Association of ORMDL3 with rhinovirus-induced endoplasmic reticulum stress and type I Interferon responses in human leucocytes

Clinical and Experimental Allergy

Volumn 47, Issue 3, 2017, Pages 371-382

  Liu, Y P ^a   Rajamanikham, V ^a   Baron, M ^b   Patel, S ^a   Mathur, S K ^a   Schwantes, E A ^a   Ober, C ^c   Jackson, D J ^a   Gern, J E ^a   Lemanske, R F ^a   Smith, J A ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

Author keywords

17q21; asthma; basic mechanisms; IFN=beta unfolded protein response; ORMDL3; Rhinovirus

Indexed keywords

BETA1 INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN A5; OROSOMUCOID; OROSOMUCOID LIKE 3; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; INTERFERON; MEMBRANE PROTEIN; MOLECULAR CHAPERONE GRP78; ORMDL3 PROTEIN, HUMAN;

ADULT; ARTICLE; ASTHMA; CELL CONTACT; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; EOSINOPHIL COUNT; FEMALE; GENOTYPE; HUMAN; HUMAN CELL; LEUKOCYTE; MALE; MIDDLE AGED; PLASMACYTOID DENDRITIC CELL; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RHINOVIRUS; WESTERN BLOTTING; B LYMPHOCYTE; CELL LINE; CHROMOSOME 17; DENDRITIC CELL; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION; GENETICS; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PICORNAVIRUS INFECTION; VIROLOGY;

ADULT; ASTHMA; B-LYMPHOCYTES; CELL LINE; CHROMOSOMES, HUMAN, PAIR 17; DENDRITIC CELLS; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HEAT-SHOCK PROTEINS; HUMANS; INTERFERON TYPE I; LEUKOCYTES; MEMBRANE PROTEINS; MIDDLE AGED; PICORNAVIRIDAE INFECTIONS; RHINOVIRUS;

EID: 85014062672     PISSN: 09547894     EISSN: 13652222     Source Type: Journal    
DOI: 10.1111/cea.12903     Document Type: Article

References (44)

