The aryl hydrocarbon receptor-activating effect of uremic toxins from tryptophan metabolism: A new concept to understand cardiovascular complications of chronic kidney disease

Toxins

Volumn 6, Issue 3, 2014, Pages 934-949

  Sallée, Marion ^a,b   Dou, Laetitia ^a   Cerini, Claire ^a   Poitevin, Stéphane ^a   Brunet, Philippe ^a,b   Burtey, Stéphane ^a,b  

^a AIX MARSEILLE UNIVERSITY   (France)

^b HÔPITAL DE LA CONCEPTION   (France)

Author keywords

Aryl hydrocarbon receptor; Cardiovascular diseases; Chronic kidney disease; Tryptophan derived uremic toxins

Indexed keywords

2, 3, 7, 8 TETRACHLORODIBENZO PARA DIOXIN; 3 HYDROXYKYNURENINE; AROMATIC HYDROCARBON RECEPTOR; CYCLOOXYGENASE 2; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 8; KYNURENINE; MACROPHAGE ELASTASE; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; POLYCHLORINATED BIPHENYL DERIVATIVE; PROCOAGULANT; TRYPTOPHAN; UNCLASSIFIED DRUG; UREMIC TOXIN; VASCULAR CELL ADHESION MOLECULE 1; VASCULOTROPIN;

CARDIOMYOPATHY; CARDIOTOXICITY; CARDIOVASCULAR DISEASE; CHRONIC KIDNEY DISEASE; ELEVATED BLOOD PRESSURE; ENDOTHELIAL DYSFUNCTION; HUMAN; LEUKOCYTE ACTIVATION; MACROPHAGE; NONHUMAN; OXIDATIVE STRESS; REVIEW; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; THROMBOSIS; TRYPTOPHAN METABOLISM; UBIQUITINATION; VASCULAR SMOOTH MUSCLE; VASCULITIS;

ANIMALS; CARDIOVASCULAR DISEASES; ENDOTHELIUM, VASCULAR; HUMANS; LEUKOCYTES; OXIDATIVE STRESS; RECEPTORS, ARYL HYDROCARBON; RENAL INSUFFICIENCY, CHRONIC; TOXINS, BIOLOGICAL; TRYPTOPHAN; UREMIA;

EID: 84897868717     PISSN: 20726651     EISSN: None     Source Type: Journal    
DOI: 10.3390/toxins6030934     Document Type: Review

References (108)

1. Vanholder, R.; Massy, Z.; Argiles, A.; Spasovski, G.; Verbeke, F.; Lameire, N. Chronic kidney disease as cause of cardiovascular morbidity and mortality. Nephrol. Dial. Transplant. 2005, 20, 1048-1056.
2. Go, A.S.; Chertow, G.M.; Fan, D.; McCulloch, C.E.; Hsu, C.Y. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N. Engl. J. Med. 2004, 351, 1296-1305.
3. Keith, D.S.; Nichols, G.A.; Gullion, C.M.; Brown, J.B.; Smith, D.H. Longitudinal follow-up and outcomes among a population with chronic kidney disease in a large managed care organization. Arch. Intern. Med. 2004, 164, 659-663.
4. Jourde-Chiche, N.; Dou, L.; Cerini, C.; Dignat-George, F.; Brunet, P. Vascular incompetence in dialysis patients-Protein-bound uremic toxins and endothelial dysfunction. Semin. Dial. 2011, 24, 327-337.
5. Vanholder, R.; De Smet, R.; Glorieux, G.; Argiles, A.; Baurmeister, U.; Brunet, P.; Clark, W.; Cohen, G.; De Deyn, P.P.; Deppisch, R.; et al. Review on uremic toxins: Classification, concentration, and interindividual variability. Kidney Int. 2003, 63, 1934-1943.
6. Schroeder, J.C.; Dinatale, B.C.; Murray, I.A.; Flaveny, C.A.; Liu, Q.; Laurenzana, E.M.; Lin, J.M.; Strom, S.C.; Omiecinski, C.J.; Amin, S.; et al. The uremic toxin 3-indoxyl sulfate is a potent endogenous agonist for the human aryl hydrocarbon receptor. Biochemistry 2010, 49, 393-400.
7. Heath-Pagliuso, S.; Rogers, W.J.; Tullis, K.; Seidel, S.D.; Cenijn, P.H.; Brouwer, A.; Denison, M.S. Activation of the Ah receptor by tryptophan and tryptophan metabolites. Biochemistry 1998, 37, 11508-11515.
