Adjuvant and Inflammatory Effects in Mice After Subchronic Inhalation of Allergen and Ozone-Initiated Limonene Reaction Products

REFERENCES

• Alberg , T. , Nilsen , A. , Hansen , J.S. , Nygaard , U. C. and Lovik , M. 2011 . Nitrogen dioxide: No influence on allergic sensitization in an intranasal mouse model with ovalbumin and diesel exhaust particles . Inhal. Toxicol , 23 : 268 – 276 .
   PubMed Web of Science ®Google Scholar
• Anderson , S. E. , Jackson , L. G. , Franko , J. and Wells , J. R. 2010 . Evaluation of dicarbonyls generated in a simulated indoor air environment using an in vitro exposure system . Toxicol. Sci , 115 : 453 – 461 .
   PubMed Web of Science ®Google Scholar
• Anderson , S. E. , Khurshid , S. S. , Meade , B. J. , Lukomska , E. and Wells , J. R. 2013 . Toxicological analysis of limonene reaction products using an in vitro exposure system . Toxicol. In Vitro , 27 : 721 – 730 .
   PubMed Web of Science ®Google Scholar
• Anderson , S. E. , Wells , J. , Fedorowicz , A. , Butterworth , L. F. , Meade , B. and Munson , A. E. 2007 . Evaluation of the contact and respiratory sensitization potential of volatile organic compounds generated by simulated indoor air chemistry . Toxicol. Sci , 97 : 355 – 363 .
   PubMed Web of Science ®Google Scholar
• Atkinson , R. and Arey , J. 2003 . Gas-phase troposheric chemistry of biogenic volatile organic compounds: A review . Atmos. Environ , 37 : S197 – S219 .
   Web of Science ®Google Scholar
• Backus , G. S. , Howden , R. , Fostel , J. , Bauer , A. K. , Cho , H. Y. , Marzec , J. , Peden , D. B. and Kleeberger , S. R. 2010 . Protective role of interleukin-10 in ozone-induced pulmonary inflammation . Environ. Health Perspect , 118 : 1721 – 1727 .
   PubMed Web of Science ®Google Scholar
• Basha , M. A. , Gross , K. B. , Gwizdala , C. J. , Haidar , A. H. and Popovich , J. Jr. 1994 . Bronchoalveolar lavage neutrophilia in asthmatic and healthy volunteers after controlled exposure to ozone and filtered purified air . Chest , 106 : 1757 – 1765 .
   PubMed Web of Science ®Google Scholar
• Bhalla , D. K. 1999 . Ozone-induced lung inflammation and mucosal barrier disruption: Toxicology, mechanisms, and implications . J. Toxicol. Environ. Health B , 2 : 31 – 86 .
   PubMed Web of Science ®Google Scholar
• Boverhof , D .R. , Billington , R. , Gollapudi , B. B. , Hotchkiss , J. A. , Krieger , S. M. , Poole , A. , Wiescinski , C. M. and Woolhiser , M. R. 2008 . Respiratory sensitization and allergy: Current research approaches and needs . Toxicol. Appl. Pharmacol , 226 : 1 – 13 .
   PubMed Web of Science ®Google Scholar
• Calogirou , A. , Larsen , B. R. and Kotzias , D. 1999 . Gas-phase terpene oxidation products: A review . Atmos. Environ , 33 : 1423 – 1439 .
   Web of Science ®Google Scholar
• Chen , X. , Hopke , P. K. and Carter , W. P. 2011 . Secondary organic aerosol from ozonolysis of biogenic volatile organic compouEnviron . Sci. Technol , 45 : 276 – 282 .
   PubMed Web of Science ®Google Scholar
• Choi , H. S. , Song , H. S. , Ukeda , H. and Sawamura , M. 2000 . Radical-scavenging activities of citrus essential oils and their components: Detection using 1,1-diphenyl-2-picrylhydrazyl . J. Agric. Food Chem , 48 : 4156 – 4161 .
   PubMed Web of Science ®Google Scholar
• Clausen , P. A. , Wilkins , C. K. , Wolkoff , P. and Nielsen , G. D. 2001 . Chemical and biological evaluation of a reaction mixture of R-(+)-limonene/ozone: Formation of strong airway irritants . Environ. Int , 26 : 511 – 522 .
