Skip to main content

Advertisement

SpringerLink
Log in

Damage-associated molecular patterns and their receptors in upper airway pathologies

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

Inflammation of the nasal (rhinitis) and sinus mucosa (sinusitis) are prevalent medical conditions of the upper airways that are concurrent in many patients; hence the terminology “rhinosinusitis”. The disease status is further defined to be “chronic” in case symptoms persist for more than 12 weeks without resolution. A diverse spectrum of external factors including viral and bacterial insults together with epithelial barrier malfunctions could be implicated in the chronicity of the inflammatory responses in chronic rhinosinusitis (CRS). However, despite massive research efforts in an attempt to unveil the pathophysiology, the exact reason for a lack of resolution still remains poorly understood. A novel set of molecules that could be implicated in sustaining the inflammatory reaction may be found within the host itself. Indeed, besides mediators of inflammation originating from outside, some endogenous intracellular and/or extracellular matrix (ECM) components from the host can be released into the extracellular space upon damage induced during the initial inflammatory reaction where they gain functions distinct from those during normal physiology. These “host-self” molecules are known to modulate inflammatory responses under pathological conditions, potentially preventing resolution and contributing to the development of chronic inflammation. These molecules are collectively classified as damage-associated molecular patterns (DAMPs). This review summarizes the current knowledge regarding DAMPs in upper airway pathologies, also covering those that were previously investigated for their intracellular and/or ECM functions often acting as an antimicrobial agent or implicated in tissue/cell homeostasis, and for which their function as a danger signaling molecule was not assessed. It is, however, of importance to assess these molecules again from a point of view as a DAMP in order to further unravel the pathogenesis of CRS.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81(1):1–5

    PubMed  CAS  Google Scholar 

  2. Lotze MT, Zeh HJ, Rubartelli A, Sparvero LJ, Amoscato AA et al (2007) The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity. Immunol Rev 220:60–81

    PubMed  CAS  Google Scholar 

  3. Oppenheim JJ, Yang D (2005) Alarmins: chemotactic activators of immune responses. Curr Opin Immunol 17(4):359–365

    PubMed  CAS  Google Scholar 

  4. Piccinini AM, Midwood KS (2010) DAMPening inflammation by modulating TLR signalling. Article ID 672395. doi:10.1155/2010/672395

  5. Rubartelli A, Lotze MT (2007) Inside, outside, upside down: damage-associated molecular-pattern molecules (DAMPs) and redox. Trends Immunol 28(10):429–436

    PubMed  CAS  Google Scholar 

  6. Vlassara H (2001) The AGE-receptor in the pathogenesis of diabetic complications. Diabetes Metab Res Rev 17(6):436–443

    PubMed  CAS  Google Scholar 

  7. Fioravanti J, Medina-Echeverz J, Berraondo P (2011) Scavenger receptor class B, type I: a promising immunotherapy target. Immunotherapy 3(3):395–406

    PubMed  CAS  Google Scholar 

  8. Jacob F, Novo CP, Bachert C, Van CK (2013) Purinergic signaling in inflammatory cells: P2 receptor expression, functional effects, and modulation of inflammatory responses. Purinergic Signal. doi:10.1007/s11302-013-9357-4

    PubMed  Google Scholar 

  9. Bachert C, Zhang N, Holtappels G, De Lobel L, Van Cauwenberge P et al (2010) Presence of IL-5 protein and IgE antibodies to staphylococcal enterotoxins in nasal polyps is associated with comorbid asthma. J Allergy Clin Immunol 126(5):962–968

    PubMed  CAS  Google Scholar 

  10. Van Crombruggen K, Van Bruaene N, Holtappels G, Bachert C (2010) Chronic sinusitis and rhinitis: clinical terminology chronic rhinosinusitis further supported. Rhinology 48(1):54–58

    PubMed  Google Scholar 

  11. Bachert C, Wagenmann M, Hauser U, Rudack C (1997) IL-5 synthesis is upregulated in human nasal polyp tissue. J Allergy Clin Immunol 99(6 Pt 1):837–842

    PubMed  CAS  Google Scholar 

  12. Van Zele T, Claeys S, Gevaert P, Van MG, Holtappels G et al (2006) Differentiation of chronic sinus diseases by measurement of inflammatory mediators. Allergy 61(11):1280–1289

    PubMed  Google Scholar 

  13. Van Bruaene N, Perez-Novo CA, Basinski TM, Van ZT, Holtappels G et al (2008) T-cell regulation in chronic paranasal sinus disease. J Allergy Clin Immunol 121(6):1435–1441

    PubMed  Google Scholar 

  14. Van Bruaene N, Derycke L, Perez-Novo CA, Gevaert P, Holtappels G et al (2009) TGF-beta signaling and collagen deposition in chronic rhinosinusitis. J Allergy Clin Immunol 124(2):253–259

    PubMed  Google Scholar 

  15. Van Bruaene N, Bachert C (2011) Tissue remodeling in chronic rhinosinusitis. Curr Opin Allergy Clin Immunol 11(1):8–11

