A new paradigm of eosinophil granulocytes: Neuroimmune interactions

Experimental Dermatology

Volumn 17, Issue 9, 2008, Pages 731-738

  Raap, Ulrike ^a   Wardlaw, Andrew J ^b  

^a HANNOVER MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

Asthma; Eosinophil granulocytes; Nerves; Neuropeptides; Neurotrophins

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; NERVE GROWTH FACTOR; NEUROKININ; NEUROTROPHIN; NEUROTROPHIN 3;

ADAPTIVE IMMUNITY; ALLERGIC ASTHMA; ALLERGIC RHINITIS; ASTHMA; CELL FUNCTION; CELL INTERACTION; CELL MATURATION; CELL MIGRATION; CELL SURFACE; EOSINOPHIL; HUMAN; IMMUNOMODULATION; IMMUNOPATHOGENESIS; INNATE IMMUNITY; NERVE FUNCTION; NONADRENERGIC NONCHOLINERGIC NERVE; NONHUMAN; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW;

ASTHMA; EOSINOPHIL GRANULE PROTEINS; EOSINOPHILS; HUMANS; NERVE GROWTH FACTORS; PERIPHERAL NERVES;

EID: 49049104012     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2008.00741.x     Document Type: Review

References (92)

1. Hogan S P. Recent advances in eosinophil biology. Int Arch Allergy Immunol 2007: 143 (Suppl. 1): 3-14.
2. Wardlaw A J, Brightling C, Green R, Woltmann G, Pavord I. Eosinophils in asthma and other allergic diseases. Br Med Bull 2000: 56: 985-1003.
3. Jacobsen E A, Taranova A G, Lee N A, Lee J J. Eosinophils: Singularly destructive effector cells or purveyors of immunoregulation? J Allergy Clin Immunol 2007: 119: 1313-1320.
4. Kapp A. The role of eosinophils in the pathogenesis of atopic dermatitis - eosinophil granule proteins as markers of disease activity. Allergy 1993: 48: 1-5.
5. Zeck-Kapp G, Czech W, Kapp A. TNF alpha-induced activation of eosinophil oxidative metabolism and morphology - comparison with IL-5. Exp Dermatol 1994: 3: 176-188.
6. Czech W, Krutmann J, Schopf E, Kapp A. Serum eosinophil cationic protein (ECP) is a sensitive measure for disease activity in atopic dermatitis. Br J Dermatol 1992: 126: 351-355.
7. Giembycz M A, Lindsay M A. Pharmacology of the eosinophil. Pharmacol Rev 1999: 51: 213-339.
8. Nagase H, Okugawa S, Ota Y et al. Expression and function of Toll-like receptors in eosinophils: Activation by Toll-like receptor 7 ligand. J Immunol 2003: 171: 3977-3982.
9. + eosinophils in the murine thymus: Developmental regulation and recruitment upon MHC class I-restricted thymocyte deletion. J Immunol 2000: 165: 1965-1975.
10. Kay A B, Phipps S, Robinson D S. A role for eosinophils in airway remodelling in asthma. Trends Immunol 2004: 25: 477-482.
11. Costello R W, Schofield B H, Kephart G M, Gleich G J, Jacoby D B, Fryer A D. Localization of eosinophils to airway nerves and effect on neuronal M2 muscarinic receptor function. Am J Physiol 1997: 1: L93-L103.
12. Denburg J A, Sehmi R, Saito H, Pil-Seob J, Inman M D, O'Byrne P M. Systemic aspects of allergic disease: Bone marrow responses. J Allergy Clin Immunol 2000: 5 (Suppl.): S242-S246.
13. Wardlaw A J, Walsh G M, Symon F A. Mechanisms of eosinophil and basophil migration. Allergy 1994: 49: 797-807.
14. + eosinophils by interleukin-5. Am J Respir Cell Mol Biol 2004: 30: 367-378.
15. Wardlaw A J. Molecular basis for selective eosinophil trafficking in asthma: A multistep paradigm. J Allergy Clin Immunol 1999: 104: 917-926.
