Metabolic regulation of hepatitis B immunopathology by myeloid-derived suppressor cells

Nature Medicine

Volumn 21, Issue 6, 2015, Pages 591-600

  Pallett, Laura J ^a   Gill, Upkar S ^b   Quaglia, Alberto ^c   Sinclair, Linda V ^d   Jover Cobos, Maria ^a   Schurich, Anna ^a   Singh, Kasha P ^a   Thomas, Niclas ^a   Das, Abhishek ^a   Chen, Antony ^a   Fusai, Giuseppe ^a   Bertoletti, Antonio ^e,f   Cantrell, Doreen A ^d   Kennedy, Patrick T ^b   Davies, Nathan A ^a   Haniffa, Muzlifah ^f,g   Maini, Mala K ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^c KING S COLLEGE HOSPITAL   (United Kingdom)

^d UNIVERSITY OF DUNDEE   (United Kingdom)

^e DUKE NUS MEDICAL SCHOOL   (Singapore)

^f AGENCY FOR SCIENCE   (Singapore)

^g NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID TRANSPORTER; ARGINASE; ARGINASE 1; ARGININE; CHEMOKINE RECEPTOR CXCR1; CHEMOKINE RECEPTOR CXCR3; CHEMOKINE RECEPTOR CXCR4; EDETIC ACID; INTERLEUKIN 8; CD11B ANTIGEN;

AMINO ACID TRANSPORT; ANTIVIRAL THERAPY; ARTICLE; BONE MARROW CELL; CD8+ T LYMPHOCYTE; CELL METABOLISM; CELL POPULATION; CELLULAR IMMUNITY; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE ACTIVITY; ENZYME BLOOD LEVEL; EX VIVO STUDY; FEMALE; GRANULOCYTE; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; IMMUNOPATHOLOGY; IMMUNOREGULATION; IN VITRO STUDY; LIVER BIOPSY; LIVER INJURY; LYMPHOCYTIC CHORIOMENINGITIS VIRUS; MALE; METABOLIC REGULATION; MYELOID DERIVED SUPPRESSOR CELL; NUTRIENT SUPPLY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; SEX DIFFERENCE; STELLATE CELL; SUPPRESSOR CELL; T LYMPHOCYTE; UPREGULATION; VIRUS LOAD; VIRUS REPLICATION; ADOLESCENT; ADULT; ANTIGEN PRESENTATION; IMMUNOLOGY; LIVER; METABOLISM; MIDDLE AGED; PATHOGENICITY; PATHOLOGY;

HEPATITIS B VIRUS;

ADOLESCENT; ADULT; ANTIGEN PRESENTATION; ANTIGENS, CD11B; ARGINASE; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HEPATIC STELLATE CELLS; HEPATITIS B; HEPATITIS B VIRUS; HUMANS; LIVER; MALE; MIDDLE AGED; MYELOID CELLS;

EID: 84930651350     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3856     Document Type: Article

References (49)

