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Inflammation
Published in: Inflammation 2/2016

01-04-2016 | ORIGINAL ARTICLE

In Vitro Oxidation of Collagen Promotes the Formation of Advanced Oxidation Protein Products and the Activation of Human Neutrophils

Authors: Guilherme Vargas Bochi, Vanessa Dorneles Torbitz, Luízi Prestes de Campos, Manuela Borges Sangoi, Natieli Flores Fernandes, Patrícia Gomes, Maria Beatriz Moretto, Fernanda Barbisan, Ivana Beatrice Mânica da Cruz, Rafael Noal Moresco

Published in: Inflammation | Issue 2/2016

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Abstract

The accumulation of advanced oxidation protein products (AOPPs) has been linked to several pathological conditions. Here, we investigated collagen as a potential source for AOPP formation and determined the effects of hypochlorous acid (HOCl)-treated collagen (collagen-AOPPs) on human neutrophil activity. We also assessed whether alpha-tocopherol could counteract these effects. Exposure to HOCl increased the levels of collagen-AOPPs. Collagen-AOPPs also stimulated the production of AOPPs, nitric oxide (NO), superoxide radicals (O2 −), and HOCl by neutrophils. Collagen-AOPPs induced apoptosis and decreased the number of viable cells. Alpha-tocopherol prevented the formation of collagen-AOPPs, strongly inhibited the collagen-AOPP-induced production of O2 − and HOCl, and increased the viability of neutrophils. Our results suggest that collagen is an important protein that interacts with HOCl to form AOPPs, and consequently, collagen-AOPP formation is related to human neutrophil activation and cell death.
Literature
1.
Nowotny, K., and T. Grune. 2014. Degradation of oxidized and glycoxidized collagen: role of collagen cross-linking. Archives of Biochemistry and Biophysics 542: 56–64.CrossRefPubMed
2.
Černý, M., J. Skalák, H. Cerna, and B. Brzobohatý. 1996. Advances in purification and separation of posttranslationally modified proteins. Journal of Proteomics 92: 2–27.
3.
Witko-Sarsat, V., M. Friedlander, C. Capeillère-Blandin, T. Nguyen-Khoa, A.T. Nguyen, J. Zingraff, P. Jungers, and B. Descamps-Latscha. 1996. Advanced oxidation protein products as a novel marker of oxidative stress in uremia. Kidney International 49: 1304–1313.CrossRefPubMed
4.
Witko-Sarsat, V., V. Gausson, A.T. Nguyen, M. Touam, T. Drüeke, F. Santangelo, and B. Descamps-Latscha. 2003. AOPP-induced activation of human neutrophil and monocyte oxidative metabolism: a potential target for N-acetylcysteine treatment in dialysis patients. Kidney International 64: 82–91.CrossRefPubMed
5.
Shi, X.Y., F.F. Hou, H.X. Niu, G. Wang, D. Xie, Z.J. Guo, Z.M. Zhou, F. Yang, J.W. Tian, and X. Zhang. 2008. Advanced oxidation protein products promote inflammation in diabetic kidney through activation of renal nicotinamide adenine dinucleotide phosphate oxidase. Endocrinology 149: 1829–1839.CrossRefPubMed
6.
Zhou, L.L., F.F. Hou, G.B. Wang, F. Yang, D. Xie, Y.P. Wang, and J.W. Tian. 2009. Accumulation of advanced oxidation protein products induces podocyte apoptosis and deletion through NADPH-dependent mechanisms. Kidney International 76: 1148–1160.CrossRefPubMed
7.
Hanasand, M., R. Omdal, K.B. Norheim, L.G. Gøransson, C. Brede, and G. Jonsson. 2012. Improved detection of advanced oxidation protein products in plasma. Clinica Chimica Acta 413: 901–906.CrossRef
8.
