Pulmonary ORMDL3 is critical for induction of Alternaria-induced allergic airways disease

Journal of Allergy and Clinical Immunology

Volumn 139, Issue 5, 2017, Pages 1496-1507.e3

  Löser, Stephan ^a   Gregory, Lisa G ^a   Zhang, Youming ^a   Schaefer, Katrein ^a   Walker, Simone A ^a   Buckley, James ^a   Denney, Laura ^a   Dean, Charlotte H ^a   Cookson, William O C ^a   Moffatt, Miriam F ^a   Lloyd, Clare M ^a  

^a NATIONAL HEART AND LUNG INSTITUTE   (United Kingdom)

Author keywords

Alternaria; asthma; ORMDL3; unfolded protein response; uric acid

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ADENO ASSOCIATED VIRUS VECTOR; ALLERGEN; ENHANCED GREEN FLUORESCENT PROTEIN; IMMUNOGLOBULIN E; INTERLEUKIN 13; INTERLEUKIN 4; INTERLEUKIN 5; ISOPROTEIN; LACTATE DEHYDROGENASE; METHACHOLINE; ORMDL3 PROTEIN; UNCLASSIFIED DRUG; URIC ACID; X BOX BINDING PROTEIN 1; MEMBRANE PROTEIN; ORMDL3 PROTEIN, MOUSE;

ADULT; AIRWAY EPITHELIUM CELL; ALTERNARIA ALTERNATA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHOSPHORYLATION; BRONCHUS EPITHELIUM; CELLULAR STRESS RESPONSE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; EOSINOPHILIA; FETUS; GENE OVEREXPRESSION; IMMUNOFLUORESCENCE; KNOCKOUT MOUSE; LUNG FUNCTION; LUNG LAVAGE; LYMPHOID CELL; MALE; MOUSE; NEWBORN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RESPIRATORY TRACT ALLERGY; UNFOLDED PROTEIN RESPONSE; ALTERNARIA; ANIMAL; ASTHMA; C57BL MOUSE; DISEASE MODEL; GENETICS; IMMUNOLOGY; LUNG; METABOLISM; RESPIRATORY MUCOSA;

ALLERGENS; ALTERNARIA; ANIMALS; ASTHMA; DISEASE MODELS, ANIMAL; LUNG; MALE; MEMBRANE PROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; RESPIRATORY MUCOSA; URIC ACID;

EID: 85006256422     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.07.033     Document Type: Article

References (46)