16. Czech W, Krutmann J, Budnik A, Schopf E, Kapp A. Induction of intercellular adhesion molecule 1 (ICAM-1) expression in normal human eosinophils by inflammatory cytokines. J Invest Dermatol 1993: 100: 417-423.
17. Symon F A, Lawrence M B, Williamson M L, Walsh G M, Watson S R, Wardlaw A J. Functional and structural characterization of the eosinophil P-selectin ligand. J Immunol 1996: 157: 1711-1719.
18. Jia G Q, Gonzalo J A, Hidalgo A, Wagner D, Cybulsky M, Gutierrez-Ramos J C. Selective eosinophil transendothelial migration triggered by eotaxin via modulation of Mac-1/ICAM-1 and VLA-4/VCAM-1 interactions. Int Immunol 1999: 11: 1-10.
19. Menzies-Gow A, Ying S, Sabroe I et al. Eotaxin (CCL11) and eotaxin-2 (CCL24) induce recruitment of eosinophils, basophils, neutrophils, and macrophages as well as features of early- and late-phase allergic reactions following cutaneous injection in human atopic and nonatopic volunteers. J Immunol 2002: 169: 2712-2718.
20. Elsner J, Petering H, Kluthe C et al. Eotaxin-2 activates chemotaxis-related events and release of reactive oxygen species via pertussis toxin-sensitive G proteins in human eosinophils. Eur J Immunol 1998: 28: 2152-2158.
21. Steinbach K H, Schick P, Trepel F et al. Estimation of kinetic parameters of neutrophilic, eosinophilic, and basophilic granulocytes in human blood. Blut 1979: 39: 27-38.
22. Leckie M J, ten Brinke A, Khan J et al. Effects of an interleukin-5 blocking monoclonal antibody on eosinophils, airway hyper-responsiveness, and the late asthmatic response. Lancet 2000: 356: 2144-2148.
23. Kiehl P, Falkenberg K, Vogelbruch M, Kapp A. Tissue eosinophilia in acute and chronic atopic dermatitis: A morphometric approach using quantitative image analysis of immunostaining. Br J Dermatol 2001: 145: 720-729.
24. Rosenberg H F, Phipps S, Foster P S. Eosinophil trafficking in allergy and asthma. J Allergy Clin Immunol 2007: 119: 1303-1310.
25. Wedi B, Raap U, Kapp A. Significant delay of apoptosis and Fas resistance in eosinophils of subjects with intrinsic and extrinsic type of atopic dermatitis. Int Arch Allergy Immunol 1999: 118: 234-235.
26. Wedi B, Raap U, Lewrick H, Kapp A. Delayed eosinophil programmed cell death in vitro: A common feature of inhalant allergy and extrinsic and intrinsic atopic dermatitis. J Allergy Clin Immunol 1997: 100: 536-543.
27. Levi-Schaffer F, Temkin V, Malamud V, Feld S, Zilberman Y. Mast cells enhance eosinophil survival in vitro: Role of TNF-alpha and granulocyte-macrophage colony-stimulating factor. J Immunol 1998: 160: 5554-5562.
28. Simon H U. Molecules involved in the regulation of eosinophil apoptosis. Chem Immunol Allergy 2006: 91: 49-58.
29. Dewson G, Walsh G M, Wardlaw A J. Expression of Bcl-2 and its homologues in human eosinophils. Modulation by interleukin-5. Am J Respir Cell Mol Biol 1999: 20: 720-728.
30. Simon H U, Yousefi S, Schranz C, Schapowal A, Bachert C, Blaser K. Direct demonstration of delayed eosinophil apoptosis as a mechanism causing tissue eosinophilia. J Immunol 1997: 158: 3902-3908.
31. Tachimoto H, Bochner B S. The surface phenotype of human eosinophils. In: Marone G, ed. Human Eosinophils - Biological and Clinical Aspects. Naples: Karger AG, 2000: 45-62.
32. Rothenberg M E, Hogan S P. The eosinophil. Annu Rev Immunol 2006: 24: 147-174.
33. Noga O, Englmann C, Hanf G, Grutzkau A, Guhl S, Kunkel G. Activation of the specific neurotrophin receptors TrkA, TrkB and TrkC influences the function of eosinophils. Clin Exp Allergy 2002: 32: 1348-1354.
