Innate Immune Receptors in Human Airway Smooth Muscle Cells: Activation by TLR1/2, TLR3, TLR4, TLR7 and NOD1 Agonists

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Månsson Kvarnhammar, Anne ^a   Tengroth, Lotta ^a   Adner, Mikael ^a   Cardell, Lars Olaf ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CYSTEINYLLEUKOTRIENE 1 RECEPTOR; EOTAXIN; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HLA DR ANTIGEN; IMIQUIMOD; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 6; INTERLEUKIN 8; LEUKOTRIENE RECEPTOR; LIPOPOLYSACCHARIDE; MESSENGER RNA; MYOSIN LIGHT CHAIN KINASE; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN LIKE RECEPTOR; PATTERN RECOGNITION RECEPTOR; POLYINOSINIC POLYCYTIDYLIC ACID; RANTES; RETINOIC ACID INDUCIBLE PROTEIN I; RETINOIC ACID INDUCIBLE PROTEIN I LIKE RECEPTOR; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 6; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ARTICLE; BREATHING MUSCLE; CELL PROLIFERATION; CELL SURFACE; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; INNATE IMMUNITY; PROTEIN EXPRESSION; SMOOTH MUSCLE CONTRACTILITY; SMOOTH MUSCLE FIBER; UPREGULATION;

AMINOQUINOLINES; BIOLOGICAL MARKERS; CELL PROLIFERATION; CYTOKINES; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, INNATE; LIPOPEPTIDES; LIPOPOLYSACCHARIDES; MYOCYTES, SMOOTH MUSCLE; NOD SIGNALING ADAPTOR PROTEINS; POLY I-C; RNA, MESSENGER; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTORS; TRACHEA;

EID: 84879804905     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0068701     Document Type: Article

References (55)

