Neuroimmune crosstalk in asthma: Dual role of the neurotrophin receptor p75NTR

Journal of Allergy and Clinical Immunology

Volumn 120, Issue 5, 2007, Pages 1089-1096

  Nassenstein, Christina ^a   Kammertoens, Thomas ^b,c   Veres, Tibor Zoltan ^a   Uckert, Wolfgang ^d   Spies, Emma ^a   Fuchs, Barbara ^a   Krug, Norbert ^a   Braun, Armin ^a  

^a FRAUNHOFER INSTITUTE FOR TOXICOLOGY AND EXPERIMENTAL MEDICINE   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d HUMBOLDT UNIVERSITY   (Germany)

Author keywords

airway hyperreactivity; airway inflammation; asthma; bone marrow chimeras; capsaicin; Neuroimmune interaction; neurotrophin receptors; neurotrophins; p75NTR; sensory nerves

Indexed keywords

CAPSAICIN; CYTOKINE; NEUROTROPHIN; NEUROTROPHIN RECEPTOR; NEUROTROPHIN RECEPTOR P75; UNCLASSIFIED DRUG;

ALLERGIC ASTHMA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; BRONCHUS HYPERREACTIVITY; CONTROLLED STUDY; FEMALE; IMMUNOCOMPETENT CELL; LEUKOCYTE DIFFERENTIAL COUNT; LUNG LAVAGE; MOUSE; NERVE CELL; NEUROIMMUNOLOGY; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RESPIRATORY TRACT INFLAMMATION; SENSITIZATION; SENSORY NERVE; SIGNAL TRANSDUCTION;

AFFERENT PATHWAYS; ANIMALS; ASTHMA; BRONCHOALVEOLAR LAVAGE FLUID; INFLAMMATION; MICE; MICE, KNOCKOUT; NERVE GROWTH FACTORS; NEURONS, AFFERENT; RECEPTORS, NERVE GROWTH FACTOR;

EID: 35648956746     PISSN: 00916749     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jaci.2007.07.007     Document Type: Article

References (34)

