Sialic acid rescues repurified lipopolysaccharide-induced acute renal failure via inhibiting TLR4/PKC/gp91-mediated endoplasmic reticulum stress, apoptosis, autophagy, and pyroptosis signaling

Toxicological Sciences

Volumn 141, Issue 1, 2014, Pages 155-165

  Yang, Chih Ching ^b,c   Yao, Chien An ^c   Yang, Jyh Chin ^d   Chien, Chiang Ting ^a  

^a Ministry of Health and Welfare   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^d NATIONAL TAIWAN NORMAL UNIVERSITY   (Taiwan)

Author keywords

Apoptosis; Autophagy; Lipopolysaccharide; Pyroptosis; Reactive oxygen species; Sialic acid; Toll like receptors

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ALBUMIN; AUTOPHAGY PROTEIN 12; AUTOPHAGY PROTEIN 5; BECLIN 1; BIOLOGICAL MARKER; FAS ASSOCIATED DEATH DOMAIN PROTEIN; GAMMA INTERFERON; GLUCOSE REGULATED PROTEIN 78; GLYCOPROTEIN GP 91; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LC3 II PROTEIN; LIPOPOLYSACCHARIDE; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN BAX; PROTEIN IRE1; PROTEIN KINASE C ALPHA; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SIALIC ACID; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; ATG5 PROTEIN, RAT; CYBB PROTEIN, RAT; ENDOTOXIN; ENDOTOXIN, ESCHERICHIA COLI; MEMBRANE PROTEIN; N ACETYLNEURAMINIC ACID; PROTEIN; TLR4 PROTEIN, RAT;

ACUTE KIDNEY FAILURE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTERIAL PRESSURE; ARTICLE; AUTOPHAGY; BINDING AFFINITY; BLOOD FLOW; CELL INFILTRATION; CONTROLLED STUDY; DOSE TIME EFFECT RELATION; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; FEMALE; HEMODYNAMICS; HISTOPATHOLOGY; INTRACELLULAR SIGNALING; KIDNEY FUNCTION; KIDNEY PROXIMAL TUBULE; MICROCIRCULATION; NEPHROTOXICITY; NONHUMAN; RAT; RENAL PROTECTION; VASCULAR RESISTANCE; ACUTE KIDNEY INJURY; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; GENETICS; INTRAVENOUS DRUG ADMINISTRATION; METABOLISM; PATHOLOGY; TIME; WESTERN BLOTTING; WISTAR RAT;

ACUTE KIDNEY INJURY; ANIMALS; APOPTOSIS; AUTOPHAGY; BLOTTING, WESTERN; ENDOPLASMIC RETICULUM STRESS; ENDOTOXINS; FEMALE; INJECTIONS, INTRAVENOUS; MEMBRANE GLYCOPROTEINS; N-ACETYLNEURAMINIC ACID; NADPH OXIDASE; PROTEIN KINASE C-ALPHA; PROTEINS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; TIME FACTORS; TOLL-LIKE RECEPTOR 4;

EID: 84913611594     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu121     Document Type: Article

References (50)

