, Bini V, Mameli MG, Filetti S, Gerli R, Macchiarulo A, Melillo RM, Tallini G, Santoro M, Puccetti P, Avenia N, Puxeddu E 2014 Indoleamine 2,3-dioxygenase 1 (IDO1) is unregulated in thyroid carcinoma and drives the development of an immunosuppressant tumor microenvironment. J Clin Endocrinol Metab 99:E832-840.
24. Smallridge RC, Chindris AM, Asmann YW, Casler JD, Serie DJ, Reddi HV, Cradic KW, Rivera M, Grebe SK, Necela BM, Eberhardt NL, Carr JM, McIver B, Copland JA, Aubrey Thompson E 2014 RNA sequencing identifies multiple fusion transcripts, differentially expressed genes, and reduced expression of immune function genes in BRAF (V600E) mutant vs BRAF wild-type papillary thyroid carcinoma. J Clin Endocrinol Metab 99:E338-347.
25. Cunha LL, Marcello MA, Morari EC, Nonogaki S, Conte FF, Gerhard R, Soares FA, Vassallo J, Ward LS 2013 Differentiated thyroid carcinomas may elude the immune system by B7H1 upregulation. Endocr Relat Cancer 20:103-110.
26. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, Davis N, Dicks E, Ewing R, Floyd Y, Gray K, Hall S, Hawes R, Hughes J, Kosmidou V, Menzies A, Mould C, Parker A, Stevens C, Watt S, Hooper S, Wilson R, Jayatilake H, Gusterson BA, Cooper C, Shipley J, Hargrave D, Pritchard-Jones K, Maitland N, Chenevix-Trench G, Riggins GJ, Bigner DD, Palmieri G, Cossu A, Flanagan A, Nicholson A, Ho JW, Leung SY, Yuen ST, Weber BL, Seigler HF, Darrow TL, Paterson H, Marais R, Marshall CJ, Wooster R, Stratton MR, Futreal PA 2002 Mutations of the BRAF gene in human cancer. Nature 417:949-954. (Pubitemid 34716871)
27. Ogino S, Galon J, Fuchs CS, Dranoff G 2011 Cancer immunology-analysis of host and tumor factors for personalized medicine. Nat Rev Clin Oncol 8:711-9.
28. Xing M 2007 BRAF mutation in papillary thyroid cancer: pathogenic role, molecular bases, and clinical implications. Endocr Rev 28:742-762. (Pubitemid 350294294)
29. Afreen S, Dermime S 2014 The immunoinhibitory B7-H1 molecule as a potential target in cancer: killing many birds with one stone. Hematol Oncol Stem Cell Ther 7:1-17.
30. Cunha LL, Marcello MA, Ward LS 2014 The role of the inflammatory microenvironment in thyroid carcinogenesis. Endocr Relat Cancer 21:R85-R103.
31. Zhang L, Gajewski TF, Kline J 2009 PD-1/PD-L1 interactions inhibit antitumor immune responses in a murine acute myeloid leukemia model. Blood 114:1545-1552.
32. Sznol M, Chen L 2013 Antagonist antibodies to PD-1 and B7-H1 (PD-L1) in the treatment of advanced human cancer. Clin Cancer Res 19:1021-1034.
33. Silva TG, Crispim JC, Miranda FA, Hassumi MK, de Mello JM, Simões RT, Souto F, Soares EG, Donadi EA, Soares CP 2011 Expression of the nonclassical HLA-G and HLAE molecules in laryngeal lesions as biomarkers of tumor invasiveness. Histol Histopathol 26:1487-1497.
34. Curigliano G, Criscitiello C, Gelao L, Goldhirsch A 2013 Molecular pathways: human leukocyte antigen G (HLA-G). Clin Cancer Res 19:5564-5571.
35. Yie SM, Hu Z 2011 Human leukocyte antigen-G (HLA-G) as a marker for diagnosis, prognosis and tumor immune escape in human malignancies. Histol Histopathol 26:409-420.
36. Rouas-Freiss N, Moreau P, Ferrone S, Carosella ED 2005 HLA-G proteins in cancer: do they provide tumor cells with an escape mechanism? Cancer Res 65:10139-10144. (Pubitemid 41743699)
37. Figueiredo Feitosa NL, Oliveira Crispim JC, Zanetti BR, Magalhães PK, Soares CP, Soares EG, Neder L, Donadi EA, Maciel LM 2014 HLA-G is differentially expressed in thyroid Tissues. Thyroid 24:585-592.
38. Nunes LM, Ayres FM, Francescantonio IC, Saddi VA, Avelino MA, Alencarrde C, Silva RC, Meneghini AJ, Wastowski IJ 2013 Association between the HLA-G molecule and lymph node metastasis in papillary thyroid cancer. Human Immunol 74:447-450.