1. Tracey K.J. The inflammatory reflex. Nature 420 (2002) 853-859
2. Kradin R., MacLean J., Duckett S., Schneeberger E.E., Waeber C., and Pinto C. Pulmonary response to inhaled antigen: neuroimmune interactions promote the recruitment of dendritic cells to the lung and the cellular immune response to inhaled antigen. Am J Pathol 150 (1997) 1735-1743
3. Evans C.M., Fryer A.D., Jacoby D.B., Gleich G.J., and Costello R.W. Pretreatment with antibody to eosinophil major basic protein prevents hyperresponsiveness by protecting neuronal M2 muscarinic receptors in antigen-challenged guinea pigs. J Clin Invest 100 (1997) 2254-2262
4. Barnes P.J. Overview of neural mechanisms in asthma. Pulm Pharmacol 8 (1995) 151-159
5. Fischer A., McGregor G.P., Saria A., Philippin B., and Kummer W. Induction of tachykinin gene and peptide expression in guinea pig nodose primary afferent neurons by allergic airway inflammation. J Clin Invest 98 (1996) 2284-2291
6. Saria A., Martling C.R., Yan Z., Theodorsson-Norheim E., Gamse R., and Lundberg J.M. Release of multiple tachykinins from capsaicin-sensitive sensory nerves in the lung by bradykinin, histamine, dimethylphenyl piperazinium, and vagal nerve stimulation. Am Rev Respir Dis 137 (1988) 1330-1335
7. Barnes P.J. Neurogenic inflammation and asthma. J Asthma 29 (1992) 165-180
8. Kerzel S., Path G., Nockher W.A., Quarcoo D., Raap U., Groneberg D.A., et al. Pan-neurotrophin receptor p75 contributes to neuronal hyperreactivity and airway inflammation in a murine model of experimental asthma. Am J Respir Cell Mol Biol 28 (2003) 170-178
9. Nassenstein C., Dawbarn D., Pollock K., Allen S.J., Erpenbeck V.J., Spies E., et al. Pulmonary distribution, regulation and functional role of Trk receptors in a murine model of asthma. J Allergy Clin Immunol 118 (2006) 597-605
10. Undem B.J., Hunter D.D., Liu M., Haak-Frendscho M., Oakragly A., and Fischer A. Allergen-induced sensory neuroplasticity in airways. Int Arch Allergy Immunol 118 (1999) 150-153
11. Lee L.Y., Gu Q., and Gleich G.J. Effects of human eosinophil granule-derived cationic proteins on C-fiber afferents in the rat lung. J Appl Physiol 91 (2001) 1318-1326
12. Braun A., Appel E., Baruch R., Herz U., Botchkarev V., Paus R., et al. Role of nerve growth factor in a mouse model of allergic airway inflammation and asthma. Eur J Immunol 28 (1998) 3240-3251
13. Virchow J.C., Julius P., Lommatzsch M., Luttmann W., Renz H., and Braun A. Neurotrophins are increased in bronchoalveolar lavage fluid after segmental allergen provocation. Am J Respir Crit Care Med 158 (1998) 2002-2005
14. Nassenstein C., Schulte-Herbruggen O., Renz H., and Braun A. Nerve growth factor: the central hub in the development of allergic asthma?. Eur J Pharmacol 533 (2006) 195-206
15. Goedert M., Stoeckel K., and Otten U. Biological importance of the retrograde axonal transport of nerve growth factor in sensory neurons. Proc Natl Acad Sci U S A 78 (1981) 5895-5898
16. Braun A., Quarcoo D., Schulte-Herbruggen O., Lommatzsch M., Hoyle G., and Renz H. Nerve growth factor induces airway hyperresponsiveness in mice. Int Arch Allergy Immunol 124 (2001) 205-207
17. Braun A., Lommatzsch M., Neuhaus-Steinmetz U., Quarcoo D., Glaab T., McGregor G.P., et al. Brain-derived neurotrophic factor (BDNF) contributes to neuronal dysfunction in a model of allergic airway inflammation. Br J Pharmacol 141 (2004) 431-440
18. Nassenstein C., Braun A., Erpenbeck V.J., Lommatzsch M., Schmidt S., Krug N., et al. The neurotrophins nerve growth factor, brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4 are survival and activation factors for eosinophils in patients with allergic bronchial asthma. J Exp Med 198 (2003) 455-467
19. Lee K.F., Li E., Huber L.J., Landis S.C., Sharpe A.H., Chao M.V., et al. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell 69 (1992) 737-749
20. Leckie M.J., ten Brinke A., Khan J., Diamant Z., O'Connor B.J., Walls C.M., et al. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyper-responsiveness, and the late asthmatic response. Lancet 356 (2000) 2144-2148
21. Quarcoo D., Schulte-Herbruggen O., Lommatzsch M., Schierhorn K., Hoyle G.W., Renz H., et al. Nerve growth factor induces increased airway inflammation via a neuropeptide-dependent mechanism in a transgenic animal model of allergic airway inflammation. Clin Exp Allergy 34 (2004) 1146-1151
22. Chavolla-Calderon M., Bayer M.K., and Fontan J.J. Bone marrow transplantation reveals an essential synergy between neuronal and hemopoietic cell neurokinin production in pulmonary inflammation. J Clin Invest 111 (2003) 973-980
23. Hoyle G.W., Graham R.M., Finkelstein J.B., Nguyen K.P., Gozal D., and Friedman M. Hyperinnervation of the airways in transgenic mice overexpressing nerve growth factor. Am J Respir Cell Mol Biol 18 (1998) 149-157
24. Barouch R., Appel E., Kazimirsky G., Braun A., Renz H., and Brodie C. Differential regulation of neurotrophin expression by mitogens and neurotransmitters in mouse lymphocytes. J Neuroimmunol 103 (2000) 112-121
25. Bracci-Laudiero L., Aloe L., Buanne P., Finn A., Stenfors C., Vigneti E., et al. NGF modulates CGRP synthesis in human B-lymphocytes: a possible anti-inflammatory action of NGF?. J Neuroimmunol 123 (2002) 58-65
26. Obata K., Katsura H., Sakurai J., Kobayashi K., Yamanaka H., Dai Y., et al. Suppression of the p75 neurotrophin receptor in uninjured sensory neurons reduces neuropathic pain after nerve injury. J Neurosci 26 (2006) 11974-11986
27. Nilsson G., Alving K., Ahlstedt S., Hokfelt T., and Lundberg J.M. Peptidergic innervation of rat lymphoid tissue and lung: relation to mast cells and sensitivity to capsaicin and immunization. Cell Tissue Res 262 (1990) 125-133
28. Kingham P.J., Costello R.W., and McLean W.G. Eosinophil and airway nerve interactions. Pulm Pharmacol Ther 16 (2003) 9-13
29. Janiszewski J., Bienenstock J., and Blennerhassett M.G. Activation of rat peritoneal mast cells in coculture with sympathetic neurons alters neuronal physiology. Brain Behav Immun 4 (1990) 139-150
30. Sawatzky D.A., Kingham P.J., Durcan N., McLean W.G., and Costello R.W. Eosinophil-induced release of acetylcholine from differentiated cholinergic nerve cells. Am J Physiol Lung Cell Mol Physiol 285 (2003) L1296-L1304
31. Morgan R.K., Kingham P.J., Walsh M.T., Curran D.C., Durcan N., McLean W.G., et al. Eosinophil adhesion to cholinergic IMR-32 cells protects against induced neuronal apoptosis. J Immunol 173 (2004) 5963-5970
32. De Swert K.O., and Joos G.F. Extending the understanding of sensory neuropeptides. Eur J Pharmacol 533 (2006) 171-181
33. Sanico A.M., Atsuta S., Proud D., and Togias A. Dose-dependent effects of capsaicin nasal challenge: in vivo evidence of human airway neurogenic inflammation. J Allergy Clin Immunol 100 (1997) 632-641
34. Davies D., Spicer B.A., Smith H., and Haynes L.W. Effect of neonatal capsaicin on peptide-containing primary afferent fibres, eosinophil distribution and hyperresponsiveness in rat lung tissue following experimentally induced eosinophilia. Neuroimmunomodulation 1 (1994) 308-314