Chitosan oligosaccharides block LPS-induced O-GlcNAcylation of NF-κB and endothelial inflammatory response

Carbohydrate Polymers

Volumn 99, Issue , 2014, Pages 568-578

  Li, Yu ^a,b,c   Liu, Hongtao ^c   Xu, Qing Song ^a   Du, Yu Guang ^a   Xu, Jian ^c  

^a DALIAN INSTITUTE OF CHEMICAL PHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c BSEB 325 ^*  (United States)

Author keywords

B cells (NF B); Chitosan oligosaccharides; Endothelial cells; Inflammatory response; Lipopolysaccharides (LPS); Nuclear factor kappa light chain enhancer of activated; O GlcNAcylation

Indexed keywords

B CELLS; CHITOSAN OLIGOSACCHARIDE; INFLAMMATORY RESPONSE; LIPOPOLYSACCHARIDES; NUCLEAR FACTORS; O-GLCNACYLATION;

ENDOTHELIAL CELLS; OLIGOSACCHARIDES;

CHITOSAN;

MUS;

CHITOSAN; LIPOPOLYSACCHARIDE; N ACETYLGLUCOSAMINE; N ACETYLGLUCOSAMINYLTRANSFERASE; O GLCNAC TRANSFERASE; O-GLCNAC TRANSFERASE; OLIGOSACCHARIDE; TRANSCRIPTION FACTOR RELA;

ACYLATION; ANIMAL; ARTICLE; CATTLE; CELL CULTURE; CHEMISTRY; CHITOSAN OLIGOSACCHARIDES; CYTOLOGY; DRUG EFFECT; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; INFLAMMATION; LIPOPOLYSACCHARIDES (LPS); METABOLISM; MOUSE; NUCLEAR FACTOR KAPPA-LIGHT-CHAIN-ENHANCER OF ACTIVATED B CELLS (NF-ΚB); O-GLCNACYLATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION;

CHITOSAN OLIGOSACCHARIDES; ENDOTHELIAL CELLS; INFLAMMATORY RESPONSE; LIPOPOLYSACCHARIDES (LPS); NUCLEAR FACTOR KAPPA-LIGHT-CHAIN-ENHANCER OF ACTIVATED B CELLS (NF-ΚB); O-GLCNACYLATION;

ACETYLGLUCOSAMINE; ACYLATION; ANIMALS; CATTLE; CELLS, CULTURED; CHITOSAN; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION; LIPOPOLYSACCHARIDES; MICE; N-ACETYLGLUCOSAMINYLTRANSFERASES; OLIGOSACCHARIDES; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR RELA;

EID: 84884332579     PISSN: 01448617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.carbpol.2013.08.082     Document Type: Article

References (68)

