Diacetyl increases sensory innervation and substance p production in rat trachea

Toxicologic Pathology

Volumn 42, Issue 3, 2014, Pages 582-590

  Goravanahally, Madhusudan P ^a,b   Hubbs, Ann F ^a   Fedan, Jeffery S ^a   Kashon, Michael L ^a   Battelli, Lori A ^a   Mercer, Robert R ^a   Goldsmith, W Travis ^a   Jackson, Mark C ^a   Cumpston, Amy ^a   Frazer, David G ^a   Dey, Richard D ^b  

^a NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

^b WEST VIRGINIA UNIVERSITY   (United States)

Author keywords

airway epithelium; airway inflammation; airway innervation; cough; flavorings; inhalation toxicity

Indexed keywords

2,3 BUTANEDIONE; SUBSTANCE P; FLUORESCENT DYE;

ANIMAL EXPERIMENT; ARTICLE; BASEMENT MEMBRANE; CONTROLLED STUDY; GENE PRODUCT; IMMUNOREACTIVITY; INHALATION; MALE; NERVE FIBER; NERVE FIBER DENSITY; NERVE FIBER TRANSPORT; NERVOUS SYSTEM PARAMETERS; NODOSE GANGLION; NONHUMAN; PRIORITY JOURNAL; RAT; RESPIRATORY EPITHELIUM; SENSORY NERVE; TRACHEA MUCOSA; VAGUS NERVE; ANIMAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; EXPOSURE; METABOLISM; NERVE CELL; RESPIRATORY TRACT MUCOSA; SPRAGUE DAWLEY RAT; TOXICITY; TRACHEA;

ANIMALS; DIACETYL; FLUORESCENT DYES; INHALATION EXPOSURE; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RESPIRATORY MUCOSA; SUBSTANCE P; TRACHEA;

EID: 84899117886     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623313493689     Document Type: Article

References (55)

