Ammonia drives dendritic cells into dysfunction

Journal of Immunology

Volumn 193, Issue 3, 2014, Pages 1080-1089

  Luo, Can ^a   Shen, Guobo ^a   Liu, Ning ^a   Gong, Fengming ^a   Wei, Xiawei ^a   Yao, Shaohua ^a   Liu, Dan ^b   Teng, Xiu ^a   Ye, Ning ^a   Zhang, Nan ^a   Zhou, Xikun ^a   Li, Jiong ^a   Yang, Li ^a,b   Zhao, Xia ^a   Xiang, Rong ^c   Wei, Yu Quan ^a  

^a SICHUAN UNIVERSITY   (China)

^b SICHUAN UNIVERSITY   (China)

^c NANKAI UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; AMMONIUM CHLORIDE; GAMMA INTERFERON; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2B; REACTIVE OXYGEN METABOLITE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY TITER; ARTICLE; CANCER INHIBITION; CELL COUNT; CELL DIFFERENTIATION; CELL MATURATION; CELLULAR IMMUNITY; CLINICAL ARTICLE; COLON CARCINOMA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DISORDERS OF MITOCHONDRIAL FUNCTIONS; FEMALE; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; LIVER CIRRHOSIS; LYMPHOCYTE ACTIVATION; MALE; MOUSE; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; TUMOR GROWTH; TUMOR IMMUNITY;

AMMONIUM CHLORIDE; ANIMALS; BONE MARROW CELLS; CELL COUNT; CELL LINE, TUMOR; COCULTURE TECHNIQUES; DENDRITIC CELLS; HUMANS; LIVER CIRRHOSIS; LYMPHOCYTE CULTURE TEST, MIXED; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MIDDLE AGED; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; PHAGOCYTOSIS; PRIMARY CELL CULTURE;

EID: 84906074577     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1303218     Document Type: Article

References (48)