1. Kumagai Y, Akira S, (2010) Identification and functions of pattern-recognition receptors. J Allergy Clin Immunol 125: 985-992.
2. Takeuchi O, Akira S, (2010) Pattern recognition receptors and inflammation. Cell 140: 805-820.
3. Bachar O, Adner M, Uddman R, Cardell LO, (2004) Toll-like receptor stimulation induces airway hyper-responsiveness to bradykinin, an effect mediated by JNK and NF-kappa B signaling pathways. Eur J Immunol 34: 1196-1207.
4. Patel M, Xu D, Kewin P, Choo-Kang B, McSharry C, et al. (2005) TLR2 agonist ameliorates established allergic airway inflammation by promoting Th1 response and not via regulatory T cells. J Immunol 174: 7558-7563.
5. Ekman AK, Adner M, Cardell LO, (2011) Toll-like receptor 7 activation reduces the contractile response of airway smooth muscle. Eur J Pharmacol 652: 145-151.
6. Kaufman EH, Fryer AD, Jacoby DB, (2011) Toll-like receptor 7 agonists are potent and rapid bronchodilators in guinea pigs. J Allergy Clin Immunol 127: 462-469.
7. Parker LC, Prince LR, Sabroe I, (2007) Translational mini-review series on Toll-like receptors: networks regulated by Toll-like receptors mediate innate and adaptive immunity. Clin Exp Immunol 147: 199-207.
8. Bowie AG, (2007) Translational mini-review series on Toll-like receptors: recent advances in understanding the role of Toll-like receptors in anti-viral immunity. Clin Exp Immunol 147: 217-226.
9. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, et al. (1999) Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162: 3749-3752.
10. Hayashi F, Smith KD, Ozinsky A, Hawn TR, Yi EC, et al. (2001) The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410: 1099-1103.
11. Akira S, Hemmi H, (2003) Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett 85: 85-95.
12. Hemmi H, Takeuchi O, Kawai T, Kaisho T, Sato S, et al. (2000) A Toll-like receptor recognizes bacterial DNA. Nature 408: 740-745.
13. Ting JP, Lovering RC, Alnemri ES, Bertin J, Boss JM, et al. (2008) The NLR gene family: a standard nomenclature. Immunity 28: 285-287.
14. Carneiro LA, Magalhaes JG, Tattoli I, Philpott DJ, Travassos LH, (2008) Nod-like proteins in inflammation and disease. J Pathol 214: 136-148.
15. Kaparakis M, Philpott DJ, Ferrero RL, (2007) Mammalian NLR proteins; discriminating foe from friend. Immunol Cell Biol 85: 495-502.
16. Chamaillard M, Hashimoto M, Horie Y, Masumoto J, Qiu S, et al. (2003) An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4: 702-707.
17. Girardin SE, Boneca IG, Carneiro LA, Antignac A, Jehanno M, et al. (2003) Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300: 1584-1587.
18. Girardin SE, Boneca IG, Viala J, Chamaillard M, Labigne A, et al. (2003) Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278: 8869-8872.
19. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, et al. (2006) 5'-Triphosphate RNA is the ligand for RIG-I. Science 314: 994-997.
20. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, et al. (2008) Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 205: 1601-1610.
21. Kawai T, Akira S, (2009) The roles of TLRs, RLRs and NLRs in pathogen recognition. Int Immunol 21: 317-337.
22. Zuyderduyn S, Sukkar MB, Fust A, Dhaliwal S, Burgess JK, (2008) Treating asthma means treating airway smooth muscle cells. Eur Respir J 32: 265-274.
23. Sukkar MB, Xie S, Khorasani NM, Kon OM, Stanbridge R, et al. (2006) Toll-like receptor 2, 3, and 4 expression and function in human airway smooth muscle. J Allergy Clin Immunol 118: 641-648.
24. Morris GE, Parker LC, Ward JR, Jones EC, Whyte MK, et al. (2006) Cooperative molecular and cellular networks regulate Toll-like receptor-dependent inflammatory responses. FASEB J 20: 2153-2155.
25. Morris GE, Whyte MK, Martin GF, Jose PJ, Dower SK, et al. (2005) Agonists of toll-like receptors 2 and 4 activate airway smooth muscle via mononuclear leukocytes. Am J Respir Crit Care Med 171: 814-822.
26. Chung KF, (2000) Airway smooth muscle cells: contributing to and regulating airway mucosal inflammation? Eur Respir J 15: 961-968.
27. Absher M, Makrides W, Shapiro P, Evans JN, (1994) Hyperoxia Inhibits Proliferation of Cultured Rat Tracheal Smooth-Muscle Cells. American Journal of Physiology 267: L101-L105.
28. Takahashi K, Asabe S, Wieland S, Garaigorta U, Gastaminza P, et al. (2010) Plasmacytoid dendritic cells sense hepatitis C virus-infected cells, produce interferon, and inhibit infection. Proceedings of the National Academy of Sciences of the United States of America 107: 7431-7436.
29. Bogefors J, Rydberg C, Uddman R, Fransson M, Mansson A, et al. (2010) Nod1, Nod2 and Nalp3 receptors, new potential targets in treatment of allergic rhinitis? Allergy 65: 1222-1226.
30. Petterson T, Jendholm J, Mansson A, Bjartell A, Riesbeck K, et al. (2011) Effects of NOD-like receptors in human B lymphocytes and crosstalk between NOD1/NOD2 and Toll-like receptors. J Leukoc Biol 89: 177-187.
