Skip to main content
Top
Published in: Journal of Translational Medicine 1/2012

Open Access 01-12-2012 | Research

Perioperative dynamic alterations in peripheral regulatory T and B cells in patients with hepatocellular carcinoma

Authors: Tianxiang Chen, Dongli Song, Zhihui Min, Xiangdong Wang, Yu Gu, Bajin Wei, Jia Yao, Kangjie Chen, Zhijun Jiang, Haiyang Xie, Lin Zhou, Shusen Zheng

Published in: Journal of Translational Medicine | Issue 1/2012

Login to get access

Abstract

Background

Intratumoral and circulating regulatory T cells (Tregs) have been shown to be critical in the pathogenesis of hepatocellular carcinoma (HCC). However there is limited knowledge on the alterations of regulatory B cells (Bregs). We here investigated perioperative dynamic alterations of peripheral circulating Tregs and Bregs in HCC patients to reveal the relationship between regulatory lymphocytes and its clinical implications.

Methods

36 patients with HCC, 6 with chronic hepatitis B infection and 10 healthy donors were enrolled for this study. Frequencies of peripheral Tregs and Bregs were measured by flow cytometry with antibodies against CD4, CD25, CD127, CD19 and IL-10 before, and after radical surgery. Then, clinical informatics of HCC patients was achieved through Digital Evaluation Score System (DESS) for the assessment of disease severity. Finally, we analysed correlations between digitalized clinical features and kinetics of circulating regulatory lymphocytes.

Results

Level of circulating CD4+CD25+CD127- Tregs in HCC patients was significantly lower than that in healthy donors and patients with chronic hepatitis B infection before surgery, but was increased after surgery. Preoperative level of CD19+ IL-10+ Bregs in HCC patients was also significantly lower than the other groups. However it dramatically was elevated right after surgery and remained elevated compared to controls (about 7 days after surgery, P = 0.04). Frequency of circulating Tregs was correlated with circulating leukocytes, ferritin, and clinical features suggesting tumor aggressiveness including portal vein thrombosis, hepatic vein involvement and advanced clinical stages. Frequency of circulating Bregs was associated with Hepatitis B e Antigen (HBeAg) and Hepatitis B virus (HBV) DNA copy number. In addition, DESS was significantly and positively correlated with other staging systems.

