Potentiation of pulmonary reflex response to capsaicin 24 h following whole-body acrolein exposure is mediated by TRPV1

Respiratory Physiology and Neurobiology

Volumn 160, Issue 2, 2008, Pages 160-171

  Hazari, Mehdi S ^a   Rowan, William H ^b   Winsett, Darrell W ^b   Ledbetter, Allen D ^b   Haykal Coates, Najwa ^b   Watkinson, William P ^b   Costa, Daniel L ^b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

Author keywords

Air pollutants; Airway chemoreflex; Apnea; Hyperresponsiveness; Pulmonary C fibers; Sensitization

Indexed keywords

ACROLEIN; CAPSAICIN; VANILLOID RECEPTOR 1;

APNEA; ARTICLE; BRONCHOSPASM; CHEMORECEPTOR REFLEX; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; HERING BREUER REFLEX; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

ACROLEIN; AIR POLLUTANTS; ANIMALS; CAPSAICIN; CHEMORECEPTORS; DRUG SYNERGISM; IRRITANTS; MALE; NERVE FIBERS, UNMYELINATED; PULMONARY VENTILATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, NEUROKININ-1; REFLEX; RESPIRATION; RESPIRATORY MECHANICS; RESPIRATORY SYSTEM; SENSORY SYSTEM AGENTS; SUBSTANCE P; TRPV CATION CHANNELS;

EID: 38649085305     PISSN: 15699048     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.resp.2007.09.003     Document Type: Article

References (65)