34. Kaplan D R, Hempstead B L, Martin-Zanca D, Chao M V, Parada L F. The trk proto-oncogene product: A signal transducing receptor for nerve growth factor. Science 1991: 252: 554-558.
35. Ip N Y, Ibanez C F, Nye S H et al. Mammalian neurotrophin-4: Structure, chromosomal localization, tissue distribution, and receptor specificity. Proc Natl Acad Sci U S A 1992: 89: 3060-3064.
36. Lamballe F, Klein R, Barbacid M. trkC, a new member of the trk family of tyrosine protein kinases, is a receptor for neurotrophin-3. Cell 1991: 66: 967-979.
37. Nassenstein C, Braun A, Erpenbeck V J 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 2003: 198: 455-467.
38. Radeke M J, Misko T P, Hsu C, Herzenberg L A, Shooter E M. Gene transfer and molecular cloning of the rat nerve growth factor receptor. Nature 1987: 325: 593-597.
39. Johnson D, Lanahan A, Buck CR et al. Expression and structure of the human NGF receptor. Cell 1986: 47: 545-554.
40. Raap U, Goltz C, Deneka N et al. Brain-derived neurotrophic factor is increased in atopic dermatitis and modulates eosinophil functions compared with that seen in nonatopic subjects. J Allergy Clin Immunol 2005: 115: 1268-1275.
41. el Shazly A E, Masuyama K, Eura M, Ishikawa T. Immunoregulatory effect of substance P in human eosinophil migratory function. Immunol Invest 1996: 25: 191-201.
42. Renzi D, Pellegrini B, Tonelli F, Surrenti C, Calabro A. Substance P (neurokinin-1) and neurokinin A (neurokinin-2) receptor gene and protein expression in the healthy and inflamed human intestine. Am J Pathol 2000: 157: 1511-1522.
43. Nockher W A, Renz H. Neurotrophins in allergic diseases: From neuronal growth factors to intercellular signaling molecules. J Allergy Clin Immunol 2006: 117: 583-589.
44. Johansson O, Liang Y, Marcusson J A, Reimert C M. Eosinophil cationic protein- and eosinophil-derived neurotoxin/eosinophil protein X-immunoreactive eosinophils in prurigo nodularis. Arch Dermatol Res 2000: 292: 371-378.
45. Durack D T, Sumi S M, Klebanoff S J. Neurotoxicity of human eosinophils. Proc Natl Acad Sci U S A 1979: 76: 1443-1447.
46. Morgan R K, Costello R W, Durcan N et al. Diverse effects of eosinophil cationic granule proteins on IMR-32 nerve cell signalling and survival. Am J Respir Cell Mol Biol 2005: 33: 169-177.
47. Jacoby D B, Costello R M, Fryer A D. Eosinophil recruitment to the airway nerves. J Allergy Clin Immunol 2001: 107: 211-218.
48. Walsh M T, Curran D R, Kingham P J et al. Effect of eosinophil adhesion on intracellular signalling in cholinergic nerve cells. Am J Respir Cell Mol Biol 2004: 30: 333-341.
49. Raap U, Kapp A. Neuroimmunological findings in allergic skin diseases. Curr Opin Allergy Clin Immunol 2005: 5: 419-424.
50. Peters E M, Raap U, Welker P et al. Neurotrophins act as neuroendocrine regulators of skin homeostasis in health and disease. Horm Metab Res 2007: 39: 110-124.
51. Bonini S, Lambiase A, Bonini S et al. Circulating nerve growth factor levels are increased in humans with allergic diseases and asthma. Proc Natl Acad Sci U S A 1996: 93: 10955-10960.
52. Namura K, Hasegawa G, Egawa M et al. Relationship of serum brain-derived neurotrophic factor level with other markers of disease severity in patients with atopic dermatitis. Clin Immunol 2007: 122: 181-186.