31. Petterson T, Mansson A, Riesbeck K, Cardell LO, (2011) Nucleotide-binding and oligomerization domain-like receptors and retinoic acid inducible gene-like receptors in human tonsillar T lymphocytes. Immunology 133: 84-93.
32. Mansson A, Adner M, Hockerfelt U, Cardell LO, (2006) A distinct Toll-like receptor repertoire in human tonsillar B cells, directly activated by PamCSK, R-837 and CpG-2006 stimulation. Immunology 118: 539-548.
33. Mansson Kvarnhammar A, Petterson T, Cardell L, (2011) NOD-like receptors and RIG-I-like receptors in human eosinophils: Activation by NOD1 and NOD2 agonists. Immunology 134: 314-315.
34. Kuo C, Lim S, King NJ, Johnston SL, Burgess JK, et al. (2011) Rhinovirus infection induces extracellular matrix protein deposition in asthmatic and nonasthmatic airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 300: L951-957.
35. Halayko AJ, Salari H, Ma X, Stephens NL, (1996) Markers of airway smooth muscle cell phenotype. Am J Physiol 270: L1040-1051.
36. Szefler SJ, Martin RJ (2010) Lessons learned from variation in response to therapy in clinical trials. J Allergy Clin Immunol 125: 285-292; quiz 293-284.
37. Niimi K, Asano K, Shiraishi Y, Nakajima T, Wakaki M, et al. (2007) TLR3-mediated synthesis and release of eotaxin-1/CCL11 from human bronchial smooth muscle cells stimulated with double-stranded RNA. J Immunol 178: 489-495.
38. Shan X, Hu A, Veler H, Fatma S, Grunstein JS, et al. (2006) Regulation of Toll-like receptor 4-induced proasthmatic changes in airway smooth muscle function by opposing actions of ERK1/2 and p38 MAPK signaling. Am J Physiol Lung Cell Mol Physiol 291: L324-333.
39. Lee CW, Chien CS, Yang CM, (2004) Lipoteichoic acid-stimulated p42/p44 MAPK activation via Toll-like receptor 2 in tracheal smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 286: L921-930.
40. Cooper PR, Lamb R, Day ND, Branigan PJ, Kajekar R, et al. (2009) TLR3 activation stimulates cytokine secretion without altering agonist-induced human small airway contraction or relaxation. Am J Physiol Lung Cell Mol Physiol 297: L530-537.
41. Bachar O, Adner M, Cardell LO, (2006) Toll-like receptor activation in airway smooth muscle: dual actions via separate MAPK pathways. Am J Physiol Lung Cell Mol Physiol 291: L322-323.
42. Moreno L, McMaster SK, Gatheral T, Bailey LK, Harrington LS, et al. (2010) Nucleotide oligomerization domain 1 is a dominant pathway for NOS2 induction in vascular smooth muscle cells: comparison with Toll-like receptor 4 responses in macrophages. Br J Pharmacol 160: 1997-2007.
43. Cartwright N, Murch O, McMaster SK, Paul-Clark MJ, van Heel DA, et al. (2007) Selective NOD1 agonists cause shock and organ injury/dysfunction in vivo. Am J Respir Crit Care Med 175: 595-603.
44. Lee IT, Lee CW, Tung WH, Wang SW, Lin CC, et al. (2010) Cooperation of TLR2 with MyD88, PI3K, and Rac1 in lipoteichoic acid-induced cPLA2/COX-2-dependent airway inflammatory responses. Am J Pathol 176: 1671-1684.
45. Lee IT, Wang SW, Lee CW, Chang CC, Lin CC, et al. (2008) Lipoteichoic acid induces HO-1 expression via the TLR2/MyD88/c-Src/NADPH oxidase pathway and Nrf2 in human tracheal smooth muscle cells. J Immunol 181: 5098-5110.
46. Vignola AM, Chanez P, Chiappara G, Merendino A, Pace E, et al. (1997) Transforming growth factor-beta expression in mucosal biopsies in asthma and chronic bronchitis. Am J Respir Crit Care Med 156: 591-599.
47. Lee KY, Ho SC, Lin HC, Lin SM, Liu CY, et al. (2006) Neutrophil-derived elastase induces TGF-beta1 secretion in human airway smooth muscle via NF-kappaB pathway. Am J Respir Cell Mol Biol 35: 407-414.
48. Akira S, Takeda K, (2004) Toll-like receptor signalling. Nat Rev Immunol 4: 499-511.
49. Kawai T, Akira S, (2008) Toll-like receptor and RIG-I-like receptor signaling. Ann N Y Acad Sci 1143: 1-20.
50. Morishima H, Kajiwara K, Akiyama K, Yanagihara Y, (2008) Ligation of Toll-like receptor 3 differentially regulates M2 and M3 muscarinic receptor expression and function in human airway smooth muscle cells. Int Arch Allergy Immunol 145: 163-174.
51. Niimi K, Ge Q, Moir LM, Ammit AJ, Trian T, et al. (2012) beta2-Agonists upregulate PDE4 mRNA but not protein or activity in human airway smooth muscle cells from asthmatic and nonasthmatic volunteers. Am J Physiol Lung Cell Mol Physiol 302: L334-342.
52. Trian T, Burgess JK, Niimi K, Moir LM, Ge Q, et al. (2011) beta2-Agonist induced cAMP is decreased in asthmatic airway smooth muscle due to increased PDE4D. PLoS One 6: e20000.
53. Luo SF, Wang CC, Chiu CT, Chien CS, Hsiao LD, et al. (2000) Lipopolysaccharide enhances bradykinin-induced signal transduction via activation of Ras/Raf/MEK/MAPK in canine tracheal smooth muscle cells. Br J Pharmacol 130: 1799-1808.
54. Ekman AK, Adner M, Cardell LO, (2011) Toll-like receptor 7 activation reduces the contractile response of airway smooth muscle. European Journal of Pharmacology 652: 145-151.
55. Moller-Larsen S, Nyegaard M, Haagerup A, Vestbo J, Kruse TA, et al. (2008) Association analysis identifies TLR7 and TLR8 as novel risk genes in asthma and related disorders. Thorax 63: 1064-1069.