Cysteinyl leukotriene receptor 1 expression identifies a subset of neutrophils during the antiviral response that contributes to postviral atopic airway disease

Journal of Allergy and Clinical Immunology

Volumn 142, Issue 4, 2018, Pages 1206-1217.e5

  Cheung, Dorothy S ^a,d   Sigua, Jerome A ^a,e   Simpson, Pippa M ^a   Yan, Ke ^a   Hussain, Syed Rehan A ^b,c   Santoro, Jennifer L ^a,b,c   Buell, Erika J ^a   Hunter, Desire A ^a   Rohlfing, Michelle ^a,b,c   Patadia, Deepa ^a,b,f   Grayson, Mitchell H ^a,b,c  

^a MEDICAL COLLEGE OF WISCONSIN   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c THE RESEARCH INSTITUTE AT NATIONWIDE CHILDREN S HOSPITAL   (United States)

^d GENENTECH INC   (United States)

^e VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^f LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Asthma; cysteinyl leukotrienes; nasal lavage; neutrophils; viral infection

Indexed keywords

ALPHA4 INTEGRIN; CYSTEINYL LEUKOTRIENE RECEPTOR 1; LEUKOTRIENE RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; PRANLUKAST; RANTES; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG; LEUKOTRIENE D4 RECEPTOR;

ADOLESCENT; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ASTHMA; ASTHMATIC STATE; CHILD; CONTROLLED STUDY; CONVALESCENCE; FEMALE; FLOW CYTOMETRY; FOLLOW UP; FORCED EXPIRATORY VOLUME; HUMAN; HUMAN CELL; IN VIVO STUDY; MALE; MOUSE; NASAL LAVAGE; NASAL LAVAGE FLUID; NEUTROPHIL; NONHUMAN; NOSE SMEAR; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RESPIRATORY BURST; RESPIRATORY TRACT DISEASE; SENDAI VIRUS INFECTION; UPPER RESPIRATORY TRACT INFECTION; VIRAL RESPIRATORY TRACT INFECTION; VIRUS DETECTION; ANIMAL; CYTOLOGY; IMMUNOLOGY; MIDDLE AGED; NOSE MUCOSA; PRESCHOOL CHILD; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT INFECTION; RESPIROVIRUS INFECTION; SENDAI VIRUS; VIROLOGY; YOUNG ADULT;

ADOLESCENT; ADULT; ANIMALS; CHILD; CHILD, PRESCHOOL; FEMALE; HUMANS; INTEGRIN ALPHA4; MALE; MICE; MIDDLE AGED; NASAL MUCOSA; NEUTROPHILS; RECEPTORS, LEUKOTRIENE; RESPIRATORY HYPERSENSITIVITY; RESPIRATORY TRACT INFECTIONS; RESPIROVIRUS INFECTIONS; SENDAI VIRUS; YOUNG ADULT;

EID: 85040679730     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2017.11.026     Document Type: Article

References (42)