    PubMed  Google Scholar 

  16. Li X, Meng J, Qiao X, Liu Y, Liu F et al (2010) Expression of TGF, matrix metalloproteinases, and tissue inhibitors in Chinese chronic rhinosinusitis. J Allergy Clin Immunol 125(5):1061–1068

    PubMed  CAS  Google Scholar 

  17. Van Zele T, Gevaert P, Watelet JB, Claeys G, Holtappels G et al (2004) Staphylococcus aureus colonization and IgE antibody formation to enterotoxins is increased in nasal polyposis. J Allergy Clin Immunol 114(4):981–983

    PubMed  Google Scholar 

  18. Patou J, Gevaert P, Van Zele T, Holtappels G, van Cauwenberge P et al (2008) Staphylococcus aureus enterotoxin B, protein A, and lipoteichoic acid stimulations in nasal polyps. J Allergy Clin Immunol 121(1):110–115

    PubMed  CAS  Google Scholar 

  19. Takeuchi O, Akira S (2010) Pattern recognition receptors and inflammation. Cell 140(6):805–820

    PubMed  CAS  Google Scholar 

  20. Bierhaus A, Humpert PM, Morcos M, Wendt T, Chavakis T et al (2005) Understanding RAGE, the receptor for advanced glycation end products. J Mol Med 83(11):876–886

    PubMed  CAS  Google Scholar 

  21. Fritz G (2011) RAGE: a single receptor fits multiple ligands. Trends Biochem Sci 36(12):625–632

    PubMed  CAS  Google Scholar 

  22. Van Crombruggen K, Holtappels G, De Ruyck N, Derycke L, Tomassen P et al (2012) RAGE processing in chronic airway conditions: involvement of Staphylococcus aureus and ECP. J Allergy Clin Immunol 129(6):1515–1521

    PubMed  Google Scholar 

  23. Bopp C, Bierhaus A, Hofer S, Bouchon A, Nawroth PP et al (2008) Bench-to-bedside review: the inflammation-perpetuating pattern-recognition receptor RAGE as a therapeutic target in sepsis. Crit Care 12(1):201

    PubMed  Google Scholar 

  24. Raucci A, Cugusi S, Antonelli A, Barabino SM, Monti L et al (2008) A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J 22(10):3716–3727

    PubMed  CAS  Google Scholar 

  25. Hudson BI, Carter AM, Harja E, Kalea AZ, Arriero M et al (2008) Identification, classification, and expression of RAGE gene splice variants. FASEB J 22(5):1572–1580

    PubMed  CAS  Google Scholar 

  26. Zhang L, Bukulin M, Kojro E, Roth A, Metz VV et al (2008) Receptor for advanced glycation end products is subjected to protein ectodomain shedding by metalloproteinases. J Biol Chem 283(51):35507–35516

    PubMed  CAS  Google Scholar 

  27. Yamakawa N, Uchida T, Matthay MA, Makita K (2011) Proteolytic release of the receptor for advanced glycation end products from in vitro and in situ alveolar epithelial cells. Am J Physiol Lung Cell Mol Physiol 300(4):L516–L525

    PubMed  CAS  Google Scholar 

  28. Wang Y, Wang H, Piper MG, McMaken S, Mo X et al (2010) sRAGE induces human monocyte survival and differentiation. J Immunol 185(3):1822–1835

    PubMed  CAS  Google Scholar 

  29. Pullerits R, Brisslert M, Jonsson IM, Tarkowski A (2006) Soluble receptor for advanced glycation end products triggers a proinflammatory cytokine cascade via beta2 integrin Mac-1. Arthritis Rheum 54(12):3898–3907

    PubMed  CAS  Google Scholar 

  30. Englert JM, Hanford LE, Kaminski N, Tobolewski JM, Tan RJ et al (2008) A role for the receptor for advanced glycation end products in idiopathic pulmonary fibrosis. Am J Pathol 172(3):583–591

    PubMed  CAS  Google Scholar 

  31. Brett J, Schmidt AM, Yan SD, Zou YS, Weidman E et al (1993) Survey of the distribution of a newly characterized receptor for advanced glycation end products in tissues. Am J Pathol 143(6):1699–1712

    PubMed  CAS  Google Scholar 

  32. Demling N, Ehrhardt C, Kasper M, Laue M, Knels L et al (2006) Promotion of cell adherence and spreading: a novel function of RAGE, the highly selective differentiation marker of human alveolar epithelial type I cells. Cell Tissue Res 323(3):475–488

    PubMed  CAS  Google Scholar 

  33. He M, Kubo H, Ishizawa K, Hegab AE, Yamamoto Y et al (2007) The role of the receptor for advanced glycation end-products in lung fibrosis. Am J Physiol Lung Cell Mol Physiol 293(6):L1427–L1436

    PubMed  CAS  Google Scholar 

  34. Watelet JB, Bachert C, Claeys C, Van Cauwenberge P (2004) Matrix metalloproteinases MMP-7, MMP-9 and their tissue inhibitor TIMP-1: expression in chronic sinusitis vs. nasal polyposis. Allergy 59(1):54–60

