Tumor infiltrating immune cells and outcome of merkel cell carcinoma: A population-based study

Clinical Cancer Research

Volumn 18, Issue 10, 2012, Pages 2872-2881

  Sihto, Harri ^a   Beohling, Tom ^a   Kavola, Heli ^b   Koljonen, Virve ^b   Salmi, Marko ^c   Jalkanen, Sirpa ^c   Joensuu, Heikki ^a,b  

^a UNIVERSITY OF HELSINKI   (Finland)

^b HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD163 ANTIGEN; CD3 ANTIGEN; CD4 ANTIGEN; CD68 ANTIGEN; CD8 ANTIGEN; CYCLIN D1; CYCLIN E; KI 67 ANTIGEN; MERKEL CELL POLYOMAVIRUS DNA; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; VIRUS DNA;

AGE; AGED; ANTIGEN EXPRESSION; ARTICLE; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CD3+ T LYMPHOCYTE; CD4 CD8 RATIO; CD4 LYMPHOCYTE COUNT; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; COPY NUMBER VARIATION; DISTANT METASTASIS; FEMALE; FOXP3 CD4 RATIO; HUMAN; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE COUNT; MACROPHAGE; MAJOR CLINICAL STUDY; MALE; MERKEL CELL POLYOMAVIRUS; MERKEL CELL TUMOR; NATURAL KILLER CELL; OVERALL SURVIVAL; POLYOMAVIRUS INFECTION; PRIORITY JOURNAL; SURVIVAL TIME; TUMOR ASSOCIATED LEUKOCYTE; VIRUS DETECTION;

ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; CARCINOMA, MERKEL CELL; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DNA, VIRAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; LYMPHOCYTE COUNT; LYMPHOCYTES, TUMOR-INFILTRATING; MACROPHAGES; MALE; MERKEL CELL POLYOMAVIRUS; RECEPTORS, CELL SURFACE; RECEPTORS, IGG; SKIN NEOPLASMS; SURVIVAL RATE;

EID: 84861169056     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-3020     Document Type: Article

References (48)