1. Asher, M.I., Montefort, S., Bjorksten, B., Lai, C.K., Strachan, D.P., Weiland, S.K., et al. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet 368 (2006), 733–743.
2. Centers for Disease Control and Prevention, Vital signs: asthma prevalence, disease characteristics, and self-management education—United States, 2001-2009. MMWR Morb Mortal Wkly Rep 60 (2011), 547–552.
3. Meltzer, E.O., Bukstein, D.A., The economic impact of allergic rhinitis and current guidelines for treatment. Ann Allergy Asthma Immunol 106:suppl (2011), S12–S16.
4. Chipps, B.E., Zeiger, R.S., Borish, L., Wenzel, S.E., Yegin, A., Hayden, M.L., et al. Key findings and clinical implications from The Epidemiology and Natural History of Asthma: Outcomes and Treatment Regimens (TENOR) study. J Allergy Clin Immunol 130 (2012), 332–342.e10.
5. Sigurs, N., Aljassim, F., Kjellman, B., Robinson, P.D., Sigurbergsson, F., Bjarnason, R., et al. Asthma and allergy patterns over 18 years after severe RSV bronchiolitis in the first year of life. Thorax 65 (2010), 1045–1052.
6. Sigurs, N., A cohort of children hospitalised with acute RSV bronchiolitis: impact on later respiratory disease. Paediatr Respir Rev 3 (2002), 177–183.
7. Carroll, K.N., Hartert, T.V., The impact of respiratory viral infection on wheezing illnesses and asthma exacerbations. Immunol Allergy Clin North Am 28 (2008), 539–561 viii.
8. Escobar, G.J., Ragins, A., Li, S.X., Prager, L., Masaquel, A.S., Kipnis, P., Recurrent wheezing in the third year of life among children born at 32 weeks’ gestation or later: relationship to laboratory-confirmed, medically attended infection with respiratory syncytial virus during the first year of life. Arch Pediatr Adolesc Med 164 (2010), 915–922.
9. Simoes, E.A., Carbonell-Estrany, X., Rieger, C.H., Mitchell, I., Fredrick, L., Groothuis, J.R., The effect of respiratory syncytial virus on subsequent recurrent wheezing in atopic and nonatopic children. J Allergy Clin Immunol 126 (2010), 256–262.
10. Bem, R.A., Domachowske, J.B., Rosenberg, H.F., Animal models of human respiratory syncytial virus disease. Am J Physiol Lung Cell Mol Physiol 301 (2011), L148–L156.
11. Grayson, M.H., Cheung, D., Rohlfing, M.M., Kitchens, R., Spiegel, D.E., Tucker, J., et al. Induction of high-affinity IgE receptor on lung dendritic cells during viral infection leads to mucous cell metaplasia. J Exp Med 204 (2007), 2759–2769.
12. Cheung, D.S., Ehlenbach, S.J., Kitchens, R.T., Riley, D.A., Thomas, L.L., Holtzman, M.J., et al. Cutting edge: CD49d+ neutrophils induce Fc epsilon RI expression on lung dendritic cells in a mouse model of postviral asthma. J Immunol 185 (2010), 4983–4987.
13. Holtzman, M.J., Asthma as a chronic disease of the innate and adaptive immune systems responding to viruses and allergens. J Clin Invest 122 (2012), 2741–2748.
14. Pitrez, P.M., Brennan, S., Sly, P.D., Inflammatory profile in nasal secretions of infants hospitalized with acute lower airway tract infections. Respirology 10 (2005), 365–370.
15. Cheung, D.S., Grayson, M.H., Role of viruses in the development of atopic disease in pediatric patients. Curr Allergy Asthma Rep 12 (2012), 613–620.
16. Sigua, J.A., Buelow, B., Cheung, D.S., Buell, E., Hunter, D., Klancnik, M., et al. CD49d-expressing neutrophils differentiate atopic from nonatopic individuals. J Allergy Clin Immunol 133 (2014), 901–904.e5.
17. Khan, S.H., Grayson, M.H., Cross-linking IgE augments human conventional dendritic cell production of CC chemokine ligand 28. J Allergy Clin Immunol 125 (2010), 265–267.
18. Subrata, L.S., Bizzintino, J., Mamessier, E., Bosco, A., McKenna, K.L., Wikstrom, M.E., et al. Interactions between innate antiviral and atopic immunoinflammatory pathways precipitate and sustain asthma exacerbations in children. J Immunol 183 (2009), 2793–2800.
19. Sadik, C.D., Kim, N.D., Luster, A.D., Neutrophils cascading their way to inflammation. Trends Immunol 32 (2011), 452–460.
20. Figueroa, D.J., Borish, L., Baramki, D., Philip, G., Austin, C.P., Evans, J.F., Expression of cysteinyl leukotriene synthetic and signalling proteins in inflammatory cells in active seasonal allergic rhinitis. Clin Exp Allergy 33 (2003), 1380–1388.
21. Fullmer, J.J., Khan, A.M., Elidemir, O., Chiappetta, C., Stark, J.M., Colasurdo, G.N., Role of cysteinyl leukotrienes in airway inflammation and responsiveness following RSV infection in BALB/c mice. Pediatr Allergy Immunol 16 (2005), 593–601.
22. Akk, A.M., Simmons, P.M., Chan, H.W., Agapov, E., Holtzman, M.J., Grayson, M.H., et al. Dipeptidyl peptidase I-dependent neutrophil recruitment modulates the inflammatory response to Sendai virus infection. J Immunol 180 (2008), 3535–3542.