Conclusion

Frequencies of peripheral Tregs and Bregs in HCC patients increased after surgery. These results suggest that a postoperative combination of therapies against Tregs and Bregs may be beneficial for better outcome of HCC patients after resection.
Appendix
Available only for authorised users
Literature
1.
go back to reference Nishikawa H, Sakaguchi S: Regulatory T cells in tumor immunity. Int J Cancer. 2010, 127: 759-767.PubMed Nishikawa H, Sakaguchi S: Regulatory T cells in tumor immunity. Int J Cancer. 2010, 127: 759-767.PubMed
3.
go back to reference Gao Q, Qiu SJ, Fan J, Zhou J, Wang XY, Xiao YS, Xu Y, Li YW, Tang ZY: Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol. 2007, 25: 2586-2593. 10.1200/JCO.2006.09.4565.CrossRefPubMed Gao Q, Qiu SJ, Fan J, Zhou J, Wang XY, Xiao YS, Xu Y, Li YW, Tang ZY: Intratumoral balance of regulatory and cytotoxic T cells is associated with prognosis of hepatocellular carcinoma after resection. J Clin Oncol. 2007, 25: 2586-2593. 10.1200/JCO.2006.09.4565.CrossRefPubMed
4.
go back to reference Chen KJ, Zhou L, Xie HY, Ahmed TE, Feng XW, Zheng SS: Intratumoral regulatory T cells alone or in combination with cytotoxic T cells predict prognosis of hepatocellular carcinoma after resection. Med Oncol. 2011 Chen KJ, Zhou L, Xie HY, Ahmed TE, Feng XW, Zheng SS: Intratumoral regulatory T cells alone or in combination with cytotoxic T cells predict prognosis of hepatocellular carcinoma after resection. Med Oncol. 2011
5.
go back to reference Lee WC, Wu TJ, Chou HS, Yu MC, Hsu PY, Hsu HY, Wang CC: The impact of CD4(+)CD25(+) T cells in the tumor microenvironment of hepatocellular carcinoma. Surgery. 2011 Lee WC, Wu TJ, Chou HS, Yu MC, Hsu PY, Hsu HY, Wang CC: The impact of CD4(+)CD25(+) T cells in the tumor microenvironment of hepatocellular carcinoma. Surgery. 2011
6.
go back to reference Ormandy LA, Hillemann T, Wedemeyer H, Manns MP, Greten TF, Korangy F: Increased populations of regulatory T cells in peripheral blood of patients with hepatocellular carcinoma. Cancer Res. 2005, 65: 2457-2464. 10.1158/0008-5472.CAN-04-3232.CrossRefPubMed Ormandy LA, Hillemann T, Wedemeyer H, Manns MP, Greten TF, Korangy F: Increased populations of regulatory T cells in peripheral blood of patients with hepatocellular carcinoma. Cancer Res. 2005, 65: 2457-2464. 10.1158/0008-5472.CAN-04-3232.CrossRefPubMed
7.
go back to reference Yang XH, Yamagiwa S, Ichida T, Matsuda Y, Sugahara S, Watanabe H, Sato Y, Abo T, Horwitz DA, Aoyagi Y: Increase of CD4+ CD25+ regulatory T-cells in the liver of patients with hepatocellular carcinoma. J Hepatol. 2006, 45: 254-262. 10.1016/j.jhep.2006.01.036.CrossRefPubMed Yang XH, Yamagiwa S, Ichida T, Matsuda Y, Sugahara S, Watanabe H, Sato Y, Abo T, Horwitz DA, Aoyagi Y: Increase of CD4+ CD25+ regulatory T-cells in the liver of patients with hepatocellular carcinoma. J Hepatol. 2006, 45: 254-262. 10.1016/j.jhep.2006.01.036.CrossRefPubMed
8.
go back to reference Mauri C, Blair PA: Regulatory B cells in autoimmunity: developments and controversies. Nat Rev Rheumatol. 2010, 6: 636-643. 10.1038/nrrheum.2010.140.CrossRefPubMed Mauri C, Blair PA: Regulatory B cells in autoimmunity: developments and controversies. Nat Rev Rheumatol. 2010, 6: 636-643. 10.1038/nrrheum.2010.140.CrossRefPubMed
9.
go back to reference Inoue S, Leitner WW, Golding B, Scott D: Inhibitory effects of B cells on antitumor immunity. Cancer Res. 2006, 66: 7741-7747. 10.1158/0008-5472.CAN-05-3766.CrossRefPubMed Inoue S, Leitner WW, Golding B, Scott D: Inhibitory effects of B cells on antitumor immunity. Cancer Res. 2006, 66: 7741-7747. 10.1158/0008-5472.CAN-05-3766.CrossRefPubMed
10.
