From the gastrointestinal tract (GIT) to the Kidneys: Live bacterial cultures (probiotics) mediating reductions of uremic toxin levels via free radical signaling

Toxins

Volumn 5, Issue 11, 2013, Pages 2042-2057

  Vitetta, Luis ^a,b   Linnane, Anthony W ^b,c   Gobe, Glenda C ^a,d  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b Medlab   (Australia)

^c MONASH UNIVERSITY   (Australia)

^d PRINCESS ALEXANDRA HOSPITAL   (Australia)

Author keywords

Chronic kidney disease; Commensal bacteria; Probiotics; Reactive oxygen species (ROS); Toxins; Uremia

Indexed keywords

ASCORBIC ACID; FREE RADICAL; HYDROGEN PEROXIDE; INULIN; PREBIOTIC AGENT; PROBIOTIC AGENT; REACTIVE OXYGEN METABOLITE; UREMIC TOXIN;

ADAPTATION; ANTIOXIDANT ACTIVITY; BACTERIUM CULTURE; CHRONIC KIDNEY DISEASE; CLINICAL TRIAL (TOPIC); COMMENSAL; DIET SUPPLEMENTATION; DISEASE ASSOCIATION; DRUG DOSE ESCALATION; DRUG TARGETING; HUMAN; INTESTINE EPITHELIUM; INTESTINE FLORA; INTRACELLULAR SIGNALING; KINESIOTHERAPY; LIFESTYLE MODIFICATION; METABOLOMICS; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PHASE 1 CLINICAL TRIAL (TOPIC); PHASE 2 CLINICAL TRIAL (TOPIC); REVIEW; SIGNAL TRANSDUCTION; UREMIA;

ANIMALS; GASTROINTESTINAL TRACT; HUMANS; KIDNEY; METABOLOME; PREBIOTICS; PROBIOTICS; REACTIVE OXYGEN SPECIES; RENAL INSUFFICIENCY, CHRONIC; SIGNAL TRANSDUCTION; TOXINS, BIOLOGICAL; UREMIA;

EID: 84887570558     PISSN: 20726651     EISSN: None     Source Type: Journal    
DOI: 10.3390/toxins5112042     Document Type: Review

References (73)