    PubMed  CAS  Google Scholar 

  35. Queisser MA, Kouri FM, Konigshoff M, Wygrecka M, Schubert U et al (2008) Loss of RAGE in pulmonary fibrosis: molecular relations to functional changes in pulmonary cell types. Am J Respir Cell Mol Biol 39(3):337–345

    PubMed  CAS  Google Scholar 

  36. Hanford LE, Enghild JJ, Valnickova Z, Petersen SV, Schaefer LM et al (2004) Purification and characterization of mouse soluble receptor for advanced glycation end products (sRAGE). J Biol Chem 279(48):50019–50024

    PubMed  CAS  Google Scholar 

  37. Chen Y, Akirav EM, Chen W, Henegariu O, Moser B et al (2008) RAGE ligation affects T cell activation and controls T cell differentiation. J Immunol 181(6):4272–4278

    PubMed  CAS  Google Scholar 

  38. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11(5):373–384

    PubMed  CAS  Google Scholar 

  39. Guan Y, Ranoa DR, Jiang S, Mutha SK, Li X et al (2010) Human TLRs 10 and 1 share common mechanisms of innate immune sensing but not signaling. J Immunol 184(9):5094–5103

    PubMed  CAS  Google Scholar 

  40. Lane AP, Truong-Tran QA, Schleimer RP (2006) Altered expression of genes associated with innate immunity and inflammation in recalcitrant rhinosinusitis with polyps. Am J Rhinol 20(2):138–144

    PubMed  Google Scholar 

  41. McCurdy JD, Olynych TJ, Maher LH, Marshall JS (2003) Cutting edge: distinct Toll-like receptor 2 activators selectively induce different classes of mediator production from human mast cells. J Immunol 170(4):1625–1629

    PubMed  CAS  Google Scholar 

  42. Claeys S, De Belder T, Holtappels G, Gevaert P, Verhasselt B et al (2003) Human beta-defensins and Toll-like receptors in the upper airway. Allergy 58(8):748–753

    PubMed  CAS  Google Scholar 

  43. Pitzurra L, Bellocchio S, Nocentini A, Bonifazi P, Scardazza R et al (2004) Antifungal immune reactivity in nasal polyposis. Infect Immun 72(12):7275–7281

    PubMed  CAS  Google Scholar 

  44. Ramanathan M Jr, Lee WK, Dubin MG, Lin S, Spannhake EW et al (2007) Sinonasal epithelial cell expression of Toll-like receptor 9 is decreased in chronic rhinosinusitis with polyps. Am J Rhinol 21(1):110–116

    PubMed  Google Scholar 

  45. Nonaka M, Ogihara N, Fukumoto A, Sakanushi A, Pawankar R et al (2008) Toll-like receptor 2, 3, 4, 5 ligands and interleukin-4 synergistically induce TARC production in nasal polyp fibroblasts. Auris Nasus Larynx 35(4):515–520

    PubMed  Google Scholar 

  46. Takahashi N, Yamada T, Narita N, Fujieda S (2006) Double-stranded RNA induces production of RANTES and IL-8 by human nasal fibroblasts. Clin Immunol 118(1):51–58

    PubMed  CAS  Google Scholar 

  47. Vandermeer J, Sha Q, Lane AP, Schleimer RP (2004) Innate immunity of the sinonasal cavity: expression of messenger RNA for complement cascade components and Toll-like receptors. Arch Otolaryngol Head Neck Surg 130(12):1374–1380

    PubMed  Google Scholar 

  48. Tieu DD, Peters AT, Carter RG, Suh L, Conley DB et al (2010) Evidence for diminished levels of epithelial psoriasin and calprotectin in chronic rhinosinusitis. J Allergy Clin Immunol 125(3):667–675

    PubMed  CAS  Google Scholar 

  49. Richer SL, Truong-Tran AQ, Conley DB, Carter R, Vermylen D et al (2008) Epithelial genes in chronic rhinosinusitis with and without nasal polyps. Am J Rhinol 22(3):228–234

    PubMed  Google Scholar 

  50. Glaser R, Harder J, Lange H, Bartels J, Christophers E et al (2005) Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 6(1):57–64

    PubMed  Google Scholar 

  51. Meyer JE, Harder J, Sipos B, Maune S, Kloppel G et al (2008) Psoriasin (S100A7) is a principal antimicrobial peptide of the human tongue. Mucosal Immunol 1(3):239–243

    PubMed  CAS  Google Scholar 

  52. Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C et al (2007) Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 13(9):1042–1049

    PubMed  CAS  Google Scholar 

  53. Loser K, Vogl T, Voskort M, Lueken A, Kupas V et al (2010) The Toll-like receptor 4 ligands Mrp8 and Mrp14 are crucial in the development of autoreactive CD8+ T cells. Nat Med 16(6):713–717

    PubMed  CAS  Google Scholar 

  54. Sparvero LJ, Safu-Adjei D, Kang R, Tang D, Amin N et al (2009) RAGE (receptor for advanced glycation end-products), RAGE ligands, and their role in cancer and inflammation. J Transl Med 7:17

    PubMed  Google Scholar 

  55. Bryborn M, Adner M, Cardell LO (2005) Psoriasin, one of several new proteins identified in nasal lavage fluid from allergic and non-allergic individuals using 2-dimensional gel electrophoresis and mass spectrometry. Respir Res 6:118

