Indoxyl sulfate (IS)-mediated immune dysfunction provokes endothelial damage in patients with end-stage renal disease (ESRD)

Scientific Reports

Volumn 7, Issue 1, 2017, Pages

  Kim, Hee Young ^a   Yoo, Tae Hyun ^b   Hwang, Yuri ^a   Lee, Ga Hye ^a   Kim, Bonah ^a   Jang, Jiyeon ^a   Yu, Hee Tae ^c   Kim, Min Chang ^a   Cho, Joo Youn ^a   Lee, Chan Joo ^d   Kim, Hyeon Chang ^c   Park, Sungha ^c   Lee, Won Woo ^a,e  

^a Seoul National University College of Medicine   (South Korea)

^b Yonsei University   (South Korea)

^c Yonsei University College of Medicine   (South Korea)

^d Yonsei University College of Medicine   (South Korea)

^e Seoul National University College of Medicine   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; CHEMOKINE RECEPTOR CX3CR1; CX3CR1 PROTEIN, HUMAN; CXCL1 CHEMOKINE; CXCL1 PROTEIN, HUMAN; INDICAN; TUMOR NECROSIS FACTOR;

ADULT; AGED; APOPTOSIS; CASE CONTROL STUDY; CD4+ T LYMPHOCYTE; CELL CULTURE; CHRONIC KIDNEY FAILURE; DRUG EFFECT; FEMALE; HUMAN; IMMUNOLOGY; MALE; METABOLISM; MIDDLE AGED; PATHOLOGY; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

ADULT; AGED; APOPTOSIS; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CHEMOKINE CXCL1; CX3C CHEMOKINE RECEPTOR 1; ENDOTHELIUM, VASCULAR; FEMALE; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INDICAN; KIDNEY FAILURE, CHRONIC; MALE; MIDDLE AGED; RECEPTORS, ARYL HYDROCARBON; TUMOR NECROSIS FACTOR-ALPHA;

EID: 85020425206     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-017-03130-z     Document Type: Article

References (67)