1. Angus, D. C., Linde-Zwirble, W. T., Lidicker, J., Clermont, G., Carcillo, J. and Pinsky,M. R. (2001). Epidemiology of severe sepsis in the United States: Analysis of incidence, outcome, and associated costs of care. Crit. Care Med. 29, 1303-1310.
2. Azuma, Y., Higurashi, K. and Matsumoto, K. (2007). Immobilized alpha2,6-linked sialic acid suppresses caspase-3 activation during anti-IgM antibody-induced apoptosis in Ramos cells. Biochim. Biophys. Acta 1770, 279-285.
3. Bannan, J., Visvanathan, K. and Zabriskie, J. B. (1999). Structure and function of streptococcal and staphylococcal superantigens in septic shock. Infect. Dis. Clin. North Am. 13, 387-396.
4. Bhattacharyya, J., Biswas, S. and Datta, A. G. (2004). Mode of action of endotoxin: Role of free radicals and antioxidants. Curr. Med. Chem. 11, 359-368.
5. Bortoluci, K. R. and Medzhitov, R. (2010). Control of infection by pyroptosis and autophagy: Role of TLR and NLR. Cell. Mol. Life Sci. 67, 1643-1651.
6. Bosshart, H. and Heinzelmann, M. (2007). Targeting bacterial endotoxin: Two sides of a coin. Ann. N. Y. Acad. Sci. 1096, 1-17.
7. Chien, C. T., Lee, P. H., Chen, C. F., Ma, M. C., Lai, M. K. and Hsu, S. M. (2001). De novo demonstration and co-localization of free-radical production and apoptosis formation in rat kidney subjected to ischemia/reperfusion. J. Am. Soc. Nephrol. 12, 973-982.
8. Chung, S. D., Lai, T. Y., Chien, C. T. and Yu, H. J. (2012). Activating nrf-2 signaling depresses unilateral ureteral obstructionevoked mitochondrial stress-related autophagy, apoptosis and pyroptosis in kidney. PLoS One 7, e47299.
9. Codogno, P. andMeijer, A. J. (2006) Atg5: More than an autophagy factor. Nat. Cell Biol. 8, 1045-1047.
10. Cullen, T. W., Giles, D. K., Wolf, L. N., Ecobichon, C., Boneca, I. G. and Trent, M. S. (2011). Helicobacter pylori versus the host: Remodeling of the bacterial outer membrane is required for survival in the gastric mucosa. PLoS Pathog. 7, e1002454.
11. Dalpke, A. H. and Heeg, K. (2003). Synergistic and antagonistic interactions between LPS and superantigens. J. Endotoxin Res. 9, 51-54.
12. Danner, R. L., Joiner, K. A., Rubin, M., Patterson, W. H., Johnson, N., Ayers, K. M. and Parrillo, J. E. (1989). Purification, toxicity, and antiendotoxin activity of polymyxin B nonapeptide. Antimicrob. Agents Chemother. 33, 1428-1434.
13. Drake, A. W., Tang, M. L., Papalia, G. A., Landes, G., Haak- Frendscho, M. and Klakamp, S. L. (2012). Biacore surface matrix effects on the binding kinetics and affinity of an antigen/antibody complex. Analyt. Biochem. 429, 58-69.
14. Fink, S. L. and Cookson, B. T. (2005). Apoptosis, pyroptosis, and necrosis: Mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 73, 1907-1916.
15. Fink, S. L. and Cookson, B. T. (2007). Pyroptosis and host cell death responses during Salmonella infection. Cell Microbiol. 9, 2562-2570.
16. Forbes,M. S., Thornhill, B. A., Minor, J. J., Gordon, K. A., Galarreta, C. I. and Chevalier, R. L. (2012) Fight-or-flight: Murine unilateral ureteral obstruction causes extensive proximal tubular degeneration, collecting duct dilatation, and minimal fibrosis. Am. J. Physiol. Renal Physiol. 303, F120-129.
17. Gallay, P., Heumann, D., Le Roy, D., Barras, C. and Glauser, M. P. (1994). Mode of action of anti-lipopolysaccaride-binding protein antibodies for prevention of endotoxemic shock in mice. Proc. Natl. Acad. Sci. U.S.A. 91, 7922-7926.
