Defective thymopoiesis and poor peripheral homeostatic replenishment of T-helper cells cause T-cell lymphopenia in cirrhosis

Journal of Hepatology

Volumn 59, Issue 4, 2013, Pages 723-730

  Lario, Margaret ^a   Muñoz, Leticia ^a,b   Ubeda, María ^a,b   Borrero, María José ^a   Martínez, Javier ^c   Monserrat, Jorge ^a   Díaz, David ^a   Álvarez Mon, Melchor ^a,b,d   Albillos, Agustín ^a,b,c  

^a UNIVERSITY OF ALCALÁ   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c HOSPITAL RAMÓN Y CAJAL   (Spain)

^d HOSPITAL UNIVERSITARIO PRÍNCIPE DE ASTURIAS   (Spain)

Author keywords

Bacterial translocation; Naive Th cells; Peripheral homeostatic proliferation; Recent thymic emigrants; Th cell depletion

Indexed keywords

CD31 ANTIGEN; HLA DR ANTIGEN; KI 67 ANTIGEN; LIPOCORTIN 5; LIPOPOLYSACCHARIDE; SOMATOMEDIN C;

ADULT; APOPTOSIS; ARTICLE; BACTERIAL TRANSLOCATION; CELL ACTIVATION; CELL PROLIFERATION; CLINICAL FEATURE; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; HELPER CELL; HEMATOPOIESIS; HUMAN; LIVER CIRRHOSIS; LYMPHOCYTOPENIA; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEIN EXPRESSION; SPLEEN SIZE; T CELL DEPLETION; T LYMPHOCYTE SUBPOPULATION; THYMOPOIESIS; THYMUS;

BACTERIAL TRANSLOCATION; IGF-L; INSULIN-LIKE GROWTH FACTOR-1; INTERQUARTILE RANGE; IQR; LBP; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE BINDING PROTEIN; LPS; MABS; MONOCLONAL ANTIBODIES; NAIVE TH CELLS; PBMCS; PERIPHERAL BLOOD MONONUCLEAR CELLS; PERIPHERAL HOMEOSTATIC PROLIFERATION; PHA; PHYTOHEMAGGLUTININ; RECENT THYMIC EMIGRANTS; T-CELL RECEPTOR; T-CYTOTOXIC; T-HELPER; TC; TCR; TH; TH-CELL DEPLETION; TNF-Α; TUMOR NECROSIS FACTOR-ALPHA;

ACUTE-PHASE PROTEINS; ANTIGENS, CD31; APOPTOSIS; CARRIER PROTEINS; CASE-CONTROL STUDIES; CELL PROLIFERATION; FEMALE; HOMEOSTASIS; HUMANS; IMMUNOLOGIC MEMORY; LIVER CIRRHOSIS; LYMPHOCYTE ACTIVATION; LYMPHOPENIA; MALE; MEMBRANE GLYCOPROTEINS; MIDDLE AGED; PROSPECTIVE STUDIES; SPLEEN; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER; THYMUS GLAND;

EID: 84884411916     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2013.05.042     Document Type: Article

References (31)