1. Betjes, M. G. Immune cell dysfunction and inflammation in end-stage renal disease. Nature reviews. Nephrology 9, 255-265, doi:10.1038/nrneph.2013.44 (2013).
2. Girndt, M., Sester, M., Sester, U., Kaul, H. & Kohler, H. Molecular aspects of T- and B-cell function in uremia. Kidney international. Supplement 78, S206-211 (2001).
3. Meier, P., Dayer, E., Blanc, E. & Wauters, J. P. Early T cell activation correlates with expression of apoptosis markers in patients with end-stage renal disease. Journal of the American Society of Nephrology: JASN 13, 204-212 (2002).
4. Sarnak, M. J. & Jaber, B. L. Mortality caused by sepsis in patients with end-stage renal disease compared with the general population. Kidney international 58, 1758-1764, doi:10.1111/j.1523-1755.2000.00337.x (2000).
5. Verkade, M. A. et al. Peripheral blood dendritic cells and GM-CSF as an adjuvant for hepatitis B vaccination in hemodialysis patients. Kidney international 66, 614-621, doi:10.1111/j.1523-1755.2004.00781.x (2004).
6. Stewart, J. H. et al. The pattern of excess cancer in dialysis and transplantation. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association - European Renal Association 24, 3225-3231, doi:10.1093/ndt/gfp331 (2009).
7. Foley, R. N., Parfrey, P. S. & Sarnak, M. J. Clinical epidemiology of cardiovascular disease in chronic renal disease. American journal of kidney diseases: the official journal of the National Kidney Foundation 32, S112-119 (1998).
8. Vaziri, N. D. Oxidative stress in uremia: nature, mechanisms, and potential consequences. Seminars in nephrology 24, 469-473 (2004).
9. Pecoits-Filho, R. et al. Associations between circulating inflammatory markers and residual renal function in CRF patients. American journal of kidney diseases: the official journal of the National Kidney Foundation 41, 1212-1218 (2003).
10. Locatelli, F. et al. Oxidative stress in end-stage renal disease: an emerging threat to patient outcome. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association - European Renal Association 18, 1272-1280 (2003).
11. Betjes, M. G., Huisman, M., Weimar, W. & Litjens, N. H. Expansion of cytolytic CD4+ CD28-T cells in end-stage renal disease. Kidney international 74, 760-767, doi:10.1038/ki.2008.301 (2008).
12. Yadav, A. K. & Jha, V. CD4+ CD28null cells are expanded and exhibit a cytolytic profile in end-stage renal disease patients on peritoneal dialysis. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association-European Renal Association 26, 1689-1694, doi:10.1093/ndt/gfr010 (2011).
13. Scherberich, J. E., Estner, H. & Segerer, W. Impact of different immunosuppressive regimens on antigen-presenting blood cells in kidney transplant patients. Kidney & blood pressure research 27, 177-180, doi:10.1159/000079807 (2004).
14. Heine, G. H. et al. CD14(++)CD16+ monocytes but not total monocyte numbers predict cardiovascular events in dialysis patients. Kidney international 73, 622-629, doi:10.1038/sj.ki.5002744 (2008).
15. Rogacev, K. S. et al. CD14++ CD16+ monocytes and cardiovascular outcome in patients with chronic kidney disease. Eur Heart J 32, 84-92, doi:10.1093/eurheartj/ehq371 (2011).
16. Heine, G. H. et al. Monocyte subpopulations and cardiovascular risk in chronic kidney disease. Nature reviews. Nephrology 8, 362-369, doi:10.1038/nrneph.2012.41 (2012).
17. Sun, Z. et al. Association of Graves' disease and prevalence of circulating IFN-gamma-producing CD28(-) T cells. Journal of clinical immunology 28, 464-472, doi:10.1007/s10875-008-9213-4 (2008).
18. Markovic-Plese, S., Cortese, I., Wandinger, K. P., McFarland, H. F. & Martin, R. CD4+ CD28-costimulation-independent T cells in multiple sclerosis. The Journal of clinical investigation 108, 1185-1194, doi:10.1172/JCI12516 (2001).
19. Schmidt, D., Goronzy, J. J. & Weyand, C. M. CD4+ CD7-CD28-T cells are expanded in rheumatoid arthritis and are characterized by autoreactivity. The Journal of clinical investigation 97, 2027-2037, doi:10.1172/JCI118638 (1996).
20. Nadareishvili, Z. G. et al. Elevated pro-inflammatory CD4+ CD28-lymphocytes and stroke recurrence and death. Neurology 63, 1446-1451 (2004).
21. Yoon, B. R. et al. Functional phenotype of synovial monocytes modulating inflammatory T-cell responses in rheumatoid arthritis (RA). PloS one 9, e109775, doi:10.1371/journal.pone.0109775 (2014).
22. Betjes, M. G., Meijers, R. W., de Wit, L. E. & Litjens, N. H. A killer on the road: circulating CD4(+)CD28null T cells as cardiovascular risk factor in ESRD patients. Journal of nephrology 25, 183-191, doi:10.5301/jn.5000057 (2012).
23. Vanholder, R. et al. Uremic toxicity: present state of the art. The International journal of artificial organs 24, 695-725 (2001).