8. Fatokun, A.A.; Hunt, N.H.; Ball, H.J. Indoleamine 2,3-dioxygenase 2 (IDO2) and the kynurenine pathway: Characteristics and potential roles in health and disease. Amino Acids 2013, 45, 1319-1329.
9. Saito, K.; Fujigaki, S.; Heyes, M.P.; Shibata, K.; Takemura, M.; Fujii, H.; Wada, H.; Noma, A.; Seishima, M. Mechanism of increases in L-kynurenine and quinolinic acid in renal insufficiency. Am. J. Physiol. Renal Physiol. 2000, 279, F565-F572.
10. Pawlak, D.; Pawlak, K.; Malyszko, J.; Mysliwiec, M.; Buczko, W. Accumulation of toxic products degradation of kynurenine in hemodialyzed patients. Int. Urol. Nephrol. 2001, 33, 399-404.
11. Zhu, W.; Stevens, A.P.; Dettmer, K.; Gottfried, E.; Hoves, S.; Kreutz, M.; Holler, E.; Canelas, A.B.; Kema, I.; Oefner, P.J. Quantitative profiling of tryptophan metabolites in serum, urine, and cell culture supernatants by liquid chromatography-tandem mass spectrometry. Anal. Bioanal. Chem. 2011, 401, 3249-3261.
12. Aronov, P.A.; Luo, F.J.; Plummer, N.S.; Quan, Z.; Holmes, S.; Hostetter, T.H.; Meyer, T.W. Colonic contribution to uremic solutes. J. Am. Soc. Nephrol. 2011, 22, 1769-1776.
13. Meyer, T.W.; Hostetter, T.H. Uremic solutes from colon microbes. Kidney Int. 2012, 81, 949-954
14. Koga, J.; Syono, K.; Ichikawa, T.; Adachi, T. Involvement of L-tryptophan aminotransferase in indole-3-acetic acid biosynthesis in Enterobacter cloacae. Biochim. Biophys. Acta 1994, 1209, 241-247.
15. Duranton, F.; Cohen, G.; De Smet, R.; Rodriguez, M.; Jankowski, J.; Vanholder, R.; Argiles, A. Normal and pathologic concentrations of uremic toxins. J. Am. Soc. Nephrol. 2012, 23, 1258-1270.
16. Bock, K.W. The human Ah receptor: Hints from dioxin toxicities to deregulated target genes and physiological functions. Biol. Chem. 2013, 394, 729-739.
17. Denison, M.S.; Nagy, S.R. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol. 2003, 43, 309-334.
18. Schmidt, J.V.; Bradfield, C.A. Ah receptor signaling pathways. Annu. Rev. Cell. Dev. Biol. 1996, 12, 55-89.
19. Fisher, J.M.; Jones, K.W.; Whitlock, J.P., Jr. Activation of transcription as a general mechanism of 2,3,7,8-tetrachlorodibenzo-p-dioxin action. Mol. Carcinog. 1989, 1, 216-221.
20. Denison, M.S.; Soshilov, A.A.; He, G.; DeGroot, D.E.; Zhao, B. Exactly the same but different: Promiscuity and diversity in the molecular mechanisms of action of the aryl hydrocarbon (dioxin) receptor. Toxicol. Sci. 2011, 124, 1-22.
21. Matsumura, F. The significance of the nongenomic pathway in mediating inflammatory signaling of the dioxin-activated Ah receptor to cause toxic effects. Biochem. Pharmacol. 2009, 77, 608-626.
22. Tan, Z.; Chang, X.; Puga, A.; Xia, Y. Activation of mitogen-activated protein kinases (MAPKs) by aromatic hydrocarbons: Role in the regulation of aryl hydrocarbon receptor (AHR) function. Biochem. Pharmacol. 2002, 64, 771-780.
23. Park, S.J.; Yoon, W.K.; Kim, H.J.; Son, H.Y.; Cho, S.W.; Jeong, K.S.; Kim, T.H.; Kim, S.H.; Kim, S.R.; Ryu, S.Y. 2,3,7,8-Tetrachlorodibenzo-p-dioxin activates ERK and p38 mitogen-activated protein kinases in RAW 264.7 cells. Anticancer Res. 2005, 25, 2831-2836.
24. Weiss, C.; Faust, D.; Durk, H.; Kolluri, S.K.; Pelzer, A.; Schneider, S.; Dietrich, C.; Oesch, F.; Gottlicher, M. TCDD induces c-jun expression via a novel Ah (dioxin) receptor-mediated p38-MAPK-dependent pathway. Oncogene 2005, 24, 4975-4983.