    PubMed  Google Scholar 

  56. Kishore U, Greenhough TJ, Waters P, Shrive AK, Ghai R et al (2006) Surfactant proteins SP-A and SP-D: structure, function and receptors. Mol Immunol 43(9):1293–1315

    PubMed  CAS  Google Scholar 

  57. Nayak A, Dodagatta-Marri E, Tsolaki AG, Kishore U (2012) An insight into the diverse roles of surfactant proteins, SP-A and SP-D in innate and adaptive immunity. Front Immunol 3:131

    PubMed  Google Scholar 

  58. Guillot L, Balloy V, McCormack FX, Golenbock DT, Chignard M et al (2002) Cutting edge: the immunostimulatory activity of the lung surfactant protein-A involves Toll-like receptor 4. J Immunol 168(12):5989–5992

    PubMed  CAS  Google Scholar 

  59. Henning LN, Azad AK, Parsa KV, Crowther JE, Tridandapani S et al (2008) Pulmonary surfactant protein A regulates TLR expression and activity in human macrophages. J Immunol 180(12):7847–7858

    PubMed  CAS  Google Scholar 

  60. Murakami S, Iwaki D, Mitsuzawa H, Sano H, Takahashi H et al (2002) Surfactant protein A inhibits peptidoglycan-induced tumor necrosis factor-alpha secretion in U937 cells and alveolar macrophages by direct interaction with Toll-like receptor 2. J Biol Chem 277(9):6830–6837

    PubMed  CAS  Google Scholar 

  61. Ohya M, Nishitani C, Sano H, Yamada C, Mitsuzawa H et al (2006) Human pulmonary surfactant protein D binds the extracellular domains of Toll-like receptors 2 and 4 through the carbohydrate recognition domain by a mechanism different from its binding to phosphatidylinositol and lipopolysaccharide. Biochemistry 45(28):8657–8664

    PubMed  CAS  Google Scholar 

  62. Yamada C, Sano H, Shimizu T, Mitsuzawa H, Nishitani C et al (2006) Surfactant protein A directly interacts with TLR4 and MD-2 and regulates inflammatory cellular response. Importance of supratrimeric oligomerization. J Biol Chem 281(31):21771–21780

    PubMed  CAS  Google Scholar 

  63. Lee HM, Kang HJ, Woo JS, Chae SW, Lee SH et al (2006) Upregulation of surfactant protein A in chronic rhinosinusitis. Laryngoscope 116(2):328–330

    PubMed  CAS  Google Scholar 

  64. Wang X, Zhao C, Liu M (2010) Expression and significance of surfactant A in nasal polyps of chronic rhinosinusitis. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi 24(14):652–654

    PubMed  Google Scholar 

  65. Woodworth BA, Wood R, Baatz JE, Schlosser RJ (2007) Sinonasal surfactant protein A1, A2, and D gene expression in cystic fibrosis: a preliminary report. Otolaryngol Head Neck Surg 137(1):34–38

    PubMed  Google Scholar 

  66. Skinner ML, Schlosser RJ, Lathers D, Neal JG, Woodworth BA et al (2007) Innate and adaptive mediators in cystic fibrosis and allergic fungal rhinosinusitis. Am J Rhinol 21(5):538–541

    PubMed  Google Scholar 

  67. Ooi EH, Wormald PJ, Carney AS, James CL, Tan LW (2007) Surfactant protein d expression in chronic rhinosinusitis patients and immune responses in vitro to Aspergillus and Alternaria in a nasal explant model. Laryngoscope 117(1):51–57

    PubMed  CAS  Google Scholar 

  68. Chong KT, Thangavel RR, Tang X (2008) Enhanced expression of murine beta-defensins (MBD-1, -2, -3, and -4) in upper and lower airway mucosa of influenza virus-infected mice. Virology 380(1):136–143

    PubMed  CAS  Google Scholar 

  69. Rosenberg HF (2008) Eosinophil-derived neurotoxin/RNase 2: connecting the past, the present and the future. Curr Pharm Biotechnol 9(3):135–140

    PubMed  CAS  Google Scholar 

  70. Yang D, Chen Q, Su SB, Zhang P, Kurosaka K et al (2008) Eosinophil-derived neurotoxin acts as an alarmin to activate the TLR2-MyD88 signal pathway in dendritic cells and enhances Th2 immune responses. J Exp Med 205(1):79–90

    PubMed  CAS  Google Scholar 

  71. Kalfa VC, Spector SL, Ganz T, Cole AM (2004) Lysozyme levels in the nasal secretions of patients with perennial allergic rhinitis and recurrent sinusitis. Ann Allergy Asthma Immunol 93(3):288–292

    PubMed  CAS  Google Scholar 

  72. Bascom R, Pipkorn U, Proud D, Dunnette S, Gleich GJ et al (1989) Major basic protein and eosinophil-derived neurotoxin concentrations in nasal-lavage fluid after antigen challenge: effect of systemic corticosteroids and relationship to eosinophil influx. J Allergy Clin Immunol 84(3):338–346