1. 1 Wenzel, S.E., Asthma phenotypes: the evolution from clinical to molecular approaches. Nat Med 18 (2012), 716–725.
2. 2 Holgate, S.T., The sentinel role of the airway epithelium in asthma pathogenesis. Immunol Rev 242 (2011), 205–219.
3. 3 Moffatt, M.F., Kabesch, M., Liang, L., Dixon, A.L., Strachan, D., Heath, S., et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature 448 (2007), 470–473.
4. 4 Hjelmqvist, L., Tuson, M., Marfany, G., Herrero, E., Balcells, S., Gonzalez-Duarte, R., ORMDL proteins are a conserved new family of endoplasmic reticulum membrane proteins. Genome Biol, 3, 2002 RESEARCH0027.
5. 5 Miller, M., Tam, A.B., Cho, J.Y., Doherty, T.A., Pham, A., Khorram, N., et al. ORMDL3 is an inducible lung epithelial gene regulating metalloproteases, chemokines, OAS, and ATF6. PNAS 109 (2012), 16648–16653.
6. 6 Breslow, D.K., Collins, S.R., Bodenmiller, B., Aebersold, R., Simons, K., Shevchenko, A., et al. Orm family proteins mediate sphingolipid homeostasis. Nature 463 (2010), 1048–1053.
7. 7 Worgall, T.S., Veerappan, A., Sung, B., Kim, B.I., Weiner, E., Bholah, R., et al. Impaired sphingolipid synthesis in the respiratory tract induces airway hyperreactivity. Sci Transl Med, 5, 2013, 186ra67.
8. 8 Oyeniran, C., Sturgill, J.L., Hait, N.C., Huang, W.C., Avni, D., Maceyka, M., et al. Aberrant ORM (yeast)-like protein isoform 3 (ORMDL3) expression dysregulates ceramide homeostasis in cells and ceramide exacerbates allergic asthma in mice. J Allergy Clin Immunol 136 (2015), 1035–1046.e6.
9. 9 Miller, M., Rosenthal, P., Beppu, A., Mueller, J.L., Hoffman, H.M., Tam, A.B., et al. ORMDL3 transgenic mice have increased airway remodeling and airway responsiveness characteristic of asthma. J Immunol 192 (2014), 3475–3487.
10. 10 Lodish, H.F., Kong, N., Wikstrom, L., Calcium is required for folding of newly made subunits of the asialoglycoprotein receptor within the endoplasmic reticulum. J Biol Chem 267 (1992), 12753–12760.
11. 11 Bertolotti, A., Zhang, Y., Hendershot, L.M., Harding, H.P., Ron, D., Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2 (2000), 326–332.
12. 12 Shen, J., Chen, X., Hendershot, L., Prywes, R., ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell 3 (2002), 99–111.
13. 13 Adachi, Y., Yamamoto, K., Okada, T., Yoshida, H., Harada, A., Mori, K., ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum. Cell Struct Funct 33 (2008), 75–89.
14. 14 Cantero-Recasens, G., Fandos, C., Rubio-Moscardo, F., Valverde, M.A., Vicente, R., The asthma-associated ORMDL3 gene product regulates endoplasmic reticulum-mediated calcium signaling and cellular stress. Hum Mol Genet 19 (2010), 111–121.
15. 15 Seibler, J., Zevnik, B., Küter-Luks, B., Andreas, S., Kern, H., Hennek, T., et al. Rapid generation of inducible mouse mutants. Nucleic Acids Res, 31, 2003, e12.
16. 16 Snelgrove, R.J., Gregory, L.G., Peiro, T., Akthar, S., Campbell, G.A., Walker, S.A., et al. Alternaria-derived serine protease activity drives IL-33-mediated asthma exacerbations. J Allergy Clin Immunol 134 (2014), 583–592.e6.
17. 17 Ha, S.G., Ge, X.N., Bahaie, N.S., Kang, B.N., Rao, A., Rao, S.P., et al. ORMDL3 promotes eosinophil trafficking and activation via regulation of integrins and CD48. Nat Commun, 4, 2013, 2479.
18. 18 Todd, D.J., Lee, A.-H., Glimcher, L.H., The endoplasmic reticulum stress response in immunity and autoimmunity. Nat Rev Immunol 8 (2008), 663–674.
19. 19 Harding, H.P., Zhang, Y., Bertolotti, A., Zeng, H., Ron, D., Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5 (2000), 897–904.
20. 20 Harding, H.P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M., et al. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6 (2000), 1099–1108.
21. 21 Yoshida, H., Matsui, T., Yamamoto, A., Okada, T., Mori, K., XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107 (2001), 881–891.
22. 22 Shoulders, M.D., Ryno, L.M., Genereux, J.C., Moresco, J.J., Tu, P.G., Wu, C., et al. Stress-independent activation of XBP1s and/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep 3 (2013), 1279–1292.
23. 23 Shi, Y., Porter, K., Parameswaran, N., Bae, H.K., Pestka, J.J., Role of GRP78/BiP degradation and ER stress in deoxynivalenol-induced interleukin-6 upregulation in the macrophage. Toxicol Sci 109 (2009), 247–255.
24. 24 Menu, P., Mayor, A., Zhou, R., Tardivel, A., Ichijo, H., Mori, K., et al. ER stress activates the NLRP3 inflammasome via an UPR-independent pathway. Cell Death Dis, 3, 2012, e261.
25. 25 Bell, C.L., Vandenberghe, L.H., Bell, P., Limberis, M.P., Gao, G.P., Van Vliet, K., et al. The AAV9 receptor and its modification to improve in vivo lung gene transfer in mice. J Clin Invest 121 (2011), 2427–2435.