1. I. Al Ghouleh, and S. Magder Nicotinamide adenine dinucleotide phosphate (reduced form) oxidase is important for LPS-induced endothelial cell activation Shock 29 5 2008 553 559 (Pubitemid 351544074)
2. D.F. Allison, J.J. Wamsley, M. Kumar, D. Li, L.G. Gray, and G.W. Hart Modification of RelA by O-linked N-acetylglucosamine links glucose metabolism to NF-kappaB acetylation and transcription Proceedings of the National Academy of Sciences 109 42 2012 16888 16893
3. I.S. Arvanitoyannis, A. Nakayama, and A.I. Aiba Chitosan and gelatin based edible films: state diagrams, mechanical and permeation properties Carbohydrate Polymers 37 1998 371 382 (Pubitemid 128427742)
4. A. Bierhaus, J. Chen, B. Liliensiek, and P.P. Nawroth LPS and cytokine-activated endothelium Seminars in Thrombosis and Hemostasis 26 5 2000 571 587
5. S.H. Chan, K.S. Hsu, C.C. Huang, L.L. Wang, C.C. Ou, and J.Y. Chan NADPH oxidase-derived superoxide anion mediates angiotensin II-induced pressor effect via activation of p38 mitogen-activated protein kinase in the rostral ventrolateral medulla Circulation Research 97 8 2005 772 780 (Pubitemid 41447127)
6. E.H. Choi, H.P. Yang, and H.S. Chun Chitooligosaccharide ameliorates diet-induced obesity in mice and affects adipose gene expression involved in adipogenesis and inflammation Nutrition Research 32 3 2012 218 228
7. E.J. Chung, J.N. Chun, S.A. Jung, J.W. Cho, and J.H. Lee TGF-beta-stimulated aberrant expression of class III beta-tubulin via the ERK signaling pathway in cultured retinal pigment epithelial cells Biochemical and Biophysical Research Communications 415 2 2011 367 372
8. M.J. Chung, J.K. Park, and Y. Il Park Anti-inflammatory effects of low-molecular weight chitosan oligosaccharides in IgE-antigen complex-stimulated RBL-2H3 cells and asthma model mice International Immunopharmacology 12 2 2012 453 459
9. C.A. Da Silva, P. Pochard, C.G. Lee, and J.A. Elias Chitin particles are multifaceted immune adjuvants American Journal of Respiratory and Critical Care Medicine 182 12 2010 1482 1491
10. A.E. Dikalova, A.T. Bikineyeva, K. Budzyn, R.R. Nazarewicz, L. McCann, and W. Lewis Therapeutic targeting of mitochondrial superoxide in hypertension Circulation Research 107 1 2010 106 116
11. Y.Z. Du, L. Wang, H. Yuan, X.H. Wei, and F.Q. Hu Preparation and characteristics of linoleic acid-grafted chitosan oligosaccharide micelles as a carrier for doxorubicin Colloids and Surfaces B: Biointerfaces 69 2 2009 257 263
12. C.D. Dumitru, J.D. Ceci, C. Tsatsanis, D. Kontoyiannis, K. Stamatakis, and J.H. Lin TNF-alpha induction by LPS is regulated posttranscriptionally via a Tpl2/ERK-dependent pathway Cell 103 7 2000 1071 1083 (Pubitemid 32040907)
13. V.G.H. Eijsink, B.B. Aam, E.B. Heggset, A.L. Norberg, M. Sorlie, and K.M. Varum Production of chitooligosaccharides and their potential applications in medicine Marine Drugs 8 5 2010 1482 1517
14. J. Fernandes, J. Sereno, P. Garrido, B. Parada, M. Cunha, and F. Reis Inhibition of bladder tumor growth by chitooligosaccharides in an experimental carcinogenesis model Marine Drugs 10 12 2012 2661 2675
15. J.C. Fernandes, H. Spindola, V. de Sousa, A. Santos-Silva, M.E. Pintado, and F.X. Malcata Anti-inflammatory activity of chitooligosaccharides in vivo Marine Drugs 8 6 2010 1763 1768
16. H. Goldberg, C. Whiteside, and I.G. Fantus O-linked beta-N- acetylglucosamine supports p38 MAPK activation by high glucose in glomerular mesangial cells American Journal of Physiology-Endocrinology and Metabolism 301 4 2011 E713 E726