1. Lemos BD, Storer BE, Iyer JG, Phillips JL, Bichakjian CK, Fang LC, et al. Pathologic nodal evaluation improves prognostic accuracy in Merkel cell carcinoma: Analysis of 5823 cases as the basis of the first consensus staging system. J Am Acad Dermatol 2010; 63:751-61.
2. Feng H, Shuda M, Chang Y, Moore PS. Clonal integration of a polyomavirus in human merkel cell carcinoma. Science 2008;319: 1096-100. (Pubitemid 351300792) (Pubitemid 351300792)
3. Bhatia K, Goedert JJ, Modali R, Preiss L, Ayers LW. Immunological detection of viral large T antigen identifies subset of Merkel cell carcinoma tumors with higher viral abundance and better clinical outcome. Int J Cancer 2010;127:1493-6.
4. Sihto H, Kukko H, Koljonen V, Sankila R, Böhling T, Joensuu H. Clinical factors associated with Merkel cell polyomavirus infection in Merkel cell carcinoma. J Natl Cancer Inst 2009;101:938-45.
5. Hodgson NC. Merkel cell carcinoma: changing incidence trends. J Surg Oncol 2005;89:1-4. (Pubitemid 40075960) (Pubitemid 40075960)
6. Lunder EJ, Stern RS. Merkel-cell carcinomas in patients treated with methoxsalen and ultraviolet A radiation. N Engl J Med 1998; 339:1247-8. (Pubitemid 28482140) (Pubitemid 28482140)
7. Engels EA, Frisch M, Goedert JJ, Biggar RJ, Miller RW. Merkel cell carcinoma and HIV infection. Lancet 2002;359:497-8. (Pubitemid 34164301) (Pubitemid 34164301)
8. Koljonen V, Kukko H, Tukiainen E,Böhling T, Sankila R, Pukkala E, et al. Merkel cell carcinoma in renal transplant patients-a nationwide study. Nephrol Dial Transplant 2009;24:3231-5.
9. Koljonen V, Kukko H, Pukkala E, Sankila R,Böhling T, Tukiainen E, et al. Chronic lymphocytic leukaemia patients have a high risk of Merkel cell carcinoma polyoma virus DNA-positive Merkel cell carcinoma. Br J Cancer 2009;101:1444-7.
10. Touze A, Le Bidre E, Laude H, Fleury MJ, Cazal R, Arnold F, et al. High levels of antibodies against merkel cell polyomavirus identify a subset of patients with merkel cell carcinoma with better clinical outcome. J Clin Oncol 2011;29:1612-9.
11. Schrama D, Peitsch WK, Zapatka M, Kneitz H, Houben R, Eib S, et al. Merkel cell polyomavirus status is not associated with clinical course of Merkel cell carcinoma. J Invest Dermatol 2011;131: 1631-8.
12. Sihto H, Kukko H, Koljonen V, Sankila R, Böhling T, Joensuu H. Merkel cell polyomavirus infection, large T antigen, retinoblastoma protein and outcome in Merkel cell carcinoma. Clin Cancer Res 2011;17:4806-13.
13. Sato E, Olson SH, Ahn J, Bundy B, Nishikawa H, Qian F, et al. 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 U S A 2005;102: 18538-43. (Pubitemid 43011261) (Pubitemid 43011261)
14. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagés C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006; 313:1960-4. (Pubitemid 44498003) (Pubitemid 44498003)
15. Sinicrope FA, Rego RL, Ansell SM, Knutson KL, Foster NR, Sargent DJ. Intraepithelial effector (CD3+)/regulatory (FoxP3+) T-cell ratio predicts a clinical outcome of human colon carcinoma. Gastroenterology 2009;137:1270-9.
16. Shumacher K, Haensch W, Röefzaad C, Schlag PM. Prognostic significance of activated CD8+ T cell infiltrations within esophageal carcinomas. Cancer Res 2001;61:3932-6. (Pubitemid 32720953) (Pubitemid 32720953)
17. Vesalainen S, Lipponen P, Talja M, Syrjänen K. Histological grade, perinoural infiltration, tumor-infiltrating lymphocytes and apoptosis as determinants of long-term prognosis in prostatic adenocarcinoma. Eur J Cancer 1994;30A:1797-803. (Pubitemid 24377155) (Pubitemid 24377155)
18. Mahmoud SM, Paisch EC, Powe DG, Macmillan RD, Grainge MJ, Lee AH, et al. Tumor-infiltrating CD8+ lymphocytes predict clinical outcome in breast cancer. J Clin Oncol 2011;29:1949-55.
19. Solinas G, Germano G, Mantovani A, Allavena P. Tumor-associated macrophages (TAM) as major player of the cancer-related inflammation. J Leukoc Biol 2009;86:1065-73.
20. DeNardo DG, Barreto JB, Andreu P, Vasquez L, Tawfik D, Kolhatkar N, et al. CD4(+) T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages. Cancer Cell 2009;16:91-102.
21. Inoue T, Yoneda K, Manabe M, Demitsu T. Spontaneous regression of merkel cell carcinoma: a comparative study of TUNEL index and tumor-infiltrating lymphocytes between spontaneous regression and non-regression group. J Dermatol Sci 2000;24:203-11.
22. Turk T, Orlic ZC, Smoljan I, Nacinovic A, Bekafigo IS, Radic J, et al. Spontaneous regression of Merkel cell carcinoma in a patient with chronic lymphocytic leukemia: a case report. J Med Case Reports 2009;3:7270.
23. Burack J, Altschuler EL. Sustained remission of metastatic Merkel cell carcinoma with treatment of HIV infection. J R Soc Med 2003; 96:238-9. (Pubitemid 36561074)
24. Herrmann G, Groth W, Krieg T, Mauch C. Complete remission of Merkel cell carcinoma of the scalp with local and regional metastases after topical treatment with dinitrochlorobenzol. J Am Acad Dermatol 2004;50:965-9. (Pubitemid 38685784) (Pubitemid 38685784)
