B cells and ectopic follicular structures: Novel players in anti-tumor programming with prognostic power for patients with metastatic colorectal cancer

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Meshcheryakova, Anastasia ^a   Tamandl, Dietmar ^b   Bajna, Erika ^a   Stift, Judith ^b   Mittlboeck, Martina ^b   Svoboda, Martin ^a   Heiden, Denise ^a   Stremitzer, Stefan ^b   Jensen Jarolim, Erika ^a,b   Grünberger, Thomas ^b   Bergmann, Michael ^b   Mechtcheriakova, Diana ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b MEDICAL UNIVERSITY OF VIENNA   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION INDUCED CYTIDINE DEAMINASE; CD20 ANTIGEN; CD45 ANTIGEN; LEUKOCYTE ANTIGEN;

ADULT; AGED; ALGORITHM; ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CANCER PATIENT; CANCER PROGNOSIS; CANCER RECURRENCE; CELL INFILTRATION; CELL LINEAGE; CONTROLLED STUDY; ECTOPIC TISSUE; FEMALE; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; LEUKOCYTE; LIVER METASTASIS; MAJOR CLINICAL STUDY; MALE; METASTATIC COLORECTAL CANCER; MICROSCOPY; OVERALL SURVIVAL; RECURRENCE RISK; SURVIVAL TIME; TISSUE SECTION; TUMOR IMMUNITY; COLORECTAL TUMOR; CYTOLOGY; IMMUNOLOGY; LIVER NEOPLASMS; MACROPHAGE; METABOLISM; MIDDLE AGED; PATHOLOGY; PROGNOSIS; SECONDARY; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ALGORITHMS; ANTIGENS, CD; B-LYMPHOCYTES; COLORECTAL NEOPLASMS; FEMALE; HUMANS; LIVER NEOPLASMS; MACROPHAGES; MALE; MIDDLE AGED; PROGNOSIS;

EID: 84902583668     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0099008     Document Type: Article

References (62)

1. De RW, Jonker DJ, Di NF, Sartore-Bianchi A, Tu D, et al. (2010) Association of KRAS p.G13D mutation with outcome in patients with chemotherapyrefractory metastatic colorectal cancer treated with cetuximab. JAMA 304: 1812-1820. 304/16/1812 [pii]; doi:10.1001/jama.2010.1535.
2. Saltz LB, Clarke S, Diaz-Rubio E, Scheithauer W, Figer A, et al. (2008) Bevacizumab in combination with oxaliplatin-based chemotherapy as first-line therapy in metastatic colorectal cancer: a randomized phase III study. J Clin Oncol 26: 2013-2019. 26/12/2013 [pii]; doi:10.1200/JCO.2007.14.9930.
3. Halama N, Michel S, Kloor M, Zoernig I, Benner A, et al. (2011) Localization and density of immune cells in the invasive margin of human colorectal cancer liver metastases are prognostic for response to chemotherapy. Cancer Res 71: 5670-5677. 0008-5472.CAN-11-0268 [pii]; doi:10.1158/0008-5472. CAN-11-0268.
4. Fridman WH, Pages F, Sautes-Fridman C, Galon J (2012) The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer 12: 298-306. nrc3245 [pii]; doi:10.1038/nrc3245.
5. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144: 646-674. S0092-8674(11)00127-9 [pii]; doi:10.1016/j.cell.2011.02.013.
6. Galon J, Angell HK, Bedognetti D, Marincola FM (2013) The continuum of cancer immunosurveillance: prognostic, predictive, and mechanistic signatures. Immunity 39: 11-26. S1074-7613(13)00292-6 [pii]; doi:10.1016/j.immuni.2013.07. 008.
7. Chen DS, Mellman I (2013) Oncology meets immunology: the cancer-immunity cycle. Immunity 39: 1-10. S1074-7613(13)00296-3 [pii]; doi:10.1016/j.immuni. 2013.07.012.