17. S.E. Goldblum, T.W. Brann, X. Ding, J. Pugin, and P.S. Tobias Lipopolysaccharide (LPS)-binding protein and soluble CD14 function as accessory molecules for LPS-induced changes in endothelial barrier function, in vitro Journal of Clinical Investigation 93 2 1994 692 702 (Pubitemid 24072811)
18. A. Golks, T.T. Tran, J.F. Goetschy, and D. Guerini Requirement for O-linked N-acetylglucosaminyltransferase in lymphocytes activation EMBO Journal 26 20 2007 4368 4379 (Pubitemid 47587656)
19. G.W. Hart, and R.J. Copeland Glycomics hits the big time Cell 143 5 2010 672 676
20. G.W. Hart, M.P. Housley, and C. Slawson Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins Nature 446 7139 2007 1017 1022 (Pubitemid 46676063)
21. K.S. Heo, E. Chang, N.T. Le, H. Cushman, E.T. Yeh, and K. Fujiwara De-SUMOylation Enzyme of Sentrin/SUMO-Specific Protease 2 regulates disturbed flow-induced SUMOylation of ERK5 and p53 that leads to endothelial dysfunction and atherosclerosis Circulation Research 112 6 2013 911 923
22. R.H. Hilgers, D. Xing, K. Gong, Y.F. Chen, J.C. Chatham, and S. Oparil Acute O-GlcNAcylation prevents inflammation-induced vascular dysfunction American Journal of Physiology. Heart and Circulatory Physiology 303 5 2012 H513 H522
23. I. Hussain, T. Singh, and C. Chittenden Preparation of chitosan oligomers and characterization: their antifungal activities and decay resistance Holzforschung 66 1 2012 119 125
24. L.R. James, D. Tang, A. Ingram, H. Ly, K. Thai, and L. Cai Flux through the hexosamine pathway is a determinant of nuclear factor kappaB-dependent promoter activation Diabetes 51 4 2002 1146 1156 (Pubitemid 34438362)
25. H.Y. Jin, B. Song, G.Y. Oudit, S.T. Davidge, H.M. Yu, and Y.Y. Jiang ACE2 deficiency enhances angiotensin II-mediated aortic profilin-1 expression, inflammation and peroxynitrite production PLoS ONE 7 6 2012 e38502
26. A. Kadl, and N. Leitinger The role of endothelial cells in the resolution of acute inflammation Antioxidants & Redox Signaling 7 11-12 2005 1744 1754 (Pubitemid 41768006)
27. J.A. Kim, B.N. Ahn, C.S. Kong, and S.K. Kim Chitooligomers inhibit UV-A-induced photoaging of skin by regulating TGF-beta/Smad signaling cascade Carbohydrate Polymers 88 2 2012 490 495
28. S.-K. Kim, and N. Rajapakse Enzymatic production and biological activities of chitosan oligosaccharides (COS) Carbohydrate Polymers 62 4 2005 357 368 (Pubitemid 41745217)
29. T. Kisseleva, L. Song, M. Vorontchikhina, N. Feirt, J. Kitajewski, and C. Schindler NF-kappaB regulation of endothelial cell function during LPS-induced toxemia and cancer Journal of Clinical Investigation 116 11 2006 2955 2963 (Pubitemid 44684480)
30. Q. Li, and I.M. Verma NF-kappaB regulation in the immune system Nature Reviews Immunology 2 10 2002 725 734
31. V.V. Lima, F.R. Giachini, F.S. Carneiro, Z.N. Carneiro, M.A. Saleh, and D.M. Pollock O-GlcNAcylation contributes to augmented vascular reactivity induced by endothelin 1 Hypertension 55 1 2010 180 188
32. V.V. Lima, F.R. Giachini, F.S. Carneiro, M.H. Carvalho, Z.B. Fortes, and R.C. Webb O-GlcNAcylation contributes to the vascular effects of ET-1 via activation of the RhoA/Rho-kinase pathway Cardiovascular Research 89 3 2011 614 622
33. V.V. Lima, F.R. Giachini, H. Choi, F.S. Carneiro, Z.N. Carneiro, and Z.B. Fortes Impaired vasodilator activity in deoxycorticosterone acetate-salt hypertension is associated with increased protein O-GlcNAcylation Hypertension 53 2 2009 166 174
34. H. Liu, S. Yu, W. Xu, and J. Xu Enhancement of 26S proteasome functionality connects oxidative stress and vascular endothelial inflammatory response in diabetes mellitus Arteriosclerosis, Thrombosis, and Vascular Biology 32 9 2012 2131 2140
