Cooperation between mast cells and neurons is essential for antigen-mediated bronchoconstriction

Journal of Immunology

Volumn 182, Issue 12, 2009, Pages 7430-7439

  Cyphert, Jaime M ^a   Kovarova, Martina ^b   Allen, Irving C ^a   Hartney, John M ^a   Murphy, Dennis L ^c   Wess, Jürgen ^d   Koller, Beverly H ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^d NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ANTIGEN; ATROPINE; CAPSAICIN; IMMUNOGLOBULIN E; SEROTONIN;

AIRWAY RESISTANCE; ALLERGY; ANAPHYLAXIS; ANIMAL EXPERIMENT; ARTICLE; BRONCHOSPASM; CHOLINERGIC SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOGLOBULIN PRODUCTION; LUNG; MAST CELL; MAST CELL DEGRANULATION; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE CELL; SEROTONIN RELEASE; SMOOTH MUSCLE; ANIMAL; C57BL MOUSE; IMMUNOLOGY; NERVE CELL; PHYSIOLOGY; SECRETION; VAGOTOMY;

ANAPHYLAXIS; ANIMALS; ANTIGENS; BRONCHOCONSTRICTION; MAST CELLS; MICE; MICE, INBRED C57BL; NEURONS; SEROTONIN; VAGOTOMY;

EID: 67649207280     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0900039     Document Type: Article

References (55)