24. Fukagawa, M. & Watanabe, Y. Role of uremic toxins and oxidative stress in chronic kidney disease. Therapeutic apheresis and dialysis: official peer-reviewed journal of the International Society for Apheresis, the Japanese Society for Apheresis, the Japanese Society for Dialysis Therapy 15, 119, doi:10.1111/j.1744-9987.2010.00881.x (2011).
25. Vanholder, R., Schepers, E., Pletinck, A., Nagler, E. V. & Glorieux, G. The uremic toxicity of indoxyl sulfate and p-cresyl sulfate: a systematic review. Journal of the American Society of Nephrology: JASN 25, 1897-1907, doi:10.1681/ASN.2013101062 (2014).
26. Nii-Kono, T. et al. Indoxyl sulfate induces skeletal resistance to parathyroid hormone in cultured osteoblastic cells. Kidney international 71, 738-743, doi:10.1038/sj.ki.5002097 (2007).
27. Lekawanvijit, S., Kompa, A. R., Wang, B. H., Kelly, D. J. & Krum, H. Cardiorenal syndrome: the emerging role of protein-bound uremic toxins. Circ Res 111, 1470-1483, doi:10.1161/CIRCRESAHA.112.278457 (2012).
28. Vanholder, R., Schepers, E., Pletinck, A., Neirynck, N. & Glorieux, G. An update on protein-bound uremic retention solutes. J Ren Nutr 22, 90-94, doi:10.1053/j.jrn.2011.10.026 (2012).
29. Poesen, R., Meijers, B. & Evenepoel, P. The colon: an overlooked site for therapeutics in dialysis patients. Semin Dial 26, 323-332, doi:10.1111/sdi.12082 (2013).
30. Stenvinkel, P. et al. IL-10, IL-6, and TNF-alpha: central factors in the altered cytokine network of uremia-the good, the bad, and the ugly. Kidney international 67, 1216-1233, doi:10.1111/j.1523-1755.2005.00200.x (2005).
31. Girndt, M. et al. Production of interleukin-6, tumor necrosis factor alpha and interleukin-10 in vitro correlates with the clinical immune defect in chronic hemodialysis patients. Kidney international 47, 559-565 (1995).
32. Schroeder, J. C. et al. The uremic toxin 3-indoxyl sulfate is a potent endogenous agonist for the human aryl hydrocarbon receptor. Biochemistry 49, 393-400, doi:10.1021/bi901786x (2010).
33. Nebert, D. W., Puga, A. & Vasiliou, V. Role of the Ah receptor and the dioxin-inducible [Ah] gene battery in toxicity, cancer, and signal transduction. Annals of the New York Academy of Sciences 685, 624-640 (1993).
34. Ito, S. et al. Reduction of indoxyl sulfate by AST-120 attenuates monocyte inflammation related to chronic kidney disease. Journal of leukocyte biology 93, 837-845, doi:10.1189/jlb.0112023 (2013).
35. Ketelhuth, D. F. & Hansson, G. K. Adaptive Response of T and B Cells in Atherosclerosis. Circ Res 118, 668-678, doi:10.1161/CIRCRESAHA.115.306427 (2016).
36. Teupser, D. et al. Major reduction of atherosclerosis in fractalkine (CX3CL1)-deficient mice is at the brachiocephalic artery, not the aortic root. Proceedings of the National Academy of Sciences of the United States of America 101, 17795-17800, doi:10.1073/pnas.0408096101 (2004).
37. Weng, N. P., Akbar, A. N. & Goronzy, J. CD28(-) T cells: their role in the age-associated decline of immune function. Trends in immunology 30, 306-312, doi:10.1016/j.it.2009.03.013 (2009).
38. Yu, H. T., Park, S., Shin, E. C. & Lee, W. W. T cell senescence and cardiovascular diseases. Clin Exp Med. doi:10.1007/s10238-015-0376-z (2015).
39. Bryl, E. et al. Modulation of CD28 expression with anti-tumor necrosis factor alpha therapy in rheumatoid arthritis. Arthritis Rheum 52, 2996-3003, doi:10.1002/art.21353 (2005).
40. Appay, V. The physiological role of cytotoxic CD4(+) T-cells: the holy grail? Clinical and experimental immunology 138, 10-13, doi:10.1111/j.1365-2249.2004.02605.x (2004).
41. Raveney, B. J. et al. Eomesodermin-expressing T-helper cells are essential for chronic neuroinflammation. Nat Commun 6, 8437, doi:10.1038/ncomms9437 (2015).
42. Takeuchi, A. & Saito, T. CD4 CTL, a Cytotoxic Subset of CD4+ T Cells, Their Differentiation and Function. Front Immunol 8, 194, doi:10.3389/fimmu.2017.00194 (2017).
43. Tonelli, M., Karumanchi, S. A. & Thadhani, R. Epidemiology and Mechanisms of Uremia-Related Cardiovascular Disease. Circulation 133, 518-536, doi:10.1161/CIRCULATIONAHA.115.018713 (2016).
44. Girndt, M., Sester, U., Sester, M., Kaul, H. & Kohler, H. Impaired cellular immune function in patients with end-stage renal failure. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association - European Renal Association 14, 2807-2810 (1999).
45. Koch, S., Kucharzik, T., Heidemann, J., Nusrat, A. & Luegering, A. Investigating the role of proinflammatory CD16+ monocytes in the pathogenesis of inflammatory bowel disease. Clinical and experimental immunology 161, 332-341, doi:10.1111/j.1365-2249.2010.04177.x (2010).