8. Gajewski TF (2012) Cancer immunotherapy. Mol Oncol 6: 242-250. S1574-7891(12)00003-8 [pii]; doi:10.1016/j.molonc.2012.01.002.
9. Rabinovich GA, Gabrilovich D, Sotomayor EM (2007) Immunosuppressive strategies that are mediated by tumor cells. Annu Rev Immunol 25: 267-296. doi:10.1146/annurev.immunol.25.022106.141609. (Pubitemid 46697910)
10. Ostrand-Rosenberg S, Sinha P, Beury DW, Clements VK (2012) Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression. Semin Cancer Biol 22: 275-281. S1044-579X(12)00013-2 [pii]; doi:10.1016/j.semcancer.2012.01.011.
11. Ruffell B, Affara NI, Coussens LM (2012) Differential macrophage programming in the tumor microenvironment. Trends Immunol 33: 119-126. S1471-4906(11)00213-4 [pii]; doi:10.1016/j.it.2011.12.001.
12. Aguilar LK, Guzik BW, Aguilar-Cordova E (2011) Cytotoxic immunotherapy strategies for cancer: mechanisms and clinical development. J Cell Biochem 112: 1969-1977. doi:10.1002/jcb.23126.
13. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, et al. (2006) Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 313: 1960-1964. 313/5795/1960 [pii]; doi:10.1126/science.1129139.
14. Menon AG, Janssen-van Rhijn CM, Morreau H, Putter H, Tollenaar RA, et al. (2004) Immune system and prognosis in colorectal cancer: a detailed immunohistochemical analysis. Lab Invest 84: 493-501. 3700055 [pii]. doi:10.1038/labinvest.3700055.
15. Naito Y, Saito K, Shiiba K, Ohuchi A, Saigenji K, et al. (1998) CD8+T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. Cancer Res 58: 3491-3494. (Pubitemid 28376536)
16. Pages F, Berger A, Camus M, Sanchez-Cabo F, Costes A, et al. (2005) Effector memory T cells, early metastasis, and survival in colorectal cancer. N Engl J Med 353: 2654-2666. 353/25/2654 [pii]; doi:10.1056/NEJMoa051424.
17. Yeo L, Toellner KM, Salmon M, Filer A, Buckley CD, et al. (2011) Cytokine mRNA profiling identifies B cells as a major source of RANKL in rheumatoid arthritis. Ann Rheum Dis 70: 2022-2028. ard.2011.153312 [pii]; doi:10.1136/ard.2011.153312.
18. Andreu P, Johansson M, Affara NI, Pucci F, Tan T, et al. (2010) FcRgamma activation regulates inflammation-associated squamous carcinogenesis. Cancer Cell 17: 121-134. S1535-6108(09)00431-0 [pii]; doi:10.1016/j.ccr.2009.12.019.
19. Erez N, Truitt M, Olson P, Arron ST, Hanahan D (2010) Cancer-Associated Fibroblasts Are Activated in Incipient Neoplasia to Orchestrate Tumor-Promoting Inflammation in an NF-kappaB-Dependent Manner. Cancer Cell 17: 135-147. S1535-6108(10)00004-8 [pii]; doi:10.1016/j.ccr.2009.12.041.
20. Mizoguchi A, Mizoguchi E, Takedatsu H, Blumberg RS, Bhan AK (2002) Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 16: 219-230. S1074761302002741 [pii].
21. Tian J, Zekzer D, Hanssen L, Lu Y, Olcott A, et al. (2001) Lipopolysaccharide-activated B cells down-regulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice. J Immunol 167: 1081-1089. (Pubitemid 32660868)
22. Wong SC, Puaux AL, Chittezhath M, Shalova I, Kajiji TS, et al. (2010) Macrophage polarization to a unique phenotype driven by B cells. Eur J Immunol 40: 2296-2307. doi:10.1002/eji.200940288.
23. Humby F, Bombardieri M, Manzo A, Kelly S, Blades MC, et al. (2009) Ectopic lymphoid structures support ongoing production of class-switched autoantibodies in rheumatoid synovium. PLoS Med 6: 56-75.