1. Guidotti, L.G. & Chisari, F.V. Immunobiology and pathogenesis of viral hepatitis. Annu. Rev. Pathol. 1, 23-61 (2006).
2. Maini, M.K. et al. The role of virus-specific CD8(+) cells in liver damage and viral control during persistent hepatitis B virus infection. J. Exp. Med. 191, 1269-1280 (2000).
3. Bertoletti, A. & Maini, M.K. Protection or damage: a dual role for the virus-specific cytotoxic T lymphocyte response in hepatitis B and C infection? Curr. Opin. Immunol. 12, 403-408 (2000).
4. Kakimi, K. et al. Blocking chemokine responsive to gamma-2/interferon (IFN)-gamma inducible protein and monokine induced by IFN-gamma activity in vivo reduces the pathogenetic but not the antiviral potential of hepatitis B virus-specific cytotoxic T lymphocytes. J. Exp. Med. 194, 1755-1766 (2001).
5. Sitia, G. et al. MMPs are required for recruitment of antigen-nonspecific mononuclear cells into the liver by CTLs. J. Clin. Invest. 113, 1158-1167 (2004).
6. Das, A. et al. Functional skewing of the global CD8 T cell population in chronic hepatitis B virus infection. J. Exp. Med. 205, 2111-2124 (2008).
7. Sinclair, L.V. et al. Control of amino acid transport by antigen receptors coordinates the metabolic reprogramming essential for T cell differentiation. Nat. Immunol. 14, 500-508 (2013).
8. Pearce, E.L., Poffenberger, M.C., Chang, C.H. & Jones, R.G. Fueling immunity: insights into metabolism and lymphocyte function. Science 342, 1242454 (2013).
9. Gabrilovich, D.I., Ostrand-Rosenberg, S. & Bronte, V. Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12, 253-268 (2012).
10. Norris, B.A. et al. Chronic but not acute virus infection induces sustained expansion of myeloid suppressor cell numbers that inhibit viral-specific T cell immunity. Immunity 38, 309-321 (2013).
11. Qin, A. et al. Expansion of monocytic myeloid-derived suppressor cells dampens T cell function in HIV-1-seropositive individuals. J. Virol. 87, 1477-1490 (2013).
12. Tacke, R.S. et al. Myeloid suppressor cells induced by hepatitis C virus suppress T-cell responses through the production of reactive oxygen species. Hepatology 55, 343-353 (2012).
13. Vollbrecht, T. et al. Chronic progressive HIV-1 infection is associated with elevated levels of myeloid-derived suppressor cells. AIDS 26, F31-F37 (2012).
14. Kotsakis, A. et al. Myeloid-derived suppressor cell measurements in fresh and cryopreserved blood samples. J. Immunol. Methods 381, 14-22 (2012).
15. Brandau, S., Moses, K. & Lang, S. The kinship of neutrophils and granulocytic myeloid-derived suppressor cells in cancer: cousins, siblings or twins? Semin. Cancer Biol. 23, 171-182 (2013).
16. Rodriguez, P.C. et al. Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res. 69, 1553-1560 (2009).
17. Chu, C.M., Sheen, I.S., Lin, S.M. & Liaw, Y.F. Sex difference in chronic hepatitis B virus infection: studies of serum HBeAg and alanine aminotransferase levels in 10, 431 asymptomatic Chinese HBsAg carriers. Clin. Infect. Dis. 16, 709-713 (1993).
18. Cloke, T., Munder, M., Taylor, G., Muller, I. & Kropf, P. Characterization of a novel population of low-density granulocytes associated with disease severity in HIV-1 infection. PLoS ONE 7, e48939 (2012).
19. Munder, M. et al. Arginase I is constitutively expressed in human granulocytes and participates in fungicidal activity. Blood 105, 2549-2556 (2005).
20. Frumento, G. et al. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2, 3-dioxygenase. J. Exp. Med. 196, 459-468 (2002).
21. Folley, S.J. & Greenbaum, A.L. Determination of the arginase activities of homogenates of liver and mammary gland: effects of pH and substrate concentration and especially of activation by divalent metal ions. Biochem. J. 43, 537-549 (1948).
22. Ikemoto, M. et al. A useful ELISA system for human liver-type arginase, and its utility in diagnosis of liver diseases. Clin. Biochem. 34, 455-461 (2001).
23. van de Poll, M.C. et al. Elevated plasma arginase-1 does not affect plasma arginine in patients undergoing liver resection. Clin. Sci. (Lond.) 114, 231-241 (2008).
24. Rotondo, R. et al. Exocytosis of azurophil and arginase 1-containing granules by activated polymorphonuclear neutrophils is required to inhibit T lymphocyte proliferation. J. Leukoc. Biol. 89, 721-727 (2011).