25. Diry, M.; Tomkiewicz, C.; Koehle, C.; Coumoul, X.; Bock, K.W.; Barouki, R.; Transy, C. Activation of the dioxin/aryl hydrocarbon receptor (AhR) modulates cell plasticity through a JNK-dependent mechanism. Oncogene 2006, 25, 5570-5574.
26. Park, S.; Mazina, O.; Kitagawa, A.; Wong, P.; Matsumura, F. TCDD causes suppression of growth and differentiation of MCF10A, human mammary epithelial cells by interfering with their insulin receptor signaling through c-Src kinase and ERK activation. J. Biochem. Mol. Toxicol. 2004, 18, 322-331.
27. Xie, G.; Peng, Z.; Raufman, J.P. Src-mediated aryl hydrocarbon and epidermal growth factor receptor cross talk stimulates colon cancer cell proliferation. Am. J. Physiol. Gastrointest. Liver Physiol. 2012, 302, G1006-G1015.
28. Tian, Y.; Rabson, A.B.; Gallo, M.A. Ah receptor and NF-kappaB interactions: mechanisms and physiological implications. Chem. Biol. Interact. 2002, 141, 97-115.
29. Vogel, C.F.; Sciullo, E.; Li, W.; Wong, P.; Lazennec, G.; Matsumura, F. RelB, a new partner of aryl hydrocarbon receptor-mediated transcription. Mol. Endocrinol. 2007, 21, 2941-2955.
30. Gondouin, B.; Cerini, C.; Dou, L.; Sallee, M.; Duval-Sabatier, A.; Pletinck, A.; Calaf, R.; Lacroix, R.; Jourde-Chiche, N.; Poitevin, S.; et al. Indolic uremic solutes increase tissue factor production in endothelial cells by the aryl hydrocarbon receptor pathway. Kidney Int. 2013, 84, 733-744.
31. Frumento, G.; Rotondo, R.; Tonetti, M.; Damonte, G.; Benatti, U.; Ferrara, G.B. Tryptophan-derived catabolites are responsible for inhibition of T and natural killer cell proliferation induced by indoleamine 2,3-dioxygenase. J. Exp. Med. 2002, 196, 459-468.
32. Opitz, C.A.; Litzenburger, U.M.; Sahm, F.; Ott, M.; Tritschler, I.; Trump, S.; Schumacher, T.; Jestaedt, L.; Schrenk, D.; Weller, M.; et al. An endogenous tumour-promoting ligand of the human aryl hydrocarbon receptor. Nature 2011, 478, 197-203.
33. Shin, J.H.; Zhang, L.; Murillo-Sauca, O.; Kim, J.; Kohrt, H.E.; Bui, J.D.; Sunwoo, J.B. Modulation of natural killer cell antitumor activity by the aryl hydrocarbon receptor. Proc. Natl. Acad. Sci. USA 2013, 110, 12391-12396.
34. Schefold, J.C.; Zeden, J.P.; Fotopoulou, C.; von Haehling, S.; Pschowski, R.; Hasper, D.; Volk, H.D.; Schuett, C.; Reinke, P. Increased indoleamine 2,3-dioxygenase (IDO) activity and elevated serum levels of tryptophan catabolites in patients with chronic kidney disease: A possible link between chronic inflammation and uraemic symptoms. Nephrol. Dial. Transplant. 2009, 24, 1901-1908.
35. DiNatale, B.C.; Murray, I.A.; Schroeder, J.C.; Flaveny, C.A.; Lahoti, T.S.; Laurenzana, E.M.; Omiecinski, C.J.; Perdew, G.H. Kynurenic acid is a potent endogenous aryl hydrocarbon receptor ligand that synergistically induces interleukin-6 in the presence of inflammatory signaling. Toxicol. Sci. 2010, 115, 89-97.
36. Humblet, O.; Birnbaum, L.; Rimm, E.; Mittleman, M.A.; Hauser, R. Dioxins and cardiovascular disease mortality. Environ. Health Perspect 2008, 116, 1443-1448.
37. Institute of Medicine of the National Academies. Veterans and Agent Orange: Update 2012; The National Academies Press: Washington, DC, USA, 2013.
38. Everett, C.J.; Mainous, A.G., 3rd; Frithsen, I.L.; Player, M.S.; Matheson, E.M. Association of polychlorinated biphenyls with hypertension in the 1999-2002 national health and nutrition examination survey. Environ. Res. 2008, 108, 94-97.