   PubMed Web of Science ®Google Scholar
• Clausen , S. K. , Bergqvist , M. , Poulsen , L. K. , Poulsen , O. M. and Nielsen , G. D. 2003 . Development of sensitisation or tolerance following repeated OVA inhalation in BALB/cJ mice. Dose-dependency and modulation by the Al(OH)3 adjuvant . Toxicology , 184 : 51 – 68 .
   PubMed Web of Science ®Google Scholar
• Faquim-Mauro , E. L. , Coffman , R. L. , Abrahamsohn , I. and Macedo , M. S. 1999 . Cutting edge: Mouse IgG1 antibodies comprise two functionally distinct types that are differentially regulated by IL-4 and IL-12 . J. Immunol , 163 : 3572 – 3576 .
   PubMed Web of Science ®Google Scholar
• Finkelman , F. D. , Rothenberg , M. E. , Brandt , E. B. , Morris , S. C. and Strait , R. T. 2005 . Molecular mechanisms of anaphylaxis: Lessons from studies with murine models . J. Allergy Clin. Immunol , 115 : 449 – 457 .
   PubMed Web of Science ®Google Scholar
• Fraternale , D. , Giamperi , L. , Bucchini , A. and Ricci , D. 2007 . Essential oil composition and antioxidant activity of aerial parts of Grindelia robusta from Central Italy . Fitoterapia , 78 : 443 – 445 .
   PubMed Web of Science ®Google Scholar
• Funabashi , H. , Shima , M. , Kuwaki , T. , Hiroshima , K. and Kuriyama , T. 2004 . Effects of repeated ozone exposure on pulmonary function and bronchial responsiveness in mice sensitized with ovalbumin . Toxicology , 204 : 75 – 83 .
   PubMed Web of Science ®Google Scholar
• Fukui , Y. , Sudo , N. , Yu , X.N. , Nukina , H. , Sogawa , H. and Kubo , C. 1997 . The restraint stress-induced reduction in lymphocyte cell number in lymphoid organs correlates with the suppression of in vivo antibody production . J. Neuroimmunol , 79 : 211 – 217 .
   PubMed Web of Science ®Google Scholar
• Hansen , J. S. , Larsen , S. T. , Poulsen , L. K. and Nielsen , G. D. 2007a . Adjuvant effects of inhaled mono-2-ethylhexyl phthalate in BALB/cJ mice . Toxicology , 232 : 79 – 88 .
   PubMed Web of Science ®Google Scholar
• Hansen , J. S. , Larsen , S. T. , Poulsen , L. K. and Nielsen , G. D. 2007b . Does lipophilicity per se cause adjuvant effects? Methyl palmitate as model substance does not affect ovalbumin sensitization . J. Toxicol. Environ. Health A , 70 : 128 – 137 .
   PubMed Web of Science ®Google Scholar
• Hirota , R. , Nakamura , H. , Bhatti , S. A. , Ngatu , N. R. , Muzembo , B. A. , Dumavibhat , N. , Eitoku , M. , Sawamura , M. and Suganuma , N. 2012 . Limonene inhalation reduces allergic airway inflammation in Dermatophagoides farinae-treated mice . Inhal. Toxicol , 24 : 373 – 381 .
   PubMed Web of Science ®Google Scholar
• Hogenesch , H. 2012 . Mechanism of immunopotentiation and safety of aluminum adjuvants . Front Immunol , 3 : 406
   PubMed Web of Science ®Google Scholar
• Keinan , E. , Alt , A. , Amir , G. , Bentur , L. , Bibi , H. and Shoseyov , D. 2005 . Natural ozone scavenger prevents asthma in sensitized rats . Bioorg. Med. Chem , 13 : 557 – 562 .
   PubMed Web of Science ®Google Scholar
• Kim , Y. W. , Kim , M. J. , Chung , B. Y. , Bang , D. Y. , Lim , S. K. , Choi , S. M. , Lim , D. S. , Cho , M. C. , Yoon , K. , Kim , H. S. , Kim , K. B. , Kim , Y. S. , Kwack , S. J. and Lee , B.-M. 2013 . Safety evaluation and risk assessment of d-limonene . J. Toxicol. Environ. Health B , 16 : 17 – 38 .
   PubMed Web of Science ®Google Scholar
• Larsen , S. T. , Hansen , J. S. , Hansen , E. W. , Clausen , P. A. and Nielsen , G. D. 2007 . Airway inflammation and adjuvant effect after repeated airborne exposures to di-(2-ethylhexyl) phthalate and ovalbumin in BALB/c mice . Toxicology , 235 : 119 – 129 .
