Increased regulatory T cells in patients with liver cirrhosis correlated with hyperbilirubinemia and predict bacterial complications

Journal of Gastroenterology and Hepatology (Australia)

Volumn 30, Issue 4, 2015, Pages 775-783

  Huang, Chien Hao ^a,c   Jeng, Wen Juei ^a   Ho, Yu Pin ^a   Teng, Wei ^a   Chen, Wei Ting ^a   Chen, Yi Cheng ^a,b   Lin, Shi Ming ^a,b   Chiu, Cheng Tang ^a,b   Sheen, I Shyan ^a,b   Lin, Chun Yen ^a,b  

^a CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

Bacterial infections; Child Turcotte Pugh classification; Liver cirrhosis; Regulatory T cells; Soluble tumor necrosis factor receptor II; Tumor necrosis factor receptor II

Indexed keywords

BILIRUBIN; CD4 ANTIGEN; CD45RO ANTIGEN; INTERLEUKIN 2 RECEPTOR ALPHA; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA RECEPTOR; TUMOR NECROSIS FACTOR ALPHA RECEPTOR II; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR 2;

ADULT; ARTICLE; BACTERIAL INFECTION; BILIRUBIN BLOOD LEVEL; CASE CONTROL STUDY; CONTROLLED STUDY; FEMALE; HUMAN; HUMAN CELL; HYPERBILIRUBINEMIA; LIVER CIRRHOSIS; MAJOR CLINICAL STUDY; MALE; MULTIPLE LINEAR REGRESSION ANALYSIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PREDICTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SUPERNATANT; AGED; BACTERIAL INFECTIONS; BLOOD; COMPLICATION; FORECASTING; IMMUNOCOMPROMIZED PATIENT; IMMUNOLOGY; LYMPHOCYTE COUNT; MIDDLE AGED; STATISTICAL MODEL;

ADULT; AGED; BACTERIAL INFECTIONS; BILIRUBIN; BIOMARKERS; CASE-CONTROL STUDIES; FEMALE; FORECASTING; HUMANS; HYPERBILIRUBINEMIA; IMMUNOCOMPROMISED HOST; LINEAR MODELS; LIVER CIRRHOSIS; LYMPHOCYTE COUNT; MALE; MIDDLE AGED; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE II; T-LYMPHOCYTES, REGULATORY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84924764827     PISSN: 08159319     EISSN: 14401746     Source Type: Journal    
DOI: 10.1111/jgh.12781     Document Type: Article

References (45)