39. Lind, P.M.; van Bavel, B.; Salihovic, S.; Lind, L. Circulating levels of persistent organic pollutants (POPs) and carotid atherosclerosis in the elderly. Environ. Health Perspect 2012, 120, 38-43.
40. Jokinen, M.P.; Walker, N.J.; Brix, A.E.; Sells, D.M.; Haseman, J.K.; Nyska, A. Increase in cardiovascular pathology in female Sprague-Dawley rats following chronic treatment with 2,3,7,8-tetrachlorodibenzo-p-dioxin and 3,3',4,4',5-pentachlorobiphenyl. Cardiovasc. Toxicol. 2003, 3, 299-310.
41. Kopf, P.G.; Huwe, J.K.; Walker, M.K. Hypertension, cardiac hypertrophy, and impaired vascular relaxation induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin are associated with increased superoxide. Cardiovasc. Toxicol. 2008, 8, 181-193.
42. Lind, P.M.; Orberg, J.; Edlund, U.B.; Sjoblom, L.; Lind, L. The dioxin-like pollutant PCB 126 (3,3',4,4',5-pentachlorobiphenyl) affects risk factors for cardiovascular disease in female rats. Toxicol. Lett. 2004, 150, 293-299.
43. Dalton, T.P.; Kerzee, J.K.; Wang, B.; Miller, M.; Dieter, M.Z.; Lorenz, J.N.; Shertzer, H.G.; Nerbert, D.W.; Puga, A. Dioxin exposure is an environmental risk factor for ischemic heart disease. Cardiovasc. Toxicol. 2001, 1, 285-298.
44. Arsenescu, V.; Arsenescu, R.; Parulkar, M.; Karounos, M.; Zhang, X.; Baker, N.; Cassis, L.A. Polychlorinated biphenyl 77 augments angiotensin II-induced atherosclerosis and abdominal aortic aneurysms in male apolipoprotein E deficient mice. Toxicol. Appl. Pharmacol. 2011, 257, 148-154.
45. Wu, D.; Nishimura, N.; Kuo, V.; Fiehn, O.; Shahbaz, S.; Van Winkle, L.; Matsumura, F.; Vogel, C.F. Activation of aryl hydrocarbon receptor induces vascular inflammation and promotes atherosclerosis in apolipoprotein E-/-mice. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 1260-1267.
46. Barreto, F.C.; Barreto, D.V.; Liabeuf, S.; Meert, N.; Glorieux, G.; Temmar, M.; Choukroun, G.; Vanholder, R.; Massy, Z.A. Serum indoxyl sulfate is associated with vascular disease and mortality in chronic kidney disease patients. Clin. J. Am. Soc. Nephrol. 2009, 4, 1551-1558.
47. Melamed, M.L.; Plantinga, L.; Shafi, T.; Parekh, R.; Meyer, T.W.; Hostetter, T.H.; Coresh, J.; Powe, N.R. Retained organic solutes, patient characteristics and all-cause and cardiovascular mortality in hemodialysis: Results from the retained organic solutes and clinical outcomes (ROSCO) investigators. BMC Nephrol. 2013, 14, 134.
48. Chiu, C.A.; Lu, L.F.; Yu, T.H.; Hung, W.C.; Chung, F.M.; Tsai, I.T.; Yang, C.Y.; Hsu, C.C.; Lu, Y.C.; Wang, C.P.; et al. Increased levels of total P-Cresylsulphate and indoxyl sulphate are associated with coronary artery disease in patients with diabetic nephropathy. Rev. Diabet. Stud. 2010, 7, 275-284.
49. Sato, B.; Yoshikawa, D.; Ishii, H.; Suzuki, S.; Inoue, Y.; Takeshita, K.; Tanaka, M.; Kumagai, S.; Matsumoto, M.; Okumura, S.; et al. Relation of plasma indoxyl sulfate levels and estimated glomerular filtration rate to left ventricular diastolic dysfunction. Am. J. Cardiol. 2013, 111, 712-716.
50. Yisireyili, M.; Shimizu, H.; Saito, S.; Enomoto, A.; Nishijima, F.; Niwa, T. Indoxyl sulfate promotes cardiac fibrosis with enhanced oxidative stress in hypertensive rats. Life Sci. 2013, 92, 1180-1185.
51. Fujii, H.; Nishijima, F.; Goto, S.; Sugano, M.; Yamato, H.; Kitazawa, R.; Kitazawa, S.; Fukagawa, M. Oral charcoal adsorbent (AST-120) prevents progression of cardiac damage in chronic kidney disease through suppression of oxidative stress. Nephrol. Dial. Transplant. 2009, 24, 2089-2095.