   PubMed Web of Science ®Google Scholar
• Larsen , S. T. , Matsubara , S. , McConville , G. , Poulsen , S. S. and Gelfand , E. W. 2010 . Ozone increases airway hyperreactivity and mucus hyperproduction in mice previously exposed to allergen . J. Toxicol. Environ. Health A , 73 : 738 – 747 .
   PubMed Web of Science ®Google Scholar
• Lippmann , M. 1989 . Health effects of ozone. A critical review . J. Air Pollut. Control Assoc , 39 : 672 – 695 .
   Google Scholar
• Nazaroff , W. W. and Weschler , C. J. 2004 . Cleaning products and air fresheners: Exposure to primary and secondary air pollutants . Atmos. Environ , 38 : 2841 – 2865 .
   Web of Science ®Google Scholar
• Neuhaus-Steinmetz , U. , Uffhausen , F. , Herz , U. and Renz , H. 2000 . Priming of allergic immune responses by repeated ozone exposure in mice . Am. J. Respir. Cell Mol. Biol , 23 : 228 – 233 .
   PubMed Web of Science ®Google Scholar
• Nielsen , G. D. , Hansen , J. S. , Lund , R. M. , Bergqvist , M. , Larsen , S. T. , Clausen , S. K. , Thygesen , P. and Poulsen , O. M. 2002 . IgE-mediated asthma and rhinitis I: A role of allergen exposure? . Pharmacol. Toxicol , 90 : 231 – 242 .
   PubMedGoogle Scholar
• Nielsen , G. D. , Hougaard , K. S. , Larsen , S. T. , Hammer , M. , Wolkoff , P. , Clausen , P. A. , Wilkins , C. K. and Alarie , Y. 1999 . Acute airway effects of formaldehyde and ozone in BALB/c mice . Hum. Exp. Toxicol , 18 : 400 – 409 .
   PubMed Web of Science ®Google Scholar
• Norgaard , A. W. , Vibenholt , A. , Benassi , M. , Clausen , P. A. and Wolkoff , P. 2013 . Study of ozone-initiated limonene reaction products by low temperature plasma ionization mass spectrometry . J. Am. Soc. Mass Spectrom , 24 : 1090 – 1096 .
   PubMed Web of Science ®Google Scholar
• Osebold , J. W. , Zee , Y. C. and Gershwin , L. J. 1988 . Enhancement of allergic lung sensitization in mice by ozone inhalation . Proc. Soc. Exp. Biol. Med , 188 : 259 – 264 .
   PubMed Web of Science ®Google Scholar
• Oshiba , A. , Hamelmann , E. , Takeda , K. , Bradley , K. L. , Loader , J. E. , Larsen , G. L. and Gelfand , E. W. 1996 . Passive transfer of immediate hypersensitivity and airway hyperresponsiveness by allergen-specific immunoglobulin (Ig) E and IgG1 in mice . J. Clin. Invest , 97 : 1398 – 1408 .
   PubMed Web of Science ®Google Scholar
• Park , C. S. , Kim , T. B. , Lee , K. Y. , Moon , K. A. , Bae , Y. J. , Jang , M. K. , Cho , Y. S. and Moon , H. B. 2009 . Increased oxidative stress in the airway and development of allergic inflammation in a mouse model of asthma . Ann. Allergy Asthma Immunol , 103 : 238 – 247 .
   PubMed Web of Science ®Google Scholar
• Roberto , D. , Micucci , P. , Sebastian , T. , Graciela , F. and Anesini , C. 2010 . Antioxidant activity of limonene on normal murine lymphocytes: Relation to H2O2 modulation and cell proliferation . Basic Clin. Pharmacol. Toxicol , 106 : 38 – 44 .
   PubMed Web of Science ®Google Scholar
• Rohr , A. C. , Wilkins , C. K. , Clausen , P. A. , Hammer , M. , Nielsen , G. D. , Wolkoff , P. and Spengler , J. D. 2002 . Upper airway and pulmonary effects of oxidation products of (+)-α-pinene, d-limonene, and isoprene in BALB/c mice . Inhal. Toxicol , 14 : 663 – 684 .