39. Löb S, Königsrainer A, Rammensee HG, Opelz G, Terness P 2009 Inhibitors of indoleamine-2,3-dioxygenase for cancer therapy: can we see the wood for the trees? Nat Rev Cancer 9:445-452.
40. Feldt-Rasmussen U1, Rasmussen AK 2010 Autoimmunity in differentiated thyroid cancer: significance and related clinical problems. Hormones (Athens) 9:109-117.
41. Spencer CA 2011 Clinical review: clinical utility of thyroglobulin antibody (TgAb) measurements for patients with differentiated thyroid cancers (DTC). J Clin Endocrinol Metab 96:3615-3627.
42. Grebe SK 2010 Thyroglobulin autoantibodies, thyroid nodules, and new insights into some old questions. Thyroid 20:841-842.
43. Ryder M, Ghossein RA, Ricarte-Filho JC, Knauf JA, Fagin JA 2008 Increased density of tumor-associated macrophages is associated with decreased survival in advanced thyroid cancer. Endocr Relat Cancer 15:1069-1074.
44. French JD, Weber ZJ, Fretwell DL, Said S, Klopper JP, Haugen BR 2010 Tumor-associated lymphocytes and increased FoxP3 + regulatory T cell frequency correlate with more aggressive papillary thyroid cancer. J Clin Endocrinol Metab 95:2325-2333.
45. Cunha LL, Morari EC, Nonogaki S, Soares FA, Vassallo J, Ward LS 2012 Foxp3 expression is associated with aggressiveness in differentiated thyroid carcinomas. Clinics (Sao Paulo) 67:483-488.
46. Qing W, Fang WY, Ye L, Shen LY, Zhang XF, Fei XC, Chen X, Wang WQ, Li XY, Xiao JC, Ning G 2012 Density of tumor-associated macrophages correlates with lymph node metastasis in papillary thyroid carcinoma. Thyroid 22:905-910.
47. Cunha LL, Morari EC, Guihen AC, Razolli D, Gerhard R, Nonogaki S, Soares FA, Vassallo J, Ward LS 2012 Infiltration of a mixture of different immune cells may be related to molecular profile of differentiated thyroid cancer. Endocr Relat Cancer 19:L31-36.
48. Gogali F, Paterakis G, Rassidakis GZ, Kaltsas G, Liakou CI, Gousis P, Neonakis E, Manoussakis MN, Liapi C 2012 Phenotypical analysis of lymphocytes with suppressive and regulatory properties (Tregs) and NK cells in the papillary carcinoma of thyroid. J Clin Endocrinol Metab 97:1474-1482.
49. Ogino S, Nosho K, Irahara N, Meyerhardt JA, Baba Y, Shima K, Glickman JN, Ferrone CR, Mino-Kenudson M, Tanaka N, Dranoff G, Giovannucci EL, Fuchs CS 2009 Lymphocytic reaction to colorectal cancer is associated with longer survival, independent of lymph node count, microsatellite instability, and CpG island methylator phenotype. Clin Cancer Res 15:6412-6420.
50. Knight DA, Ngiow SF, Li M, Parmenter T, Mok S, Cass A, Haynes NM, Kinross K, Yagita H, Koya RC, Graeber TG, Ribas A, McArthur GA, Smyth MJ 2013 Host immunity contributes to the anti-melanoma activity of BRAF inhibitors. J Clin Invest 123:1371-1378.
51. Sumimoto H, Imabayashi F, Iwata T, Kawakami Y 2006 The BRAF-MAPK signaling pathway is essential for cancer-immune evasion in human melanoma cells. J Exp Med 203:1651-1656. (Pubitemid 44036269)
52. Heusinkveld M1, van der Burg SH 2011 Identification and manipulation of tumor associated macrophages in human cancers. J Transl Med 9:216.
53. Kristiansen M1, Graversen JH, Jacobsen C, Sonne O, Hoffman HJ, Law SK, Moestrup SK 2001 Identification of the haemoglobin scavenger receptor. Nature 409:198-201.
54. Buechler C, Ritter M, Orso E, Langmann T, Klucken J, Schmitz G 2000 Regulation of scavenger receptor CD163 expression in human monocytes and macrophages by pro and antiinflammatory stimuli. J Leukoc Biol 67:97-103. (Pubitemid 30046823)
55. Ryder M1, Gild M, Hohl TM, Pamer E, Knauf J, Ghossein R, Joyce JA, Fagin JA. 2013 Genetic and pharmacological targeting of CSF-1/CSF-1R inhibits tumor-associated macrophages and impairs BRAF-induced thyroid cancer progression. PLoS One 8:e54302.
56. Marigo I, Dolcetti L, Serafini P, Zanovello P, Bronte V 2008 Tumor induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev 222:162-179. (Pubitemid 351430364)