1. Ahluwalia A., Maggi C.A., Santicioli P., Lecci A., and Giuliani S. Characterization of the capsaicin-sensitive component of cyclophosphamide-induced inflammation in the rat urinary bladder. Br. J. Pharmacol. 111 (1994) 1017-1022
2. Akabori H., Yamamoto H., Tsuchihashi H., Mori T., Fujino K., Shimizu T., Endo Y., and Tani T. Transient receptor potential vanilloid 1 antagonist, capsazepine, improves survival in a rat hemorrhagic shock model. Ann. Surg. 246 6 (2007) 964-970
3. Alarie Y. Sensory irritation by airborne chemicals. Crit. Rev. Toxicol. 24 (1973) 299-363
4. Alarie Y. Computer-based bioassay for evaluation of sensory irritation of airborne chemicals and its limit of detection. Arch. Toxicol. 72 5 (1998) 277-288
5. Andrade E.L., Ferreira J., Andre E., and Calixto J.B. Contractile mechanisms coupled to TRPA1 receptor activation in rat urinary bladder. Biochem. Pharmacol. 72 1 (2006) 104-114
6. Barnes P.J., Baraniuk J.N., and Belvisi M.G. Neuropeptides in the respiratory tract. Part 1. Am. Rev. Respir. Dis. 144 (1991) 1187-1198
7. Bautista D.M., Jordt S.-E., Nikai T., Tsuruda P.R., Read A.J., Poblete J., Yamoah E.N., Basbaum A.I., and Julius D. TRPA1 mediates the inflammatory actions of environmental irritants and proalgesic agents. Cell 124 (2006) 1269-1282
8. Bonham A.C., Chen C.Y., Mutoh T., and Joad J.P. Lung C-fiber CNS reflex: role in the respiratory consequences of extended environmental tobacco smoke exposure in young guinea pigs. Environ. Health Perspect. 109 suppl. 4 (2001) 573-578
9. Campen M.J., Costa D.L., and Watkinson W.P. Cardiac and thermoregulatory toxicity of residual oil fly ash in cardiopulmonary-compromised rats. Inhal. Toxicol. 12 (2000) 7-22
10. Coleridge H.M., and Coleridge J.C.G. Pulmonary reflexes: neural mechanisms of pulmonary defense. Annu. Rev. Physiol. 56 (1994) 69-91
11. Dinis P., Charrua A., Avelino A., Yaqoob M., Bevan C., Nagy I., and Cruz F. Anandamide-evoked activation of vanilloid receptor 1 contributes to the development of bladder hyperreflexia and nociceptive transmission to spinal dorsal horn neurons in cystitis. J. Neurosci. 24 (2004) 11253-11263
12. Egle J.L. Retention of inhaled formaldehyde, proprionaldehyde, and acrolein in the dog. Arch. Environ. Health 25 (1972) 119-124
13. Fang L.B., Morton R.F., Wang A.L., and Lee L.-Y. Bronchoconstriction and delayed rapid shallow breathing induced by cigarette smoke inhalation in anesthetized rats. Lung 169 3 (1991) 153-164
14. Gu Q., Ruan T., Hong J.-H., Burki N., and Lee L.-Y. Hypersensitivity of pulmonary C fibers induced by adenosine in anesthetized rats. J. Appl. Physiol. 95 (2003) 1315-1324
15. Ho C.Y., and Lee L.-Y. Ozone enhances excitabilities of pulmonary C-fibers to chemical and mechanical stimuli in anesthetized rats. J. Appl. Physiol. 85 4 (1998) 1509-1515
16. Hong J.L., Rodger I.W., and Lee L.-Y. Cigarette smoke-induced bronchoconstriction: involvement of cholinergic mechanisms, tachykinins and cycloxygenase products. J. Appl. Physiol. 78 (1995) 2260-2266
17. Kobayashi K., Fukuoaka T., Obaka K., Yamanaka H., Dai Y., Tokunaga A., and Noguchi K. Distinct expression of TRPM8, TRPA1, and TRPV1 mRNAs in rat primary afferent neurons with adelta/c-fibers and colocalization with trk receptors. J. Comp. Neurol. 493 4 (2005) 596-606
18. Kou Y.R., and Lee L.-Y. Stimulation of rapidly adapting receptors in canine lungs by a single breath of cigarette smoke. J. Appl. Physiol. 68 3 (1990) 1203-1210
19. Kratschmer F. Reflexe von der Nasenschleimhaut auf Athmung und Kreislauf. Sitzber. Akad. Wiss. Wien. 62 (1870) 147-170
20. Kratschmer F. On reflexes from the nasal mucous membrane on respiration and circulation. Respir. Physiol. 127 2/3 (2001) 93-104
21. Kwong K., Wu Z.-X., Kashon M.L., Krajnak K.M., Wise P.M., and Lee L.-Y. Chronic smoking enhances tachykinin synthesis and airway responsiveness in guinea pigs. Am. J. Respir. Cell Mol. Biol. 25 (2001) 299-305
22. Lai C.J., and Kou Y.R. Stimulation of pulmonary rapidly adapting receptors by inhaled wood smoke in rats. J. Physiol. 508 2 (1998) 597-607