24. Mechtcheriakova D, Sobanov Y, Holtappels G, Bajna E, Svoboda M, et al. (2011) Activation-induced cytidine deaminase (AID)-associated multigene signature to assess impact of AID in etiology of diseases with inflammatory component. PLoS One 6: e25611.;PONE-D-11-10751 [pii]. doi:10.1371/journal.pone. 0025611.
25. Takhar P, Corrigan CJ, Smurthwaite L, O'Connor BJ, Durham SR, et al. (2007) Class switch recombination to IgE in the bronchial mucosa of atopic and nonatopic patients with asthma. Journal of Allergy and Clinical Immunology 119: 213-218. (Pubitemid 46037820)
26. Vicario M, Blanchard C, Stringer KF, Collins MH, Mingler MK, et al. (2010) Local B cells and IgE production in the oesophageal mucosa in eosinophilic oesophagitis. Gut 59: 12-20. gut.2009.178020 [pii]; doi:10.1136/gut.2009.178020.
27. Aloisi F, Pujol-Borrell R (2006) Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol 6: 205-217. (Pubitemid 43290990)
28. Mechtcheriakova D, Svoboda M, Meshcheryakova A, Jensen-Jarolim E (2012) Activation-induced cytidine deaminase (AID) linking immunity, chronic inflammation, and cancer. Cancer Immunol Immunother. doi:10.1007/s00262-012- 1255-z.
29. Dieu-Nosjean MC, Antoine M, Danel C, Heudes D, Wislez M, et al. (2008) Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 26: 4410-4417. 26/27/4410 [pii]; doi:10.1200/JCO.2007.15.0284.
30. Germain C, Gnjatic S, Tamzalit F, Knockaert S, Remark R, et al. (2014) Presence of B Cells in Tertiary Lymphoid Structures is Associated with a Protective Immunity in Lung Cancer Patients. Am J Respir Crit Care Med. doi:10.1164/rccm.201309-1611OC.
31. Coronella JA, Spier C, Welch M, Trevor KT, Stopeck AT, et al. (2002) Antigen-driven oligoclonal expansion of tumor-infiltrating B cells in infiltrating ductal carcinoma of the breast. J Immunol 169: 1829-1836. (Pubitemid 34857644)
32. Coppola D, Nebozhyn M, Khalil F, Dai H, Yeatman T, et al. (2011) Unique ectopic lymph node-like structures present in human primary colorectal carcinoma are identified by immune gene array profiling. Am J Pathol 179: 37-45. S0002-9440(11)00320-8 [pii]; doi :10.1016/j.ajpath.2011.03.007.
33. Halama N, Zoernig I, Spille A, Michel S, Kloor M, et al. (2010) Quantification of prognostic immune cell markers in colorectal cancer using whole slide imaging tumor maps. Anal Quant Cytol Histol 32: 333-340.
34. Keim S, Zoernig I, Spille A, Lahrmann B, Brand K, et al. (2012) Sequential metastases of colorectal cancer: Immunophenotypes and spatial distributions of infiltrating immune cells in relation to time and treatments. Oncoimmunology 1: 593-599.;2012ONCOIMM0082 [pii]. doi:10.4161/onci.20179.
35. Lahrmann B, Halama N, Sinn HP, Schirmacher P, Jaeger D, et al. (2011) Automatic tumor-stroma separation in fluorescence TMAs enables the quantitative high-throughput analysis of multiple cancer biomarkers. PLoS One 6: e28048.;PONE-D-11-18704 [pii]. doi:10.1371/journal.pone.0028048.
36. Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, et al. (2011) Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol 29: 610-618. JCO.2010.30.5425 [pii]; doi:10.1200/JCO.2010.30.5425.
37. Pages F, Kirilovsky A, Mlecnik B, Asslaber M, Tosolini M, et al. (2009) In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. J Clin Oncol 27: 5944-5951. JCO.2008.19.6147 [pii]; doi:10.1200/JCO.2008.19.6147.