1. Olde Damink, S. W., R. Jalan, D. N. Redhead, P. C. Hayes, N. E. Deutz, and P. B. Soeters. 2002. Interorgan ammonia and amino acid metabolism in metabolically stable patients with cirrhosis and a TIPSS. Hepatology 36: 1163-1171.
2. Tandon, P., and G. Garcia-Tsao. 2008. Bacterial infections, sepsis, and multiorgan failure in cirrhosis. Semin. Liver Dis. 28: 26-42.
3. Bonnel, A. R., C. Bunchorntavakul, and K. R. Reddy. 2011. Immune dysfunction and infections in patients with cirrhosis. Clin. Gastroenterol. Hepatol. 9: 727-738.
4. Shawcross, D. L., G. A. Wright, V. Stadlbauer, S. J. Hodges, N. A. Davies, C. Wheeler-Jones, A. A. Pitsillides, and R. Jalan. 2008. Ammonia impairs neutrophil phagocytic function in liver disease. Hepatology 48: 1202-1212.
5. Shawcross, D. L., S. S. Shabbir, N. J. Taylor, and R. D. Hughes. 2010. Ammonia and the neutrophil in the pathogenesis of hepatic encephalopathy in cirrhosis. Hepatology 51: 1062-1069.
6. Kroemer, G., and J. Pouyssegur. 2008. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 13: 472-482.
7. Dang, C. V. 2010. Rethinking the Warburg effect with Myc micromanaging glutamine metabolism. Cancer Res. 70: 859-862.
8. Eng, C. H., K. Yu, J. Lucas, E. White, and R. T. Abraham. 2010. Ammonia derived from glutaminolysis is a diffusible regulator of autophagy. Sci. Signal. 3: ra31.
9. Fischer, K., P. Hoffmann, S. Voelkl, N. Meidenbauer, J. Ammer, M. Edinger, E. Gottfried, S. Schwarz, G. Rothe, S. Hoves, et al. 2007. Inhibitory effect of tumor cell-derived lactic acid on human T cells. Blood 109: 3812-3819.
10. Gottfried, E., L. A. Kunz-Schughart, S. Ebner, W. Mueller-Klieser, S. Hoves, R. Andreesen, A. Mackensen, and M. Kreutz. 2006. Tumor-derived lactic acid modulates dendritic cell activation and antigen expression. Blood 107: 2013-2021.
11. Janeway, C. A., Jr., and R. Medzhitov. 2002. Innate immune recognition. Annu. Rev. Immunol. 20: 197-216.
12. Coombes, J. L., and F. Powrie. 2008. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8: 435-446.
13. Auffermann-Gretzinger, S., E. B. Keeffe, and S. Levy. 2001. Impaired dendritic cell maturation in patients with chronic, but not resolved, hepatitis C virus infection. Blood 97: 3171-3176.
14. Ninomiya, T., S. M. Akbar, T. Masumoto, N. Horiike, and M. Onji. 1999. Dendritic cells with immature phenotype and defective function in the peripheral blood from patients with hepatocellular carcinoma. J. Hepatol. 31: 323-331.
15. Ma, Y., L. Aymeric, C. Locher, G. Kroemer, and L. Zitvogel. 2011. The dendritic cell-tumor cross-talk in cancer. Curr. Opin. Immunol. 23: 146-152.
16. Palucka, K., and J. Banchereau. 2012. Cancer immunotherapy via dendritic cells. Nat. Rev. Cancer 12: 265-277.
17. Yang, A. S., and E. C. Lattime. 2003. Tumor-induced interleukin 10 suppresses the ability of splenic dendritic cells to stimulate CD4 and CD8 T-cell responses. Cancer Res. 63: 2150-2157.
18. Byrne, S. N., and G. M. Halliday. 2002. Dendritic cells: making progress with tumour regression? Immunol. Cell Biol. 80: 520-530.
19. Rama Rao, K. V., A. R. Jayakumar, and M. D. Norenberg. 2005. Role of oxidative stress in the ammonia-induced mitochondrial permeability transition in cultured astrocytes. Neurochem. Int. 47: 31-38.
20. Morelli, A. E., A. F. Zahorchak, A. T. Larregina, B. L. Colvin, A. J. Logar, T. Takayama, L. D. Falo, and A. W. Thomson. 2001. Cytokine production by mouse myeloid dendritic cells in relation to differentiation and terminal maturation induced by lipopolysaccharide or CD40 ligation. Blood 98: 1512-1523.
21. Görg, B., N. Qvartskhava, V. Keitel, H. J. Bidmon, O. Selbach, F. Schliess, and D. Häussinger. 2008. Ammonia induces RNA oxidation in cultured astrocytes and brain in vivo. Hepatology 48: 567-579.
22. Häussinger, D., and B. Görg. 2010. Interaction of oxidative stress, astrocyte swelling and cerebral ammonia toxicity. Curr. Opin. Clin. Nutr. Metab. Care 13: 87-92.
23. Jayakumar, A. R., K. V. Rama Rao, X. Y. Tong, and M. D. Norenberg. 2009. Calcium in the mechanism of ammonia-induced astrocyte swelling. J. Neurochem. 109(Suppl 1): 252-257.
24. Virmani, R., D. Warren, R. Rees, L. M. Fink, and D. English. 1983. Effects of perfluorochemical on phagocytic function of leukocytes. Transfusion 23: 512-515.
25. Ducharme, G., E. W. Newell, C. Pinto, and L. C. Schlichter. 2007. Smallconductance Cl-channels contribute to volume regulation and phagocytosis in microglia. Eur. J. Neurosci. 26: 2119-2130.
26. Zaccagnino, P., M. Saltarella, S. Maiorano, A. Gaballo, G. Santoro, B. Nico, M. Lorusso, and A. Del Prete. 2012. An active mitochondrial biogenesis occurs during dendritic cell differentiation. Int. J. Biochem. Cell Biol. 44: 1962-1969.
