Prognostic impact of tumour-infiltrating B cells and plasma cells in colorectal cancer

International Journal of Cancer

Volumn 139, Issue 5, 2016, Pages 1129-1139

  Berntsson, Jonna ^a   Nodin, Björn ^a   Eberhard, Jakob ^a   Micke, Patrick ^b   Jirström, Karin ^a  

^a LUND UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

Author keywords

B cells; CD138; CD20; colorectal cancer; IGKC; plasma cells

Indexed keywords

BIOLOGICAL MARKER; CD20 ANTIGEN; IMMUNOGLOBULIN KAPPA CHAIN; SYNDECAN 1;

ADULT; AGE; AGED; ARTICLE; B LYMPHOCYTE; CANCER PROGNOSIS; CANCER STAGING; CANCER SURVIVAL; CELL INFILTRATION; CLINICAL FEATURE; COLORECTAL CANCER; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; OVERALL SURVIVAL; PLASMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SURVIVAL RATE; SURVIVAL TIME; TISSUE MICROARRAY; TUMOR INFILTRATING B LYMPHOCYTE; CANCER GRADING; COLORECTAL NEOPLASMS; IMMUNOLOGY; KAPLAN MEIER METHOD; LYMPHOCYTE SUBPOPULATION; METABOLISM; MIDDLE AGED; MORTALITY; PATHOLOGY; PHENOTYPE; PROGNOSIS; PROPORTIONAL HAZARDS MODEL; REGISTER; SWEDEN; TUMOR ASSOCIATED LEUKOCYTE; TUMOR MICROENVIRONMENT; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ANTIGENS, CD20; BIOMARKERS; COLORECTAL NEOPLASMS; FEMALE; HUMANS; KAPLAN-MEIER ESTIMATE; LYMPHOCYTE SUBSETS; LYMPHOCYTES, TUMOR-INFILTRATING; MALE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM STAGING; PHENOTYPE; PLASMA CELLS; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; REGISTRIES; SWEDEN; SYNDECAN-1; TUMOR MICROENVIRONMENT;

EID: 84966440346     PISSN: 00207136     EISSN: 10970215     Source Type: Journal    
DOI: 10.1002/ijc.30138     Document Type: Article

References (50)