go back to reference Mauri C, Ehrenstein MR: The 'short' history of regulatory B cells. Trends Immunol. 2008, 29: 34-40. 10.1016/j.it.2007.10.004.CrossRefPubMed Mauri C, Ehrenstein MR: The 'short' history of regulatory B cells. Trends Immunol. 2008, 29: 34-40. 10.1016/j.it.2007.10.004.CrossRefPubMed
12.
go back to reference Vitale G, Mion F, Pucillo C: Regulatory B cells: evidence, developmental origin and population diversity. Mol Immunol. 2010, 48: 1-8. 10.1016/j.molimm.2010.09.010.CrossRefPubMed Vitale G, Mion F, Pucillo C: Regulatory B cells: evidence, developmental origin and population diversity. Mol Immunol. 2010, 48: 1-8. 10.1016/j.molimm.2010.09.010.CrossRefPubMed
13.
go back to reference Matsushita T, Yanaba K, Bouaziz JD, Fujimoto M, Tedder TF: Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest. 2008, 118: 3420-3430.PubMedPubMedCentral Matsushita T, Yanaba K, Bouaziz JD, Fujimoto M, Tedder TF: Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J Clin Invest. 2008, 118: 3420-3430.PubMedPubMedCentral
14.
go back to reference Watanabe R, Ishiura N, Nakashima H, Kuwano Y, Okochi H, Tamaki K, Sato S, Tedder TF, Fujimoto M: Regulatory B cells (B10 cells) have a suppressive role in murine lupus: CD19 and B10 cell deficiency exacerbates systemic autoimmunity. J Immunol. 2010, 184: 4801-4809. 10.4049/jimmunol.0902385.CrossRefPubMedPubMedCentral Watanabe R, Ishiura N, Nakashima H, Kuwano Y, Okochi H, Tamaki K, Sato S, Tedder TF, Fujimoto M: Regulatory B cells (B10 cells) have a suppressive role in murine lupus: CD19 and B10 cell deficiency exacerbates systemic autoimmunity. J Immunol. 2010, 184: 4801-4809. 10.4049/jimmunol.0902385.CrossRefPubMedPubMedCentral
15.
go back to reference Yanaba K, Yoshizaki A, Asano Y, Kadono T, Tedder TF, Sato S: IL-10-producing regulatory B10 cells inhibit intestinal injury in a mouse model. Am J Pathol. 2011, 178: 735-743. 10.1016/j.ajpath.2010.10.022.CrossRefPubMedPubMedCentral Yanaba K, Yoshizaki A, Asano Y, Kadono T, Tedder TF, Sato S: IL-10-producing regulatory B10 cells inhibit intestinal injury in a mouse model. Am J Pathol. 2011, 178: 735-743. 10.1016/j.ajpath.2010.10.022.CrossRefPubMedPubMedCentral
16.
go back to reference Olkhanud PB, Damdinsuren B, Bodogai M, Gress RE, Sen R, Wejksza K, Malchinkhuu E, Wersto RP, Biragyn A: Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4 T cells to T-regulatory cells. Cancer Res. 2011, 71: 3505-3515. 10.1158/0008-5472.CAN-10-4316.CrossRefPubMedPubMedCentral Olkhanud PB, Damdinsuren B, Bodogai M, Gress RE, Sen R, Wejksza K, Malchinkhuu E, Wersto RP, Biragyn A: Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4 T cells to T-regulatory cells. Cancer Res. 2011, 71: 3505-3515. 10.1158/0008-5472.CAN-10-4316.CrossRefPubMedPubMedCentral
17.
go back to reference DiLillo DJ, Matsushita T, Tedder TF: B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci. 2010, 1183: 38-57. 10.1111/j.1749-6632.2009.05137.x.CrossRefPubMed DiLillo DJ, Matsushita T, Tedder TF: B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann N Y Acad Sci. 2010, 1183: 38-57. 10.1111/j.1749-6632.2009.05137.x.CrossRefPubMed
18.
go back to reference Schioppa T, Moore R, Thompson RG, Rosser EC, Kulbe H, Nedospasov S, Mauri C, Coussens LM, Balkwill FR: B regulatory cells and the tumor-promoting actions of TNF-alpha during squamous carcinogenesis. Proc Natl Acad Sci USA. 2011, 108: 10662-10667. 10.1073/pnas.1100994108.CrossRefPubMedPubMedCentral Schioppa T, Moore R, Thompson RG, Rosser EC, Kulbe H, Nedospasov S, Mauri C, Coussens LM, Balkwill FR: B regulatory cells and the tumor-promoting actions of TNF-alpha during squamous carcinogenesis. Proc Natl Acad Sci USA. 2011, 108: 10662-10667. 10.1073/pnas.1100994108.CrossRefPubMedPubMedCentral
19.