1. J. Zhu, and W.E. Paul CD4 T cells: fates, functions, and faults Blood 112 2008 1557 1569
2. S.C. Jameson Maintaining the norm: T-cell homeostasis Nat Rev Immunol 2 2002 547 556 (Pubitemid 37328730)
3. J.J. Goronzy, and C.M. Weyand T cell development and receptor diversity during aging Curr Opin Immunol 17 2005 468 475 (Pubitemid 41207948)
4. G. Tritto, Z. Bechlis, V. Stadlbauer, N. Davies, R. Frances, and N. Shah Evidence of neutrophil functional defect despite inflammation in stable cirrhosis J Hepatol 55 2011 574 581
5. F.J. Laso, J.I. Madruga, J.A. Giron, A. Lopez, J. Ciudad, and J.F. San Miguel Decreased natural killer cytotoxic activity in chronic alcoholism is associated with alcohol liver disease but not active ethanol consumption Hepatology 25 1997 1096 1100 (Pubitemid 27199933)
6. A. Albillos, L. Hera Ad Ade, E. Reyes, J. Monserrat, L. Munoz, and M. Nieto Tumour necrosis factor-alpha expression by activated monocytes and altered T-cell homeostasis in ascitic alcoholic cirrhosis: amelioration with norfloxacin J Hepatol 40 2004 624 631 (Pubitemid 38367784)
7. J.A. Giron-Gonzalez, C. Martinez-Sierra, C. Rodriguez-Ramos, M.A. Macias, P. Rendon, and F. Diaz Implication of inflammation-related cytokines in the natural history of liver cirrhosis Liver Int 24 2004 437 445 (Pubitemid 40484557)
8. D. Schuppan, and N.H. Afdhal Liver cirrhosis Lancet 371 2008 838 851 (Pubitemid 351323895)
9. B.H. McGovern, Y. Golan, M. Lopez, D. Pratt, A. Lawton, and G. Moore The impact of cirrhosis on CD4+ T cell counts in HIV-seronegative patients Clin Infect Dis 44 2007 431 437 (Pubitemid 46147629)
10. N.L. Yonkers, S. Sieg, B. Rodriguez, and D.D. Anthony Reduced naive CD4 T cell numbers and impaired induction of CD27 in response to T cell receptor stimulation reflect a state of immune activation in chronic hepatitis C virus infection J Infect Dis 203 2011 635 645
11. H. Zhang, and G.G. Meadows Chronic alcohol consumption in mice increases the proportion of peripheral memory T cells by homeostatic proliferation J Leukoc Biol 78 2005 1070 1080 (Pubitemid 41572470)
12. K. Koetz, E. Bryl, K. Spickschen, W.M. O'Fallon, J.J. Goronzy, and C.M. Weyand T cell homeostasis in patients with rheumatoid arthritis Proc Natl Acad Sci U S A 97 2000 9203 9208 (Pubitemid 30626698)
13. D.C. Douek, M.R. Betts, B.J. Hill, S.J. Little, R. Lempicki, and J.A. Metcalf Evidence for increased T cell turnover and decreased thymic output in HIV infection J Immunol 167 2001 6663 6668 (Pubitemid 33081605)
14. M. Marquez, C. Fernandez-Gutierrez, M. Montes-de-Oca, M.J. Blanco, F. Brun, and C. Rodriguez-Ramos Chronic antigenic stimuli as a possible explanation for the immunodepression caused by liver cirrhosis Clin Exp Immunol 158 2009 219 229
15. B.J. Manfras, H. Weidenbach, K.H. Beckh, P. Kern, P. Moller, and G. Adler Oligoclonal CD8+ T-cell expansion in patients with chronic hepatitis C is associated with liver pathology and poor response to interferon-alpha therapy J Clin Immunol 24 2004 258 271 (Pubitemid 39030673)
16. A. Szuster-Ciesielska, J. Daniluk, and A. Bojarska-Junak Apoptosis of blood mononuclear cells in alcoholic liver cirrhosis. The influence of in vitro ethanol treatment and zinc supplementation Toxicology 212 2005 124 134 (Pubitemid 40981969)
17. A. Albillos, A. de la Hera, M. Gonzalez, J.L. Moya, J.L. Calleja, and J. Monserrat Increased lipopolysaccharide binding protein in cirrhotic patients with marked immune and hemodynamic derangement Hepatology 37 2003 208 217 (Pubitemid 36042162)
18. S. Kimmig, G.K. Przybylski, C.A. Schmidt, K. Laurisch, B. Mowes, and A. Radbruch Two subsets of naive T helper cells with distinct T cell receptor excision circle content in human adult peripheral blood J Exp Med 195 2002 789 794 (Pubitemid 34259723)
19. C.D. Surh, and J. Sprent Homeostasis of naive and memory T cells Immunity 29 2008 848 862
20. K.M. Williams, F.T. Hakim, and R.E. Gress T cell immune reconstitution following lymphodepletion Semin Immunol 19 2007 318 330 (Pubitemid 350181530)
21. J. Gerdes, H. Lemke, H. Baisch, H.H. Wacker, U. Schwab, and H. Stein Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by the monoclonal antibody Ki-67 J Immunol 133 1984 1710 1715 (Pubitemid 14035254)
22. P.H. Krammer, R. Arnold, and I.N. Lavrik Life and death in peripheral T cells Nat Rev Immunol 7 2007 532 542 (Pubitemid 46987784)
23. K. Bonefeld, and S. Moller Insulin-like growth factor-I and the liver Liver Int 31 2011 911 919
24. G. Morrhaye, H. Kermani, J.J. Legros, F. Baron, Y. Beguin, and M. Moutschen Impact of growth hormone (GH) deficiency and GH replacement upon thymus function in adult patients PLoS One 4 2009 e5668
25. N. Assy, Y. Pruzansky, D. Gaitini, Z. Shen Orr, Z. Hochberg, Z. Hochberg, and Y. Baruch Growth hormone-stimulated IGF-1 generation in cirrhosis reflects hepatocellular dysfunction J Hepatol 49 2008 34 42
26. R.D. Kilpatrick, T. Rickabaugh, L.E. Hultin, P. Hultin, M.A. Hausner, and R. Detels Homeostasis of the naive CD4+ T cell compartment during aging J Immunol 180 2008 1499 1507
27. I. den Braber, T. Mugwagwa, N. Vrisekoop, L. Westera, R. Mogling, and A.B. de Boer Maintenance of peripheral naive T cells is sustained by thymus output in mice but not humans Immunity 36 2012 288 297
28. R.I. Azevedo, M.V. Soares, J.T. Barata, R. Tendeiro, A. Serra-Caetano, and R.M. Victorino IL-7 sustains CD31 expression in human naive CD4+ T cells and preferentially expands the CD31+ subset in a PI3K-dependent manner Blood 113 2009 2999 3007
29. M. Úbeda, L. Munoz, M.J. Borrero, D. Diaz, R. Frances, and J. Monserrat Critical role of the liver in the induction of systemic inflammation in rats with preascitic cirrhosis Hepatology 52 2010 2086 2095
30. L. Munoz, A. Albillos, M. Nieto, E. Reyes, L. Lledo, and J. Monserrat Mesenteric Th1 polarization and monocyte TNF-alpha production: first steps to systemic inflammation in rats with cirrhosis Hepatology 42 2005 411 419 (Pubitemid 41061094)
31. F.N. Bashour, J.C. Teran, and K.D. Mullen Prevalence of peripheral blood cytopenias (hypersplenism) in patients with nonalcoholic chronic liver disease Am J Gastroenterol 95 2000 2936 2939