1. Akpinar-Elci M., Travis W. D., Lynch D. A., Kreiss K.. Bronchiolitis obliterans syndrome in popcorn production plant workers. Eur Respir J. 2004 ; 24: 298-302 (Pubitemid 39139800)
2. Anderson S. E., Wells J., Fedorowicz A., Butterworth L., Meade B., Munson A. E.. Evaluation of the contact and respiratory sensitization potential of volatile organic compounds generated by simulated indoor air chemistry. Toxicol Sci. 2007 ; 97: 355-63 (Pubitemid 47073851)
3. Barnes P. J.. Asthma as an axon reflex. Lancet. 1986 ; 1: 242-45 (Pubitemid 16132855)
4. Barnes P. J.. Neurogenic inflammation in airways and its modulation. Arch Int Pharmacodyn Ther. 1990 ; 303: 67-82 (Pubitemid 20192251)
5. Canning B. J., Mori N., Mazzone S. B.. Vagal afferent nerves regulating the cough reflex. Respir Physiol Neurobiol. 2006 ; 152: 223-42 (Pubitemid 44037512)
6. Colin W., Donoff R. B., Foote W. E.. Fluorescent latex microspheres as a retrograde tracer in the peripheral nervous system. Brain Res. 1989 ; 486: 334-39 (Pubitemid 19135145)
7. Dey R. D., Satterfield B., Altemus J. B.. Innervation of tracheal epithelium and smooth muscle by neurons in airway ganglia. Anat Rec. 1999 ; 254: 166-72 (Pubitemid 29053220)
8. Fedan J. S., Dowdy J. A., Fedan K. B., Hubbs A. F.. Popcorn worker's lung: In vitro exposure to diacetyl, an ingredient in microwave popcorn butter flavoring, increases reactivity to methacholine. Toxicol Appl Pharmacol. 2006 ; 215: 17-22 (Pubitemid 44118401)
9. Gloede E., Cichocki J. A., Baldino J. B., Morris J. B.. A validated hybrid computational fluid dynamics-physiologically based pharmacokinetic model for respiratory tract vapor absorption in the human and rat and its application to inhalation dosimetry of diacetyl. Toxicol Sci. 2011 ; 123: 231-46
10. Hubbs A. F., Battelli L. A., Goldsmith W. T., Porter D. W., Frazer D., Friend S., Schwegler-Berry D., Mercer R. R., Reynolds J. S., Grote A., Castranova V., Kullman G., Fedan J. S., Dowdy J., Jones W. G.. Necrosis of nasal and airway epithelium in rats inhaling vapors of artificial butter flavoring. Toxicol Appl Pharmacol. 2002 ; 185: 128-35 (Pubitemid 36062803)
11. Hubbs A. F., Goldsmith W. T., Kashon M. L., Frazer D., Mercer R. R., Battelli L. A., Kullman G. J., Schwegler-Berry D., Friend S., Castranova V.. Respiratory toxicologic pathology of inhaled diacetyl in Sprague-Dawley rats. Toxicol Pathol. 2008 ; 36: 330-44 (Pubitemid 351534484)
12. Hunter D. D., Carrell-Jacks L. A., Batchelor T. P., Dey R. D.. Role of nerve growth factor in ozone-induced neural responses in early postnatal airway development. Am J Respir Cell Mol Biol. 2011 ; 45: 359-65
13. Hunter D. D., Satterfield B. E., Huang J., Fedan J. S., Dey R. D.. Toluene diisocyanate enhances substance P in sensory neurons innervating the nasal mucosa. Am J Respir Crit Care Med. 2000 ; 161: 543-49 (Pubitemid 30129465)
14. Hunter D. D., Undem B. J.. Identification and substance P content of vagal afferent neurons innervating the epithelium of the guinea pig trachea. Am J Respir Crit Care Med. 1999 ; 159: 1943-48 (Pubitemid 29275067)
15. Inoue A., Ikoma K., Morioka N., Kumagai K., Hashimoto T., Hide I., Nakata Y.. Interleukin-1beta induces substance P release from primary afferent neurons through the cyclooxygenase-2 system. J Neurochem. 1999 ; 73: 2206-13 (Pubitemid 29491836)
16. Joos G. F., Germonpre P. R., Kips J. C., Peleman R. A., Pauwels R. A.. Sensory neuropeptides and the human lower airways: Present state and future directions. Eur Respir J. 1994 ; 7: 1161-71 (Pubitemid 24187338)
17. Kanwal R.. Bronchiolitis obliterans in workers exposed to flavoring chemicals. Curr Opin Pulm Med. 2008 ; 14: 141-46 (Pubitemid 351324803)