52. Yamamoto, S.; Zuo, Y.; Ma, J.; Yancey, P.G.; Hunley, T.E.; Motojima, M.; Fogo, A.B.; Linton, M.F.; Fazio, S.; Ichikawa, I.; et al. Oral activated charcoal adsorbent (AST-120) ameliorates extent and instability of atherosclerosis accelerated by kidney disease in apolipoprotein E-deficient mice. Nephrol. Dial. Transplant. 2011, 26, 2491-2497.
53. Pawlak, K.; Domaniewski, T.; Mysliwiec, M.; Pawlak, D. The kynurenines are associated with oxidative stress, inflammation and the prevalence of cardiovascular disease in patients with end-stage renal disease. Atherosclerosis 2009, 204, 309-314.
54. Darlington, L.G.; Mackay, G.M.; Forrest, C.M.; Stoy, N.; George, C.; Stone, T.W. Altered kynurenine metabolism correlates with infarct volume in stroke. Eur. J. Neurosci. 2007, 26, 2211-2221.
55. Pertovaara, M.; Raitala, A.; Juonala, M.; Lehtimaki, T.; Huhtala, H.; Oja, S.S.; Jokinen, E.; Viikari, J.S.; Raitakari, O.T.; Hurme, M. Indoleamine 2,3-dioxygenase enzyme activity correlates with risk factors for atherosclerosis: The cardiovascular risk in young finns study. Clin. Exp. Immunol. 2007, 148, 106-111.
56. Niinisalo, P.; Raitala, A.; Pertovaara, M.; Oja, S.S.; Lehtimaki, T.; Kahonen, M.; Reunanen, A.; Jula, A.; Moilanen, L.; Kesaniemi, Y.A.; et al. Indoleamine 2,3-dioxygenase activity associates with cardiovascular risk factors: The health 2000 study. Scand. J. Clin. Lab. Invest. 2008, 68, 767-770.
57. Kato, A.; Suzuki, Y.; Suda, T.; Suzuki, M.; Fujie, M.; Takita, T.; Furuhashi, M.; Maruyama, Y.; Chida, K.; Hishida, A. Relationship between an increased serum kynurenine/tryptophan ratio and atherosclerotic parameters in hemodialysis patients. Hemodial. Int. 2010, 14, 418-424.
58. Gokce, N.; Keaney, J.F., Jr.; Hunter, L.M.; Watkins, M.T.; Menzoian, J.O.; Vita, J.A. Risk stratification for postoperative cardiovascular events via noninvasive assessment of endothelial function: A prospective study. Circulation 2002, 105, 1567-1572.
59. Gokce, N.; Keaney, J.F., Jr.; Hunter, L.M.; Watkins, M.T.; Nedeljkovic, Z.S.; Menzoian, J.O.; Vita, J.A. Predictive value of noninvasively determined endothelial dysfunction for long-term cardiovascular events in patients with peripheral vascular disease. J. Am. Coll. Cardiol. 2003, 41, 1769-1775.
60. Kopf, P.G.; Scott, J.A.; Agbor, L.N.; Boberg, J.R.; Elased, K.M.; Huwe, J.K.; Walker, M.K. Cytochrome P4501A1 is required for vascular dysfunction and hypertension induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol. Sci. 2010, 117, 537-546.
61. Perticone, F.; Maio, R.; Tripepi, G.; Zoccali, C. Endothelial dysfunction and mild renal insufficiency in essential hypertension. Circulation 2004, 110, 821-825.
62. Yu, M.; Kim, Y.J.; Kang, D.H. Indoxyl sulfate-induced endothelial dysfunction in patients with chronic kidney disease via an induction of oxidative stress. Clin. J. Am. Soc. Nephrol. 2011, 6, 30-39.
63. Namikoshi, T.; Tomita, N.; Satoh, M.; Sakuta, T.; Kuwabara, A.; Kobayashi, S.; Higuchi, Y.; Nishijima, F.; Kashihara, N. Oral adsorbent AST-120 ameliorates endothelial dysfunction independent of renal function in rats with subtotal nephrectomy. Hypertens. Res. 2009, 32, 194-200.
64. Juan, S.H.; Lee, J.L.; Ho, P.Y.; Lee, Y.H.; Lee, W.S. Antiproliferative and antiangiogenic effects of 3-methylcholanthrene, an aryl-hydrocarbon receptor agonist, in human umbilical vascular endothelial cells. Eur. J. Pharmacol. 2006, 530, 1-8.