53. Raap U, Werfel T, Goltz C et al. Circulating levels of brain-derived neurotrophic factor correlate with disease severity in the intrinsic type of atopic dermatitis. Allergy 2006: 61: 1416-1418.
54. Lewin G R, Barde Y A. Physiology of the neurotrophins. Annu Rev Neurosci 1996: 19: 289-317.
55. Solomon A, Aloe L, Pe'er J et al. Nerve growth factor is preformed in and activates human peripheral blood eosinophils. J Allergy Clin Immunol 1998: 102: 454-460.
56. Noga O, Englmann C, Hanf G, Grutzkau A, Seybold J, Kunkel G. The production, storage and release of the neurotrophins nerve growth factor, brain-derived neurotrophic factor and neurotrophin-3 by human peripheral eosinophils in allergics and non-allergics. Clin Exp Allergy 2003: 33: 649-654.
57. Kobayashi H, Gleich G J, Butterfield J H, Kita H. Human eosinophils produce neurotrophins and secrete nerve growth factor on immunologic stimuli. Blood 2002: 99: 2214-2220.
58. Toyoda M, Nakamura M, Makino T, Morohashi M. Localization and content of nerve growth factor in peripheral blood eosinophils of atopic dermatitis patients. Clin Exp Allergy 2003: 33: 950-955.
59. Hamada A, Watanabe N, Ohtomo H, Matsuda H. Nerve growth factor enhances survival and cytotoxic activity of human eosinophils. Br J Haematol 1996: 93: 299-302.
60. Raap U. Have we forgotten about the role of nerves in asthma? DOI 10.1594/eaacinet2007/EO/4-300307.
61. Joos G F, De Swert K O, Schelfhout V, Pauwels R A. The role of neural inflammation in asthma and chronic obstructive pulmonary disease. Ann N Y Acad Sci 2003: 992: 218-230.
62. Metwali A, Blum A M, Ferraris L, Klein J S, Fiocchi C, Weinstock J V. Eosinophils within the healthy or inflamed human intestine produce substance P and vasoactive intestinal peptide. J Neuroimmunol 1994: 52: 69-78.
63. Aliakbari J, Sreedharan S P, Turck C W, Goetzl E J. Selective localization of vasoactive intestinal peptide and substance P in human eosinophils. Biochem Biophys Res Commun 1987: 148: 1440-1445.
64. el Shazly A E, Masuyama K, Ishikawa T. Mechanisms involved in activation of human eosinophil exocytosis by substance P: An in vitro model of sensory neuroimmunomodulation. Immunol Invest 1997: 26: 615-629.
65. Kroegel C, Giembycz M A, Barnes P J. Characterization of eosinophil cell activation by peptides. Differential effects of substance P, melittin, and FMET-Leu-Phe. J Immunol 1990: 145: 2581-2587.
66. De Simone C, Ferrari M, Ferrarelli G, Rumi C, Pugnaloni L, Sorice F. The effects of substance P on human eosinophil receptors and functions. Ann N Y Acad Sci 1987: 496: 226-232.
67. Matsuda H, Kawakita K, Kiso Y, Nakano T, Kitamura Y. Substance P induces granulocyte infiltration through degranulation of mast cells. J Immunol 1989: 142: 927-931.
68. Bailey S R, Cunningham F M. Adherence of eosinophils from allergic and normal ponies to cultured equine endothelial cells. Inflamm Res 2001: 50: 32-38.
69. Tiberio I F, Leick-Maldonado E A, Miyahara L et al. Effects of neurokinins on airway and alveolar eosinophil recruitment. Exp Lung Res 2003: 29: 165-177.
70. Fajac I, Braunstein G, Ickovic M R, Lacronique J, Frossard N. Selective recruitment of eosinophils by substance P after repeated allergen exposure in allergic rhinitis. Allergy 1995: 50: 970-975.