1. Galli, S. J. 1993. New concepts about the mast cell. N. Engl. J. Med. 328: 257-265.
2. Brightling, C. E., P. Bradding, F. A. Symon, S. T. Holgate, A. J. Wardlaw, and I. D. Pavord. 2002. Mast-cell infiltration of airway smooth muscle in asthma. N. Engl. J. Med. 346: 1699-1705.
3. Billington, C. K., and R. B. Penn. 2003. Signaling and regulation of G protein-coupled receptors in airway smooth muscle. Respir. Res. 4: 2.
4. Panettieri, R. A., R. K. Murray, L. R. DePalo, P. A. Yadvish, and M. I. Kotlikoff. 1989. A human airway smooth muscle cell line that retains physiological responsiveness. Am. J. Physiol. 256: C329-C335.
5. 4. Am. J. Physiol. 286: L992-L1001.
6. Tolloczko, B., Y. L. Jia, and J. G. Martin. 1995. Serotonin-evoked calcium transients in airway smooth muscle cells. Am. J. Physiol. 269: L234-L240.
7. Powers, M. J., B. A. Peterson, and J. C. Hardwick. 2001. Regulation of para-sympathetic neurons by mast cells and histamine in the guinea pig heart. Auton. Neurosci. 87: 37-45.
8. Jiang, W., M. E. Kreis, C. Eastwood, A. J. Kirkup, P. P. Humphrey, and D. Grundy. 2000. 5-HT3 and histamine H1 receptors mediate afferent nerve sensitivity to intestinal anaphylaxis in rats. Gastroenterology 119: 1267-1275.
9. Barbara, G., B. Wang, V. Stanghellini, R. de Giorgio, C. Cremon, G. Di Nardo, M. Trevisani, B. Campi, P. Geppetti, M. Tonini, et al. 2007. Mast cell-dependent excitation of visceral-nociceptive sensory neurons in irritable bowel syndrome. Gastroenterology 132: 26-37.
10. Bienenstock, J., G. MacQueen, P. Sestini, J. S. Marshall, R. H. Stead, and M. H. Perdue. 1991. Mast cell/nerve interactions in vitro and in vivo. Am. Rev. Respir. Dis. 143: S55-S58.
11. Bienenstock, J., M. Perdue, M. Blennerhassett, R. Stead, N. Kakuta, P. Sestini, C. Vancheri, and J. Marshall. 1988. Inflammatory cells and the epithelium: mast cell/nerve interactions in the lung in vitro and in vivo. Am. Rev. Respir. Dis. 138: S31-S34. (Pubitemid 19004144)
12. Sestini, P., M. Dolovich, C. Vancheri, R. H. Stead, J. S. Marshall, M. Perdue, J. Gauldie, and J. Bienenstock. 1989. Antigen-induced lung solute clearance in rats is dependent on capsaicin-sensitive nerves. Am. Rev. Respir. Dis. 139: 401-406. (Pubitemid 19057416)
13. Myers, A. C., B. J. Undem, and D. Weinreich. 1991. Influence of antigen on membrane properties of guinea pig bronchial ganglion neurons. J. Appl. Physiol. 71: 970-976.
14. Myers, A. C., and B. J. Undem. 1995. Antigen depolarizes guinea pig bronchial parasympathetic ganglion neurons by activation of histamine H1 receptors. Am. J. Physiol. 268: L879-L884.
15. Zeitz, K. P., N. Guy, A. B. Malmberg, S. Dirajlal, W. J. Martin, L. Sun, D. W. Bonhaus, C. L. Stucky, D. Julius, and A. I. Basbaum. 2002. The 5-HT3 subtype of serotonin receptor contributes to nociceptive processing via a novel subset of myelinated and unmyelinated nociceptors. J. Neurosci. 22: 1010-1019.
16. 2 on submucosal neurons and secretion in guinea pig colon. Am. J. Physiol. 266: G132-G139.
17. Schmidlin, F., S. Amadesi, K. Dabbagh, D. E. Lewis, P. Knott, N. W. Bunnett, P. R. Gater, P. Geppetti, C. Bertrand, and M. E. Stevens. 2002. Protease-activated receptor 2 mediates eosinophil infiltration and hyperreactivity in allergic inflammation of the airway. J. Immunol. 169: 5315-5321. (Pubitemid 35217205)
18. Yamada, M., T. Miyakawa, A. Duttaroy, A. Yamanaka, T. Moriguchi, R. Makita, M. Ogawa, C. J. Chou, B. Xia, J. N. Crawley, et al. 2001. Mice lacking the M3 muscarinic acetylcholine receptor are hypophagic and lean. Nature 410: 207-212.
19. Fisahn, A., M. Yamada, A. Duttaroy, J. W. Gan, C. X. Deng, C. J. McBain, and J. Wess. 2002. Muscarinic induction of hippocampal gamma oscillations requires coupling of the M1 receptor to two mixed cation currents. Neuron 33: 615-624.