65. Andersson, H.; Garscha, U.; Brittebo, E. Effects of PCB126 and 17beta-oestradiol on endothelium-derived vasoactive factors in human endothelial cells. Toxicology 2011, 285, 46-56.
66. Chang, C.C.; Tsai, S.Y.; Lin, H.; Li, H.F.; Lee, Y.H.; Chou, Y.; Jen, C.Y.; Juan, S.H. Aryl-hydrocarbon receptor-dependent alteration of FAK/RhoA in the inhibition of HUVEC motility by 3-methylcholanthrene. Cell. Mol. Life Sci. 2009, 66, 3193-3205.
67. Van Grevenynghe, J.; Monteiro, P.; Gilot, D.; Fest, T.; Fardel, O. Human endothelial progenitors constitute targets for environmental atherogenic polycyclic aromatic hydrocarbons. Biochem. Biophys. Res. Commun. 2006, 341, 763-769.
68. Dou, L.; Bertrand, E.; Cerini, C.; Faure, V.; Sampol, J.; Vanholder, R.; Berland, Y.; Brunet, P. The uremic solutes p-cresol and indoxyl sulfate inhibit endothelial proliferation and wound repair. Kidney Int. 2004, 65, 442-451.
69. Kharait, S.; Haddad, D.J.; Springer, M.L. Nitric oxide counters the inhibitory effects of uremic toxin indoxyl sulfate on endothelial cells by governing ERK MAP kinase and myosin light chain activation. Biochem. Biophys. Res. Commun. 2011, 409, 758-763.
70. Peng, Y.S.; Lin, Y.T.; Chen, Y.; Hung, K.Y.; Wang, S.M. Effects of indoxyl sulfate on adherens junctions of endothelial cells and the underlying signaling mechanism. J. Cell. Biochem. 2012, 113, 1034-1043.
71. Jourde-Chiche, N.; Dou, L.; Sabatier, F.; Calaf, R.; Cerini, C.; Robert, S.; Camoin-Jau, L.; Charpiot, P.; Argiles, A.; Dignat-George, F.; et al. Levels of circulating endothelial progenitor cells are related to uremic toxins and vascular injury in hemodialysis patients. J. Thromb. Haemost. 2009, 7, 1576-1584.
72. Slim, R.; Toborek, M.; Robertson, L.W.; Hennig, B. Antioxidant protection against PCB-mediated endothelial cell activation. Toxicol. Sci. 1999, 52, 232-239.
73. Majkova, Z.; Layne, J.; Sunkara, M.; Morris, A.J.; Toborek, M.; Hennig, B. Omega-3 fatty acid oxidation products prevent vascular endothelial cell activation by coplanar polychlorinated biphenyls. Toxicol. Appl. Pharmacol. 2011, 251, 41-49.
74. Kopf, P.G.; Walker, M.K. 2,3,7,8-tetrachlorodibenzo-p-dioxin increases reactive oxygen species production in human endothelial cells via induction of cytochrome P4501A1. Toxicol. Appl. Pharmacol. 2010, 245, 91-99.
75. Pawlak, K.; Domaniewski, T.; Mysliwiec, M.; Pawlak, D. Kynurenines and oxidative status are independently associated with thrombomodulin and von Willebrand factor levels in patients with end-stage renal disease. Thromb. Res. 2009, 124, 452-457.
76. Itoh, Y.; Ezawa, A.; Kikuchi, K.; Tsuruta, Y.; Niwa, T. Protein-bound uremic toxins in hemodialysis patients measured by liquid chromatography/tandem mass spectrometry and their effects on endothelial ROS production. Anal. Bioanal. Chem. 2012, 403, 1841-1850.
77. Dou, L.; Jourde-Chiche, N.; Faure, V.; Cerini, C.; Berland, Y.; Dignat-George, F.; Brunet, P. The uremic solute indoxyl sulfate induces oxidative stress in endothelial cells. J. Thromb. Haemost. 2007, 5, 1302-1308.
78. Watanabe, I.; Tatebe, J.; Namba, S.; Koizumi, M.; Yamazaki, J.; Morita, T. Activation of aryl hydrocarbon receptor mediates indoxyl sulfate-induced monocyte chemoattractant protein-1 expression in human umbilical vein endothelial cells. Circ. J. 2013, 77, 224-230.
79. Muteliefu, G.; Enomoto, A.; Niwa, T. Indoxyl sulfate promotes proliferation of human aortic smooth muscle cells by inducing oxidative stress. J. Ren. Nutr. 2009, 19, 29-32.