go back to reference Chen H, Song Z, Qian M, Bai C, Wang X: Selection of disease-specific biomarkers by integrating inflammatory mediators with clinical informatics in AECOPD patients: a preliminary study. J Cell Mol Med. 2011 Chen H, Song Z, Qian M, Bai C, Wang X: Selection of disease-specific biomarkers by integrating inflammatory mediators with clinical informatics in AECOPD patients: a preliminary study. J Cell Mol Med. 2011
20.
go back to reference Ganem D, Prince AM: Hepatitis B virus infection--natural history and clinical consequences. N Engl J Med. 2004, 350: 1118-1129. 10.1056/NEJMra031087.CrossRefPubMed Ganem D, Prince AM: Hepatitis B virus infection--natural history and clinical consequences. N Engl J Med. 2004, 350: 1118-1129. 10.1056/NEJMra031087.CrossRefPubMed
21.
go back to reference Chun YH, Kim SU, Park JY, Kim DY, Han KH, Chon CY, Kim BK, Choi GH, Kim KS, Choi JS, Ahn SH: Prognostic value of the 7th edition of the AJCC staging system as a clinical staging system in patients with hepatocellular carcinoma. Eur J Cancer. 2011 Chun YH, Kim SU, Park JY, Kim DY, Han KH, Chon CY, Kim BK, Choi GH, Kim KS, Choi JS, Ahn SH: Prognostic value of the 7th edition of the AJCC staging system as a clinical staging system in patients with hepatocellular carcinoma. Eur J Cancer. 2011
22.
go back to reference Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J, Dauguet C, Axler-Blin C, Vezinet-Brun F, Rouzioux C: Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science. 1983, 220: 868-871. 10.1126/science.6189183.CrossRefPubMed Barre-Sinoussi F, Chermann JC, Rey F, Nugeyre MT, Chamaret S, Gruest J, Dauguet C, Axler-Blin C, Vezinet-Brun F, Rouzioux C: Isolation of a T-lymphotropic retrovirus from a patient at risk for acquired immune deficiency syndrome (AIDS). Science. 1983, 220: 868-871. 10.1126/science.6189183.CrossRefPubMed
23.
go back to reference Bull M, Lee D, Stucky J, Chiu YL, Rubin A, Horton H, McElrath MJ: Defining blood processing parameters for optimal detection of cryopreserved antigen-specific responses for HIV vaccine trials. J Immunol Methods. 2007, 322: 57-69. 10.1016/j.jim.2007.02.003.CrossRefPubMedPubMedCentral Bull M, Lee D, Stucky J, Chiu YL, Rubin A, Horton H, McElrath MJ: Defining blood processing parameters for optimal detection of cryopreserved antigen-specific responses for HIV vaccine trials. J Immunol Methods. 2007, 322: 57-69. 10.1016/j.jim.2007.02.003.CrossRefPubMedPubMedCentral
24.
go back to reference Hein F, Massin F, Cravoisy-Popovic A, Barraud D, Levy B, Bollaert PE, Gibot S: The relationship between CD4+CD25+CD127- regulatory T cells and inflammatory response and outcome during shock states. Crit Care. 2010, 14: R19-10.1186/cc8876.CrossRefPubMedPubMedCentral Hein F, Massin F, Cravoisy-Popovic A, Barraud D, Levy B, Bollaert PE, Gibot S: The relationship between CD4+CD25+CD127- regulatory T cells and inflammatory response and outcome during shock states. Crit Care. 2010, 14: R19-10.1186/cc8876.CrossRefPubMedPubMedCentral
25.
go back to reference Knippenberg S, Peelen E, Smolders J, Thewissen M, Menheere P, Cohen Tervaert JW, Hupperts R, Damoiseaux J: Reduction in IL-10 producing B cells (Breg) in multiple sclerosis is accompanied by a reduced naive/memory Breg ratio during a relapse but not in remission. J Neuroimmunol. 2011 Knippenberg S, Peelen E, Smolders J, Thewissen M, Menheere P, Cohen Tervaert JW, Hupperts R, Damoiseaux J: Reduction in IL-10 producing B cells (Breg) in multiple sclerosis is accompanied by a reduced naive/memory Breg ratio during a relapse but not in remission. J Neuroimmunol. 2011
26.
go back to reference Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, Venturi GM, Szabolcs PM, Bernstein SH, Magro CM, Williams AD: Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011, 117: 530-541. 10.1182/blood-2010-07-294249.CrossRefPubMedPubMedCentral Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, Venturi GM, Szabolcs PM, Bernstein SH, Magro CM, Williams AD: Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011, 117: 530-541. 10.1182/blood-2010-07-294249.CrossRefPubMedPubMedCentral