1. Wen, C.P.; Cheng, T.Y.; Tsai, M.K.; Chang, Y.C.; Chan, H.T.; Tsai, S.P.; Chiang, P.H.; Hsu, C.C.; Sung, P.K.; Hsu, Y.H.; et al. All-cause mortality attributable to chronic kidney disease: A prospective cohort study based on 462 293 adults in Taiwan. Lancet 2008, 371, 2173-2182.
2. Vitetta, L.; Gobe, G. Uremia and chronic kidney disease: The role of the gut microflora and therapies with pro-and prebiotics. Mol. Nutr. Food Res. 2013, 57, 824-832.
3. Wu, G.D.; Chen, J.; Hoffmann, C.; Bittinger, K.; Chen, Y.-Y.; Keilbaugh, S.A.; Bewtra, M.; Knights, D.; Walters, W.A.; et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 2011, 334, 105-108.
4. Arumugam, M.; Raes, J.; Pelletier, E.; Le Paslier, D.; Yamada, T.; Mende, D.R.; Fernandes, G.R.; Tap, J.; Bruls, T.; Batto, J.-M.; et al. Enterotypes of the human gut microbiome. Nature 2011, 473, 174-180.
5. Vitetta, L.; Alford, H. The pharmacobiotic potential of the gastrointestinal tract micro-biometabolome-probiotic connect: A brief commentary. Drug Dev. Res. 2013, 74, 353-359.
6. Zheng, X.; Zhao, A.; Xie, G.; Chi, Y.; Zhao, L.; Li, H.; Wang, C.; Bao, Y.; Jia, W.; Luther, M.; et al. Melamine-induced renal toxicity is mediated by the gut microbiota. Sci. Transl. Med. 2013, 5, 172ra22.
7. Fasano, A. Toxins and the gut: Role in human disease. Gut 2002, 50(Suppl. 3), III9-III14.
8. Bengmark, S. Gut microbiota, immune development and function. Pharmacol. Res. 2013, 69, 87-113.
9. Stecher, B.; Maier, L.; Hardt, W.D. 'Blooming' in the gut: How dysbiosis might contribute to pathogen evolution. Nat. Rev. Microbiol. 2013, 11, 277-284.
10. Cani, P.D.; Delzenne, N.M. Gut microflora as a target for energy and metabolic homeostasis. Curr. Opin. Clin. Nutr. Metab. Care 2007, 10, 729-734.
11. Macfarlane, G.T.; Macfarlane, S. Bacteria, colonic fermentation, and gastrointestinal health. J. AOAC Int. 2012, 95, 50-60.
12. 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.
13. Duranton, F.; Cohen, G.; De Smet, R.; Rodriguez, M.; Jankowski, J.; Vanholder, R.; Argiles, A.; European Uremic Toxin Work Group. Normal and pathologic concentrations of uremic toxins. J. Am. Soc. Nephrol. 2012, 23, 1258-1270.
14. Charney, D.I.; Walton, D.F.; Cheung, A.K. Atherosclerosis in chronic renal failure. Curr. Opin. Nephrol. Hypertens. 1993, 2, 876-882.
15. Schepers, E.; Meert, N.; Glorieux, G.; Goeman, J.; Van der Eycken, J.; Vanholder, R. P-cresylsulphate, the main in vivo metabolite of p-cresol, activates leucocyte free radical production. Nephrol. Dial. Transplant. 2007, 22, 592-596.
16. Motojima, M.; Hosokawa, A.; Yamato, H.; Muraki, T.; Yoshioka, T. Uremic toxins of organic anions up-regulate PAI-1 expression by induction of NF-kappaB and free radical in proximal tubular cells. Kidney Int. 2003, 63, 1671-1680.
17. Dou, L.; Bertrand, E.; Cerini, C.; Faure, V.; Sampol, J.; Vanholder, R.; Berland, Y.; Brunet, P. The uremic solutes p-cresol and indoxylsulfate inhibit endothelial proliferation and wound repair. Kidney Int. 2004, 65, 442-451.
18. Vitetta, L.; Briskey, D.; Hayes, E.; Shing, C.; Peake, J. A review of the pharmacobiotic regulation of gastrointestinal inflammation by probiotics, commensal bacteria and prebiotics. Inflammopharmacology 2013, 20, 251-266.
19. Anders, H.J.; Andersen, K.; Stecher, B. The intestinal microbiota, a leaky gut, and abnormal immunity in kidney disease. Kidney Int. 2013, 83, 1010-1016.
20. Hida, M.; Aiba, Y.; Sawamura, S.; Suzuki, N.; Satoh, T.; Koga, Y. Inhibition of the accumulation of uremic toxins in the blood and their precursors in the feces after oral administration of lebenin, a lactic acid bacteria preparation, to uremic patients undergoing hemodialysis. Nephron 1996, 74, 349-355.