20. Bengel, D., D. L. Murphy, A. M. Andrews, C. H. Wichems, D. Feltner, A. Heils, R. Mossner, H. Westphal, and K. P. Lesch. 1998. Altered brain serotonin homeostasis and locomotor insensitivity to 3,4-methylenedioxymethamphetamine ("ecstasy") in serotonin transporter-deficient mice. Mol. Pharmacol. 53: 649-655. (Pubitemid 28196486)
21. Allen, I. C., A. J. Pace, L. A. Jania, J. G. Ledford, A. M. Latour, J. N. Snouwaert, V. Bernier, R. Stocco, A. G. Therien, and B. H. Koller. 2006. Expression and function of NPSR1/GPRA in the lung before and after induction of asthma-like disease. Am. J. Physiol. 291: L1005-LL1017.
22. Hantos, Z., A. Adamicza, E. Govaerts, and B. Daroczy. 1992. Mechanical impedances of lungs and chest wall in the cat. J. Appl. Physiol. 73: 427-433.
23. Tomioka, S., J. H. Bates, and C. G. Irvin. 2002. Airway and tissue mechanics in a murine model of asthma: alveolar capsule vs. forced oscillations. J. Appl. Physiol. 93: 263-270. (Pubitemid 34686220)
24. Kaczka, D. W., E. P. Ingenito, E. Israel, and K. R. Lutchen. 1999. Airway and lung tissue mechanics in asthma: effects of albuterol. Am. J. Respir. Crit. Care Med. 159: 169-178. (Pubitemid 29036521)
25. Miyajima, I., D. Dombrowicz, T. R. Martin, J. V. Ravetch, J. P. Kinet, and S. J. Galli. 1997. Systemic anaphylaxis in the mouse can be mediated largely through IgG1 and FcγRIII: assessment of the cardiopulmonary changes, mast cell degranulation, and death associated with active or IgE- or IgG1-dependent passive anaphylaxis. J. Clin. Invest. 99: 901-914. (Pubitemid 27123627)
26. Morris, J. B., P. T. Symanowicz, J. E. Olsen, R. S. Thrall, M. M. Cloutier, and A. K. Hubbard. 2003. Immediate sensory nerve-mediated respiratory responses to irritants in healthy and allergic airway-diseased mice. J. Appl. Physiol. 94: 1563-1571.
27. Morris, J. B., W. S. Wilkie, and D. J. Shusterman. 2005. Acute respiratory responses of the mouse to chlorine. Toxicol. Sci. 83: 380-387.
28. Holzer, P., M. A. Pabst, I. T. Lippe, B. M. Peskar, B. A. Peskar, E. H. Livingston, and P. H. Guth. 1990. Afferent nerve-mediated protection against deep mucosal damage in the rat stomach. Gastroenterology 98: 838-848.
29. Steinhoff, M., N. Vergnolle, S. H. Young, M. Tognetto, S. Amadesi, H. S. Ennes, M. Trevisani, M. D. Hollenberg, J. L. Wallace, G. H. Caughey, et al. 2000. Agonists of proteinase-activated receptor 2 induce inflammation by a neurogenic mechanism. Nat. Med. 6: 151-158.
30. 3 muscarinic acetylcholine receptor-dependent mechanism. Am. J. Physiol. 290: L526-L533.
31. Gersch, C., O. Dewald, M. Zoerlein, L. H. Michael, M. L. Entman, and N. G. Frangogiannis. 2002. Mast cells and macrophages in normal C57/BL/6 mice. Histochem. Cell Biol. 118: 41-49. (Pubitemid 34762318)
32. Irvin, C. G., and J. H. Bates. 2003. Measuring the lung function in the mouse: the challenge of size. Respir. Res. 4: 4.
33. Williams, C. M., and S. J. Galli. 2000. Mast cells can amplify airway reactivity and features of chronic inflammation in an asthma model in mice. J. Exp. Med. 192: 455-462.
34. Henderson, W. R., Jr., D. B. Lewis, R. K. Albert, Y. Zhang, W. J. Lamm, G. K. Chiang, F. Jones, P. Eriksen, Y. T. Tien, M. Jonas, and E. Y. Chi. 1996. The importance of leukotrienes in airway inflammation in a mouse model of asthma. J. Exp. Med. 184: 1483-1494.
35. Murakami, M., C. O. Bingham, 3rd, R. Matsumoto, K. F. Austen, and J. P. Arm. 1995. IgE-dependent activation of cytokine-primed mouse cultured mast cells induces a delayed phase of prostaglandin D2 generation via prostaglandin endoperoxide synthase-2. J. Immunol. 155: 4445-4453.
36. Su, X., E. Camerer, J. R. Hamilton, S. R. Coughlin, and M. A. Matthay. 2005. Protease-activated receptor-2 activation induces acute lung inflammation by neuropeptide-dependent mechanisms. J. Immunol. 175: 2598-2605. (Pubitemid 41113873)