27.
go back to reference Kawaoka T, Aikata H, Takaki S, Hashimoto Y, Katamura Y, Hiramatsu A, Waki K, Takahashi S, Kamada K, Kitamoto M: Transcatheter chemoembolization for unresectable hepatocellular carcinoma and comparison of five staging systems. Hepatol Res. 2010, 40: 1082-1091. 10.1111/j.1872-034X.2010.00714.x.CrossRefPubMed Kawaoka T, Aikata H, Takaki S, Hashimoto Y, Katamura Y, Hiramatsu A, Waki K, Takahashi S, Kamada K, Kitamoto M: Transcatheter chemoembolization for unresectable hepatocellular carcinoma and comparison of five staging systems. Hepatol Res. 2010, 40: 1082-1091. 10.1111/j.1872-034X.2010.00714.x.CrossRefPubMed
28.
go back to reference Yuen MF, Chan AO, Wong BC, Hui CK, Ooi GC, Tso WK, Yuan HJ, Wong DK, Lai CL: Transarterial chemoembolization for inoperable, early stage hepatocellular carcinoma in patients with Child-Pugh grade A and B: results of a comparative study in 96 Chinese patients. Am J Gastroenterol. 2003, 98: 1181-1185.PubMed Yuen MF, Chan AO, Wong BC, Hui CK, Ooi GC, Tso WK, Yuan HJ, Wong DK, Lai CL: Transarterial chemoembolization for inoperable, early stage hepatocellular carcinoma in patients with Child-Pugh grade A and B: results of a comparative study in 96 Chinese patients. Am J Gastroenterol. 2003, 98: 1181-1185.PubMed
29.
go back to reference Santambrogio R, Opocher E, Costa M, Barabino M, Zuin M, Bertolini E, De Filippi F, Bruno S: Hepatic Resection for "BCLC Stage A" Hepatocellular Carcinoma. The Prognostic Role of Alpha-Fetoprotein. Ann Surg Oncol. 2011 Santambrogio R, Opocher E, Costa M, Barabino M, Zuin M, Bertolini E, De Filippi F, Bruno S: Hepatic Resection for "BCLC Stage A" Hepatocellular Carcinoma. The Prognostic Role of Alpha-Fetoprotein. Ann Surg Oncol. 2011
30.
go back to reference Kudo M, Chung H, Osaki Y: Prognostic staging system for hepatocellular carcinoma (CLIP score): its value and limitations, and a proposal for a new staging system, the Japan Integrated Staging Score (JIS score). J Gastroenterol. 2003, 38: 207-215. 10.1007/s005350300038.CrossRefPubMed Kudo M, Chung H, Osaki Y: Prognostic staging system for hepatocellular carcinoma (CLIP score): its value and limitations, and a proposal for a new staging system, the Japan Integrated Staging Score (JIS score). J Gastroenterol. 2003, 38: 207-215. 10.1007/s005350300038.CrossRefPubMed
31.
go back to reference Zabala M, Lasarte JJ, Perret C, Sola J, Berraondo P, Alfaro M, Larrea E, Prieto J, Kramer MG: Induction of immunosuppressive molecules and regulatory T cells counteracts the antitumor effect of interleukin-12-based gene therapy in a transgenic mouse model of liver cancer. J Hepatol. 2007, 47: 807-815. 10.1016/j.jhep.2007.07.025.CrossRefPubMed Zabala M, Lasarte JJ, Perret C, Sola J, Berraondo P, Alfaro M, Larrea E, Prieto J, Kramer MG: Induction of immunosuppressive molecules and regulatory T cells counteracts the antitumor effect of interleukin-12-based gene therapy in a transgenic mouse model of liver cancer. J Hepatol. 2007, 47: 807-815. 10.1016/j.jhep.2007.07.025.CrossRefPubMed
32.
go back to reference Patel SA, Meyer JR, Greco SJ, Corcoran KE, Bryan M, Rameshwar P: Mesenchymal stem cells protect breast cancer cells through regulatory T cells: role of mesenchymal stem cell-derived TGF-beta. J Immunol. 2010, 184: 5885-5894. 10.4049/jimmunol.0903143.CrossRefPubMed Patel SA, Meyer JR, Greco SJ, Corcoran KE, Bryan M, Rameshwar P: Mesenchymal stem cells protect breast cancer cells through regulatory T cells: role of mesenchymal stem cell-derived TGF-beta. J Immunol. 2010, 184: 5885-5894. 10.4049/jimmunol.0903143.CrossRefPubMed
33.