35. H. Liu, S. Yu, H. Zhang, and J. Xu Angiogenesis impairment in diabetes: role of methylglyoxal-induced receptor for advanced glycation endproducts, autophagy and vascular endothelial growth factor receptor 2 PLoS ONE 7 10 2012 e46720
36. H.-T. Liu, J.-L. He, W.-M. Li, Z. Yang, Y.-X. Wang, and X.-F. Bai Chitosan oligosaccharides protect human umbilical vein endothelial cells from hydrogen peroxide-induced apoptosis Carbohydrate Polymers 80 4 2010 1062 1071
37. H.T. Liu, P. Huang, P. Ma, Q.S. Liu, C. Yu, and Y.G. Du Chitosan oligosaccharides suppress LPS-induced IL-8 expression in human umbilical vein endothelial cells through blockade of p38 and Akt protein kinases Acta Pharmacologica Sinica 32 4 2011 478 486
38. H.T. Liu, W.M. Li, X.Y. Li, Q.S. Xu, Q.S. Liu, and X.F. Bai Chitosan oligosaccharides inhibit the expression of interleukin-6 in lipopolysaccharide- induced human umbilical vein endothelial cells through p38 and ERK1/2 protein kinases Basic & Clinical Pharmacology & Toxicology 106 5 2010 362 371
39. P. Ma, H.-T. Liu, P. Wei, Q.-S. Xu, X.-F. Bai, and Y.-G. Du Chitosan oligosaccharides inhibit LPS-induced over-expression of IL-6 and TNF-α in RAW264.7 macrophage cells through blockade of mitogen-activated protein kinase (MAPK) and PI3K/Akt signaling pathways Carbohydrate Polymers 84 4 2011 1391 1398
40. F.X. Malcata, J.C. Fernandes, F.K. Tavaria, S.C. Fonseca, O.S. Ramos, and M.E. Pintado In vitro screening for antimicrobial activity of chitosans and chitooligosaccharides, aiming at potential uses in functional textiles Journal of Microbiology and Biotechnology 20 2 2010 311 318
41. M. Marques, S.A. Brown, P. Rodrigues-Pereira, M. Natalia, D.S. Cordeiro, and A. Morales-Helguera Animal model of implant capsular contracture: effects of chitosan Aesthetic Surgery Journal 31 5 2011 540 550
42. D.A. McClain, and E.D. Crook Hexosamines and insulin resistance Diabetes 45 8 1996 1003 1009 (Pubitemid 26260150)
43. F.M. Meier, K.W. Frommer, M.A. Peters, F. Brentano, S. Lefevre, and D. Schroder Visfatin/pre-B-cell colony-enhancing factor (PBEF), a proinflammatory and cell motility-changing factor in rheumatoid arthritis Journal of Biological Chemistry 287 34 2012 28378 28385
44. K.S. Nam, M.K. Kim, and Y.H. Shon Chemopreventive effect of chitosan oligosaccharide against colon carcinogenesis Journal of Microbiology and Biotechnology 17 9 2007 1546 1549
45. G. Natoli Little things that count in transcriptional regulation Cell 118 4 2004 406 408 (Pubitemid 39485660)
46. G. Natoli NF-kappaB and chromatin: ten years on the path from basic mechanisms to candidate drugs Immunological Reviews 246 1 2012 183 192
47. K. Nishimura, S. Nishimura, N. Nishi, I. Saiki, S. Tokura, and I. Azuma Immunological activity of chitin and its derivatives Vaccine 2 1 1984 93 99 (Pubitemid 15167639)
48. S. Ozcan, S.S. Andrali, and J.E. Cantrell Modulation of transcription factor function by O-GlcNAc modification Biochimica et Biophysica Acta 1799 5/6 2010 353 364
49. R.R. Packard, and P. Libby Inflammation in atherosclerosis: from vascular biology to biomarker discovery and risk prediction Clinical Chemistry 54 1 2008 24 38 (Pubitemid 351182593)
50. L. Pan, Y. Li, L. Jia, Y. Qin, G. Qi, and J. Cheng Cathepsin S deficiency results in abnormal accumulation of autophagosomes in macrophages and enhances Ang II-induced cardiac inflammation PLoS ONE 7 4 2012 e35315
51. R. Pangestuti, S.S. Bak, and S.K. Kim Attenuation of pro-inflammatory mediators in LPS-stimulated BV2 microglia by chitooligosaccharides via the MAPK signaling pathway International Journal of Biological Macromolecules 49 4 2011 599 606