18. Kanwal R., Kullman G., Piacitelli C., Boylstein R., Sahakian N., Martin S., Fedan K., Kreiss K.. Evaluation of flavorings-related lung disease risk at six microwave popcorn plants. J Occup Environ Med. 2006 ; 48: 149-57 (Pubitemid 43237946)
19. Kanwal R., Kullman G., Sahakian N., Harber H., Materna B., Kreiss K.. Severe fixed obstructive lung disease in flavoring workers. Am J Respir Crit Care Med. 2007 ; 175: A427
20. Katz L. C., Burkhalter A., Dreyer W. J.. Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature. 1984 ; 310: 498-500 (Pubitemid 14052411)
21. Kessler J. A., Freidin M. M., Kalberg C., Chandross K. J.. Cytokines regulate substance P expression in sympathetic neurons. Regul Pept. 1993 ; 46: 70-75
22. King T. E.. Bronchiolitis obliterans. Lung. 1989 ; 167: 69-93
23. Kreiss K.. Flavoring-related bronchiolitis obliterans. Curr Opin Allergy Clin Immunol. 2007 ; 7: 162-67 (Pubitemid 46411517)
24. Kreiss K., Gomaa A., Kullman G., Fedan K., Simoes E. J., Enright P. L.. Clinical bronchiolitis obliterans in workers at a microwave-popcorn plant. N Engl J Med. 2002 ; 347: 330-38 (Pubitemid 34815355)
25. Lauweryns J. M., van Ranst L.. Protein gene product 9.5 expression in the lungs of humans and other mammals. Immunocytochemical detection in neuroepithelial bodies, neuroendocrine cells and nerves. Neurosci Lett. 1988 ; 85: 311-16 (Pubitemid 18050863)
26. Lee L. Y., Kwong K., Lin Y. S., Gu Q.. Hypersensitivity of bronchopulmonary C-fibers induced by airway mucosal inflammation: Cellular mechanisms. Pulm Pharmacol Ther. 2002 ; 15: 199-204 (Pubitemid 34754106)
27. Lundberg J. M., Hokfelt T., Martling C. R., Saria A., Cuello C.. Substance P-immunoreactive sensory nerves in the lower respiratory tract of various mammals including man. Cell Tissue Res. 1984 ; 235: 251-61 (Pubitemid 14189762)
28. Lundberg J. M., Saria A.. Capsaicin-induced desensitization of airway mucosa to cigarette smoke, mechanical and chemical irritants. Nature. 1983 ; 302: 251-53 (Pubitemid 13109195)
29. Mapp C. E., Lucchini R. E., Miotto D., Chitano P., Jovine L., Saetta M., Maestrelli P., Springall D. R., Polak J., Fabbri L. M.. Immunization and challenge with toluene diisocyanate decrease tachykinin and calcitonin gene-related peptide immunoreactivity in guinea pig central airways. Am J Respir Crit Care Med. 1998 ; 158: 263-69 (Pubitemid 28337190)
30. Morgan D. L., Flake G. P., Kirby P. J., Palmer S. M.. Respiratory toxicity of diacetyl in C57BL/6 mice. Toxicol Sci. 2008 ; 103: 169-80 (Pubitemid 351524488)
31. Morris J. B.. Biologically-based modeling insights in inhaled vapor absorption and dosimetry. Pharmacol Ther. 2012 ; 136: 401-13
32. Morris J. B., Hubbs A. F.. Inhalation dosimetry of diacetyl and butyric acid, two components of butter flavoring vapors. Toxicol Sci. 2009 ; 108: 173-83
33. Guide for the care and use of laboratory animals. Washington, DC: National Academic Press ; 2011 :
34. Nieber K., Baumgarten C. R., Rathsack R., Furkert J., Oehme P., Kunkel G.. Substance P and beta-endorphin-like immunoreactivity in lavage fluids of subjects with and without allergic asthma. J Allergy Clin Immunol. 1992 ; 90: 646-52
35. Nieber K., Baumgarten C. R., Witzel A., Rathsack R., Oehme P., Brunnee T., Kleine-Tebbe J., Kunkel G.. The possible role of substance P in the allergic reaction, based on two different provocation models. Int Arch Allergy Appl Immunol. 1991 ; 94: 334-38
36. Washington, DC: Department of Health and Human Services ; 2011: 1-321.
37. Ollerenshaw S. L., Jarvis D., Sullivan C. E., Woolcock A. J.. Substance P immunoreactive nerves in airways from asthmatics and nonasthmatics. Eur Respir J. 1991 ; 4: 673-82