go back to reference Xiong B, Feng G, Luo S, Liang H, Qiu L, Zheng C, Liu X, Zhou G: Changes of CD4(+) CD25 (+) regulatory T cells in peripheral blood in patients with hepatocellular carcinoma before and after TACE. J Huazhong Univ Sci Technolog Med Sci. 2008, 28: 645-648. 10.1007/s11596-008-0606-7.CrossRefPubMed Xiong B, Feng G, Luo S, Liang H, Qiu L, Zheng C, Liu X, Zhou G: Changes of CD4(+) CD25 (+) regulatory T cells in peripheral blood in patients with hepatocellular carcinoma before and after TACE. J Huazhong Univ Sci Technolog Med Sci. 2008, 28: 645-648. 10.1007/s11596-008-0606-7.CrossRefPubMed
34.
go back to reference Feng X, Li B, Ye H, Long D: Increased frequency of CD4+CD25(high)FoxP3+ regulatory T cells in patients with hepatocellular carcinoma. Arch Immunol Ther Exp (Warsz). 2011, 59: 309-314. 10.1007/s00005-011-0127-0.CrossRef Feng X, Li B, Ye H, Long D: Increased frequency of CD4+CD25(high)FoxP3+ regulatory T cells in patients with hepatocellular carcinoma. Arch Immunol Ther Exp (Warsz). 2011, 59: 309-314. 10.1007/s00005-011-0127-0.CrossRef
35.
go back to reference Liu W, Putnam AL, Xu-Yu Z, Szot GL, Lee MR, Zhu S, Gottlieb PA, Kapranov P, Gingeras TR, Fazekas de St, Groth B: CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J Exp Med. 2006, 203: 1701-1711. 10.1084/jem.20060772.CrossRefPubMedPubMedCentral Liu W, Putnam AL, Xu-Yu Z, Szot GL, Lee MR, Zhu S, Gottlieb PA, Kapranov P, Gingeras TR, Fazekas de St, Groth B: CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells. J Exp Med. 2006, 203: 1701-1711. 10.1084/jem.20060772.CrossRefPubMedPubMedCentral
36.
go back to reference Zou W: Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol. 2006, 6: 295-307. 10.1038/nri1806.CrossRefPubMed Zou W: Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol. 2006, 6: 295-307. 10.1038/nri1806.CrossRefPubMed
37.
go back to reference Chen KJ, Lin SZ, Zhou L, Xie HY, Zhou WH, Taki-Eldin A, Zheng SS: Selective Recruitment of Regulatory T Cell through CCR6-CCL20 in Hepatocellular Carcinoma Fosters Tumor Progression and Predicts Poor Prognosis. PLoS One. 2011, 6: e24671-10.1371/journal.pone.0024671.CrossRefPubMedPubMedCentral Chen KJ, Lin SZ, Zhou L, Xie HY, Zhou WH, Taki-Eldin A, Zheng SS: Selective Recruitment of Regulatory T Cell through CCR6-CCL20 in Hepatocellular Carcinoma Fosters Tumor Progression and Predicts Poor Prognosis. PLoS One. 2011, 6: e24671-10.1371/journal.pone.0024671.CrossRefPubMedPubMedCentral
38.
go back to reference Wang Y, Wang W, Wang L, Wang X, Xia J: Regulatory mechanisms of interleukin 8 production induced by tumor necrosis factor-alpha in human hepatocellular carcinoma cells. J Cell Mol Med. 2011 Wang Y, Wang W, Wang L, Wang X, Xia J: Regulatory mechanisms of interleukin 8 production induced by tumor necrosis factor-alpha in human hepatocellular carcinoma cells. J Cell Mol Med. 2011
39.
go back to reference Mizoguchi A, Mizoguchi E, Takedatsu H, Blumberg RS, Bhan AK: Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity. 2002, 16: 219-230. 10.1016/S1074-7613(02)00274-1.CrossRefPubMed Mizoguchi A, Mizoguchi E, Takedatsu H, Blumberg RS, Bhan AK: Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity. 2002, 16: 219-230. 10.1016/S1074-7613(02)00274-1.CrossRefPubMed
40.
go back to reference Matsushita T, Horikawa M, Iwata Y, Tedder TF: Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J Immunol. 2010, 185: 2240-2252. 10.4049/jimmunol.1001307.CrossRefPubMedPubMedCentral Matsushita T, Horikawa M, Iwata Y, Tedder TF: Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J Immunol. 2010, 185: 2240-2252. 10.4049/jimmunol.1001307.CrossRefPubMedPubMedCentral
41.