38. Galon J, Pages F, Marincola FM, Angell HK, Thurin M, et al. (2012) Cancer classification using the Immunoscore: a worldwide task force. J Transl Med 10: 205. 1479-5876-10-205 [pii]; doi:10.1186/1479-5876-10-205.
39. Stremitzer S, Stift J, Gruenberger B, Tamandl D, Aschacher T, et al. (2012) KRAS status and outcome of liver resection after neoadjuvant chemotherapy including bevacizumab. Br J Surg 99: 1575-1582. doi:10.1002/bjs.8909.
40. Cattoretti G, Buttner M, Shaknovich R, Kremmer E, Alobeid B, et al. (2006) Nuclear and cytoplasmic AID in extrafollicular and germinal center B cells. Blood 107: 3967-3975. (Pubitemid 43726803)
41. Shinmura K, Igarashi H, Goto M, Tao H, Yamada H, et al. (2011) Aberrant Expression and Mutation-Inducing Activity of AID in Human Lung Cancer. Ann Surg Oncol. doi:10.1245/s10434-011-1568-8.
42. Bogusz AM, Baxter RH, Currie T, Sinha P, Sohani AR, et al. (2012) Quantitative immunofluorescence reveals the signature of active B-cell receptor signaling in diffuse large B-cell lymphoma. Clin Cancer Res 18: 6122-6135. 1078-0432.CCR-12-0397 [pii]; doi:10.1158/1078-0432.CCR-12-0397.
43. Laimer D, Dolznig H, Kollmann K, Vesely PW, Schlederer M, et al. (2012) PDGFR blockade is a rational and effective therapy for NPM-ALK-driven lymphomas. Nat Med 18: 1699-1704. nm.2966 [pii]; doi:10.1038/nm.2966.
44. Bindea G, Mlecnik B, Tosolini M, Kirilovsky A, Waldner M, et al. (2013) Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity 39: 782-795. S1074-7613(13)00437-8 [pii]; doi:10.1016/j.immuni.2013.10.003.
45. Remark R, Alifano M, Cremer I, Lupo A, Dieu-Nosjean MC, et al. (2013) Characteristics and clinical impacts of the immune environments in colorectal and renal cell carcinoma lung metastases: influence of tumor origin. Clin Cancer Res 19: 4079-4091. 1078-0432.CCR-12-3847 [pii]; doi:10.1158/1078-0432.CCR-12- 3847.
46. Leandro MJ (2013) B-cell subpopulations in humans and their differential susceptibility to depletion with anti-CD20 monoclonal antibodies. Arthritis Res Ther 15 Suppl 1: S3. ar3908 [pii]; doi:10.1186/ar3908.
47. Czuczman MS, Olejniczak S, Gowda A, Kotowski A, Binder A, et al. (2008) Acquirement of rituximab resistance in lymphoma cell lines is associated with both global CD20 gene and protein down-regulation regulated at the pretranscriptional and posttranscriptional levels. Clin Cancer Res 14: 1561-1570. 14/5/1561 [pii]; doi:10.1158/1078-0432.CCR-07-1254.
48. Bil J, Winiarska M, Nowis D, Bojarczuk K, Dabrowska-Iwanicka A, et al. (2010) Bortezomib modulates surface CD20 in B-cell malignancies and affects rituximab-mediated complement-dependent cytotoxicity. Blood 115: 3745-3755. blood-2009-09-244129 [pii]; doi:10.1182/blood-2009-09-244129.
49. Mankai A, Bordron A, Renaudineau Y, Martins-Carvalho C, Takahashi S, et al. (2008) Purine-rich box-1-mediated reduced expression of CD20 alters rituximab-induced lysis of chronic lymphocytic leukemia B cells. Cancer Res 68: 7512-7519. 68/18/7512 [pii]; doi:10.1158/0008-5472.CAN-07-6446.