    PubMed  CAS  Google Scholar 

  73. Alvarado-Valdes CA, Blomgren J, Weiler D, Gleich GJ, Reed CE et al (1997) The effect of fluticasone propionate aqueous nasal spray on eosinophils and cytokines in nasal secretions of patients with ragweed allergic rhinitis. Clin Ther 19(2):273–281

    PubMed  CAS  Google Scholar 

  74. Van Crombruggen K, Zhang N, Gevaert P, Tomassen P, Bachert C (2011) Pathogenesis of chronic rhinosinusitis: inflammation. J Allergy Clin Immunol 128(4):728–732

    PubMed  Google Scholar 

  75. Singh P, Carraher C, Schwarzbauer JE (2010) Assembly of fibronectin extracellular matrix. Annu Rev Cell Dev Biol 26397–419

  76. White ES, Baralle FE, Muro AF (2008) New insights into form and function of fibronectin splice variants. J Pathol 216(1):1–14

    PubMed  CAS  Google Scholar 

  77. Okamura Y, Watari M, Jerud ES, Young DW, Ishizaka ST et al (2001) The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem 276(13):10229–10233

    PubMed  CAS  Google Scholar 

  78. Bilodeau L, Boulay ME, Prince P, Boisvert P, Boulet LP (2010) Comparative clinical and airway inflammatory features of asthmatics with or without polyps. Rhinology 48(4):420–425

    PubMed  Google Scholar 

  79. Nakagawa T, Yamane H, Shigeta T, Takashima T, Nakai Y (1999) Interaction between fibronectin and eosinophils in the growth of nasal polyps. Laryngoscope 109(4):557–561

    PubMed  CAS  Google Scholar 

  80. Menzies BE (2003) The role of fibronectin binding proteins in the pathogenesis of Staphylococcus aureus infections. Curr Opin Infect Dis 16(3):225–229

    PubMed  CAS  Google Scholar 

  81. Henderson B, Nair S, Pallas J, Williams MA (2011) Fibronectin: a multidomain host adhesin targeted by bacterial fibronectin-binding proteins. FEMS Microbiol Rev 35(1):147–200

    PubMed  CAS  Google Scholar 

  82. Dhirapong A, Lleo A, Leung P, Gershwin ME, Liu FT (2009) The immunological potential of galectin-1 and -3. Autoimmun Rev 8(5):360–363

    PubMed  CAS  Google Scholar 

  83. Vasta GR (2009) Roles of galectins in infection. Nat Rev Microbiol 7(6):424–438

    PubMed  CAS  Google Scholar 

  84. Jouault T, El Abed-El BM, Martinez-Esparza M, Breuilh L, Trinel PA et al (2006) Specific recognition of Candida albicans by macrophages requires galectin-3 to discriminate Saccharomyces cerevisiae and needs association with TLR2 for signaling. J Immunol 177(7):4679–4687

    PubMed  CAS  Google Scholar 

  85. Vlassara H, Li YM, Imani F, Wojciechowicz D, Yang Z et al (1995) Identification of galectin-3 as a high-affinity binding protein for advanced glycation end products (AGE): a new member of the AGE-receptor complex. Mol Med 1(6):634–646

    PubMed  CAS  Google Scholar 

  86. Iacobini C, Menini S, Oddi G, Ricci C, Amadio L et al (2004) Galectin-3/AGE-receptor 3 knockout mice show accelerated AGE-induced glomerular injury: evidence for a protective role of galectin-3 as an AGE receptor. FASEB J 18(14):1773–1775

    PubMed  CAS  Google Scholar 

  87. Fernandes AM, Babeto E, Rahal P, Provazzi PJ, Hidalgo CA et al (2010) Expression of genes that encode the annexin-1 and galectin-1 proteins in nasal polyposis and their modulation by glucocorticoid. Br J Otorhinolaryngol 76(2):213–218

    Google Scholar 

  88. Delbrouck C, Gabius HJ, Kaltner H, Decaestecker C, Kiss R et al (2003) Expression patterns of galectin-1 and galectin-3 in nasal polyps and middle and inferior turbinates in relation to growth regulation and immunosuppression. Arch Otolaryngol Head Neck Surg 129(6):665–669

    PubMed  Google Scholar 

  89. Han JL, Ding RY, Zhao L, Ren Z, Jiang XJ (2008) Rosiglitazone attenuates allergic inflammation and inhibits expression of galectin-3 in a mouse model of allergic rhinitis. J Int Med Res 36(4):830–836

    PubMed  CAS  Google Scholar 

  90. Negrete-Garcia MC, Jimenez-Torres CY, Alvarado-Vasquez N, Montes-Vizuet AR, Velazquez-Rodriguez JR et al (2012) Galectin-10 is released in the nasal lavage fluid of patients with aspirin-sensitive respiratory disease. Sci World J 2012. Article ID 474020. doi:10.1100/2012/474020

  91. Chiquet-Ehrismann R, Chiquet M (2003) Tenascins: regulation and putative functions during pathological stress. J Pathol 200(4):488–499

    PubMed  CAS  Google Scholar 

  92. Midwood KS, Orend G (2009) The role of tenascin-C in tissue injury and tumorigenesis. J Cell Commun Signal 3(3–4):287–310

    PubMed  Google Scholar 

  93. Chiquet-Ehrismann R, Tucker RP (2011) Tenascins and the importance of adhesion modulation. Cold Spring Harb Perspect Biol 3 (5). doi:10.1101/cshperspecta004960

  94. Midwood K, Sacre S, Piccinini AM, Inglis J, Trebaul A et al (2009) Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Nat Med 15(7):774–780

    PubMed  CAS  Google Scholar 

  95. Liu R, He Y, Li B, Liu J, Ren Y et al (2012) Tenascin-C produced by oxidized LDL-stimulated macrophages increases foam cell formation through Toll-like receptor-4. Mol Cells 34(1):35–41

    PubMed  Google Scholar 

  96. Goh FG, Piccinini AM, Krausgruber T, Udalova IA, Midwood KS (2010) Transcriptional regulation of the endogenous danger signal tenascin-C: a novel autocrine loop in inflammation. J Immunol 184(5):2655–2662

    PubMed  CAS  Google Scholar 

  97. Liu Z, Lu X, Wang H, Gao Q, Cui Y (2006) The up-regulated expression of tenascin C in human nasal polyp tissues is related to eosinophil-derived transforming growth factor beta1. Am J Rhinol 20(6):629–633

    PubMed  Google Scholar 

  98. Payne SC, Han JK, Huyett P, Negri J, Kropf EZ et al (2008) Microarray analysis of distinct gene transcription profiles in non-eosinophilic chronic sinusitis with nasal polyps. Am J Rhinol 22(6):568–581

    PubMed  Google Scholar 

  99. Tucker RP, Chiquet-Ehrismann R (2009) The regulation of tenascin expression by tissue microenvironments. Biochim Biophys Acta 1793(5):888–892

    PubMed  CAS  Google Scholar 

  100. Rettig WJ, Erickson HP, Albino AP, Garin-Chesa P (1994) Induction of human tenascin (neuronectin) by growth factors and cytokines: cell type-specific signals and signalling pathways. J Cell Sci 107(Pt 2):487–497

    PubMed  CAS  Google Scholar 

  101. Silvestri M, Sabatini F, Scarso L, Cordone A, Dasic G et al (2002) Fluticasone propionate downregulates nasal fibroblast functions involved in airway inflammation and remodeling. Int Arch Allergy Immunol 128(1):51–58

    PubMed  CAS  Google Scholar 

  102. Powers MR, Qu Z, LaGesse PC, Liebler JM, Wall MA et al (1998) Expression of basic fibroblast growth factor in nasal polyps. Ann Otol Rhinol Laryngol 107(10 Pt 1):891–897

    PubMed  CAS  Google Scholar 

  103. Norlander T, Westermark A, van Setten G, Valtonen H, Ishizaki H et al (2001) Basic fibroblast growth factor in nasal polyps immunohistochemical and quantitative findings. Rhinology 39(2):88–92

    PubMed  CAS  Google Scholar 

  104. Kim HJ, Jung HH, Lee SH (2006) Expression of acidic fibroblast growth factor and basic fibroblast growth factor in nasal polyps. Acta Otolaryngol 126(6):600–605

    PubMed  CAS  Google Scholar 

  105. Paallysaho T, Tervo K, Kivela T, Virtanen I, Tarkkanen A et al (1993) Cellular fibronectin and tenascin in an orbital nylon prosthesis removed because of infection caused by Staphylococcus aureus. Graefes Arch Clin Exp Ophthalmol 231(2):61–65

    PubMed  CAS  Google Scholar 

  106. Doss M, White MR, Tecle T, Hartshorn KL (2010) Human defensins and LL-37 in mucosal immunity. J Leukoc Biol 87(1):79–92

    PubMed  CAS  Google Scholar 

  107. Lai Y, Gallo RL (2009) AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol 30(3):131–141

    PubMed  CAS  Google Scholar 

  108. Pazgier M, Hoover DM, Yang D, Lu W, Lubkowski J (2006) Human beta-defensins. Cell Mol Life Sci 63(11):1294–1313

    PubMed  CAS  Google Scholar 

  109. Biragyn A, Ruffini PA, Leifer CA, Klyushnenkova E, Shakhov A et al (2002) Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 298(5595):1025–1029

    PubMed  CAS  Google Scholar 

  110. Funderburg N, Lederman MM, Feng Z, Drage MG, Jadlowsky J et al (2007) Human-defensin-3 activates professional antigen-presenting cells via Toll-like receptors 1 and 2. Proc Natl Acad Sci USA 104(47):18631–18635

    PubMed  CAS  Google Scholar 

  111. Yamin M, Holbrook EH, Gray ST, Harold R, Busaba N et al (2008) Cigarette smoke combined with Toll-like receptor 3 signaling triggers exaggerated epithelial regulated upon activation, normal T-cell expressed and secreted/CCL5 expression in chronic rhinosinusitis. J Allergy Clin Immunol 122(6):1145–1153

    PubMed  CAS  Google Scholar 

  112. Ramanathan M Jr, Lee WK, Spannhake EW, Lane AP (2008) Th2 cytokines associated with chronic rhinosinusitis with polyps down-regulate the antimicrobial immune function of human sinonasal epithelial cells. Am J Rhinol 22(2):115–121

    PubMed  Google Scholar 

  113. Ong PY, Ohtake T, Brandt C, Strickland I, Boguniewicz M et al (2002) Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 347(15):1151–1160

    PubMed  CAS  Google Scholar 

  114. Bachert C, Gevaert P, Howarth P, Holtappels G, van Cauwenberge P et al (2003) IgE to Staphylococcus aureus enterotoxins in serum is related to severity of asthma. J Allergy Clin Immunol 111(5):1131–1132

    PubMed  Google Scholar 

  115. Bachert C, Zhang N, Van ZT, Gevaert P, Patou J et al (2007) Staphylococcus aureus enterotoxins as immune stimulants in chronic rhinosinusitis. Clin Allergy Immunol 20:163–175

    PubMed  CAS  Google Scholar 

  116. Claeys S, Van HH, Holtappels G, Gevaert P, De BT et al (2005) Nasal polyps in patients with and without cystic fibrosis: a differentiation by innate markers and inflammatory mediators. Clin Exp Allergy 35(4):467–472

    PubMed  CAS  Google Scholar 

  117. Melvin TA, Lane AP, Nguyen MT, Lin SY (2013) Sinonasal epithelial cell expression of Toll-like receptor 9 is elevated in cystic fibrosis-associated chronic rhinosinusitis. Am J Rhinol Allergy 27(1):30–33

    PubMed  Google Scholar 

  118. Dubyak GR (2012) P2X7 receptor regulation of non-classical secretion from immune effector cells. Cell Microbiol 14(11):1697–1706

    PubMed  CAS  Google Scholar 

  119. Ghavami S, Rashedi I, Dattilo BM, Eshraghi M, Chazin WJ et al (2008) S100A8/A9 at low concentration promotes tumor cell growth via RAGE ligation and MAP kinase-dependent pathway. J Leukoc Biol 83(6):1484–1492

    PubMed  CAS  Google Scholar 

  120. Boyd JH, Kan B, Roberts H, Wang Y, Walley KR (2008) S100A8 and S100A9 mediate endotoxin-induced cardiomyocyte dysfunction via the receptor for advanced glycation end products. Circ Res 102(10):1239–1246

    PubMed  CAS  Google Scholar 

  121. Kerkhoff C, Sorg C, Tandon NN, Nacken W (2001) Interaction of S100A8/S100A9-arachidonic acid complexes with the scavenger receptor CD36 may facilitate fatty acid uptake by endothelial cells. Biochemistry 40(1):241–248

    PubMed  CAS  Google Scholar 

  122. Leclerc E, Fritz G, Vetter SW, Heizmann CW (2009) Binding of S100 proteins to RAGE: an update. Biochim Biophys Acta 1793(6):993–1007

    PubMed  CAS  Google Scholar 

  123. Park JS, Svetkauskaite D, He Q, Kim JY, Strassheim D et al (2004) Involvement of Toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J Biol Chem 279(9):7370–7377

    PubMed  CAS  Google Scholar 

  124. Tian J, Avalos AM, Mao SY, Chen B, Senthil K et al (2007) Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat Immunol 8(5):487–496

    PubMed  CAS  Google Scholar 

  125. Ivanov S, Dragoi AM, Wang X, Dallacosta C, Louten J et al (2007) A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 110(6):1970–1981

    PubMed  CAS  Google Scholar 

  126. Hori O, Brett J, Slattery T, Cao R, Zhang J et al (1995) The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and co-expression of rage and amphoterin in the developing nervous system. J Biol Chem 270(43):25752–25761

    PubMed  CAS  Google Scholar 

  127. Taguchi A, Blood DC, del Toro G, Canet A, Lee DC et al (2000) Blockade of RAGE-amphoterin signalling suppresses tumour growth and metastases. Nature 405(6784):354–360

    PubMed  CAS  Google Scholar 

  128. Vabulas RM, Ahmad-Nejad P, Da CC, Miethke T, Kirschning CJ et al (2001) Endocytosed HSP60s use Toll-like receptor 2 (TLR2) and TLR4 to activate the Toll/interleukin-1 receptor signaling pathway in innate immune cells. J Biol Chem 276(33):31332–31339

    PubMed  CAS  Google Scholar 

  129. Vabulas RM, Braedel S, Hilf N, Singh-Jasuja H, Herter S et al (2002) The endoplasmic reticulum-resident heat shock protein Gp96 activates dendritic cells via the Toll-like receptor 2/4 pathway. J Biol Chem 277(23):20847–20853

    PubMed  CAS  Google Scholar 

  130. Asea A, Rehli M, Kabingu E, Boch JA, Bare O et al (2002) Novel signal transduction pathway utilized by extracellular HSP70: role of Toll-like receptor (TLR) 2 and TLR4. J Biol Chem 277(17):15028–15034