23. Lai C.J., and Kou Y.R. Stimulation of vagal pulmonary C fibers by inhaled wood smoke in rats. J. Appl. Physiol. 84 1 (1998) 30-36
24. Larsen S.T., and Nielsen G.D. Effects of methacrolein on the respiratory tract in mice. Toxicol. Lett. 114 (2000) 197-202
25. Lee L.-Y., and Widdicombe J.G. Modulation of airway sensitivity to inhaled irritants: role of inflammatory mediators. Environ. Health Perspect. 109 4 (2001) 585-589
26. Lee L.-Y., Kou Y.R., Frazier D.T., Beck E.R., Pisarri T.E., Coleridge H.M., and Coleridge J.C. Stimulation of vagal pulmonary C-fibers by a single breath of cigarette smoke in dogs. J. Appl. Physiol. 66 5 (1989) 2032-2038
27. Lee B.P., Morton R.F., and Lee L.-Y. Acute effects of acrolein on breathing: role of vagal bronchopulmonary afferents. J. Appl. Physiol. 72 3 (1992) 1050-1056
28. Lunbald L., Saria A., Lundberg J.M., and Anggard A. Increased vascular permeability in rat nasal mucosa induced by substance P and stimulation of capsaicin-sensitive trigeminal neurons. Acta Otolaryngol. 96 (1983) 479-484
29. Lundberg J.M., Lundlbad L., Saria A., and Anggard A. Inhibition of cigarette smoke-induced oedema in the nasal mucosa by capsaicin pretreatment and a substance P antagonist. Arch. Pharmacol. 326 (1984) 181-185
30. Maggi C.A., Lecci A., Santicioli P., Del Bianco E., and Guiliani S. Cyclophosphamide cystitis in rats: involvement of capsaicin-sensitive primary afferents. J. Auton. Nerv. Syst. 38 (1992) 201-208
31. Mitchell J.E., Campbell A.P., New N.E., Sadofsky L.R., Kastelik J.A., Mulrennan S.A., Compton S.J., and Morice A.H. Expression and characterization of the intracellular vanilloid receptor (TRPV1) in bronchi from patients with chronic cough. Exp. Lung Res. 31 3 (2005) 296-306
32. Mohapatra D.P., and Nau C. Desensitization of capsaicin-activated currents in the vanilloid receptor TRPV1 is decreased by the cyclic AMP-dependent protein kinase pathway. J. Biol. Chem. 278 (2003) 50080-50090
33. Morris J.B., Stanek J., and Gianutsos G. Sensory nerve-mediated immediate nasal responses to inspired acrolein. J. Appl. Physiol. 87 5 (1999) 1877-1886
34. Mutoh T., Bonham A.C., and Joad J.P. Substance P in the nucleus of the solitary tract augments bronchopulmonary C fiber reflex output. Am. J. Physiol. Regul. Integr. Comp. Physiol. 279 (2000) R1215-R1223
35. Mutoh T., Joad J.P., and Bonham A.C. Chronic passive cigarette smoke exposure augments bronchopulmonary C-fibre inputs to nucleus tractus solitarii neurons and reflex output in young guinea pigs. J. Physiol. 523 (2000) 223-233
36. Myers A.C., Kajekar R., and Undem B.J. Allergic inflammation-induced neuropeptide production in rapidly adapting afferent nerves in guinea pig airways. Am. J. Physiol. Lung Cell. Mol. Physiol. 282 (2002) L775-L781
37. Ni D., Gu Q., Hu H.Z., Gao N., Zhu M.X., and Lee L.-Y. Thermal sensitivity of isolated vagal pulmonary sensory neurons: role of transient receptor potential vanilloid receptors. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291 3 (2006) R541-R550
38. Nielsen G. Mechanism of activation of the sensory irritant receptor by airborne chemicals. Crit. Rev. Toxicol. 21 (1991) 183-208
39. Nishino T., Kochi T., and Ishii M. Differences in respiratory reflex responses from the larynx, trachea, and bronchi in anesthetized female subjects. Anesthesiology 84 (1996) 70-74
40. Oortgiesen M., Veronesi B., Eichenbaum G., Kiser P.F., and Simon S.A. Residual oil fly ash and charged polymers activate epithelial cells and nociceptive sensory neurons. Am. J. Physiol. Lung Cell Mol. Physiol. 278 4 (2000) L683-L695
41. Ramirez J.M., and Viemari J.C. Determinants of inspiratory activity. Respir. Physiol. Neurobiol. 147 2/3 (2005) 145-157
42. Reinhardt T.E., and Ottmar R.D. Baseline measurements of smoke exposure amoung wildland firefighters. J. Occup. Environ. Hyg. 1 9 (2004) 593-606
43. Sekizawa S., and Tsubone H. Nasal receptors responding to noxious chemical irritants. Respir. Physiol. 96 (1994) 37-48
44. Shibamori M., Ogino K., Kambayashi Y., and Ishiyama H. Intranasal mite allergen induces allergic asthma-like responses in NC/Nga mice. Life Sci. 78 9 (2006) 987-994