go back to reference Carter NA, Vasconcellos R, Rosser EC, Tulone C, Munoz-Suano A, Kamanaka M, Ehrenstein MR, Flavell RA, Mauri C: Mice lacking endogenous IL-10-producing regulatory B cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J Immunol. 2011, 186: 5569-5579. 10.4049/jimmunol.1100284.CrossRefPubMed Carter NA, Vasconcellos R, Rosser EC, Tulone C, Munoz-Suano A, Kamanaka M, Ehrenstein MR, Flavell RA, Mauri C: Mice lacking endogenous IL-10-producing regulatory B cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J Immunol. 2011, 186: 5569-5579. 10.4049/jimmunol.1100284.CrossRefPubMed
42.
go back to reference Geng L, Deng J, Jiang G, Song P, Wang Z, Jiang Z, Zhang M, Zheng S: B7-H1 up-regulated expression in human hepatocellular carcinoma tissue: correlation with tumor interleukin-10 levels. Hepatogastroenterology. 2011, 58: 960-964.PubMed Geng L, Deng J, Jiang G, Song P, Wang Z, Jiang Z, Zhang M, Zheng S: B7-H1 up-regulated expression in human hepatocellular carcinoma tissue: correlation with tumor interleukin-10 levels. Hepatogastroenterology. 2011, 58: 960-964.PubMed
43.
go back to reference Zhang HH, Mei MH, Fei R, Liao WJ, Wang XY, Qin LL, Wang JH, Wei L, Chen HS: Regulatory T cell depletion enhances tumor specific CD8 T-cell responses, elicited by tumor antigen NY-ESO-1b in hepatocellular carcinoma patients, in vitro. Int J Oncol. 2010, 36: 841-848.PubMed Zhang HH, Mei MH, Fei R, Liao WJ, Wang XY, Qin LL, Wang JH, Wei L, Chen HS: Regulatory T cell depletion enhances tumor specific CD8 T-cell responses, elicited by tumor antigen NY-ESO-1b in hepatocellular carcinoma patients, in vitro. Int J Oncol. 2010, 36: 841-848.PubMed
44.
go back to reference Bahlo DSaA: B Lymphocytes in Cancer Immunology. Experimental and Applied Immunotherapy. 2011, Part 2: 37-57. Bahlo DSaA: B Lymphocytes in Cancer Immunology. Experimental and Applied Immunotherapy. 2011, Part 2: 37-57.
45.
go back to reference Mougiakakos D, Jitschin R, Johansson CC, Okita R, Kiessling R, Le Blanc K: The impact of inflammatory licensing on heme oxygenase-1-mediated induction of regulatory T cells by human mesenchymal stem cells. Blood. 2011, 117: 4826-4835. 10.1182/blood-2010-12-324038.CrossRefPubMed Mougiakakos D, Jitschin R, Johansson CC, Okita R, Kiessling R, Le Blanc K: The impact of inflammatory licensing on heme oxygenase-1-mediated induction of regulatory T cells by human mesenchymal stem cells. Blood. 2011, 117: 4826-4835. 10.1182/blood-2010-12-324038.CrossRefPubMed
46.
go back to reference Gray CP, Franco AV, Arosio P, Hersey P: Immunosuppressive effects of melanoma-derived heavy-chain ferritin are dependent on stimulation of IL-10 production. Int J Cancer. 2001, 92: 843-850. 10.1002/ijc.1269.CrossRefPubMed Gray CP, Franco AV, Arosio P, Hersey P: Immunosuppressive effects of melanoma-derived heavy-chain ferritin are dependent on stimulation of IL-10 production. Int J Cancer. 2001, 92: 843-850. 10.1002/ijc.1269.CrossRefPubMed
47.
go back to reference Baumgartner C, Osl M, Netzer M, Baumgartner D: Bioinformatic-driven search for metabolic biomarkers in disease. J Clin Bioinforma. 2011, 1: 2-10.1186/2043-9113-1-2.CrossRefPubMedPubMedCentral Baumgartner C, Osl M, Netzer M, Baumgartner D: Bioinformatic-driven search for metabolic biomarkers in disease. J Clin Bioinforma. 2011, 1: 2-10.1186/2043-9113-1-2.CrossRefPubMedPubMedCentral
49.
Metadata
Title
Perioperative dynamic alterations in peripheral regulatory T and B cells in patients with hepatocellular carcinoma
Authors
Tianxiang Chen
Dongli Song
Zhihui Min
Xiangdong Wang
Yu Gu
Bajin Wei
Jia Yao
Kangjie Chen
Zhijun Jiang
Haiyang Xie
Lin Zhou
Shusen Zheng
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Journal of Translational Medicine / Issue 1/2012
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/1479-5876-10-14

Other articles of this Issue 1/2012

Journal of Translational Medicine 1/2012 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine