Oligomerization and Nitration of the Grass Pollen Allergen Phl p 5 by Ozone, Nitrogen Dioxide, and Peroxynitrite: Reaction Products, Kinetics, and Health Effects
Abstract
:1. Introduction
2. Results and Discussion
2.1. Oligomerization
2.2. Nitration
2.3. Comparison Oligomerization Vs. Nitration
3. Materials and Methods
3.1. Protein Modification by O3/NO2
3.2. Protein Modification by ONOO–
3.3. HPLC-DAD Analysis
3.4. MALDI-TOF-MS Analysis
3.5. SDS-PAGE and Silver Stain
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
Abbreviations
DiTyr | Dityrosine |
DD | Dityrosine degree |
MS | Mass spectrometry |
ND | Nitration degree |
NTyr | Nitrotyrosine |
RNS | Reactive nitrogen species |
ROI | Reactive oxygen intermediate |
ROS | Reactive oxygen species |
RP | Reversed-phase chromatography |
SEC | Size-exclusion chromatography |
Tyr | Tyrosine |
References
- Asher, M.I.; Montefort, S.; Björkstén, B.; Lai, C.K.W.; Strachan, D.P.; Weiland, S.K.; Williams, H. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet 2006, 368, 733–743. [Google Scholar] [CrossRef]
- Li, X.; Song, P.; Zhu, Y.; Lei, H.; Chan, K.Y.; Campbell, H.; Theodoratou, E.; Rudan, I. The disease burden of childhood asthma in China: A systematic review and meta-analysis. J. Glob. Health 2020, 10, 010801. [Google Scholar] [CrossRef] [PubMed]
- Pawankar, R. Allergic diseases and asthma: A global public health concern and a call to action. World Allergy Organ. J. 2014, 7, 12. [Google Scholar] [CrossRef][Green Version]
- Singh, S.; Sharma, B.B.; Salvi, S.; Chhatwal, J.; Jain, K.C.; Kumar, L.; Joshi, M.K.; Pandramajal, S.B.; Awasthi, S.; Bhave, S.; et al. Allergic rhinitis, rhinoconjunctivitis, and eczema: Prevalence and associated factors in children. Clin. Respir. J. 2018, 12, 547–556. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Zhang, L. Increasing Prevalence of Allergic Rhinitis in China. Allergy Asthma. Immunol. Res. 2019, 11, 156–169. [Google Scholar] [CrossRef]
- D’Amato, G.; Baena-Cagnani, C.E.; Cecchi, L.; Annesi-Maesano, I.; Nunes, C.; Ansotegui, I.; D’Amato, M.; Liccardi, G.; Sofia, M.; Canonica, W.G. Climate change, air pollution and extreme events leading to increasing prevalence of allergic respiratory diseases. Multidiscip. Respir. Med. 2013, 8, 12. [Google Scholar] [CrossRef][Green Version]
- Eguiluz-Gracia, I.; Mathioudakis, A.G.; Bartel, S.; Vijverberg, S.J.H.; Fuertes, E.; Comberiati, P.; Cai, Y.S.; Tomazic, P.V.; Diamant, Z.; Vestbo, J.; et al. The need for clean air: The way air pollution and climate change affect allergic rhinitis and asthma. Allergy 2020, 75, 2170–2184. [Google Scholar] [CrossRef]
- Pawankar, R.; Baena-Cagnani, C.E.; Bousquet, J.; Walter Canonica, G.; Cruz, A.A.; Kaliner, M.A.; Lanier, B.Q.; Henley, K. State of World Allergy Report 2008: Allergy and Chronic Respiratory Diseases. World Allergy Organ. J. 2008, 1, S4–S17. [Google Scholar] [CrossRef] [PubMed]
- Traidl-Hoffmann, C.; Jakob, T.; Behrendt, H. Determinants of allergenicity. J. Allergy Clin. Immunol. 2009, 123, 558–566. [Google Scholar] [CrossRef]
- Bowatte, G.; Lodge, C.J.; Knibbs, L.D.; Lowe, A.J.; Erbas, B.; Dennekamp, M.; Marks, G.B.; Giles, G.; Morrison, S.; Thompson, B.; et al. Traffic-related air pollution exposure is associated with allergic sensitization, asthma, and poor lung function in middle age. J. Allergy Clin. Immunol. 2017, 139, 122–129. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Deng, Q.; Lu, C.; Yu, Y.; Li, Y.; Sundell, J.; Norbäck, D. Early life exposure to traffic-related air pollution and allergic rhinitis in preschool children. Respir. Med. 2016, 121, 67–73. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Guarnieri, M.; Balmes, J.R. Outdoor air pollution and asthma. Lancet 2014, 383, 1581–1592. [Google Scholar] [CrossRef][Green Version]
- Bryce, M.; Drews, O.; Schenk, M.F.; Menzel, A.; Estrella, N.; Weichenmeier, I.; Smulders, M.J.; Buters, J.; Ring, J.; Gorg, A.; et al. Impact of urbanization on the proteome of birch pollen and its chemotactic activity on human granulocytes. Int. Arch. Allergy Immunol. 2010, 151, 46–55. [Google Scholar] [CrossRef]
- Ghiani, A.; Aina, R.; Asero, R.; Bellotto, E.; Citterio, S. Ragweed pollen collected along high-traffic roads shows a higher allergenicity than pollen sampled in vegetated areas. Allergy 2012, 67, 887–894. [Google Scholar] [CrossRef]
- Motta, A.C.; Marliere, M.; Peltre, G.; Sterenberg, P.A.; Lacroix, G. Traffic-related air pollutants induce the release of allergen-containing cytoplasmic granules from grass pollen. Int. Arch. Allergy Immunol. 2006, 139, 294–298. [Google Scholar] [CrossRef][Green Version]
- Ouyang, Y.; Xu, Z.; Fan, E.; Li, Y.; Zhang, L. Effect of nitrogen dioxide and sulfur dioxide on viability and morphology of oak pollen. Int. Forum. Allergy Rhinol. 2016, 6, 95–100. [Google Scholar] [CrossRef]
- Taylor, P.E.; Flagan, R.C.; Valenta, R.; Glovsky, M.M. Release of allergens as respirable aerosols: A link between grass pollen and asthma. J. Allergy Clin Immunol. 2002, 109, 51–56. [Google Scholar] [CrossRef]
- Taylor, P.E.; Flagan, R.C.; Miguel, A.G.; Valenta, R.; Glovsky, M.M. Birch pollen rupture and the release of aerosols of respirable allergens. Clin. Exp. Allergy 2004, 34, 1591–1596. [Google Scholar] [CrossRef] [PubMed]
- Franze, T.; Weller, M.G.; Niessner, R.; Pöschl, U. Protein Nitration by Polluted Air. Environ. Sci. Technol. 2005, 39, 1673–1678. [Google Scholar] [CrossRef] [PubMed]
- Miguel, A.G.; Cass, G.R.; Glovsky, M.M.; Weiss, J. Allergens in Paved Road Dust and Airborne Particles. Environ. Sci. Technol. 1999, 33, 4159–4168. [Google Scholar] [CrossRef][Green Version]
- Shiraiwa, M.; Selzle, K.; Yang, H.; Sosedova, Y.; Ammann, M.; Pöschl, U. Multiphase chemical kinetics of the nitration of aerosolized protein by ozone and nitrogen dioxide. Environ. Sci. Technol. 2012, 46, 6672–6680. [Google Scholar] [CrossRef] [PubMed]
- Abello, N.; Kerstjens, H.A.M.; Postma, D.S.; Bischoff, R. Protein Tyrosine Nitration: Selectivity, Physicochemical and Biological Consequences, Denitration, and Proteomics Methods for the Identification of Tyrosine-Nitrated Proteins. J. Proteome Res. 2009, 8, 3222–3238. [Google Scholar] [CrossRef] [PubMed]
- Ackaert, C.; Kofler, S.; Horejs-Hoeck, J.; Zulehner, N.; Asam, C.; von Grafenstein, S.; Fuchs, J.E.; Briza, P.; Liedl, K.R.; Bohle, B.; et al. The impact of nitration on the structure and immunogenicity of the major birch pollen allergen Bet v 1.0101. PLoS ONE 2014, 9, e104520. [Google Scholar] [CrossRef] [PubMed]
- Greenacre, S.A.B.; Ischiropoulos, H. Tyrosine nitration: Localisation, quantification, consequences for protein function and signal transduction. Free. Radic. Res. 2001, 34, 541–581. [Google Scholar] [CrossRef]
- Ischiropoulos, H. Protein tyrosine nitration–an update. Arch. Biochem. Biophys. 2009, 484, 117–121. [Google Scholar] [CrossRef]
- Gruijthuijsen, Y.K.; Grieshuber, I.; Stöcklinger, A.; Tischler, U.; Fehrenbach, T.; Weller, M.G.; Vogel, L.; Vieths, S.; Pöschl, U.; Duschl, A. Nitration Enhances the Allergenic Potential of Proteins. Int. Arch. Allergy Immunol. 2006, 141, 265–275. [Google Scholar] [CrossRef]
- Karle, A.C.; Oostingh, G.J.; Mutschlechner, S.; Ferreira, F.; Lackner, P.; Bohle, B.; Fischer, G.F.; Vogt, A.B.; Duschl, A. Nitration of the pollen allergen bet v 1.0101 enhances the presentation of bet v 1-derived peptides by HLA-DR on human dendritic cells. PLoS ONE 2012, 7, e31483. [Google Scholar] [CrossRef][Green Version]
- Reinmuth-Selzle, K.; Ackaert, C.; Kampf, C.J.; Samonig, M.; Shiraiwa, M.; Kofler, S.; Yang, H.; Gadermaier, G.; Brandstetter, H.; Huber, C.G.; et al. Nitration of the birch pollen allergen Bet v 1.0101: Efficiency and site-selectivity of liquid and gaseous nitrating agents. J. Proteome Res. 2014, 13, 1570–1577. [Google Scholar] [CrossRef] [PubMed]
- Lakey, P.S.; Berkemeier, T.; Tong, H.; Arangio, A.M.; Lucas, K.; Poschl, U.; Shiraiwa, M. Chemical exposure-response relationship between air pollutants and reactive oxygen species in the human respiratory tract. Sci. Rep. 2016, 6, 32916. [Google Scholar] [CrossRef]
- Lodovici, M.; Bigagli, E. Oxidative stress and air pollution exposure. J. Toxicol. 2011, 2011, 487074. [Google Scholar] [CrossRef]
- Reinmuth-Selzle, K.; Kampf, C.J.; Lucas, K.; Lang-Yona, N.; Fröhlich-Nowoisky, J.; Shiraiwa, M.; Lakey, P.S.J.; Lai, S.; Liu, F.; Kunert, A.T.; et al. Air Pollution and Climate Change Effects on Allergies in the Anthropocene: Abundance, Interaction, and Modification of Allergens and Adjuvants. Environ. Sci. Technol. 2017, 51, 4119–4141. [Google Scholar] [CrossRef]
- Blough, N.V.; Zafiriou, O.C. Reaction of superoxide with nitric oxide to form peroxonitrite in alkaline aqueous solution. Inorg. Chem. 1985, 24, 3502–3504. [Google Scholar] [CrossRef]
- Gunaydin, H.; Houk, K.N. Mechanisms of Peroxynitrite-Mediated Nitration of Tyrosine. Chem. Res. Toxicol. 2009, 22, 894–898. [Google Scholar] [CrossRef][Green Version]
- Pfeiffer, S.; Schmidt, K.; Mayer, B. Dityrosine formation outcompetes tyrosine nitration at low steady-state concentrations of peroxynitrite. J. Biol. Chem. 2000, 275, 6346–6352. [Google Scholar] [CrossRef][Green Version]
- Ziegler, K.; Kunert, A.T.; Reinmuth-Selzle, K.; Leifke, A.L.; Widera, D.; Weller, M.G.; Schuppan, D.; Fröhlich-Nowoisky, J.; Lucas, K.; Pöschl, U. Chemical modification of pro-inflammatory proteins by peroxynitrite increases activation of TLR4 and NF-kB: Implications for the health effects of air pollution and oxidative stress. Redox Biol. 2020, 101581. [Google Scholar] [CrossRef]
- Bufe, A.; Gehlhar, K.; Schramm, G.; Schlaak, M.; Becker, W.M. Allergenic activity of a major grass pollen allergen is elevated in the presence of nasal secretion. Am. J. Respir. Crit. Care Med. 1998, 157, 1269–1276. [Google Scholar] [CrossRef][Green Version]
- Göbl, C.; Focke-Tejkl, M.; Najafi, N.; Schrank, E.; Madl, T.; Kosol, S.; Madritsch, C.; Dorofeeva, Y.; Flicker, S.; Thalhamer, J.; et al. Flexible IgE epitope-containing domains of Phl p 5 cause high allergenic activity. J. Allergy Clin. Immunol. 2017, 140, 1187–1191. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Matthiesen, F.; Løwenstein, H. Group V allergens in grass pollens. I. Purification and characterization of the group V allergen from Phleum pratense pollen, Phl p V. Clin. Exp. Allergy 1991, 21, 297–307. [Google Scholar] [CrossRef] [PubMed]
- Shiraiwa, M.; Ammann, M.; Koop, T.; Pöschl, U. Gas uptake and chemical aging of semisolid organic aerosol particles. Proc. Natl. Acad. Sci. USA 2011, 108, 11003. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Kampf, C.J.; Liu, F.; Reinmuth-Selzle, K.; Berkemeier, T.; Meusel, H.; Shiraiwa, M.; Pöschl, U. Protein Cross-Linking and Oligomerization through Dityrosine Formation upon Exposure to Ozone. Environ. Sci. Technol. 2015, 49, 10859–10866. [Google Scholar] [CrossRef][Green Version]
- Liu, F.; Lakey, P.S.J.; Berkemeier, T.; Tong, H.; Kunert, A.T.; Meusel, H.; Cheng, Y.; Su, H.; Fröhlich-Nowoisky, J.; Lai, S.; et al. Atmospheric protein chemistry influenced by anthropogenic air pollutants: Nitration and oligomerization upon exposure to ozone and nitrogen dioxide. Faraday Discuss. 2017, 200, 413–427. [Google Scholar] [CrossRef][Green Version]
- Shiraiwa, M.; Sosedova, Y.; Rouvière, A.; Yang, H.; Zhang, Y.; Abbatt, J.P.; Ammann, M.; Pöschl, U. The role of long-lived reactive oxygen intermediates in the reaction of ozone with aerosol particles. Nat. Chem. 2011, 3, 291. [Google Scholar] [CrossRef]
- Bedini, A.; Maurino, V.; Minero, C.; Vione, D. Theoretical and experimental evidence of the photonitration pathway of phenol and 4-chlorophenol: A mechanistic study of environmental significance. Photochem. Photobiol. Sci. 2012, 11, 418–424. [Google Scholar] [CrossRef][Green Version]
- Fuentes-Lemus, E.; Silva, E.; Barrias, P.; Aspee, A.; Escobar, E.; Lorentzen, L.G.; Carroll, L.; Leinisch, F.; Davies, M.J.; Lopez-Alarcon, C. Aggregation of alpha- and beta- caseins induced by peroxyl radicals involves secondary reactions of carbonyl compounds as well as di-tyrosine and di-tryptophan formation. Free Radic. Biol. Med. 2018, 124, 176–188. [Google Scholar] [CrossRef]
- Stadtman, E.R. Protein oxidation and aging. Free Radic. Res. 2006, 40, 1250–1258. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Lymar, S.V.; Hurst, J.K. Rapid reaction between peroxonitrite ion and carbon dioxide: Implications for biological activity. J. Am. Chem. Soc. 1995, 117, 8867–8868. [Google Scholar] [CrossRef]
- Lymar, S.V.; Jiang, Q.; Hurst, J.K. Mechanism of Carbon Dioxide-Catalyzed Oxidation of Tyrosine by Peroxynitrite. Biochemistry 1996, 35, 7855–7861. [Google Scholar] [CrossRef] [PubMed]
- Quijano, C.; Romero, N.; Radi, R. Tyrosine nitration by superoxide and nitric oxide fluxes in biological systems: Modeling the impact of superoxide dismutase and nitric oxide diffusion. Free Radic. Biol. Med. 2005, 39, 728–741. [Google Scholar] [CrossRef] [PubMed]
- Ke, Z.; Huang, Q. Effect of protein structure and/or conformation on the dityrosine cross-linking induced by haem-hydrogen peroxide. Biochim. Biophys. Acta (BBA) Gen. Subj. 2016, 1860, 2232–2238. [Google Scholar] [CrossRef]
- Correia, M.; Neves-Petersen, M.T.; Jeppesen, P.B.; Gregersen, S.; Petersen, S.B. UV-Light Exposure of Insulin: Pharmaceutical Implications upon Covalent Insulin Dityrosine Dimerization and Disulphide Bond Photolysis. PLoS ONE 2012, 7, e50733. [Google Scholar] [CrossRef][Green Version]
- Lehrer, S.S.; Fasman, G.D. Ultraviolet Irradiation Effects in Poly-L-tyrosine and Model Compounds. Identification of Bityrosine as a Photoproduct*. Biochemistry 1967, 6, 757–767. [Google Scholar] [CrossRef]
- Malencik, D.A.; Anderson, S.R. Fluorometric characterization of dityrosine: Complex formation with boric acid and borate ion. Biochem. Biophys. Res. Commun. 1991, 178, 60–67. [Google Scholar] [CrossRef]
- Liu, F.; Reinmuth-Selzle, K.; Lai, S.; Weller, M.G.; Pöschl, U.; Kampf, C.J. Simultaneous determination of nitrated and oligomerized proteins by size exclusion high-performance liquid chromatography coupled to photodiode array detection. J. Chromatogr. A 2017, 1495, 76–82. [Google Scholar] [CrossRef]
- Selzle, K.; Ackaert, C.; Kampf, C.J.; Kunert, A.T.; Duschl, A.; Oostingh, G.J.; Pöschl, U. Determination of nitration degrees for the birch pollen allergen Bet v 1. Anal. Bioanal. Chem. 2013, 405, 8945–8949. [Google Scholar] [CrossRef]
- Yang, H.; Zhang, Y.; Pöschl, U. Quantification of nitrotyrosine in nitrated proteins. Anal. Bioanal. Chem. 2010, 397, 879–886. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Zhang, Y.; Yang, H.; Pöschl, U. Analysis of nitrated proteins and tryptic peptides by HPLC-chip-MS/MS: Site-specific quantification, nitration degree, and reactivity of tyrosine residues. Anal. Bioanal. Chem. 2011, 399, 459–471. [Google Scholar] [CrossRef] [PubMed]
- Sander, R. Compilation of Henry’s law constants (version 4.0) for water as solvent. Atmos. Chem. Phys. 2015, 15, 4399–4981. [Google Scholar] [CrossRef][Green Version]
- Umweltbundesamt. Trend der Ozon-Jahresmittelwerte. Available online: https://www.umweltbundesamt.de/sites/default/files/medien/384/bilder/dateien/7_abb_trend-ozon-jmw_2020-10-09.xlsx (accessed on 8 March 2021).
- Umweltbundesamt. Zahl der Tage mit Überschreitung des Ozon-Zielwertes (120 µg/m3) Zum Schutz der Menschlichen Gesundheit. Available online: https://www.umweltbundesamt.de/sites/default/files/medien/384/bilder/dateien/5_abb_ozon-ueberschreitung-120_2020-10-09.xlsx (accessed on 8 March 2021).
- Umweltbundesamt. Stickstoffdioxid (NO2) im Jahr 2019. Available online: https://www.umweltbundesamt.de/sites/default/files/medien/2546/dokumente/no2_2019.xlsx (accessed on 12 March 2021).
- Kouti, L.; Noroozian, M.; Akhondzadeh, S.; Abdollahi, M.; Javadi, M.R.; Faramarzi, M.A.; Mousavi, S.; Ghaeli, P. Nitric oxide and peroxynitrite serum levels in Parkinson’s disease: Correlation of oxidative stress and the severity of the disease. Eur. Rev. Med. Pharmacol. Sci. 2013, 17, 964–970. [Google Scholar]
UV | MS | ||||
---|---|---|---|---|---|
DD (%) | DiTyr | ND (%) | NTyr | NTyr | |
O3/NO2 (50/50 ppb), 10 h | 2.0 | 0.2 | 4.5 | 0.5 | 0.4 |
O3/NO2 (200/200 ppb), 2 h | 2.8 | 0.3 | 6.2 | 0.7 | 0.7 |
O3/NO2 (200/200 ppb), 10 h | 5.0 | 0.6 | 9.6 | 1.2 | 1.1 |
ONOO–/Tyr (1/1) | 3.6 | 0.4 | 16.8 | 2.0 | 1.1 |
ONOO–/Tyr (3/1) | 2.4 | 0.3 | 21.9 | 2.6 | 2.6 |
ONOO–/Tyr (5/1) | 1.5 | 0.2 | 21.8 | 2.6 | 2.7 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Backes, A.T.; Reinmuth-Selzle, K.; Leifke, A.L.; Ziegler, K.; Krevert, C.S.; Tscheuschner, G.; Lucas, K.; Weller, M.G.; Berkemeier, T.; Pöschl, U.; Fröhlich-Nowoisky, J. Oligomerization and Nitration of the Grass Pollen Allergen Phl p 5 by Ozone, Nitrogen Dioxide, and Peroxynitrite: Reaction Products, Kinetics, and Health Effects. Int. J. Mol. Sci. 2021, 22, 7616. https://doi.org/10.3390/ijms22147616
Backes AT, Reinmuth-Selzle K, Leifke AL, Ziegler K, Krevert CS, Tscheuschner G, Lucas K, Weller MG, Berkemeier T, Pöschl U, Fröhlich-Nowoisky J. Oligomerization and Nitration of the Grass Pollen Allergen Phl p 5 by Ozone, Nitrogen Dioxide, and Peroxynitrite: Reaction Products, Kinetics, and Health Effects. International Journal of Molecular Sciences. 2021; 22(14):7616. https://doi.org/10.3390/ijms22147616
Chicago/Turabian StyleBackes, Anna T., Kathrin Reinmuth-Selzle, Anna Lena Leifke, Kira Ziegler, Carola S. Krevert, Georg Tscheuschner, Kurt Lucas, Michael G. Weller, Thomas Berkemeier, Ulrich Pöschl, and Janine Fröhlich-Nowoisky. 2021. "Oligomerization and Nitration of the Grass Pollen Allergen Phl p 5 by Ozone, Nitrogen Dioxide, and Peroxynitrite: Reaction Products, Kinetics, and Health Effects" International Journal of Molecular Sciences 22, no. 14: 7616. https://doi.org/10.3390/ijms22147616