46. Cros, J. et al. Human CD14dim monocytes patrol and sense nucleic acids and viruses via TLR7 and TLR8 receptors. Immunity 33, 375-386, doi:10.1016/j.immuni.2010.08.012 (2010).
47. Niwa, T. et al. The protein metabolite hypothesis, a model for the progression of renal failure: an oral adsorbent lowers indoxyl sulfate levels in undialyzed uremic patients. Kidney international. Supplement 62, S23-28 (1997).
48. Niwa, T. Role of indoxyl sulfate in the progression of chronic kidney disease and cardiovascular disease: experimental and clinical effects of oral sorbent AST-120. Therapeutic apheresis and dialysis: official peer-reviewed journal of the International Society for Apheresis, the Japanese Society for Apheresis, the Japanese Society for Dialysis Therapy 15, 120-124, doi:10.1111/j.1744-9987.2010.00882.x (2011).
49. Niwa, T. Uremic toxicity of indoxyl sulfate. Nagoya journal of medical science 72, 1-11 (2010).
50. Adesso, S. et al. The uremic toxin indoxyl sulphate enhances macrophage response to LPS. PloS one 8, e76778, doi:10.1371/journal. pone.0076778 (2013).
51. Sallee, M. et al. The aryl hydrocarbon receptor-activating effect of uremic toxins from tryptophan metabolism: a new concept to understand cardiovascular complications of chronic kidney disease. Toxins (Basel) 6, 934-949, doi:10.3390/toxins6030934 (2014).
52. Cella, M. & Colonna, M. Aryl hydrocarbon receptor: Linking environment to immunity. Semin Immunol 27, 310-314, doi:10.1016/j.smim.2015.10.002 (2015).
53. Stockinger, B., Di Meglio, P., Gialitakis, M. & Duarte, J. H. The aryl hydrocarbon receptor: multitasking in the immune system. Annu Rev Immunol 32, 403-432, doi:10.1146/annurev-immunol-032713-120245 (2014).
54. Murray, I. A., Patterson, A. D. & Perdew, G. H. Aryl hydrocarbon receptor ligands in cancer: friend and foe. Nat Rev Cancer 14, 801-814, doi:10.1038/nrc3846 (2014).
55. Shivanna, S. et al. The Aryl Hydrocarbon Receptor is a Critical Regulator of Tissue Factor Stability and an Antithrombotic Target in Uremia. Journal of the American Society of Nephrology: JASN 27, 189-201, doi:10.1681/ASN.2014121241 (2016).
56. Frericks, M., Meissner, M. & Esser, C. Microarray analysis of the AHR system: tissue-specific flexibility in signal and target genes. Toxicology and applied pharmacology 220, 320-332, doi:10.1016/j.taap.2007.01.014 (2007).
57. Cheon, H. et al. Signaling pathway for 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced TNF-alpha production in differentiated THP-1 human macrophages. Experimental & molecular medicine 39, 524-534, doi:10.1038/emm.2007.58 (2007).
58. Kimura, A. et al. Aryl hydrocarbon receptor in combination with Stat1 regulates LPS-induced inflammatory responses. The Journal of experimental medicine 206, 2027-2035, doi:10.1084/jem.20090560 (2009).
59. Trojanowicz, B. et al. Monocytic angiotensin-converting enzyme 2 relates to atherosclerosis in patients with chronic kidney disease. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association - European Renal Association 32, 287-298, doi:10.1093/ndt/gfw206 (2017).
60. Trojanowicz, B., Ulrich, C., Seibert, E., Fiedler, R. & Girndt, M. Uremic conditions drive human monocytes to pro-atherogenic differentiation via an angiotensin-dependent mechanism. PloS one 9, e102137, doi:10.1371/journal.pone.0102137 (2014).
61. Viemann, D. et al. Transcriptional profiling of IKK2/NF-kappa B- and p38 MAP kinase-dependent gene expression in TNF-alphastimulated primary human endothelial cells. Blood 103, 3365-3373, doi:10.1182/blood-2003-09-3296 (2004).
62. Viemann, D. et al. TNF induces distinct gene expression programs in microvascular and macrovascular human endothelial cells. Journal of leukocyte biology 80, 174-185, doi:10.1189/jlb.0905530 (2006).
63. Broux, B., Markovic-Plese, S., Stinissen, P. & Hellings, N. Pathogenic features of CD4+ CD28-T cells in immune disorders. Trends in molecular medicine 18, 446-453, doi:10.1016/j.molmed.2012.06.003 (2012).
64. Bryl, E., Vallejo, A. N., Weyand, C. M. & Goronzy, J. J. Down-regulation of CD28 expression by TNF-alpha. Journal of immunology 167, 3231-3238 (2001).
65. Vallejo, A. N., Weyand, C. M. & Goronzy, J. J. Functional disruption of the CD28 gene transcriptional initiator in senescent T cells. The Journal of biological chemistry 276, 2565-2570, doi:10.1074/jbc.M005503200 (2001).
66. van Leeuwen, E. M. et al. Emergence of a CD4+ CD28-granzyme B+, cytomegalovirus-specific T cell subset after recovery of primary cytomegalovirus infection. Journal of immunology 173, 1834-1841 (2004).
67. Kikuchi, K. et al. Metabolomic analysis of uremic toxins by liquid chromatography/electrospray ionization-tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 878, 1662-1668, doi:10.1016/j.jchromb.2009.11.040 (2010).