50. Winiarska M, Bil J, Wilczek E, Wilczynski GM, Lekka M, et al. (2008) Statins impair antitumor effects of rituximab by inducing conformational changes of CD20. PLoS Med 5: e64. 07-PLME-RA-0139 [pii]; doi:10.1371/journal.pmed. 0050064.
51. Winiarska M, Nowis D, Bil J, Glodkowska-Mrowka E, Muchowicz A, et al. (2012) Prenyltransferases regulate CD20 protein levels and influence anti-CD20 monoclonal antibody-mediated activation of complement-dependent cytotoxicity. J Biol Chem 287: 31983-31993. M112.374751 [pii]; doi:10.1074/jbc.M112.374751.
52. Manser T (2004) Textbook germinal centers? J Immunol 172: 3369-3375.
53. Sasaki M, Kakuda Y, Miyakoshi M, Sato Y, Nakanuma Y (2014) Infiltration of inflammatory cells expressing mitochondrial proteins around bile ducts and in biliary epithelial layer may be involved in the pathogenesis in primary biliary cirrhosis. J Clin Pathol. jclinpath-2013-201917 [pii]; doi:10.1136/jclinpath- 2013-201917.
54. Morita S, Matsumoto Y, Okuyama S, Ono K, Kitamura Y, et al. (2011) Bile acid-induced expression of activation-induced cytidine deaminase during the development of Barrett's oesophageal adenocarcinoma. Carcinogenesis 32: 1706-1712. bgr194 [pii]; doi:10.1093/carcin/bgr194.
55. Liu YJ, Xu J, de BO, Parham CL, Grouard G, et al. (1997) Follicular dendritic cells specifically express the long CR2/CD21 isoform. J Exp Med 185: 165-170.
56. Goc J, Germain C, Vo-Bourgais TK, Lupo A, Klein C, et al. (2014) Dendritic Cells in Tumor-Associated Tertiary Lymphoid Structures Signal a Th1 Cytotoxic Immune Contexture and License the Positive Prognostic Value of Infiltrating CD8+T Cells. Cancer Res 74: 705-715. 0008-5472.CAN-13-1342 [pii]; doi:10.1158/0008-5472.CAN-13-1342.
57. Forssell J, Oberg A, Henriksson ML, Stenling R, Jung A, et al. (2007) High macrophage infiltration along the tumor front correlates with improved survival in colon cancer. Clin Cancer Res 13: 1472-1479. 13/5/1472 [pii]; doi:10.1158/1078-0432.CCR-06-2073.
58. Halama N, Spille A, Lerchl T, Brand K, Herpel E, et al. (2013) Hepatic metastases of colorectal cancer are rather homogeneous but differ from primary lesions in terms of immune cell infiltration. Oncoimmunology 2: e24116.;2012ONCOIMM0236R [pii]. doi:10.4161/onci.24116.
59. Maletzki C, Jahnke A, Ostwald C, Klar E, Prall F, et al. (2012) Ex-vivo clonally expanded B lymphocytes infiltrating colorectal carcinoma are of mature immunophenotype and produce functional IgG. PLoS One 7: e32639.;PONE-D-11-22695 [pii]. doi:10.1371/journal.pone.0032639.
60. Schmoll HJ, Van CE, Stein A, Valentini V, Glimelius B, et al. (2012) ESMO Consensus Guidelines for management of patients with colon and rectal cancer. a personalized approach to clinical decision making. Ann Oncol 23: 2479-2516. mds236 [pii]; doi:10.1093/annonc/mds236.
61. Nordlinger B, Van CE, Gruenberger T, Glimelius B, Poston G, et al. (2009) Combination of surgery and chemotherapy and the role of targeted agents in the treatment of patients with colorectal liver metastases: recommendations from an expert panel. Ann Oncol 20: 985-992. mdn735 [pii]; doi:10.1093/annonc/mdn735.
62. Vonderheide RH, Glennie MJ (2013) Agonistic CD40 Antibodies and Cancer Therapy. Clin Cancer Res 19: 1035-1043. 19/5/1035 [pii]; doi:10.1158/1078-0432. CCR-12-2064.