25. Richetta AG, Mancini M, Torroni A, Lore B, Iannetti G, Sardella B, et al. Total spontaneous regression of advanced merkel cell carcinoma after biopsy: review and a new case. Dermatol Surg 2008;34:815-22. (Pubitemid 351792299) (Pubitemid 351792299)
26. Ciudad C, Avilés JA, Alfageme F, Lecona M, Suarez R, Lazaro P. Spontaneous regression in merkel cell carcinoma: report of two cases with a description of dermoscopic features and review of the literature. Dermatol Surg 2010:36:687-93.
27. Llombart B, Monteagudo C, López-Guerrero JA, Carda C, Jorda E, Sanmartín O, et al. Clinicopathological and immunohistochemical analysis of 20 cases of Merkel cell carcinoma in search of prognostic markers. Histopathology 2005;46:622-34. (Pubitemid 40834821) (Pubitemid 40834821)
28. Andea AA, Coit DG, Amin B, Busam KJ. Merkel cell carcinoma: histologic features and prognosis. Cancer 2008;113:2549-58.
29. Paulson KG, Lyer JG, Tegeder AR, Thibodeau R, Schelter J, Koba S, et al. Transcriptome-wide studies of Merkel cell carcinoma and validation of intratumoral CD8+ lymphocyte invasion as an independent predictor of survival. J Clin Oncol 2011;29:1539-46.
30. Teppo L, Pukkala E, Saxén E. Multiple cancer-an epidemiologic exercise in Finland. J Natl Cancer Inst 1985;75:207-17. (Pubitemid 15229326) (Pubitemid 15229326)
31. Kohler S, Kerl H. Merkel cell carcinoma. In:LeBoit PE, Burg G, Weedon D, Sarasin A, editors. Pathology and genetics of skin tumours. World Health Organization Classification of Tumors. Lyon, France: IARC Press; 2006: p. 272-3.
32. Goessling W, McKee PH, Mayer RJ. Merkel cell carcinoma. J Clin Oncol 2002;20:588-98. (Pubitemid 34072544)
33. Palani S, Maksimow M, Miiluniemi M, Auvinen K, Jalkanen S, Salmi M. Stabilin-1/CLEVER-1, a type 2 macrophage marker, is an adhesion and scavenging molecule on human placental macrophages. Eur J Immunol 2011;41:2052-63.
34. Paulson KG, Lemos BD, Feng B, Jaimes N, Peñas PF, Bi X, et al. Array-CGH reveals recurrent genomic changes in Merkel cell carcinoma including amplification of L-Myc. J Invest Dermatol 2009;129:1547-55.
35. Shuda M, Feng H, Kwun HJ, Rosen ST, Gjoerup O, Moore PS, et al. T antigen mutations are a human tumor-specific signature for Merkel cell polyomavirus. Proc Natl Acad Sci U S A 2008;105:16272-7.
36. Ang KK, Harris J, Wheeler R, Weber R, Rosenthal DI, Nguyen-Tân PF, et al. Human papillomavirus and survival of patients with oropharyngeal cancer. N Engl J Med 2010;363:24-35.
37. Gillison ML, Koch WM, Capone RB, Spafford M, Westra WH, Wu L, et al. Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst 2000; 92:709-20. (Pubitemid 30365531)
38. Rampias T, Sasaki C, Weinberger P, Psyrri A. E6 and E7 gene silencing and transformed phenotype of human papillomavirus 16-positive oropharyngeal cancer cells. J Natl Cancer Inst 2009;101: 412-23.
39. Smeets SJ, Braakhuis BJ, Abbas S, Snijders PJ, Ylstra B, van de Wiel MA, et al. Genome-wide DNA copy number alterations in head and neck squamous cell carcinomas with or without oncogene-expressing human papillomavirus. Oncogene 2006;25:2558-64.
40. Rajjoub D, Basha SR, Einhorn E, Cohen MC, Marvel DM, Sewell DA. Prognostic significance of tumor-infiltrating leukocytes in oropharyngeal cancer. Ear Nose Throat J 2007;86:506-11. (Pubitemid 351268069)
41. Carter JJ, Paulson KG, Wipf CG, Miranda D, Madeleine MM, Johnson LG, et al. Association of Merkel cell polyomavirus-specific antibodies with Merkel cell carcinoma. J Natl Cancer Inst 2009;101:1510-22.
42. Paulson KG, Carter JJ, Johnson LG, Cahill KW, Iver JG, Schrama D, et al. Antibodies to merkel cell polyomavirus T antigen oncoproteins reflect tumor burden in merkel cell carcinoma patients. Cancer Res 2010;70:8388-97.
43. Pastrana DV, Wieland U, Siling S, Buck CB, Pfister H. Positive correlation between Merkel cell polyomavirus viral load and capsid-specific antibody titer. Med Microbiol Immunol 2012;201:17-23.
44. Iyer JG, Afanasiev OK, McClurkan C, Paulson K, Nagase K, Jing L, et al. Merkel cell polyomavirus-specific CD8+ and CD4+ T-cell responses identified in Merkel cell carcinomas and blood. Clin Cancer Res 2011;17:6671-80.
45. Mishra R, Chen AT, Welsh RM, Szmolanyi-Tsuda E. NK cells and gammadelta T cells mediate resistance to polyomavirus-induced tumors. PLoS Pathog 2010;6:e1000924.
46. Salama P, Phillips M, Grieu F,Morris M, Zeps N, Joseph D, et al. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. J Clin Oncol 2009;27:186-92.
47. Gooden MJM, de Bock GH, Leffers N, Daemen T, Nijman HW. The prognostic influence of tumor-infiltrating lymphocytes in cancer: a systematic review with meta-analysis. Br J Cancer 2011;105: 93-103.
48. Shuda M, Kwun HJ, Feng H, Chang Y, Moore PS. Human Merkel cell polyomavirus small T antigen is an oncoprotein targeting the 4E-BP1 translation regulator. J Clin Invest 2011;121:3623-34.