52. J.S. Pober, and W.C. Sessa Evolving functions of endothelial cells in inflammation Nature Reviews Immunology 7 10 2007 803 815 (Pubitemid 47480307)
53. Y. Qiao, X.F. Bai, and Y.G. Du Chitosan oligosaccharides protect mice from LPS challenge by attenuation of inflammation and oxidative stress International Immunopharmacology 11 1 2011 121 127
54. Y. Qiao, Y.Y. Ruan, C.N. Xiong, Q.S. Xu, P. Wei, and P. Ma Chitosan oligosaccharides suppressant LPS binding to TLR4/MD-2 receptor complex Carbohydrate Polymers 82 2 2010 405 411
55. C.R. Raetz, and C. Whitfield Lipopolysaccharide endotoxins Annual Review of Biochemistry 71 2002 635 700 (Pubitemid 34800232)
56. I.H. Ryu, and S.I. Do Denitrosylation of S-nitrosylated OGT is triggered in LPS-stimulated innate immune response Biochemical and Biophysical Research Communications 408 1 2011 52 57
57. C. Sato, K. Shikata, D. Hirota, M. Sasaki, S. Nishishita, and S. Miyamoto P-selectin glycoprotein ligand-1 deficiency is protective against obesity-related insulin resistance Diabetes 60 1 2011 189 199
58. F.K. Tavaria, J.C. Soares, I.L. Reis, M.H. Paulo, F.X. Malcata, and M.E. Pintado Chitosan: antimicrobial action upon staphylococci after impregnation onto cotton fabric Journal of Applied Microbiology 112 5 2012 1034 1041
59. S. Vallabhapurapu, and M. Karin Regulation and function of NF-kappaB transcription factors in the immune system Annual Review of Immunology 27 2009 693 733
60. L. Wells, K. Vosseller, and G.W. Hart Glycosylation of nucleocytoplasmic proteins: signal transduction and O-GlcNAc Science 291 5512 2001 2376 2378 (Pubitemid 32231793)
61. D. Xing, W. Feng, L.G. Not, A.P. Miller, Y. Zhang, and Y.F. Chen Increased protein O-GlcNAc modification inhibits inflammatory and neointimal responses to acute endoluminal arterial injury American Journal of Physiology. Heart and Circulatory Physiology 295 1 2008 H335 H342
62. J. Xu, R. Lucas, M. Schuchmann, S. Kuhnle, T. Meergans, and A.P. Barreiros GM-CSF restores innate, but not adaptive, immune responses in glucocorticoid-immunosuppressed human blood in vitro Journal of Immunology 171 2 2003 938 947 (Pubitemid 36871408)
63. M. Yanagisawa, and R.K. Yu O-linked beta-N-acetylglucosaminylation in mouse embryonic neural precursor cells Journal of Neuroscience Research 87 16 2009 3535 3545
64. W.H. Yang, S.Y. Park, H.W. Nam, H. Kim do, J.G. Kang, and E.S. Kang NFkappaB activation is associated with its O-GlcNAcylation state under hyperglycemic conditions Proceedings of the National Academy of Sciences 105 45 2008 17345 17350
65. H.J. Yoon, M.E. Moon, H.S. Park, S.Y. Im, and Y.H. Kim Chitosan oligosaccharide (COS) inhibits LPS-induced inflammatory effects in RAW 264.7 macrophage cells Biochemical and Biophysical Research Communications 358 3 2007 954 959 (Pubitemid 46802483)
66. N.E. Zachara, K. Vosseller, and G.W. Hart Detection and analysis of proteins modified by O-linked N-acetylglucosamine Current Protocols in Molecular Biology 2011 16 (Unit 17.6)
67. H. Zhang, Y. Du, X. Yu, M. Mitsutomi, and S. Aiba Preparation of chitooligosaccharides from chitosan by a complex enzyme Carbohydrate Research 320 1999 257 260 (Pubitemid 29488509)
68. L. Zou, S. Yang, V. Champattanachai, S. Hu, I.H. Chaudry, and R.B. Marchase Glucosamine improves cardiac function following trauma-hemorrhage by increased protein O-GlcNAcylation and attenuation of NF-{kappa}B signaling American Journal of Physiology. Heart and Circulatory Physiology 296 2 2009 H515 H523