18. Hamann, L., Stammec, C., Ulmera, A. J. and Schumann, R. R. (2002). Inhibition of LPS-induced activation of alveolar macrophages by high concentrations of LPS-binding protein. Biochem. Biophys. Res. Commun. 295, 553-560.
19. Heine, H., Rietschel, E. T. and Ulmer, A. J. (2001). The biology of endotoxin. Mol. Biotechnol. 19, 279-296.
20. Hetz, C (2012). The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13, 89-102.
21. Hirschfeld, M., Ma, Y., Weis, J. H., Vogel, S. N. and Weis, J. J. (2000). Cutting edge: Repurification of lipopolysaccharide eliminates signaling through both human and murine tolllike receptor 2. J. Immunol. 165, 618-622.
22. Ho, C. H., Hsu, S. P., Yang, C. C., Lee, Y. H. and Chien, C. T. (2009). Sialic acid reduces acute endotoxemia-induced liver dysfunction in the rat. Shock 32, 228-235.
23. Hotchkiss, R. S. and Karl, I. E. (2003). The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348, 138-150.
24. Howell, G. M., Gomez, H., Collage, R. D., Loughran, P., Zhang, X., Escobar, D. A., Billiar, T. R., Zuckerbraun, B. S. and Rosengart, M. R. (2013). Augmenting autophagy to treat acute kidney injury during endotoxemia in mice. PLoS One 8, e69520.
25. Hsiao, H. W., Tsai, K. L., Wang, L. F., Chen, Y. H., Chiang, P. C., Chuang, S. M. and Hsu, C. (2012). The decline of autophagy contributes to proximal tubular dysfunction during sepsis. Shock 37, 289-296.
26. Jiang, M., Wei, Q., Dong, G., Komatsu, M., Su, Y. and Dong, Z. (2012). Autophagy in proximal tubules protects against acute kidney injury. Kidney Int. 82, 1271-1283.
27. Kimura, T., Takabatake, Y., Takahashi, A., Kaimori, J. Y., Matsui, I., Namba, T., Kitamura, H., Niimura, F., Matsusaka, T., Soga, T., et al. (2011). Autophagy protects the proximal tubule from degeneration and acute ischemic injury. J. Am. Soc. Nephrol. 22, 902-913.
28. Kong, X., Thimmulappa, R., Kombairaju, P. and Biswal, S. (2010). NADPH oxidase-dependent reactive oxygen species mediate amplified TLR4 signaling and sepsis-induced mortality in Nrf2-deficient mice. J. Immunol. 185, 569-577.
29. Levy, O. and Elsbach, P. (2001). Bactericidal/permeabilityincreasing protein in host defense and its efficacy in the treatment of bacterial sepsis. Curr. Infect. Dis. Rep. 3, 407-412.
30. Miao, E. A., Rajan, J. V. and Aderem, A. (2011). Caspase-1-induced pyroptotic cell death. Immunol. Rev. 243, 206-214.
31. Oberholzer, C., Oberholzer, A., Clare-Salzler, M. and Moldawer, L. L. (2001). Apoptosis in sepsis: A new target for therapeutic exploration. FASEB J. 15, 879-892.
32. Orrenius, S., Nicotera, P. and Zhivotovsky, B. (2011). Cell death mechanisms and their implications in toxicology. Toxicol. Sci. 119, 3-19.
33. Schauer, R. and Kamerling, J. P. (1997). Chemistry, biochemistry and biology of sialic acids. In Glycoproteins II (J. Montreuil, J. F. G. Vliegenthart and H. Schachter, Eds.), pp. 241-400. Elsevier, Amsterdam.
34. Schwandner, R., Dziarski, R.,Wesche, H., Rothe, M. and Kirschning, C. J. (1999). Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by toll-like receptor 2. J. Biol. Chem. 274, 17406-17409.