21. Wang, C.P.; Lu, L.F.; Yu, T.H.; Hung, W.C.; Chiu, C.A.; Chung, F.M.; Yeh, L.R.; Chen, H.J.; Lee, Y.J.; Houng, J.Y. Serum levels of total p-cresylsulphate are associated with angiographic coronary atherosclerosis severity in stable angina patients with early stage of renal failure. Atherosclerosis 2010, 211, 579-583.
22. Massy, Z.A.; Barreto, D.V.; Barreto, F.C.; Vanholder, R. Uraemic toxins for consideration by the cardiologist-Beyond traditional and non-traditional cardiovascular risk factors. Atherosclerosis 2010, 211, 381-383.
23. Hoy, W.E. Markers for cardiovascular and renal morbidity: Expectations for an intervention program in an Australian aboriginal community. Clin. Exp. Pharmacol. Physiol. 1996, 23(Suppl. 1), S33-S37.
24. Fuller, R. Probiotics in man and animals. J. Appl. Bacteriol. 1989, 66, 365-378.
25. Timmerman, H.M.; Koning, C.J.; Mulder, L.; Rombouts, F.M.; Beynen, A.C. Monostrain, multistrain and multispecies probiotics-A comparison of functionality and efficacy. Int. J. Food Microbiol. 2004, 96, 219-233.
26. Vitetta, L.; Sali, A. Probiotics, prebiotics and gastrointestinal health. Med. Today 2008, 9, 65-70.
27. Borges, S.; Barbosa, J.; Silva, J.; Teixeira, P. Evaluation of characteristics of Pediococcus spp. to be used as a vaginal probiotic. J. Appl. Microbiol. 2013, 115, 527-538.
28. Vaziri, N.D.; Yuan, J.; Nazertehrani, S.; Ni, Z.; Liu, S. Chronic kidney disease causes disruption of gastric and small intestinal epithelial tight junction. Am. J. Nephrol. 2013, 38, 99-103.
29. Himmelfarb, J.; Stenvinkel, P.; Ikizler, T.A.; Hakim, R.M. The elephant in uremia: Oxidant stress as a unifying concept of cardiovascular disease in uremia. Kidney Int. 2002, 62, 1524-1538.
30. Terawaki, H.; Yoshimura, K.; Hasegawa, T.; Matsuyama, Y.; Negawa, T.; Yamada, K.; Matsushima, M.; Nakayama, M.; Hosoya, T.; Era, S. Oxidative stress is enhanced in correlation with renal dysfunction: examination with the redox state of albumin. Kidney Int. 2004, 66, 1988-1993.
31. Rutkowski, P.; Słominska, E.M.; Szołkiewicz, M.; Aleksandrowicz, E.; Smolenski, R.T.; Wołyniec, W.; Renke, M.; Wisterowicz, K.; Swierczynski, J.; Rutkowski, B. Relationship between uremic toxins and oxidative stress in patients with chronic renal failure. Scand J. Urol. Nephrol. 2007, 41, 243-248.
32. Chiang, C.K.; Tanaka, T.; Nangaku, M. Dysregulated oxygen metabolism of the kidney by uremic toxins: Review. J. Ren. Nutr. 2012, 22, 77-80.
33. Dounousi, E.; Papavasiliou, E.; Makedou, A.; Ioannou, K.; Katopodis, K.P.; Tselepis, A.; Siamopoulos, K.C.; Tsakiris, D. Oxidative stress is progressively enhanced with advancing stages of CKD. Am. J. Kidney Dis. 2006, 48, 752-760.
34. Cicek, M.; Yi{dotless}ldi{dotless}ri{dotless}r, A.; Okyay, K.; Yazici, A.C.; Aydinalp, A.; Kanyilmaz, S.; Muderrisoglu, H. Use of alpha-lipoic acid in prevention of contrast-induced nephropathy in diabetic patients. Ren. Fail. 2013, 35, 748-753.
35. Jun, M. Antioxidants for chronic kidney disease. Nephrology Carlton 2013, 18, 576-578.
36. Linnane, A.W.; Kios, M.; Vitetta, L. Healthy aging: Regulation of the metabolome by cellular redox modulation and prooxidant signaling systems: The essential roles of superoxide anion and hydrogen peroxide. Biogerontology 2007, 8, 445-467.