   PubMed Web of Science ®Google Scholar
• Schelegle , E. S. , Siefkin , A. D. and McDonald , R. J. 1991 . Time course of ozone-induced neutrophilia in normal humans . Am. Rev. Respir. Dis , 143 : 1353 – 1358 .
   PubMed Web of Science ®Google Scholar
• Seltzer , J. , Bigby , B. G. , Stulbarg , M. , Holtzman , M.J. , Nadel , J. A. , Ueki , I. F. , Leikauf , G. D. , Goetzl , E. J. and Boushey , H. A. 1986 . O3-induced change in bronchial reactivity to methacholine and airway inflammation in humans . J. Appl. Physiol , 60 : 1321 – 1326 .
   PubMed Web of Science ®Google Scholar
• Siegel , P. D. , Al Humadi , N. H. , Nelson , E. R. , Lewis , D. M. and Hubbs , A. F. 1997 . Adjuvant effect of respiratory irritation on pulmonary allergic sensitization: Time and site dependency . Toxicol. Appl. Pharmacol , 144 : 356 – 362 .
   PubMed Web of Science ®Google Scholar
• Silberman , D. M. , Wald , M. R. and Genaro , A. M. 2003 . Acute and chronic stress exert opposing effects on antibody responses associated with changes in stress hormone regulation of T-lymphocyte reactivity . J. Neuroimmunol , 144 : 53 – 60 .
   PubMed Web of Science ®Google Scholar
• Sumitomo , M. , Nishikawa , M. , Fukuda , T. , Kaneko , T. , Ikeda , H. , Suzuki , S. and Okubo , T. 1990 . Effects of ozone exposure on experimental asthma in guinea pigs sensitized with ovalbumin through the airway . Int. Arch. Allergy Appl. Immunol , 93 : 139 – 147 .
   PubMedGoogle Scholar
• Taube , C. , Dakhama , A. and Gelfand , E. W. 2004 . Insights into the pathogenesis of asthma utilizing murine models . Int. Arch. Allergy Immunol , 135 : 173 – 186 .
   PubMed Web of Science ®Google Scholar
• Walser , M. L. , Desyaterik , Y. , Laskin , J. , Laskin , A. and Nizkorodov , S. A. 2008 . High-resolution mass spectrometric analysis of secondary organic aerosol produced by ozonation of limonene . Phys. Chem. Chem. Phys , 10 : 1009 – 1022 .
   PubMed Web of Science ®Google Scholar
• Weschler , C. J. 2000 . Ozone in indoor environments: Concentration and chemistry . Indoor Air , 10 : 269 – 288 .
   PubMed Web of Science ®Google Scholar
• Weschler , C. J. , Wells , J. R. , Poppendieck , D. , Hubbard , H. and Pearce , T. A. 2006 . Workgroup report: Indoor chemistry and health . Environ. Health Perspect , 114 : 442 – 446 .
   PubMed Web of Science ®Google Scholar
• Wilkins , C. K. , Clausen , P. A. , Wolkoff , P. , Larsen , S. T. , Hammer , M. , Larsen , K. , Hansen , V. and Nielsen , G. D. 2001 . Formation of strong airway irritants in mixtures of isoprene/ozone and isoprene/ozone/nitrogen dioxide . Environ. Health Perspect , 109 : 937 – 941 .
   PubMed Web of Science ®Google Scholar
• Wolkoff , P. , Clausen , P.A. , Larsen , K. , Hammer , M. , Larsen , S. T. and Nielsen , G. D. 2008 . Acute airway effects of ozone-initiated d-limonene chemistry: Importance of gaseous products . Toxicol. Lett , 181 : 171 – 176 .
   PubMed Web of Science ®Google Scholar
• Wolkoff , P. , Clausen , P. A. , Larsen , S. T. , Hammer , M. and Nielsen , G. D. 2012 . Airway effects of repeated exposures to ozone-initiated limonene oxidation products as model of indoor air mixtures . Toxicol. Lett , 209 : 166 – 172 .
   PubMed Web of Science ®Google Scholar
• Yamauchi , T. , Shima , M. , Kuwaki , T. , Ando , M. , Ohmichi , M. , Fukuda , Y. and Adachi , M. 2002 . Acute effects of ozone exposure on lung function in mice sensitized to ovalbumin . Toxicology , 172 : 69 – 78 .
   PubMed Web of Science ®Google Scholar