37. Kushnir-Sukhov, N. M., J. M. Brown, Y. Wu, A. Kirshenbaum, and D. D. Metcalfe. 2007. Human mast cells are capable of serotonin synthesis and release. J. Allergy Clin. Immunol. 119: 498-499.
38. Fernandez, V. E., V. McCaskill, N. D. Atkins, and A. Wanner. 1999. Variability of airway responses in mice. Lung 177: 355-366.
39. Chen, J. J., Z. Li, H. Pan, D. L. Murphy, H. Tamir, H. Koepsell, and M. D. Gershon. 2001. Maintenance of serotonin in the intestinal mucosa and ganglia of mice that lack the high-affinity serotonin transporter: abnormal intestinal motility and the expression of cation transporters. J. Neurosci. 21: 6348-6361.
40. Homberg, J., J. Mudde, B. Braam, B. Ellenbroek, E. Cuppen, and J. A. Joles. 2006. Blood pressure in mutant rats lacking the 5-hydroxytryptamine transporter. Hypertension 48: e115-e116; author reply e117.
41. Stead, R. H., M. F. Dixon, N. H. Bramwell, R. H. Riddell, and J. Bienenstock. 1989. Mast cells are closely apposed to nerves in the human gastrointestinal mucosa. Gastroenterology 97: 575-585.
42. Eum, S. Y., X. Norel, J. Lefort, C. Labat, B. B. Vargaftig, and C. Brink. 1999. Anaphylactic bronchoconstriction in BP2 mice: interactions between serotonin and acetylcholine. Br. J. Pharmacol. 126: 312-316.
43. Wohlsen, A., S. Uhlig, and C. Martin. 2001. Immediate allergic response in small airways. Am. J. Respir. Crit. Care Med. 163: 1462-1469. (Pubitemid 32506617)
44. Wohlsen, A., C. Martin, E. Vollmer, D. Branscheid, H. Magnussen, W. M. Becker, U. Lepp, and S. Uhlig. 2003. The early allergic response in small airways of human precision-cut lung slices. Eur. Respir. J. 21: 1024-1032.
45. Millman, R. P., D. A. Silage, D. D. Peterson, and A. I. Pack. 1982. Effect of aerosolized histamine on occlusion pressure and ventilation in humans. J. Appl. Physiol. 53: 690-697. (Pubitemid 12027242)
46. Moffatt, J. D., T. M. Cocks, and C. P. Page. 2004. Role of the epithelium and acetylcholine in mediating the contraction to 5-hydroxytryptamine in the mouse isolated trachea. Br. J. Pharmacol. 141: 1159-1166.
47. Davis, C., M. S. Kannan, T. R. Jones, and E. E. Daniel. 1982. Control of human airway smooth muscle: in vitro studies. J. Appl. Physiol. 53: 1080-1087. (Pubitemid 13220589)
48. Cushley, M. J., L. H. Wee, and S. T. Holgate. 1986. The effect of inhaled 5-hydroxytryptamine (5-HT, serotonin) on airway calibre in man. Br. J. Clin. Pharmacol. 22: 487-490.
49. Greene, R., J. Fowler, D. MacGlashan, Jr., and D. Weinreich. 1988. IgE-challenged human lung mast cells excite vagal sensory neurons in vitro. J. Appl. Physiol. 64: 2249-2253.
50. Undem, B. J., M. M. Riccio, D. Weinreich, J. L. Ellis, and A. C. Myers. 1995. Neurophysiology of mast cell-nerve interactions in the airways. Int. Arch. Allergy Immunol. 107: 199-201.
51. Yu, S., M. Kollarik, A. Ouyang, A. C. Myers, and B. J. Undem. 2007. Mast cell-mediated long-lasting increases in excitability of vagal C fibers in guinea pig esophagus. Am. J. Physiol. 293: G850-G856.
52. Larsen, G. L., C. W. White, K. Takeda, J. E. Loader, D. D. Nguyen, A. Joetham, Y. Groner, and E. W. Gelfand. 2000. Mice that overexpress Cu/Zn superoxide dismutase are resistant to allergen-induced changes in airway control. Am. J. Physiol. 279: L350-L359.
53. Mitchell, R. W., I. M. Ndukuw, K. Ikeda, K. Arbetter, and A. R. Leff. 1993. Effect of immune sensitization on stimulated ACh release from trachealis muscle in vitro. Am. J. Physiol. 265: L13-L18.
54. 2+ signaling of smooth muscle cells in different generations of mouse airways. Am. J. Respir. Cell Mol. Biol. 36: 122-130.
55. Held, H. D., C. Martin, and S. Uhlig. 1999. Characterization of airway and vascular responses in murine lungs. Br. J. Pharmacol. 126: 1191-1199.