23. Parmentier, C.N., Fuerst, E., McDonald, J., Bowen, H., Lee, T.H., Pease, J.E., et al. Human T(H)2 cells respond to cysteinyl leukotrienes through selective expression of cysteinyl leukotriene receptor 1. J Allergy Clin Immunol 129 (2012), 1136–1142.
24. Trian, T., Allard, B., Dupin, I., Carvalho, G., Ousova, O., Maurat, E., et al. House dust mites induce proliferation of severe asthmatic smooth muscle cells via an epithelium-dependent pathway. Am J Respir Crit Care Med 191 (2015), 538–546.
25. Choi, J.P., Kim, Y.S., Kim, O.Y., Kim, Y.M., Jeon, S.G., Roh, T.Y., et al. TNF-alpha is a key mediator in the development of Th2 cell response to inhaled allergens induced by a viral PAMP double-stranded RNA. Allergy 67 (2012), 1138–1148.
26. Gotera, J., Giuffrida, M., Mavarez, A., Pons, H., Bermudez, J., Maldonado, M., et al. Respiratory syncytial virus infection increases regulated on activation normal T cell expressed and secreted and monocyte chemotactic protein 1 levels in serum of patients with asthma and in human monocyte cultures. Ann Allergy Asthma Immunol 108 (2012), 316–320.
27. Tasker, L., Lindsay, R.W., Clarke, B.T., Cochrane, D.W., Hou, S., Infection of mice with respiratory syncytial virus during neonatal life primes for enhanced antibody and T cell responses on secondary challenge. Clin Exp Immunol 153 (2008), 277–288.
28. Lammermann, T., Afonso, P.V., Angermann, B.R., Wang, J.M., Kastenmuller, W., Parent, C.A., et al. Neutrophil swarms require LTB4 and integrins at sites of cell death in vivo. Nature 498 (2013), 371–375.
29. Dyer, K.D., Garcia-Crespo, K.E., Killoran, K.E., Rosenberg, H.F., Antigen profiles for the quantitative assessment of eosinophils in mouse tissues by flow cytometry. J Immunol Methods 369 (2011), 91–97.
30. McGovern, T., Goldberger, M., Chen, M., Allard, B., Hamamoto, Y., Kanaoka, Y., et al. CysLT1 receptor is protective against oxidative stress in a model of irritant-induced asthma. J Immunol 197 (2016), 266–277.
31. Lewis, S.M., Treacher, D.F., Bergmeier, L., Brain, S.D., Chambers, D.J., Pearson, J.D., et al. Plasma from patients with sepsis up-regulates the expression of CD49d and CD64 on blood neutrophils. Am J Respir Cell Mol Biol 40 (2009), 724–732.
32. Meliton, A.Y., Munoz, N.M., Osan, C.M., Meliton, L.N., Leff, A.R., Leukotriene D4 activates {beta} 2-integrin adhesion in human polymorphonuclear leukocytes. Eur Respir J 35 (2010), 402–409.
33. Kolaczkowska, E., Kubes, P., Neutrophil recruitment and function in health and inflammation. Nat Rev Immunol 13 (2013), 159–175.
34. Bisgaard, H., A randomized trial of montelukast in respiratory syncytial virus postbronchiolitis. Am J Respir Crit Care Med 167 (2003), 379–383.
35. Kloepfer, K.M., DeMore, J.P., Vrtis, R.F., Swenson, C.A., Gaworski, K.L., Bork, J.A., et al. Effects of montelukast on patients with asthma after experimental inoculation with human rhinovirus 16. Ann Allergy Asthma Immunol 106 (2011), 252–257.
36. Bisgaard, H., Flores-Nunez, A., Goh, A., Azimi, P., Halkas, A., Malice, M.P., et al. Study of montelukast for the treatment of respiratory symptoms of post-respiratory syncytial virus bronchiolitis in children. Am J Respir Crit Care Med 178 (2008), 854–860.
37. Sigua, J.A., Buelow, B., Cheung, D.S., Buell, E., Hunter, D., Klancnik, M., et al. CD49d-expressing neutrophils differentiate atopic from nonatopic individuals. J Allergy Clin Immunol 133 (2014), 901–904.e5.
38. Cheung, D.S., Ehlenbach, S.J., Kitchens, R.T., Riley, D.A., Thomas, L.L., Holtzman, M.J., et al. Cutting edge: CD49d+ neutrophils induce FcepsilonRI expression on lung dendritic cells in a mouse model of postviral asthma. J Immunol 185 (2010), 4983–4987.
39. Cheung, D.S., Ehlenbach, S.J., Kitchens, T., Riley, D.A., Grayson, M.H., Development of atopy by severe paramyxoviral infection in a mouse model. Ann Allergy Asthma Immunol 105 (2010), 437–443.e1.
40. Buelow, B.J., Rohlfing, M., Jung, F., Douglas, G.J., Grayson, M.H., POL7085 or anti-CCL28 treatment inhibits development of post-paramyxoviral airway disease. Immun Inflamm Dis 5 (2017), 98–108.
41. Flandre, T.D., Leroy, P.L., Desmecht, D.J., Effect of somatic growth, strain, and sex on double-chamber plethysmographic respiratory function values in healthy mice. J Appl Physiol (1985) 94 (2003), 1129–1136.
42. Lofgren, J.L., Mazan, M.R., Ingenito, E.P., Lascola, K., Seavey, M., Walsh, A., et al. Restrained whole body plethysmography for measure of strain-specific and allergen-induced airway responsiveness in conscious mice. J Appl Physiol (1985) 101 (2006), 1495–1505.