26. 26 Dales, R.E., Cakmak, S., Burnett, R.T., Judek, S., Coates, F., Brook, J.R., Influence of ambient fungal spores on emergency visits for asthma to a regional children's hospital. Am J Respir Crit Care Med 162 (2000), 2087–2090.
27. 27 O'Driscoll, B.R., Hopkinson, L.C., Denning, D.W., Mold sensitization is common amongst patients with severe asthma requiring multiple hospital admissions. BMC Pulm Med, 5, 2005, 4.
28. 28 Bisgaard, H., Bonnelykke, K., Sleiman, P.M., Brasholt, M., Chawes, B., Kreiner-Moller, E., et al. Chromosome 17q21 gene variants are associated with asthma and exacerbations but not atopy in early childhood. Am J Respir Crit Care Med 179 (2009), 179–185.
29. 29 Tavendale, R., Macgregor, D.F., Mukhopadhyay, S., Palmer, C.N., A polymorphism controlling ORMDL3 expression is associated with asthma that is poorly controlled by current medications. J Allergy Clin Immunol 121 (2008), 860–863.
30. 30 Mahn, K., Hirst, S.J., Ying, S., Holt, M.R., Lavender, P., Ojo, O.O., et al. Diminished sarco/endoplasmic reticulum Ca2+ ATPase (SERCA) expression contributes to airway remodelling in bronchial asthma. Proc Natl Acad Sci 106 (2009), 10775–10780.
31. 31 Kool, M., Willart, M.A., van Nimwegen, M., Bergen, I., Pouliot, P., Virchow, J.C., et al. An unexpected role for uric acid as an inducer of T helper 2 cell immunity to inhaled antigens and inflammatory mediator of allergic asthma. Immunity 34 (2011), 527–540.
32. 32 Hara, K., Iijima, K., Elias, M.K., Seno, S., Tojima, I., Kobayashi, T., et al. Airway uric acid is a sensor of inhaled protease allergens and initiates type 2 immune responses in respiratory mucosa. J Immunol 192 (2014), 4032–4042.
33. 33 Li, L., Wan, C., Wen, F., An unexpected role for serum uric acid as a biomarker for severity of asthma exacerbation. Asian Pac J Allergy Immunol 32 (2014), 93–99.
34. 34 Gold, M.J., Hiebert, P.R., Park, H.Y., Stefanowicz, D., Le, A., Starkey, M.R., et al. Mucosal production of uric acid by airway epithelial cells contributes to particulate matter-induced allergic sensitization. Mucosal Immunol 9 (2015), 809–820.
35. 35 Chao, H.H., Liu, J.C., Lin, J.W., Chen, C.H., Wu, C.H., Cheng, T.H., Uric acid stimulates endothelin-1 gene expression associated with NADPH oxidase in human aortic smooth muscle cells. Acta Pharmacol Sin 29 (2008), 1301–1312.
36. 36 Albertoni, G., Schor, N., Resveratrol inhibits the intracellular calcium increase and angiotensin/endothelin system activation induced by soluble uric acid in mesangial cells. Braz J Med Biol Res 48 (2015), 51–56.
37. 37 Kim, S.R., Kim, D.I., Kang, M.R., Lee, K.S., Park, S.Y., Jeong, J.S., et al. Endoplasmic reticulum stress influences bronchial asthma pathogenesis by modulating nuclear factor kappaB activation. J Allergy Clin Immunol 132 (2013), 1397–1408.
38. 38 Zhuang, L.L., Jin, R., Zhu, L.H., Xu, H.G., Li, Y., Gao, S., et al. Promoter characterization and role of cAMP/PKA/CREB in the basal transcription of the mouse ORMDL3 gene. PLoS One, 8, 2013, e60630.
39. 39 Zhao, J., Liu, K., Lu, J., Ma, J., Zhang, X., Jiang, Y., et al. Alternariol induces DNA polymerase beta expression through the PKA-CREB signaling pathway. Int J Oncol 40 (2012), 1923–1928.
40. 40 Bonnelykke, K., Sleiman, P., Nielsen, K., Kreiner-Moller, E., Mercader, J.M., Belgrave, D., et al. A genome-wide association study identifies CDHR3 as a susceptibility locus for early childhood asthma with severe exacerbations. Nat Genet 46 (2014), 51–55.
41. 41 Downs, S.H., Mitakakis, T.Z., Marks, G.B., Car, N.G., Belousova, E.G., Leuppi, J.D., et al. Clinical importance of Alternaria exposure in children. Am J Respir Crit Care Med 164 (2001), 455–459.
42. 42 Tham, R., Dharmage, S.C., Taylor, P.E., Katelaris, C.H., Vicendese, D., Abramson, M.J., et al. Outdoor fungi and child asthma health service attendances. Pediatr Allergy Immunol 25 (2014), 439–449.
43. 43 Castanhinha, S., Sherburn, R., Walker, S., Gupta, A., Bossley, C.J., Buckley, J., et al. Pediatric severe asthma with fungal sensitization is mediated by steroid-resistant IL-33. J Allergy Clin Immunol 136 (2015), 312–322.e7.
44. 44 Walker, V., Ammonia toxicity and its prevention in inherited defects of the urea cycle. Diabetes Obes Metab 11 (2009), 823–835.
45. Juncadella, I.J., Kadl, A., Sharma, A.K., Shim, Y.M., Hochreiter-Hufford, A., Borish, L., et al. Apoptotic cell clearance by bronchial epithelial cells critically influences airway inflammation. Nature 493 (2013), 547–551.
46. Snelgrove, R.J., Gregory, L.G., Peiro, T., Akthar, S., Campbell, G.A., Walker, S.A., et al. Alternaria-derived serine protease activity drives IL-33-mediated asthma exacerbations. J Allergy Clin Immunol 134 (2014), 583–592.e6.