38. Palmer S. M., Flake G. P., Kelly F. L., Zhang H. L., Nugent J. L., Kirby P. J., Foley J. F., Gwinn W. M., Morgan D. L.. Severe airway epithelial injury, aberrant repair and bronchiolitis obliterans develops after diacetyl instillation in rats. PLoS One. 2011 ; 6: e17644
39. Pedersen K. E., Meeker S. N., Riccio M. M., Undem B. J.. Selective stimulation of jugular ganglion afferent neurons in guinea pig airways by hypertonic saline. J Appl Physiol. 1998 ; 84: 499-506 (Pubitemid 28081102)
40. Pernow B.. Role of tachykinins in neurogenic inflammation. J Immunol. 1985 ; 135: 812s - 815s
41. Roberts D. W., York M., Basketter D. A.. Structure-activity relationships in the murine local lymph node assay for skin sensitization: Alpha, beta-diketones. Contact Dermatitis. 1999 ; 41: 14-17 (Pubitemid 29324884)
42. Sekizawa K., Jia Y. X., Ebihara T., Hirose Y., Hirayama Y., Sasaki H.. Role of substance P in cough. Pulm Pharmacol. 1996 ; 9: 323-28
43. Skoff A. M., Zhao C., Adler J. E.. Interleukin-1alpha regulates substance P expression and release in adult sensory neurons. Exp Neurol. 2009 ; 217: 395-400
44. Thompson R. J., Doran J. F., Jackson P., Dhillon A. P., Rode J.. PGP 9.5 - a new marker for vertebrate neurons and neuroendocrine cells. Brain Res. 1983 ; 278: 224-28 (Pubitemid 14219291)
45. Trevisani M., Siemens J., Materazzi S., Bautista D. M., Nassini R., Campi B., Imamachi N., Andre E., Patacchini R., Cottrell G. S., Gatti R., Basbaum A. I., Bunnett N. W., Julius D., Geppetti P.. 4-Hydroxynonenal, an endogenous aldehyde, causes pain and neurogenic inflammation through activation of the irritant receptor TRPA1. Proc Natl Acad Sci USA. 2007 ; 104: 13519-24 (Pubitemid 47293977)
46. van Rooy F. G., Rooyackers J. M., Prokop M., Houba R., Smit L. A., Heederik D. J.. Bronchiolitis obliterans syndrome in chemical workers producing diacetyl for food flavorings. Am J Respir Crit Care Med. 2007 ; 176: 498-504 (Pubitemid 47358104)
47. van Rooy F. G., Smit L. A., Houba R., Zaat V. A., Rooyackers J. M., Heederik D. J.. A cross-sectional study of lung function and respiratory symptoms among chemical workers producing diacetyl for food flavourings. Occup Environ Med. 2009 ; 66: 105-110
48. Vatrella A., Montagnani S., Calabrese C., Parrella R., Pelaia G., Biscione G. L., Corcione N., Marsico S. A., Guerra G.. Neuropeptide expression in the airways of COPD patients and smokers with normal lung function. J Biol Regul Homeost Agents. 2010 ; 24: 425-32
49. Weissner W., Winterson B. J., Stuart-Tilley A., Devor M., Bove G. M.. Time course of substance P expression in dorsal root ganglia following complete spinal nerve transection. J Comp Neurol. 2006 ; 497: 78-87 (Pubitemid 43844569)
50. Wilfong E. R., Dey R. D.. Nerve growth factor and substance P regulation in nasal sensory neurons after toluene diisocyanate exposure. Am J Respir Cell Mol Biol. 2004 ; 30: 793-800 (Pubitemid 38736902)
51. Wong J., Oblinger M. M.. NGF rescues substance P expression but not neurofilament or tubulin gene expression in axotomized sensory neurons. J Neurosci. 1991 ; 11: 543-52
52. Woolf C. J., Salter M. W.. Neuronal plasticity: Increasing the gain in pain. Science. 2000 ; 288: 1765-69
53. Wu Z. X., Dey R. D.. Nerve growth factor-enhanced airway responsiveness involves substance P in ferret intrinsic airway neurons. Am J Physiol Lung Cell Mol Physiol. 2006 ; 291: L111-18
54. Wu Z. X., Satterfield B. E., Dey R. D.. Substance P released from intrinsic airway neurons contributes to ozone-enhanced airway hyperresponsiveness in ferret trachea. J Appl Physiol. 2003 ; 95: 742-50 (Pubitemid 36944300)
55. Wu Z. X., Satterfield B. E., Fedan J. S., Dey R. D.. Interleukin-1beta- induced airway hyperresponsiveness enhances substance P in intrinsic neurons of ferret airway. Am J Physiol Lung Cell Mol Physiol. 2002 ; 283: L909-17 Health