1. Moffatt MF, Kabesch M, Liang L et al. Genetic variants regulating ORMDL3 expression contribute to the risk of childhood asthma. Nature 2007; 448:470–3.
2. Ono JG, Worgall TS, Worgall S. 17q21 locus and ORMDL3: an increased risk for childhood asthma. Pediatr Res 2014; 75:165–70.
3. Moffatt MF, Gut IG, Demenais F, et al. A large-scale, consortium-based genomewide association study of asthma. N Engl J Med 2010; 363:1211–21.
4. Caliskan M, Bochkov YA, Kreiner-Moller E, et al. Rhinovirus wheezing illness and genetic risk of childhood-onset asthma. N Engl J Med 2013; 368:1398–407.
5. Murphy A, Chu JH, Xu M, et al. Mapping of numerous disease-associated expression polymorphisms in primary peripheral blood CD4+ lymphocytes. Hum Mol Genet 2010; 19:4745–57.
6. Acevedo N, Reinus LE, Greco D, et al. Risk of childhood asthma is associated with CpG-site polymorphisms, regional DNA methylation and mRNA levels at the GSDMB/ORMDL3 locus. Hum Mol Genet 2015; 24:875–90.
7. Miller M, Rosenthal P, Beppu A, et al. ORMDL3 transgenic mice have increased airway remodeling and airway responsiveness characteristic of asthma. J Immunol 2014; 192:3475–87.
8. Breslow DK, Collins SR, Bodenmiller B, et al. Orm family proteins mediate sphingolipid homeostasis. Nature 2010; 463:1048–53.
9. Cantero-Recasens G, Fandos C, Rubio-Moscardo F, Valverde MA, Vicente R et al. The asthma-associated ORMDL3 gene product regulates endoplasmic reticulum-mediated calcium signaling and cellular stress. Hum Mol Genet 2010; 19:111–21.
10. Smith JA, Barnes MD, Hong D, DeLay ML, Inman RD, Colbert RA. et al. Endoplasmic reticulum stress and the unfolded protein response are linked to synergistic IFN-beta induction via X-box binding protein 1. Eur J Immunol 2008; 38:1194–203.
11. Martinon F, Chen X, Lee AH, Glimcher LH. et al. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol, 2010; 11:411–8.
12. DeLay ML, Turner MJ, Klenk EI, Smith JA, Sowders DP, Colbert RA. et al. HLA-B27 misfolding and the unfolded protein response augment interleukin-23 production and are associated with Th17 activation in transgenic rats. Arthritis Rheum 2009; 60:2633–43.
13. Smith JA. A new paradigm: innate immune sensing of viruses via the unfolded protein response. Front Microbiol 2014; 5:222.
14. Miller M, Tarn AB, Cho JY. et al. ORMDL3 is an inducible lung epithelial gene regulating metalloproteases, chemokines, OAS, and ATF6. Proc Natl Acad Sci U S A 2012; 109:16648–53.
15. Gern JE, Dick EC, Lee WM, Murray S, Meyer K, Handzel ZT, Busse WW et al. Rhinovirus enters but does not replicate inside monocytes and airway macrophages. J Immunol 1996; 156:621–7.
16. Saba TG, Chung Y, Hong JY, Sajjan US, Bentley JK, Hershenson MB. et al. Rhinovirus-induced macrophage cytokine expression does not require endocytosis or replication. Am J Respir Cell Mol Biol 2014; 50:974–84.
17. Ilarraza R, Wu Y, Skappak CD, Ajamian F, Proud D, Adamko DJ. et al. Rhinovirus has the unique ability to directly activate human T cells in vitro. J Allergy Clin Immunol 2013; 131:395–404.
18. Gern JE, Vrtis R, Kelly EA, Dick EC, Busse WW et al. Rhinovirus produces nonspecific activation of lymphocytes through a monocyte-dependent mechanism. J Immunol 1996; 157:1605–12.
19. Aab A, Wirz O, van de Veen W, et al. Human rhinoviruses enter and induce proliferation of B lymphocytes. Allergy, 2016; 72:232–43.
20. Pritchard AL, Carroll ML, Burel JG, White OJ, Phipps S, Upham JW. et al. Innate IFNs and plasmacytoid dendritic cells constrain Th2 cytokine responses to rhinovirus: a regulatory mechanism with relevance to asthma. J Immunol 2012; 188:5898–905.
21. Handzel ZT, Busse WW, Sedgwick JB, Vrtis R, Lee WM, Kelly EA, Gern JE. et al. Eosinophils bind rhinovirus and activate virus-specific T cells. J Immunol 1998; 160:1279–84.
22. Bentley JK, Sajjan US, Dzaman MB, Jarjour NN, Lee WM, Gern JE, Hershenson MB. et al. Rhinovirus colocalizes with CD68- and CD11b-positive macrophages following experimental infection in humans. J Allergy Clin Immunol, 2013; 132:758–61.