Capeillère-Blandin, C., V. Gausson, B. Descamps-Latscha, and V. Witko-Sarsat. 2004. Biochemical and spectrophotometric significance of advanced oxidized protein products. Biochimica et Biophysica Acta 1689: 91–102.CrossRefPubMed
9.
Bochi, G.V., V.D. Torbitz, L.P. Cargnin, J.A. de Carvalho, P. Gomes, and R.N. Moresco. 2014. An alternative pathway through the Fenton reaction for the formation of advanced oxidation protein products, a new class of inflammatory mediators. Inflammation 37: 512–521.CrossRefPubMed
10.
Gorudko, I.V., D.V. Grigorieva, E.V. Shamova, V.A. Kostevich, A.V. Sokolov, E.V. Mikhalchik, S.N. Cherenkevich, J. Arnhold, and O.M. Panasenko. 2014. Hypohalous acid-modified human serum albumin induces neutrophil NADPH oxidase activation, degranulation, and shape change. Free Radic Biol Med 68: 326–334.CrossRefPubMed
11.
Torbitz, V.D., G.V. Bochi, J.A. de Carvalho, R.D. Vaucher, J.E. da Silva, and R.N. Moresco. 2014. In vitro oxidation of fibrinogen promotes functional alterations and formation of advanced oxidation protein products, an inflammation mediator. Inflammation 38: 1201–1206.CrossRef
12.
Colombo, G., M. Clerici, D. Giustarini, N. Portinaro, S. Badalamenti, R. Rossi, A. Milzani, and I. Dalle-Donne. 2015. A central role for intermolecular dityrosine cross-linking of fibrinogen in high molecular weight advanced oxidation protein product (AOPP) formation. Biochimica et Biophysica Acta 1850: 1–12.CrossRefPubMed
13.
Mazaki, Y., S. Hashimoto, T. Tsujimura, M. Morishige, A. Hashimoto, K. Aritake, A. Yamada, J.M. Nam, H. Kiyonari, K. Nakao, and H. Sabe. 2006. Neutrophil direction sensing and superoxide production linked by the GTPase-activating protein GIT2. Nature Immunology 7: 724–731.CrossRefPubMed
14.
Moncada, S., and A. Higgs. 1993. The l-arginine-nitric oxide pathway. The New England Journal of Medicine 329: 2002–2012.CrossRefPubMed
15.
Wright, C.D., A. Mulsch, R. Busse, and H. Osswald. 1989. Generation of nitric oxide by human neutrophils. Biochemical and Biophysical Research Communications 160: 813–819.CrossRefPubMed
16.
Larfars, G., and H. Gyllenhammar. 1995. Measurement of methemoglobin formation from oxyhemoglobin. A real-time, continuous assay of nitric oxide release by human polymorphonuclear leukocytes. Journal of Immunological Methods 184: 53–62.CrossRefPubMed
17.
Ahlin, A., G. Larfars, G. Elinder, J. Palmblad, and H. Gyllenhammar. 1999. Gamma interferon treatment of patients with chronic granulomatous disease is associated with augmented production of nitric oxide by polymorphonuclear neutrophils. Clinical and Diagnostic Laboratory Immunology 6: 420–424.PubMedPubMedCentral
18.
19.
Morris, J.C. 1966. The acid ionization constant of HOCl from 5 to 35°. The Journal of Physical Chemistry 70: 3798–3805.CrossRef
20.
Bochi, G.V., V.D. Torbitz, L.P. Cargnin, M.B. Sangoi, R.C. Santos, P. Gomes, and R.N. Moresco. 2012. Fructose-1,6-bisphosphate and N-acetylcysteine attenuate the formation of advanced oxidation protein products, a new class of inflammatory mediators, in vitro. Inflammation 35: 1786–1792.CrossRefPubMed
21.
McCall, M.R., A.C. Carr, T.M. Forte, and B. Frei. 2001. LDL modified by hypochlorous acid is a potent inhibitor of lecithin-cholesterol acyltransferase activity. Arteriosclerosis, Thrombosis, and Vascular Biology 21: 1040–1045.CrossRefPubMed
22.