45. Silver W.L., Farley L.G., and Finger T.E. The effects of neonatal capsaicin administration on trigeminal nerve chemoreceptors in the rat nasal cavity. Brain Res. 561 (1991) 212-216
46. Springall D.R., Edington J.A., Price P.N., Swanston D.W., Noel C., Bloom S.R., and Polak J.M. Acrolein depletes the neuropeptides CGRP and substance P in sensory nerves in the rat respiratory tract. Environ. Health Perspect. 85 (1990) 151-157
47. Symanowicz P.T., Giantusos G., and Morris J.B. Lack of role for the vanilloid receptor in response to several inspired irritant air pollutants in the C57Bl/6J mouse. Neurosci. Lett. 362 2 (2004) 150-153
48. Taylor-Clark T., and Undem B.J. Transduction mechanisms in airway sensory nerves. J. Appl. Physiol. 101 (2006) 950-959
49. Treitman R.D., Gurgess W.A., and Gold A. Air contaminants encountered by fire-fighters. Am. Ind. Hyg. Assoc. J. 41 (1980) 796-803
50. Turner C.R., Stow R.B., Talerico S.D., Christian E.P., and Williams J.C. Protective role for neuropeptides in acute pulmonary response to acrolein in guinea pigs. J. Appl. Physiol. 75 (1993) 2456-2465
51. Ulrich C.E., Haddock M.P., and Alarie Y. Airborne chemical irritants: role of the trigeminal nerve. Arch. Environ. Health 24 (1972) 37-42
52. Undem B.J., Hubbard W., and Weinreich D. Immunologically induced neuromodulation of guinea pig nodose ganglion neurons. J. Auton. Nerv. Syst. 44 1 (1993) 35-44
53. United States Environmental Protection Agency. 1999 National Air Toxics Assessment (2006), Office of Air Quality and Planning Standards, Washington, DC
54. Vaughan R.P., Szewczyk M.T., Lanosa M.J., DeSesa C.R., Gianutsos G., and Morris J.B. Adenosine sensory transduction pathways contribute to activation of the sensory irritation response to inspired irritant vapors. Toxicol. Sci. 93 2 (2006) 411-421
55. Vijayaraghavan R., Schapper M., Thompson R., Stock M.F., and Alarie Y. Characteristic modification of the breathing pattern of mice to evaluate the effects of airborne chemicals on the respiratory tract. Arch. Toxicol. 67 (1993) 478-490
56. Vijayaraghavan R., Schapper M., Thompson R., Stock M.F., Boylstein L.A., Luo J.E., and Alarie Y. Computer assisted recognition and quantitation of the effects of airborne chemicals acting at different areas of the respiratory tract in mice. Arch. Toxicol. 68 8 (1994) 490-499
57. Wang L., and Wang D.H. TRPV1 gene knockout impairs postischemic recovery in isolated perfused heart in mice. Circulation 112 23 (2005) 3617-3623
58. Wang A.L., Blackford T.L., and Lee L.-Y. Vagal bronchopulmonary C-fibers and acute ventilatory response to inhaled irritants. Respir. Physiol. 104 2/3 (1996) 231-239
59. Watkinson W.P., Wiester M.J., and Highfill J.W. Ozone toxicity in the rat I: effect of changes in ambient temperature on extrapulmonary physiological parameters. J. Appl. Physiol. 78 (1995) 1108-1120
60. Watkinson W.P., Campen M.J., Wichers L.B., Nolan J.B., and Costa D.L. Cardiac and thermoregulatory responses to inhaled pollutants in healthy and compromised rodents: modulation via interaction with environmental factors. Environ. Res. 92 (2003) 35-47
61. White S.W., and McRitchie R.J. Nasopharyngeal reflexes: integrative analysis of evoked respiratory and cardiovascular effects. Exp. Biol. Med. Sci. 51 (1973) 17-31
62. Widdicombe J.G. Reflexes from the upper respiratory tract. In: Cherniak N.S., and Widdicombe J.G. (Eds). Handbook of Physiology. Section 3: The respiratory System. Control of Breathing, Part I vol. II (1986), American Physiological Society, Washington, DC 363-394
63. Widdicombe J.G. Vagal reflexes in the airways. In: Kaliner M., and Barnes P.J. (Eds). Neural Regulation of the Airways in Health and Disease (1988), Marcel Dekker, New York 187-202
64. Widdicombe J.G., and Lee L.-Y. Airway reflexes, autonomic function, and cardiovascular responses. Environ. Health Perspect. 109 4 (2001) 579-584
65. Yu J., Lin S., Zhang J., Otmishi P., and Guardiola J.J. Airway nociceptors activated by pro-inflammatory cytokines. Respir. Physiol. Neurobiol. 156 2 (2007) 116-119