1. Jemal A, Bray F, Center MM, et al., Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90.
2. Hanahan D, Weinberg RA., Hallmarks of cancer: the next generation. Cell 2011; 144: 646-74.
3. Ostrand-Rosenberg S., Immune surveillance: a balance between protumor and antitumor immunity. Curr Opin Genet Dev 2008; 18: 11-8.
4. Grivennikov SI, Greten FR, Karin M., Immunity, inflammation, and cancer. Cell 2010; 140: 883-99.
5. Murdoch C, Muthana M, Coffelt SB, Lewis CE., The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 2008; 8: 618-31.
6. Lin WW, Karin M., A cytokine-mediated link between innate immunity, inflammation, and cancer. J Clin Invest 2007; 117: 1175-83.
7. Fridman WH, Pages F, Sautes-Fridman C, et al., The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 2012; 12: 298-306.
8. Robert C, Thomas L, Bondarenko I, et al., Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 2011; 364: 2517-26.
9. Lynch TJ, Bondarenko I, Luft A, et al., Ipilimumab in combination with paclitaxel and carboplatin as first-line treatment in stage IIIB/IV non-small-cell lung cancer: results from a randomized, double-blind, multicenter phase II study. J Clin Oncol 2012; 30: 2046-54.
10. Naito Y, Saito K, Shiiba K, et al., CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res 1998; 58: 3491-4.
11. Diederichsen AC, Hjelmborg J, Christensen PB, et al., Prognostic value of the CD4+/CD8+ ratio of tumour infiltrating lymphocytes in colorectal cancer and HLA-DR expression on tumour cells. Cancer Immunol Immunother 2003; 52: 423-8.
12. Al-Shibli KI, Donnem T, Al-Saad S, et al., Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res 2008; 14: 5220-7.
13. Nedergaard BS, Ladekarl M, Nyengaard JR, et al., A comparative study of the cellular immune response in patients with stage IB cervical squamous cell carcinoma. Low numbers of several immune cell subtypes are strongly associated with relapse of disease within 5 years. Gynecol Oncol 2008; 108: 106-11.
14. Schmidt M, Bohm D, von Torne C, et al., The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res 2008; 68: 5405-13.
15. Meshcheryakova A, Tamandl D, Bajna E, et al., B cells and ectopic follicular structures: novel players in anti-tumor programming with prognostic power for patients with metastatic colorectal cancer. PloS One 2014; 9: e99008.
16. Chen Z, Gerhold-Ay A, Gebhard S, et al., Immunoglobulin kappa C predicts overall survival in node-negative breast cancer. PloS One 2012; 7: e44741
17. Schmidt M, Hellwig B, Hammad S, et al., A comprehensive analysis of human gene expression profiles identifies stromal immunoglobulin kappa C as a compatible prognostic marker in human solid tumors. Clin Cancer Res 2012; 18: 2695-703.
18. Lohr M, Edlund K, Botling J, et al., The prognostic relevance of tumour-infiltrating plasma cells and immunoglobulin kappa C indicates an important role of the humoral immune response in non-small cell lung cancer. Cancer Lett 2013; 333: 222-8.
19. Mohammed ZM, Going JJ, Edwards J, et al., The relationship between lymphocyte subsets and clinico-pathological determinants of survival in patients with primary operable invasive ductal breast cancer. Br J Cancer 2013; 109: 1676-84.
20. Mitselou A, Skoufi U, Tsimogiannis KE, et al., Association of syndecan-1 with angiogenesis-related markers, extracellular matrix components, and clinicopathological features in colorectal carcinoma. Anticancer Res 2012; 32: 3977-85.
21. Berglund G, Elmstahl S, Janzon L, et al., The Malmo Diet and Cancer Study. Design and feasibility. J Intern Med 1993; 233: 45-51.
22. Wangefjord S, Manjer J, Gaber A, et al., Cyclin D1 expression in colorectal cancer is a favorable prognostic factor in men but not in women in a prospective, population-based cohort study. Biol Sex Diff 2011; 2: 10
23. Larsson A, Johansson ME, Wangefjord S, et al., Overexpression of podocalyxin-like protein is an independent factor of poor prognosis in colorectal cancer. Br J Cancer 2011; 105: 666-72.
24. Kononen J, Bubendorf L, Kallioniemi A, et al., Tissue microarrays for high-throughput molecular profiling of tumor specimens. Nat Med 1998; 4: 844-7.
25. Mahmoud SM, Lee AH, Paish EC, et al., The prognostic significance of B lymphocytes in invasive carcinoma of the breast. Breast Cancer Res Treat 2012; 132: 545-53.