Davies, J.M.S., D.A. Horwittz, and K.J.L. Davies. 1993. Potential roles of hypochlorous acid and N-chloramines in collagen breakdown by phagocytic cells in synovitis. Free Radical Biology and Medicine 15: 637–643.CrossRefPubMed
23.
Olszowski, S., P. Mak, E. Olszowska, and J. Marcinkiewicz. 2003. Collagen type II modification by hypochlorite. Acta Biochimica Polonica 50: 471–479.PubMed
24.
Witko-Sarsat, V., M. Friedlander, T. Nguyen Khoa, C. Capeillère-Blandin, A.T. Nguyen, S. Canteloup, J.M. Dayer, P. Jungers, T. Drüeke, and B. Descamps-Latscha. 1998. Advanced oxidation protein products as novel mediators of inflammation and monocyte activation in chronic renal failure. The Journal of Immunology 161: 2524–2532.PubMed
25.
Boyum, A. 1974. Separation of blood leukocytes, granulocytes and lymphocytes. Tissue Antigens 4: 269–274.CrossRefPubMed
26.
Tatsch, E., G.V. Bochi, R.S. Pereira, H. Kober, V.A. Agertt, M.M. de Campos, P. Gomes, M.M. Duarte, and R.N. Moresco. 2011. A simple and inexpensive automated technique for measurement of serum nitrite/nitrate. Clinical Biochemistry 44: 348–350.CrossRefPubMed
27.
Morabito, C., F. Rovetta, M. Bizzarri, G. Mazzoleni, G. Fanò, and M.A. Mariggiò. 2010. Modulation of redox status and calcium handling by extremely low frequency electromagnetic fields in C2C12 muscle cells: a real-time, single-cell approach. Free Radical Biology and Medicine 48: 579–589.CrossRefPubMed
28.
Bordignon, M., L. Da Dalt, L. Marinelli, and G. Gabai. 2014. Advanced oxidation protein products are generated by bovine neutrophils and inhibit free radical production in vitro. The Veterinary Journal 199: 162–168.CrossRefPubMed
29.
Makni-Maalej, K., M. Chiandotto, M. Hurtado-Nedelec, S. Bedouhene, M.A. Gougerot-Pocidalo, P.M. Dang, and J. El-Benna. 2013. Zymosan induces NADPH oxidase activation in human neutrophils by inducing the phosphorylation of p47phox and the activation of Rac2: involvement of protein tyrosine kinases, PI3Kinase, PKC, ERK1/2 and p38MAPkinase. Biochemical Pharmacology 85: 92–100.CrossRefPubMed
30.
Whiteman, M., D.C. Hooper, G.S. Scott, H. Koprowski, and B. Halliwell. 2002. Inhibition of hypochlorous acid-induced cellular toxicity by nitrite. Proceedings of the National Academy of Sciences of the United States of America 99: 12061–12066.CrossRefPubMedPubMedCentral
31.
Weiss, S.J., M.B. Lampert, and S.T. Test. 1983. Long-lived oxidants generated by human neutrophils: characterisation and bioactivity. Science 227: 625–628.CrossRef
32.
Daumer, K.M., A.U. Khan, and M.J. Steinbeck. 2000. Chlorination of pyridinium compounds. Possible role of hypochlorite, N-chloramines, and chlorine in the oxidation of pyridinoline cross-links of articular cartilage collagen type II during acute inflammation. The Journal of Biological Chemistry 275: 34681–34692.CrossRefPubMedPubMedCentral
33.
Nissim, A., P.G. Winyard, V. Corrigall, R. Fatah, D. Perrett, G. Panayi, and Y. Chernajovsky. 2005. Generation of neoantigenic epitopes after posttranslational modification of type II collagen by factors present within the inflamed joint. Arthritis and Rheumatism 52: 3829–3838.CrossRefPubMed
34.
Sharma, P., S.A. Raghavan, R. Saini, and M. Dikshit. 2004. Ascorbate-mediated enhancement of reactive oxygen species generation from polymorphonuclear leukocytes: modulatory effect of nitric oxide. Journal of Leukocyte Biology 75: 1070–1078.CrossRefPubMed
35.
Gal, A., S. Tamir, L.J. Kennedy, S.R. Tannenbaum, and G.N. Wogan. 1997. Nitrotyrosine formation, apoptosis, and oxidative damage: relationships to nitric oxide production in SJL mice bearing the RcsX tumor. Cancer Research 57: 1823–1828.PubMed