25. Talmadge, J.E. & Gabrilovich, D.I. History of myeloid-derived suppressor cells. Nat. Rev. Cancer 13, 739-752 (2013).
26. Eash, K.J., Means, J.M., White, D.W. & Link, D.C. CXCR4 is a key regulator of neutrophil release from the bone marrow under basal and stress granulopoiesis conditions. Blood 113, 4711-4719 (2009).
27. Ma, Q., Jones, D. & Springer, T.A. The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 10, 463-471 (1999).
28. Friedman, S.L. Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver. Physiol. Rev. 88, 125-172 (2008).
29. Chou, H.S. et al. Hepatic stellate cells regulate immune response by way of induction of myeloid suppressor cells in mice. Hepatology 53, 1007-1019 (2011).
30. Höchst, B. et al. Activated human hepatic stellate cells induce myeloid derived suppressor cells from peripheral blood monocytes in a CD44-dependent fashion. J. Hepatol. 59, 528-535 (2013).
31. Zhao, W. et al. Hepatic stellate cells promote tumor progression by enhancement of immunosuppressive cells in an orthotopic liver tumor mouse model. Lab. Invest. 94, 182-191 (2014).
32. Rodriguez, P.C. et al. Regulation of T cell receptor CD3zeta chain expression by L-arginine. J. Biol. Chem. 277, 21123-21129 (2002).
33. Hayashi, K., Jutabha, P., Endou, H., Sagara, H. & Anzai, N. LAT1 is a critical transporter of essential amino acids for immune reactions in activated human T cells. J. Immunol. 191, 4080-4085 (2013).
34. Cantor, J.M. & Ginsberg, M.H. CD98 at the crossroads of adaptive immunity and cancer. J. Cell Sci. 125, 1373-1382 (2012).
35. Campbell, W.A. et al. TA1/LAT-1/CD98 light chain and system L activity, but not 4F2/CD98 heavy chain, respond to arginine availability in rat hepatic cells. Loss Of response in tumor cells. J. Biol. Chem. 275, 5347-5354 (2000).
36. Schumacher, K., Maerker-Alzer, G. & Wehmer, U. A lymphocyte-inhibiting factor isolated from normal human liver. Nature 251, 655-656 (1974).
37. Chisari, F.V. et al. Production of two distinct and independent hepatic immunoregulatory molecules by the perfused rat liver. Hepatology 5, 735-743 (1985).
38. Sandalova, E. et al. Increased levels of arginase in patients with acute hepatitis B suppress antiviral T cells. Gastroenterology 143, 78-87 e73 (2012).
39. Walker, L.J. et al. CD8αα expression marks terminally differentiated human CD8+ T cells expanded in chronic viral infection. Front Immunol 4, 223 (2013).
40. Corzo, C.A. et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J. Exp. Med. 207, 2439-2453 (2010).
41. Rodriguez, P.C., Quiceno, D.G. & Ochoa, A.C. L-arginine availability regulates T-lymphocyte cell-cycle progression. Blood 109, 1568-1573 (2007).
42. Hara, K. et al. Amino acid sufficiency and mTOR regulate p70 S6 kinase and eIF-4E BP1 through a common effector mechanism. J. Biol. Chem. 273, 14484-14494 (1998).
43. Sitia, G. et al. Kupffer cells hasten resolution of liver immunopathology in mouse models of viral hepatitis. PLoS Pathog. 7, e1002061 (2011).
44. Dunn, C. et al. Cytokines induced during chronic hepatitis B virus infection promote a pathway for NK cell-mediated liver damage. J. Exp. Med. 204, 667-680 (2007).
45. Sander, L.E. et al. Hepatic acute-phase proteins control innate immune responses during infection by promoting myeloid-derived suppressor cell function. J. Exp. Med. 207, 1453-1464 (2010).
46. Mieulet, V. et al. TPL-2-mediated activation of MAPK downstream of TLR4 signaling is coupled to arginine availability. Sci. Signal. 3, ra61 (2010).
47. Sade-Feldman, M. et al. Tumor necrosis factor-alpha blocks differentiation and enhances suppressive activity of immature myeloid cells during chronic inflammation. Immunity 38, 541-554 (2013).
48. Kong, X., Sun, R., Chen, Y., Wei, H. & Tian, Z. gammadeltaT cells drive myeloid-derived suppressor cell-mediated CD8+ T cell exhaustion in hepatitis B virus-induced immunotolerance. J. Immunol. 193, 1645-1653 (2014).
49. Kennedy, P.T. et al. Preserved T-cell function in children and young adults with immune-tolerant chronic hepatitis B. Gastroenterology 143, 637-645 (2012).