1. Tandon P, Garcia-Tsao G. Bacterial infections, sepsis, and multiorgan failure in cirrhosis. Semin. Liver Dis. 2008; 28: 26-42.
2. Bonnel AR, Bunchorntavakul C, Reddy KR. Immune dysfunction and infections in patients with cirrhosis. Clin. Gastroenterol. Hepatol. 2011; 9: 727-738.
3. Thuluvath PJ, Morss S, Thompson R. Spontaneous bacterial peritonitis-in-hospital mortality, predictors of survival, and health care costs from 1988 to 1998. Am. J. Gastroenterol. 2001; 96: 1232-1236.
4. Huang CH, Lin CY, Sheen IS etal. Recurrence of spontaneous bacterial peritonitis in cirrhotic patients non-prophylactically treated with norfloxacin: serum albumin as an easy but reliable predictive factor. Liver Int. 2011; 31: 184-191.
5. Leber B, Spindelboeck W, Stadlbauer V. Infectious complications of acute and chronic liver disease. Semin. Respir. Crit. Care Med. 2012; 33: 80-95.
6. Rimola A, Soto R, Bory F, Arroyo V, Piera C, Rodes J. Reticuloendothelial system phagocytic activity in cirrhosis and its relation to bacterial infections and prognosis. Hepatology 1984; 4: 53-58.
7. Wasmuth HE, Kunz D, Yagmur E etal. Patients with acute on chronic liver failure display "sepsis-like" immune paralysis. J. Hepatol. 2005; 42: 195-201.
8. Lin CY, Tsai IF, Ho YP etal. Endotoxemia contributes to the immune paralysis in patients with cirrhosis. J. Hepatol. 2007; 46: 816-826.
9. Mookerjee RP, Stadlbauer V, Lidder S etal. Neutrophil dysfunction in alcoholic hepatitis superimposed on cirrhosis is reversible and predicts the outcome. Hepatology 2007; 46: 831-840.
10. Wan YY. Regulatory T cells: immune suppression and beyond. Cell. Mol. Immunol. 2010; 7: 204-210.
11. Lewis DH, Chan DL, Pinheiro D, Armitage-Chan E, Garden OA. The immunopathology of sepsis: pathogen recognition, systemic inflammation, the compensatory anti-inflammatory response, and regulatory T cells. J. Vet. Intern. Med. 2012; 26: 457-482.
12. Venet F, Chung CS, Kherouf H etal. Increased circulating regulatory T cells (CD4[+]CD25 [+]CD127 [-]) contribute to lymphocyte anergy in septic shock patients. Intensive Care Med. 2009; 35: 678-686.
13. Sanchez Rodriguez R, Pauli ML, Neuhaus IM etal. Memory regulatory T cells reside in human skin. J. Clin. Invest. 2014; 124: 1027-1036.
14. Yamaguchi T, Wing JB, Sakaguchi S. Two modes of immune suppression by Foxp3(+) regulatory T cells under inflammatory or non-inflammatory conditions. Semin. Immunol. 2011; 23: 424-430.
15. Sakaguchi S, Ono M, Setoguchi R etal. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol. Rev. 2006; 212: 8-27.
16. Dejaco C, Duftner C, Grubeck-Loebenstein B, Schirmer M. Imbalance of regulatory T cells in human autoimmune diseases. Immunology 2006; 117: 289-300.
17. Long SA, Buckner JH. CD4+FOXP3+ T regulatory cells in human autoimmunity: more than a numbers game. J. Immunol. 2011; 187: 2061-2066.
18. Stoop JN, van der Molen RG, Baan CC etal. Regulatory T cells contribute to the impaired immune response in patients with chronic hepatitis B virus infection. Hepatology 2005; 41: 771-778.
19. Boettler T, Spangenberg HC, Neumann-Haefelin C etal. T cells with a CD4+CD25+ regulatory phenotype suppress in vitro proliferation of virus-specific CD8+ T cells during chronic hepatitis C virus infection. J. Virol. 2005; 79: 7860-7867.
20. Peng G, Li S, Wu W, Sun Z, Chen Y, Chen Z. Circulating CD4+ CD25+ regulatory T cells correlate with chronic hepatitis B infection. Immunology 2008; 123: 57-65.
21. Alatrakchi N, Koziel M. Regulatory T cells and viral liver disease. J. Viral. Hepat. 2009; 16: 223-229.
22. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL. CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 2002; 420: 502-507.
23. Scott-Browne JP, Shafiani S, Tucker-Heard G etal. Expansion and function of Foxp3-expressing T regulatory cells during tuberculosis. J. Exp. Med. 2007; 204: 2159-2169.
24. Curiel TJ, Coukos G, Zou L etal. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat. Med. 2004; 10: 942-949.
25. Kono K, Kawaida H, Takahashi A etal. CD4(+)CD25high regulatory T cells increase with tumor stage in patients with gastric and esophageal cancers. Cancer Immunol. Immunother. 2006; 55: 1064-1071.
26. Fu J, Xu D, Liu Z etal. Increased regulatory T cells correlate with CD8 T-cell impairment and poor survival in hepatocellular carcinoma patients. Gastroenterology 2007; 132: 2328-2339.
27. Lin YC, Chang LY, Huang CT etal. Effector/memory but not naive regulatory T cells are responsible for the loss of concomitant tumor immunity. J. Immunol. 2009; 182: 6095-6104.
28. Lin YC, Mahalingam J, Chiang JM etal. Activated but not resting regulatory T cells accumulated in tumor microenvironment and correlated with tumor progression in patients with colorectal cancer. Int. J. Cancer. 2013; 132: 1341-1350.
29. Robinson DS, Larche M, Durham SR. Tregs and allergic disease. J. Clin. Invest. 2004; 114: 1389-1397.
30. Akdis CA, Akdis M. Mechanisms and treatment of allergic disease in the big picture of regulatory T cells. J. Allergy Clin. Immunol. 2009; 123: 735-746.
31. Wood KJ, Sakaguchi S. Regulatory T cells in transplantation tolerance. Nat. Rev. Immunol. 2003; 3: 199-210.
32. Taylor PA, Panoskaltsis-Mortari A, Swedin JM etal. L-Selectin(hi) but not the L-selectin(lo) CD4+25+ T-regulatory cells are potent inhibitors of GVHD and BM graft rejection. Blood 2004; 104: 3804-3812.
33. Dai Z, Li Q, Wang Y etal. CD4+CD25+ regulatory T cells suppress allograft rejection mediated by memory CD8+ T cells via a CD30-dependent mechanism. J. Clin. Invest. 2004; 113: 310-317.
34. Joffre O, Santolaria T, Calise D etal. Prevention of acute and chronic allograft rejection with CD4+CD25+Foxp3+ regulatory T lymphocytes. Nat. Med. 2008; 14: 88-92.
35. Booth NJ, McQuaid AJ, Sobande T etal. Different proliferative potential and migratory characteristics of human CD4+ regulatory T cells that express either CD45RA or CD45RO. J. Immunol. 2010; 184: 4317-4326.
36. Solstad T, Bains SJ, Landskron J etal. CD147 (Basigin/Emmprin) identifies FoxP3+CD45RO+CTLA4+-activated human regulatory T cells. Blood 2011; 118: 5141-5151.
37. Rosenblum MD, Gratz IK, Paw JS, Lee K, Marshak-Rothstein A, Abbas AK. Response to self antigen imprints regulatory memory in tissues. Nature 2011; 480: 538-542.
38. Lin CY, Tsai MC, Huang CT etal. Liver injury is associated with enhanced regulatory T-cell activity in patients with chronic hepatitis B. J. Viral. Hepat. 2007; 14: 503-511.
39. Haynes L, Maue AC. Effects of aging on T cell function. Curr. Opin. Immunol. 2009; 21: 414-417.
40. Liu Y, Li P, Lu J etal. Bilirubin possesses powerful immunomodulatory activity and suppresses experimental autoimmune encephalomyelitis. J. Immunol. 2008; 181: 1887-1897.
41. Wang H, Lee SS, Dell'Agnello C etal. Bilirubin can induce tolerance to islet allografts. Endocrinology 2006; 147: 762-768.
42. Rocuts F, Zhang X, Yan J etal. Bilirubin promotes de novo generation of T regulatory cells. Cell Transplant. 2010; 19: 443-451.
43. Chen X, Oppenheim JJ. TNF-alpha: an activator of CD4+FoxP3+TNFR2+ regulatory T cells. Curr. Dir. Autoimmun. 2010; 11: 119-134.
44. Chen X, Oppenheim JJ. The phenotypic and functional consequences of tumour necrosis factor receptor type 2 expression on CD4(+) FoxP3(+) regulatory T cells. Immunology 2011; 133: 426-433.
45. van Mierlo GJ, Scherer HU, Hameetman M etal. Cutting edge: TNFR-shedding by CD4+CD25+ regulatory T cells inhibits the induction of inflammatory mediators. J. Immunol. 2008; 180: 2747-2751.