37. Simenhoff, M.L.; Dunn, S.R.; Zollner, G.P.; Fitzpatrick, M.E.; Emery, S.M.; Sandine, W.E.; Ayres, J.W. Biomodulation of the toxic and nutritional effects of small bowel bacterial overgrowth in end-stage kidney disease using freeze-dried Lactobacillus acidophilus. Min. Electrolyte Metab. 1996, 22, 92-96.
38. Ranganathan, N.; Friedman, E.A.; Tam, P.; Rao, V.; Ranganathan, P.; Dheer, R. Probiotic dietary supplementation in patients with stage 3 and 4 chronic kidney disease: A 6-month pilot scale trial in Canada. Curr. Med. Res. Opin. 2009, 25, 1919-1930.
39. Ranganathan, N.; Ranganathan, P.; Friedman, E.A.; Joseph, A.; Delano, B.; Goldfarb, D.S.; Tam, P.; Rao, A.V.; Anteyi, E.; Musso, C.G. Pilot study of probiotic dietary supplementation for promoting healthy kidney function in patients with chronic kidney disease. Adv. Ther. 2010, 27, 634-647.
40. Meijers, B.K.; De Preter, V.; Verbeke, K.; Vanrenterghem, Y.; Evenepoel, P. P-cresyl sulfate serum concentrations in haemodialysis patients are reduced by the prebiotic oligofructose-enriched inulin. Nephrol. Dial. Transplant. 2010, 25, 219-224.
41. Nakabayashi, I.; Nakamura, M.; Kawakami, K.; Ohta, T.; Kato, I.; Uchida, K.; Yoshida, M. Effects of synbiotic treatment on serum level of p-cresol in haemodialysis patients: A preliminary study. Nephrol. Dial. Transplant. 2011, 26, 1094-1098.
42. Yin, D.; Sun, H.; Weaver, R.F.; Squier, T.C. Nonessential role for methionines in the productive association between calmodulin and the plasma membrane Ca-ATPase. Biochemistry 1999, 38, 13654-13660.
43. 2 modulates the ability to activate the plasma membrane Ca-ATPase. Chem. Res. Toxicol. 2000, 13, 103-110.
44. Sun, H.; Gao, J.; Ferrington, D.A.; Biesiada, H.; Williams, T.D.; Squier, T.C. Repair of oxidized calmodulin by methionine sulfoxide reductase restores ability to activate the plasma membrane Ca-ATPase. Biochemistry 1999, 38, 105-112.
45. Stolze, I.P.; Mole, D.R.; Ratcliffe, P.J. Regulation of HIF: Prolyl hydroxylases. Novartis Found Symp. 2006, 272, 15-25.
46. Bota, D.A.; Van Remmen, H.; Davies, K.J. Modulation of Lon protease activity and aconitase turnover during aging and oxidative stress. FEBS Lett. 2002, 532, 103-106.
47. Bota, D.A.; Ngo, J.K.; Davies, K.J. Down regulation of the human Lon protease impairs mitochondrial structure and function and causes cell death. Free Radic. Biol. Med. 2005, 38, 665-677.
48. Singel, D.J.; Stamler, J.S. Chemical physiology of blood flow regulation by red blood cells: The role of nitric oxide and S-nitrohemoglobin. Ann. Rev. Physiol. 2005, 67, 99-145.
49. Farout, L.; Friguet, B. Proteasome function in aging and oxidative stress: Implications in protein maintenance failure. Antioxid. Redox Signal 2006, 8, 205-216.
50. Meiners, S.; Heyken, D.; Weller, A.; Ludwig, A.; Stangl, K.; Kloetzel, P.M.; Kruger, E. Inhibition of proteasome induces concerted expression of proteasome genes and de novo formation of mammalian proteasomes. J. Biol. Chem. 2003, 278, 21517-21525.
51. Husom, A.D.; Peters, E.A.; Kolling, E.A.; Fugere, N.A.; Thompson, L.V.; Ferrington, D.A. Altered proteasome function and subunit composition in aged muscle. Arch. Biochem. Biophys. 2004, 421, 67-76
52. Hornig, D. Distribution of ascorbic acid, metabolites and analogues in man and animals. Ann. N. Y. Acad. Sci. 1975, 258, 103-118
53. Bailey, D.M.; Raman, S.; McEnery, J.; Young, I.S.; Parham, K.L.; Hullin, D.A.; Davies, B.; McKeeman, G.; McCord, J.M.; Lewis, M.H. Vitamin C prophylaxis promotes oxidative lipid damage during surgical ischemia-reperfusion. Free Radic. Biol. Med. 2006, 40, 591-600.