27. Del Prete, A., P. Zaccagnino, M. Di Paola, M. Saltarella, C. Oliveros Celis, B. Nico, G. Santoro, and M. Lorusso. 2008. Role of mitochondria and reactive oxygen species in dendritic cell differentiation and functions. Free Radic. Biol. Med. 44: 1443-1451.
28. Castera, L., A. S. Hatzfeld-Charbonnier, C. Ballot, F. Charbonnel, E. Dhuiege, T. Velu, P. Formstecher, L. Mortier, and P. Marchetti. 2009. Apoptosis-related mitochondrial dysfunction defines human monocyte-derived dendritic cells with impaired immuno-stimulatory capacities. J. Cell. Mol. Med. 13: 1321-1335.
29. Seo, J. H., J. G. Fox, R. M. Peek, Jr., and S. J. Hagen. 2011. N-methyl Daspartate channels link ammonia and epithelial cell death mechanisms in Helicobacter pylori infection. Gastroenterology 141: 2064-2075.
30. Schliess, F., N. Foster, B. Görg, R. Reinehr, and D. Häussinger. 2004. Hypoosmotic swelling increases protein tyrosine nitration in cultured rat astrocytes. Glia 47: 21-29.
31. Reinehr, R., B. Görg, S. Becker, N. Qvartskhava, H. J. Bidmon, O. Selbach, H. L. Haas, F. Schliess, and D. Häussinger. 2007. Hypoosmotic swelling and ammonia increase oxidative stress by NADPH oxidase in cultured astrocytes and vital brain slices. Glia 55: 758-771.
32. Alderman, C. J., S. Shah, J. C. Foreman, B. M. Chain, and D. R. Katz. 2002. The role of advanced oxidation protein products in regulation of dendritic cell function. Free Radic. Biol. Med. 32: 377-385.
33. Matsue, H., D. Edelbaum, D. Shalhevet, N. Mizumoto, C. Yang, M. E. Mummert, J. Oeda, H. Masayasu, and A. Takashima. 2003. Generation and function of reactive oxygen species in dendritic cells during antigen presentation. J. Immunol. 171: 3010-3018.
34. Tan, P. H., P. Sagoo, C. Chan, J. B. Yates, J. Campbell, S. C. Beutelspacher, B. M. Foxwell, G. Lombardi, and A. J. George. 2005. Inhibition of NF-kappa B and oxidative pathways in human dendritic cells by antioxidative vitamins generates regulatory T cells. J. Immunol. 174: 7633-7644.
35. Borzio, M., F. Salerno, L. Piantoni, M. Cazzaniga, P. Angeli, F. Bissoli, S. Boccia, G. Colloredo-Mels, P. Corigliano, G. Fornaciari, et al. 2001. Bacterial infection in patients with advanced cirrhosis: a multicentre prospective study. Dig. Liver Dis. 33: 41-48.
36. Serbina, N. V., T. P. Salazar-Mather, C. A. Biron, W. A. Kuziel, and E. G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19: 59-70.
37. Kakazu, E., N. Kanno, Y. Ueno, and T. Shimosegawa. 2007. Extracellular branched-chain amino acids, especially valine, regulate maturation and function of monocyte-derived dendritic cells. J. Immunol. 179: 7137-7146.
38. Zwolak, A., I. Jastrzebska, A. Surdacka, B. Kasztelan-Szczerbinska, C. T. Lozowski, J. Rolinski, B. Skrzydlo-Radomanska, P. Radwan, and J. Daniluk. 2012. Peripheral blood dendritic cells in alcoholic and autoimmune liver disorders. Hum. Exp. Toxicol. 31: 438-446.
39. Cheong, H. J., J. Y. Song, J. W. Park, J. E. Yeon, K. S. Byun, C. H. Lee, H. I. Cho, T. G. Kim, and W. J. Kim. 2006. Humoral and cellular immune responses to influenza vaccine in patients with advanced cirrhosis. Vaccine 24: 2417-2422.
40. Peter, J., O. Frey, A. Stallmach, and T. Bruns. 2013. Attenuated antigen-specific T cell responses in cirrhosis are accompanied by elevated serum interleukin-10 levels and down-regulation of HLA-DR on monocytes. BMC Gastroenterol. 13: 37.
41. Pinzon-Charry, A., T. Maxwell, and J. A. López. 2005. Dendritic cell dysfunction in cancer: a mechanism for immunosuppression. Immunol. Cell Biol. 83: 451-461.
42. Tourkova, I. L., G. V. Shurin, S. Wei, and M. R. Shurin. 2007. Small rho GTPases mediate tumor-induced inhibition of endocytic activity of dendritic cells. J. Immunol. 178: 7787-7793.
43. Wise, D. R., and C. B. Thompson. 2010. Glutamine addiction: a new therapeutic target in cancer. Trends Biochem. Sci. 35: 427-433.
44. DeBerardinis, R. J., and T. Cheng. 2010. Q's next: the diverse functions of glutamine in metabolism, cell biology and cancer. Oncogene 29: 313-324.
45. Yuneva, M. 2008. Finding an "Achilles' heel" of cancer: the role of glucose and glutamine metabolism in the survival of transformed cells. Cell Cycle 7: 2083-2089.
46. Krasteva, M., J. Kehren, F. Horand, H. Akiba, G. Choquet, M. T. Ducluzeau, R. Tédone, J. L. Garrigue, D. Kaiserlian, and J. F. Nicolas. 1998. Dual role of dendritic cells in the induction and down-regulation of antigen-specific cutaneous inflammation. J. Immunol. 160: 1181-1190.
47. Gasparini, C., B. M. Foxwell, and M. Feldmann. 2009. RelB/p50 regulates CCL19 production, but fails to promote human DC maturation. Eur. J. Immunol. 39: 2215-2223.
48. Wang, J. B., J. W. Erickson, R. Fuji, S. Ramachandran, P. Gao, R. Dinavahi, K. F. Wilson, A. L. Ambrosio, S. M. Dias, C. V. Dang, and R. A. Cerione. 2010. Targeting mitochondrial glutaminase activity inhibits oncogenic transformation. Cancer Cell 18: 207-219.