80. Shimizu, H.; Yisireyili, M.; Nishijima, F.; Niwa, T. Stat3 contributes to indoxyl sulfate-induced inflammatory and fibrotic gene expression and cellular senescence. Am. J. Nephrol. 2012, 36, 184-189.
81. Muteliefu, G.; Shimizu, H.; Enomoto, A.; Nishijima, F.; Takahashi, M.; Niwa, T. Indoxyl sulfate promotes vascular smooth muscle cell senescence with upregulation of p53, p21, and prelamin A through oxidative stress. Am. J. Physiol. Cell. Physiol. 2012, 303, C126-C134.
82. Shimizu, H.; Hirose, Y.; Nishijima, F.; Tsubakihara, Y.; Miyazaki, H. ROS and PDGF-beta [corrected] receptors are critically involved in indoxyl sulfate actions that promote vascular smooth muscle cell proliferation and migration. Am. J. Physiol. Cell. Physiol. 2009, 297, C389-C396.
83. Shimizu, H.; Hirose, Y.; Goto, S.; Nishijima, F.; Zrelli, H.; Zghonda, N.; Niwa, T.; Miyazaki, H. Indoxyl sulfate enhances angiotensin II signaling through upregulation of epidermal growth factor receptor expression in vascular smooth muscle cells. Life Sci. 2012, 91, 172-177.
84. Yamamoto, H.; Tsuruoka, S.; Ioka, T.; Ando, H.; Ito, C.; Akimoto, T.; Fujimura, A.; Asano, Y.; Kusano, E. Indoxyl sulfate stimulates proliferation of rat vascular smooth muscle cells. Kidney Int. 2006, 69, 1780-1785.
85. Meng, D.; Lv, D.D.; Zhuang, X.; Sun, H.; Fan, L.; Shi, X.L.; Fang, J. Benzo [a]pyrene induces expression of matrix metalloproteinases and cell migration and invasion of vascular smooth muscle cells. Toxicol. Lett. 2009, 184, 44-49.
86. Kerzee, J.K.; Ramos, K.S. Activation of c-Ha-ras by benzo(a)pyrene in vascular smooth muscle cells involves redox stress and aryl hydrocarbon receptor. Mol. Pharmacol. 2000, 58, 152-158.
87. Knaapen, A.M.; Curfs, D.M.; Pachen, D.M.; Gottschalk, R.W.; de Winther, M.P.; Daemen, M.J.; Van Schooten, F.J. The environmental carcinogen benzo [a]pyrene induces expression of monocyte-chemoattractant protein-1 in vascular tissue: a possible role in atherogenesis. Mutat. Res. 2007, 621, 31-41.
88. Vogel, C.F.; Nishimura, N.; Sciullo, E.; Wong, P.; Li, W.; Matsumura, F. Modulation of the chemokines KC and MCP-1 by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in mice. Arch. Biochem. Biophys. 2007, 461, 169-175.
89. Vorderstrasse, B.A.; Kerkvliet, N.I. 2,3,7,8-Tetrachlorodibenzo-p-dioxin affects the number and function of murine splenic dendritic cells and their expression of accessory molecules. Toxicol. Appl. Pharmacol. 2001, 171, 117-125.
90. Kimura, A.; Naka, T.; Nohara, K.; Fujii-Kuriyama, Y.; Kishimoto, T. Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc. Natl. Acad. Sci. USA 2008, 105, 9721-9726.
91. Choi, W.; Eum, S.Y.; Lee, Y.W.; Hennig, B.; Robertson, L.W.; Toborek, M. PCB 104-induced proinflammatory reactions in human vascular endothelial cells: Relationship to cancer metastasis and atherogenesis. Toxicol. Sci. 2003, 75, 47-56.
92. Han, S.G.; Eum, S.Y.; Toborek, M.; Smart, E.; Hennig, B. Polychlorinated biphenyl-induced VCAM-1 expression is attenuated in aortic endothelial cells isolated from caveolin-1 deficient mice. Toxicol. Appl. Pharmacol. 2010, 246, 74-82.
93. Majkova, Z.; Smart, E.; Toborek, M.; Hennig, B. Up-regulation of endothelial monocyte chemoattractant protein-1 by coplanar PCB77 is caveolin-1-dependent. Toxicol. Appl. Pharmacol. 2009, 237, 1-7.