54. Chen, Q.; Espey, M.G.; Krishna, M.C.; Mitchell, J.B.; Corpe, C.P.; Buettner, G.R.; Shacter, E.; Levine, M. Pharmacologic ascorbic acid concentrations selectively kill cancer cells: Action as a pro-drug to deliver hydrogen peroxide to tissues. Proc. Natl. Acad. Sci. USA 2005, 102, 13604-13609.
55. Vaziri, N.D.; Yuan, J.; Rahimi, A.; Ni, Z.; Said, H.; Subramanian, V.S. Disintegration of colonic epithelial tight junction in uremia: A likely cause of CKD-associated inflammation. Nephrol. Dial. Transplant. 2012, 27, 2686-2693.
56. Vinik, A. The question is, my dear watson, why did the dog not bark? The joslin 50-year medalist study. Diabetes Care 2011, 34, 1060-1063.
57. Bermudez-Brito, M.; Plaza-Diaz, J.; Munoz-Quezada, S.; Gomez-Llorente, C.; Gil, A. Probiotic mechanisms of action. Ann. Nutr. Metab. 2012, 61, 160-174.
58. Neish, A.S. Redox signaling mediated by the gut microbiota. Free Radic. Res. 2013, 47, 950-957.
59. Lin, P.W.; Myers, L.E.; Ray, L.; Song, S.C.; Nasr, T.R.; Berardinelli, A.J.; Kundu, K.; Murthy, N.; Hansen, J.M.; Neish, A.S. Lactobacillus rhamnosus blocks inflammatory signaling in vivo via reactive oxygen species generation. Free Radic. Biol. Med. 2009, 47, 1205-1211.
60. Lee, W.J. Bacterial-modulated signaling pathways in gut homeostasis. Sci. Signal 2008, 1, pe24
61. Yan, F.; Cao, H.; Cover, T.L.; Whitehead, R.; Washington, M.K.; Polk, D.B. Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 2007, 132, 562-575.
62. Patel, R.M.; Myers, L.S.; Kurundkar, A.R.; Maheshwari, A.; Nusrat, A.; Lin, P.W. Probiotic bacteria induce maturation of intestinal claudin 3 expression and barrier function. Am. J. Pathol. 2012, 180, 626-635.
63. Collier-Hyams, L.S.; Sloane, V.; Batten, B.C.; Neish, A.S. Cutting Edge: Bacterial Modulation of Epithelial Signaling via Changes in Neddylation of Cullin-1. J. Immunol. 2005, 175, 4194-4198.
64. Neish, A.S.; Gewirtz, A.T.; Zeng, H.; Young, A.N.; Hobert, M.E.; Karmali, V.; Rao, A.S.; Madara, J.L. Prokaryotic regulation of epithelial responses by inhibition of Ikappa B-alpha ubiquitination. Science 2000, 289, 1560-1563.
65. Kotchoni, S.O.; Gachomo, E.W. The reactive oxygen species network pathways: An essential prerequisite for perception of pathogen attack and the acquired disease resistance in plants. J. Biosci. 2006, 31, 389-404.
66. Ha, E.M.; Oh, C.T.; Ryu, J.H.; Bae, Y.S.; Kang, S.W.; Jang, I.H.; Brey, P.T.; Lee, W.J. An antioxidant system required for host protection against gut infection in Drosophila. Dev. Cell. 2005, 8, 125-132.
67. Circu, M.L.; Aw, T.Y. Redox biology of the intestine. Free Radic. Res. 2011, 45, 1245-1266.
68. Buchon, N.; Broderick, N.A.; Lemaitre, B. Gut homeostasis in a microbial world: Insights from Drosophila melanogaster. Nat. Rev. Microbiol. 2013, 1611, 615-626.
69. 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.
70. Vaziri, N.D. Role of dyslipidemia in impairment of energy metabolism, oxidative stress, inflammation and cardiovascular disease in chronic kidney disease. Clin. Exp. Nephrol. 2013, 24, doi: 10.1007/s10157-013-0847-z.
71. Di Cerbo, A.; Pezzuto, F.; Palmieri, L.; Rottigni, V.; Iannitti, T.; Palmieri, B. Clinical and experimental use of probiotic formulations for management of end-stage renal disease: An update. Int. Urol. Nephrol. 2013, 13, doi:10.1007/s11255-012-0335-5.
72. Howden, E.J.; Leano, R.; Petchey, W.; Coombes, J.S.; Isbel, N.M.; Marwick, T.H. Effects of exercise and lifestyle intervention on cardiovascular function in CKD. Clin. J. Am. Soc. Nephrol. 2013, 8, 1494-1501.
73. Mehal, W.Z. The Gordian Knot of dysbiosis, obesity and NAFLD. Nat. Rev. Gastroenterol. Hepatol. 2013, doi:10.1038/nrgastro.2013.146.