23. Korpi-Steiner NL, Valkenaar SM, Bates ME, Evans MD, Gern JE, Bertics PJ et al. Human monocytic cells direct the robust release of CXCL10 by bronchial epithelial cells during rhinovirus infection. Clin Exp Allergy 2010; 40:1203–13.
24. Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem 2005; 74:739–89.
25. Walter P, Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011; 334:1081–6.
26. Yamamoto K, Sato T, Matsui T, et al. Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6alpha and XBP1. Dev Cell 2007; 13:365–76.
27. Ha SG, Ge XN, Bahaie NS, Kang BN, Rao A, Rao SP, Sriramarao P. et al. ORMDL3 promotes eosinophil trafficking and activation via regulation of integrins and CD48. Nat Commun 2013; 4:2479.
28. Qiu R, Yang Y, Zhao H, et al. Signal transducer and activator of transcription 6 directly regulates human ORMDL3 expression. FEBS J 2013; 280:2014–26.
29. Schedel M, Michel S, Gaertner VD, et al. Polymorphisms related to ORMDL3 are associated with asthma susceptibility, alterations in transcriptional regulation of ORMDL3, and changes in TH2 cytokine levels. J Allergy Clin Immunol 2015; 136:893–903.e14.
30. Korsgren M, Erjefalt JS, Korsgren O, Sundler F, Persson CG. et al. Allergic eosinophil-rich inflammation develops in lungs and airways of B cell-deficient mice. J Exp Med 1997; 185:885–92.
31. Hamelmann E, Takeda K, Schwarze J, Vella AT, Irvin CG, Gelfand EW. et al. Development of eosinophilic airway inflammation and airway hyperresponsiveness requires interleukin-5 but not immunoglobulin E or B lymphocytes. Am J Respir Cell Mol Biol 1999; 21:480–9.
32. Drake LY, Iijima K, Hara K, Kobayashi T, Kephart GM, Kita H. et al. B cells play key roles in th2-type airway immune responses in mice exposed to natural airborne allergens. PLoS ONE 2015; 10:e0121660.
33. Fuertes E, Soderhall C, Acevedo N, et al. Associations between the 17q21 region and allergic rhinitis in 5 birth cohorts. J Allergy Clin Immunol 2015; 135:573–6.
34. Li S, Kong L, Yu X. The expanding roles of endoplasmic reticulum stress in virus replication and pathogenesis. Crit Rev Microbiol 2015; 41:150–64.
35. Reimold AM, Iwakoshi NN, Manis J, et al. Plasma cell differentiation requires the transcription factor XBP-1. Nature 2001; 412:300–7.
36. Hu CC, Dougan SK, McGehee AM, Love JC, Ploegh HL. et al. XBP-1 regulates signal transduction, transcription factors and bone marrow colonization in B cells. EMBO J 2009; 28:1624–36.
37. Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev 1999; 13:1211–33.
38. Price BD, Mannheim-Rodman LA, Calderwood SK. Brefeldin A, thapsigargin, and AIF4- stimulate the accumulation of GRP78 mRNA in a cycloheximide dependent manner, whilst induction by hypoxia is independent of protein synthesis. J Cell Physiol 1992; 152:545–52.
39. Liu YP, Zeng L, Tian A, et al. Endoplasmic reticulum stress regulates the innate immunity critical transcription factor IRF3. J Immunol 2012; 189:4630–9.
40. Rao J, Yue S, Fu Y, et al. ATF6 mediates a pro-inflammatory synergy between ER stress and TLR activation in the pathogenesis of liver ischemia-reperfusion injury. Am J Transplant 2014; 14:1552–61.
41. Djukanovic R, Harrison T, Johnston SL, et al. The effect of inhaled IFN-beta on worsening of asthma symptoms caused by viral infections. A randomized trial. Am J Respir Crit Care Med 2014; 190:145–54.
42. Miller EK, Hernandez JZ, Wimmenauer V, et al. A mechanistic role for type III IFN-lambda1 in asthma exacerbations mediated by human rhinoviruses. Am J Respir Crit Care Med 2012; 185:508–16.
43. Schwantes EA, Manthei DM, Denlinger LC, Evans MD, Gern JE, Jarjour NN, Mathur SK. et al. Interferon gene expression in sputum cells correlates with the Asthma Index Score during virus-induced exacerbations. Clin Exp Allergy 2014; 44:813–21.
44. Lluis A, Schedel M, Liu J, et al. Asthma-associated polymorphisms in 17q21 influence cord blood ORMDL3 and GSDMA gene expression and IL-17 secretion. J Allergy Clin Immunol 2011; 127:1587–94.e6.