26. Giraldo NA, Becht E, Vano Y, et al., The immune response in cancer: from immunology to pathology to immunotherapy. Virchows Arch 2015;467:127-35.
27. Mantovani A, Romero P, Palucka AK, et al., Tumour immunity: effector response to tumour and role of the microenvironment. Lancet 2008; 371: 771-83.
28. Shi JY, Gao Q, Wang ZC, et al., Margin-infiltrating CD20(+) B cells display an atypical memory phenotype and correlate with favorable prognosis in hepatocellular carcinoma. Clin Cancer Res 2013; 19: 5994-6005.
29. Milne K, Kobel M, Kalloger SE, et al., Systematic analysis of immune infiltrates in high-grade serous ovarian cancer reveals CD20, FoxP3 and TIA-1 as positive prognostic factors. PloS One 2009; 4: e6412.
30. Bindea G, Mlecnik B, Tosolini M, et al., Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 2013; 39: 782-95.
31. de Visser KE, Korets LV, Coussens LM., De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 2005; 7: 411-23.
32. Affara NI, Ruffell B, Medler TR, et al., B cells regulate macrophage phenotype and response to chemotherapy in squamous carcinomas. Cancer Cell 2014; 25: 809-21.
33. Chapoval AI, Fuller JA, Kremlev SG, et al., Combination chemotherapy and IL-15 administration induce permanent tumor regression in a mouse lung tumor model: NK and T cell-mediated effects antagonized by B cells. J Immunol (Baltimore, Md: 1950) 1998; 161: 6977-84.
34. Shah S, Divekar AA, Hilchey SP, et al., Increased rejection of primary tumors in mice lacking B cells: inhibition of anti-tumor CTL and TH1 cytokine responses by B cells. Int J Cancer 2005; 117: 574-86.
35. Quan N, Zhang Z, Demetrikopoulos MK, et al., Evidence for involvement of B lymphocytes in the surveillance of lung metastasis in the rat. Cancer Res 1999; 59: 1080-9.
36. DiLillo DJ, Yanaba K, Tedder TF., B cells are required for optimal CD4+ and CD8+ T cell tumor immunity: therapeutic B cell depletion enhances B16 melanoma growth in mice. J Immunol (Baltimore, Md: 1950) 2010; 184: 4006-16.
37. Nielsen JS, Sahota RA, Milne K, et al., CD20+ tumor-infiltrating lymphocytes have an atypical CD27- memory phenotype and together with CD8+ T cells promote favorable prognosis in ovarian cancer. Clin Cancer Res 2012; 18: 3281-92.
38. Julien S, Picco G, Sewell R, et al., Sialyl-Tn vaccine induces antibody-mediated tumour protection in a relevant murine model. Br J Cancer 2009; 100: 1746-54.
39. Pelletier MP, Edwardes MD, Michel RP, et al., Prognostic markers in resectable non-small cell lung cancer: a multivariate analysis. Can J Surg 2001; 44: 180-8.
40. Schmidt M, Micke P, Gehrmann M, et al., Immunoglobulin kappa chain as an immunologic biomarker of prognosis and chemotherapy response in solid tumors. Oncoimmunology 2012; 1: 1156-8.
41. Wangefjord S, Sundstrom M, Zendehrokh N, et al., Sex differences in the prognostic significance of KRAS codons 12 and 13, and BRAF mutations in colorectal cancer: a cohort study. Biol Sex Diff 2013; 4: 17.
42. Liao Y, Ou J, Deng J, et al., Clinical implications of the tumor-infiltrating lymphocyte subsets in colorectal cancer. Med Oncol (Northwood, London, England) 2013; 30: 727
43. Cipponi A, Mercier M, Seremet T, et al., Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res 2012; 72: 3997-4007.
44. Ogino S, Nosho K, Irahara N, et al., 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 2009; 15: 6412-20.
45. de la Chapelle A, Hampel H., Clinical relevance of microsatellite instability in colorectal cancer. J Clin Oncol 2010; 28: 3380-7.
46. Mennerich D, Vogel A, Klaman I, et al., Shift of syndecan-1 expression from epithelial to stromal cells during progression of solid tumours. Eur J Cancer (Oxford, England: 1990) 2004; 40: 1373-82.
47. Wang X, Zuo D, Chen Y, et al., Shed Syndecan-1 is involved in chemotherapy resistance via the EGFR pathway in colorectal cancer. Br J Cancer 2014; 111: 1965-76.
48. Schraml P, Kononen J, Bubendorf L, et al., Tissue microarrays for gene amplification surveys in many different tumor types. Clin Cancer Res 1999; 5: 1966-75.
49. Simon R, Sauter G., Tissue microarrays for miniaturized high-throughput molecular profiling of tumors. Exp Hematol 2002; 30: 1365-72.
50. Manjer J, Carlsson S, Elmstahl S, et al., The Malmo Diet and Cancer Study: representativity, cancer incidence and mortality in participants and non-participants. Eur J Cancer Prevent 2001; 10: 489-99.