71. El Shazly A, Ishikawa T. Novel co-operation between eotaxin and substance-P in inducing eosinophil-derived neurotoxin release. Mediators Inflamm 1999: 8: 177-179.
72. Foster A P, Cunningham F M. Substance P induces activation, adherence and migration of equine eosinophils. J Vet Pharmacol Ther 2003: 26: 131-138.
73. Numao T, Agrawal D K. Neuropeptides modulate human eosinophil chemotaxis. J Immunol 1992: 149: 3309-3315.
74. Dunzendorfer S, Meierhofer C, Wiedermann C J. Signaling in neuropeptide-induced migration of human eosinophils. J Leukoc Biol 1998: 64: 828-834.
75. Dunzendorfer S, Feistritzer C, Enrich B, Wiedermann C J. Neuropeptide-induced inhibition of IL-16 release from eosinophils. Neuroimmunomodulation 2002: 10: 217-223.
76. Dunzendorfer S, Wiedermann C J. Neuropeptide-induced chemotaxis of eosinophils in pulmonary diseases. Ann Med 2000: 32: 429-439.
77. Elias J A, Lee C G, Zheng T, Ma B, Homer R J, Zhu Z. New insights into the pathogenesis of asthma. J Clin Invest 2003: 111: 291-297.
78. Fixman E D, Stewart A, Martin J G. Basic mechanisms of development of airway structural changes in asthma. Eur Respir J 2007: 29: 379-389.
79. Bochner B S, Busse W W. Allergy and asthma. J Allergy Clin Immunol 2005: 115: 953-959.
80. Flood-Page P T, Menzies-Gow A N, Kay A B, Robinson D S. Eosinophil's role remains uncertain as anti-interleukin-5 only partially depletes numbers in asthmatic airway. Am J Respir Crit Care Med 2003: 167: 199-204.
81. Wardlaw A J, Brightling C E, Green R, Woltmann G, Bradding P, Pavord I D. New insights into the relationship between airway inflammation and asthma. Clin Sci (Lond) 2002: 103: 201-211.
82. Raap U, Brzoska T, Sohl S et al. Alpha-melanocyte-stimulating hormone inhibits allergic airway inflammation. J Immunol 2003: 171: 353-359.
83. Nie Z, Nelson C S, Jacoby D B, Fryer A D. Expression and regulation of intercellular adhesion molecule-1 on airway parasympathetic nerves. J Allergy Clin Immunol 2007: 119: 1415-1422.
84. Fryer A D, Stein L H, Nie Z et al. Neuronal eotaxin and the effects of CCR3 antagonist on airway hyperreactivity and M2 receptor dysfunction. J Clin Invest 2006: 116: 228-236.
85. Foley S C, Prefontaine D, Hamid Q. Images in allergy and immunology: role of eosinophils in airway remodeling. J Allergy Clin Immunol 2007: 119: 1563-1566.
86. Minshall E M, Leung D Y, Martin R J et. al. Eosinophil-associated TGF-beta1 mRNA expression and airways fibrosis in bronchial asthma. Am J Respir Cell Mol Biol 1997: 17: 326-333.
87. Durcan N, Costello R W, McLean W G et al. Eosinophil-mediated cholinergic nerve remodeling. Am J Respir Cell Mol Biol 2006: 34: 775-786.
88. Undem B J, Carr M J. The role of nerves in asthma. Curr Allergy Asthma Rep 2002: 2: 159-165.
89. Scott K A, Wardlaw A J. Eosinophilic airway disorders. Semin Respir Crit Care Med 2006: 27: 128-133.
90. Brightling C E. Chronic cough due to nonasthmatic eosinophilic bronchitis: ACCP evidence-based clinical practice guidelines. Chest 2006: 1 (Suppl.): 116S-121S.
91. Klion A D, Law M A, Noel P, Kim Y J, Haverty T P, Nutman T B. Safety and efficacy of the monoclonal anti-interleukin-5 antibody SCH55700 in the treatment of patients with hypereosinophilic syndrome. Blood 2004: 103: 2939-2941.
92. Garrett J K, Jameson S C, Thomson B et al. Anti-interleukin-5 (mepolizumab) therapy for hypereosinophilic syndromes. J Allergy Clin Immunol 2004: 113: 115-119.