36.
Foote, C.S., T.E. Goyne, and R.I. Lehrer. 1983. Assessment of chlorination by human neutrophils. Nature 301: 715–716.CrossRefPubMed
37.
Weiss, S.J. 1989. Tissue destruction by neutrophils. The New England Journal of Medicine 320: 365–376.CrossRefPubMed
38.
Kennedy, A.D., and F.R. DeLeo. 2009. Neutrophil apoptosis and the resolution of infection. Immunome Research 43: 25–61.CrossRef
39.
Kobayashi, S.D., K.R. Braughton, A.R. Whitney, J.M. Voyich, T.G. Schwan, J.M. Musser, and F.R. DeLeo. 2003. Bacterial pathogens modulate an apoptosis differentiation program in human neutrophils. Proceedings of the National Academy of Sciences of the United States of America 100: 10948–10953.CrossRefPubMedPubMedCentral
40.
Valente, A.J., T. Yoshida, R.A. Clark, P. Delafontaine, U. Siebenlist, and B. Chandrasekar. 2013. Advanced oxidation protein products induce cardiomyocyte death via Nox2/Rac1/superoxide-dependent TRAF3lP2/JNK signaling. Free Radical Biology and Medicine 60: 125–135.CrossRefPubMedPubMedCentral
41.
Mayadas, T.N., and X. Cullere. 2005. Neutrophil beta2 integrins: moderators of life or death decisions. Trends in Immunology 26: 388–395.CrossRefPubMed
42.
Williams, M.A., and J.S. Solomkin. 1999. Integrin-mediated signaling in human neutrophil functioning. Journal of Leukocyte Biology 65: 725–736.PubMed
43.
Packer, L., and Valacchi, G. Antioxidants and the response of skin to oxidative stress: vitamin E as a key indicator. Pharmacology and Applied Skin Physiological 15: 282–90.
44.
McIntyre, B.S., K.P. Briski, A. Gapor, and P.W. Sylvester. 2000. Antiproliferative and apoptotic effects of tocopherols and tocotrienols on preneoplastic and neoplastic mouse mammary epithelial cells. Proceedings of the Society for Experimental Biology and Medicine 224: 292–301.CrossRefPubMed
45.
Dean, R.T., J.V. Hunt, A.J. Grant, Y. Yamamoto, and E. Niki. 1991. Free radical damage to proteins: the influence of the relative localization of radical generation, antioxidants, and target proteins. Free Radical Biology and Medicine 11: 161–168.CrossRefPubMed
46.
Hiramatsu, K., and S. Arimori. 1988. Increased superoxide production by mononuclear cells of patients with hypertriglyceridemia and diabetes. Diabetes 37: 832–837.CrossRefPubMed
47.
Ludwig, P.W., D.B. Hunninghake, and J.R. Hoidal. 1982. Increased leukocyteoxidative metabolism in hyperlipoproteinemia. Lancet 2: 348–350.CrossRefPubMed
48.
Cao, W., J. Xu, Z.M. Zhou, G.B. Wang, F.F. Hou, and J. Nie. 2013. Advanced oxidation protein products activate intrarenal renin-angiotensin system via a CD36-mediated, redox-dependent pathway. Antioxidants and Redox Signaling 18: 19–35.CrossRefPubMedPubMedCentral
Metadata
Title
In Vitro Oxidation of Collagen Promotes the Formation of Advanced Oxidation Protein Products and the Activation of Human Neutrophils
Authors
Guilherme Vargas Bochi
Vanessa Dorneles Torbitz
Luízi Prestes de Campos
Manuela Borges Sangoi
Natieli Flores Fernandes
Patrícia Gomes
Maria Beatriz Moretto
Fernanda Barbisan
Ivana Beatrice Mânica da Cruz
Rafael Noal Moresco
Publication date
01-04-2016
Publisher
Springer US
Published in
Inflammation / Issue 2/2016
Print ISSN: 0360-3997
Electronic ISSN: 1573-2576
DOI
https://doi.org/10.1007/s10753-016-0325-3

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