94. Choi, Y.J.; Arzuaga, X.; Kluemper, C.T.; Caraballo, A.; Toborek, M.; Hennig, B. Quercetin blocks caveolae-dependent pro-inflammatory responses induced by co-planar PCBs. Environ. Int. 2010, 36, 931-934.
95. Oesterling, E.; Toborek, M.; Hennig, B. Benzo [a]pyrene induces intercellular adhesion molecule-1 through a caveolae and aryl hydrocarbon receptor mediated pathway. Toxicol. Appl. Pharmacol. 2008, 232, 309-316.
96. Mezrich, J.D.; Fechner, J.H.; Zhang, X.; Johnson, B.P.; Burlingham, W.J.; Bradfield, C.A. An interaction between kynurenine and the aryl hydrocarbon receptor can generate regulatory T cells. J. Immunol. 2010, 185, 3190-3198.
97. Lekawanvijit, S.; Adrahtas, A.; Kelly, D.J.; Kompa, A.R.; Wang, B.H.; Krum, H. Does indoxyl sulfate, a uraemic toxin, have direct effects on cardiac fibroblasts and myocytes? Eur. Heart J. 2010, 31, 1771-1779.
98. Ito, S.; Higuchi, Y.; Yagi, Y.; Nishijima, F.; Yamato, H.; Ishii, H.; Osaka, M.; Yoshida, M. Reduction of indoxyl sulfate by AST-120 attenuates monocyte inflammation related to chronic kidney disease. J. Leukoc Biol. 2013, 93, 837-845.
99. Ito, S.; Osaka, M.; Higuchi, Y.; Nishijima, F.; Ishii, H.; Yoshida, M. Indoxyl sulfate induces leukocyte-endothelial interactions through up-regulation of E-selectin. J. Biol. Chem. 2010, 285, 38869-38875.
100. Lee, C.T.; Lee, Y.T.; Ng, H.Y.; Chiou, T.T.; Cheng, C.I.; Kuo, C.C.; Wu, C.H.; Chi, P.J.; Lee, W.C. Lack of modulatory effect of simvastatin on indoxyl sulfate-induced activation of cultured endothelial cells. Life Sci. 2012, 90, 47-53.
101. Tumur, Z.; Shimizu, H.; Enomoto, A.; Miyazaki, H.; Niwa, T. Indoxyl sulfate upregulates expression of ICAM-1 and MCP-1 by oxidative stress-induced NF-kappaB activation. Am. J. Nephrol. 2010, 31, 435-441.
102. Masai, N.; Tatebe, J.; Yoshino, G.; Morita, T. Indoxyl sulfate stimulates monocyte chemoattractant protein-1 expression in human umbilical vein endothelial cells by inducing oxidative stress through activation of the NADPH oxidase-nuclear factor-kappaB pathway. Circ. J. 2010, 74, 2216-2224.
103. Dou, L.; Sallee, M. Aix Marseille Université, France, Unpublished work, 2014.
104. Lin, C.J.; Pan, C.F.; Liu, H.L.; Chuang, C.K.; Jayakumar, T.; Wang, T.J.; Chen, H.H.; Wu, C.J. The role of protein-bound uremic toxins on peripheral artery disease and vascular access failure in patients on hemodialysis. Atherosclerosis 2012, 225, 173-179.
105. Chitalia, V.C.; Shivanna, S.; Martorell, J.; Balcells, M.; Bosch, I.; Kolandaivelu, K.; Edelman, E.R. Uremic serum and solutes increase post-vascular interventional thrombotic risk through altered stability of smooth muscle cell tissue factor. Circulation 2013, 127, 365-376.
106. Ohtake, F.; Baba, A.; Takada, I.; Okada, M.; Iwasaki, K.; Miki, H.; Takahashi, S.; Kouzmenko, A.; Nohara, K.; Chiba, T.; et al. Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 2007, 446, 562-566.
107. Kopec, A.K.; Burgoon, L.D.; Ibrahim-Aibo, D.; Burg, A.R.; Lee, A.W.; Tashiro, C.; Potter, D.; Sharratt, B.; Harkema, J.R.; Rowlands, J.C.; et al. Automated dose-response analysis and comparative toxicogenomic evaluation of the hepatic effects elicited by TCDD, TCDF, and PCB126 in C57BL/6 mice. Toxicol. Sci. 2010, 118, 286-297.
108. Li, W.; Matsumura, F. Significance of the nongenomic, inflammatory pathway in mediating the toxic action of TCDD to induce rapid and long-term cellular responses in 3T3-L1 adipocytes. Biochemistry 2008, 47, 13997-14008.