35. Shah, N., Dhar, D., El Zahraa Mohammed, F., Habtesion, A., Davies, N. A., Jover-Cobos, M., Macnaughtan, J., Sharma, V., Olde Damink, S. W., Mookerjee, R. P., et al. (2012). Prevention of acute kidney injury in a rodent model of cirrhosis following selective gut decontamination is associated with reduced renal TLR4 expression. J. Hepatol. 56, 1047-1053.
36. Sumimoto, H., Miyano, K. and Takeya, R. (2005). Molecular composition and regulation of the Nox family NAD(P)H oxidases. Biochem. Biophys. Res. Commun. 338, 677-686.
37. Takahashi, A., Kimura, T., Takabatake, Y., Namba, T., Kaimori, J., Kitamura, H., Matsui, I., Niimura, F., Matsusaka, T., Fujita, N., Yoshimori, T., Isaka, Y. and Rakugi, H. (2012). Autophagy guards against cisplatin-induced acute kidney injury. Am. J. Pathol. 180, 517-525.
38. Takeuchi, O. and Akira, S. (2010). Pattern recognition receptors and inflammation. Cell 140, 805-820.
39. Taylor, D. E., Ghio, A. J. and Piantadosi, C. A. (1995). Reactive oxygen species produced by liver mitochondria of rats in sepsis. Arch. Biochem. Biophys. 316, 70-76.
40. Tsuboi, N., Yoshikai, Y., Matsuo, S., Kikuchi, T., Iwami, K., Nagai, Y., Takeuchi, O., Akira, S. and Matsuguchi, T. (2002). Roles of toll-like receptors in C-C chemokine production by renal tubular epithelial cells. J. Immunol. 169, 2026-2033.
41. Yousefi, S., Perozzo, R., Schmid, I., Ziemiecki, A., Schaffner, T., Scapozza, L., Brunner, T. and Simon, H. U. (2006). Calpainmediated cleavage of Atg5 switches autophagy to apoptosis. Nat. Cell Biol. 8, 1124-1132.
42. Varki, A. (1997). Sialic acids as ligands in recognition phenomena. FASEB J. 11, 248-255.
43. Wang,W., Jittikanont, S., Falk, S. A., Li, P., Feng, L., Gengaro, P. E., Poole, B. D., Bowler, R. P., Day, B. J., Crapo, J. D., et al. (2003). Interaction among nitric oxide, reactive oxygen species, and antioxidants during endotoxemia-related acute renal failure. Am. J. Physiol. Renal Physiol. 284, F532-F537.
44. Yang, C. C., Ma, M. C., Chien, C. T., Wu, M. S., Sun, W. K. and Chen, C. F. (2007). Hypoxic preconditioning attenuates lipopolysaccharide-induced oxidative stress in rat kidneys. J. Physiol. 582, 407-419.
45. Yang, J. C., Shun, C. T., Chien, C. T. and Wang, T. H. (2008). Effective prevention and treatment of Helicobacter pylori infection using a combination of catechins and sialic acid in AGS cells and BALB/c mice. J. Nutr. 138, 2084-2090.
46. Yang, J. C., Yang, H. C., Shun, C. T., Wang, T. H., Chien, C. T. and Kao, J. Y. (2013). Catechins and sialic acid attenuate Helicobacter pylori-triggered epithelial caspase-1 activity and eradicate Helicobacter pylori infection. Evid. Complement Alternat. Med., 2013, 248585.
47. Yu, M., Shao, D., Liu, J., Zhu, J., Zhang, Z. and Xu, J. (2007). Effects of ketamine on levels of cytokines, NF-Kappa B and TLRs in rat intestine during CLP-induced sepsis. Int. Immunopharmacol. 7, 1076-1082.
48. Zhou, F., Peng, Z., Murugan, R. and Kellum, J. A. (2013). Blood purification and mortality in sepsis: A meta-analysis of randomized trials. Crit. Care Med. 41, 2209-2220.
49. Zhande, R., Dauphinee, S. M., Thomas, J. A., Yamamoto, M., Akira, S. and Karsan, A. (2007) FADD negatively regulates lipopolysaccharide signaling by impairing interleukin- 1 receptor-associated kinase 1-MyD88 interaction. Mol. Cell. Biol. 27, 7394-7404.
50. Zimmerman, J. J. (1995). Definition the role of oxyradicals in the pathogenesis of sepsis. Crit. Care Med. 23, 616-617.