    PubMed  CAS  Google Scholar 

  131. Zanin-Zhorov A, Nussbaum G, Franitza S, Cohen IR, Lider O (2003) T cells respond to heat shock protein 60 via TLR2: activation of adhesion and inhibition of chemokine receptors. FASEB J 17(11):1567–1569

    PubMed  CAS  Google Scholar 

  132. Ohashi K, Burkart V, Flohe S, Kolb H (2000) Cutting edge: heat shock protein 60 is a putative endogenous ligand of the Toll-like receptor-4 complex. J Immunol 164(2):558–561

    PubMed  CAS  Google Scholar 

  133. Roelofs MF, Boelens WC, Joosten LA, Abdollahi-Roodsaz S, Geurts J et al (2006) Identification of small heat shock protein B8 (HSP22) as a novel TLR4 ligand and potential involvement in the pathogenesis of rheumatoid arthritis. J Immunol 176(11):7021–7027

    PubMed  CAS  Google Scholar 

  134. Kislinger T, Fu C, Huber B, Qu W, Taguchi A et al (1999) N(epsilon)-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J Biol Chem 274(44):31740–31749

    PubMed  CAS  Google Scholar 

  135. Ohgami N, Nagai R, Ikemoto M, Arai H, Miyazaki A et al (2002) CD36, serves as a receptor for advanced glycation endproducts (AGE). J Diabetes Complications 16(1):56–59

    PubMed  Google Scholar 

  136. Smiley ST, King JA, Hancock WW (2001) Fibrinogen stimulates macrophage chemokine secretion through Toll-like receptor 4. J Immunol 167(5):2887–2894

    PubMed  CAS  Google Scholar 

  137. Barrera V, Skorokhod OA, Baci D, Gremo G, Arese P et al (2011) Host fibrinogen stably bound to hemozoin rapidly activates monocytes via TLR-4 and CD11b/CD18-integrin: a new paradigm of hemozoin action. Blood 117(21):5674–5682

    PubMed  CAS  Google Scholar 

  138. Yan SD, Chen X, Fu J, Chen M, Zhu H et al (1996) RAGE and amyloid-beta peptide neurotoxicity in Alzheimer’s disease. Nature 382(6593):685–691

    PubMed  CAS  Google Scholar 

  139. Swisher JF, Burton N, Bacot SM, Vogel SN, Feldman GM (2010) Annexin A2 tetramer activates human and murine macrophages through TLR4. Blood 115(3):549–558

    PubMed  CAS  Google Scholar 

  140. Bozza S, Gaziano R, Bonifazi P, Zelante T, Pitzurra L et al (2007) Thymosin alpha1 activates the TLR9/MyD88/IRF7-dependent murine cytomegalovirus sensing for induction of anti-viral responses in vivo. Int Immunol 19(11):1261–1270

    PubMed  CAS  Google Scholar 

  141. Romani L, Bistoni F, Gaziano R, Bozza S, Montagnoli C et al (2004) Thymosin alpha 1 activates dendritic cells for antifungal Th1 resistance through Toll-like receptor signaling. Blood 103(11):4232–4239

    PubMed  CAS  Google Scholar 

  142. Satta N, Kruithof EK, Fickentscher C, Dunoyer-Geindre S, Boehlen F et al (2011) Toll-like receptor 2 mediates the activation of human monocytes and endothelial cells by antiphospholipid antibodies. Blood 117(20):5523–5531

    PubMed  CAS  Google Scholar 

  143. Mulla MJ, Brosens JJ, Chamley LW, Giles I, Pericleous C et al (2009) Antiphospholipid antibodies induce a pro-inflammatory response in first trimester trophoblast via the TLR4/MyD88 pathway. Am J Reprod Immunol 62(2):96–111

    PubMed  CAS  Google Scholar 

  144. Prinz N, Clemens N, Strand D, Putz I, Lorenz M et al (2011) Antiphospholipid antibodies induce translocation of TLR7 and TLR8 to the endosome in human monocytes and plasmacytoid dendritic cells. Blood 118(8):2322–2332

    PubMed  CAS  Google Scholar 

  145. Devaney JM, Greene CM, Taggart CC, Carroll TP, O’Neill SJ et al (2003) Neutrophil elastase up-regulates interleukin-8 via Toll-like receptor 4. FEBS Lett 544(1–3):129–132

    PubMed  CAS  Google Scholar 

  146. Ando K, Hasegawa K, Shindo K, Furusawa T, Fujino T et al (2010) Human lactoferrin activates NF-kappaB through the Toll-like receptor 4 pathway while it interferes with the lipopolysaccharide-stimulated TLR4 signaling. FEBS J 277(9):2051–2066

    PubMed  CAS  Google Scholar 

  147. He RL, Zhou J, Hanson CZ, Chen J, Cheng N et al (2009) Serum amyloid A induces G-CSF expression and neutrophilia via Toll-like receptor 2. Blood 113(2):429–437

    PubMed  CAS  Google Scholar 

  148. Hiratsuka S, Watanabe A, Sakurai Y, Akashi-Takamura S, Ishibashi S et al (2008) The S100A8-serum amyloid A3-TLR4 paracrine cascade establishes a pre-metastatic phase. Nat Cell Biol 10(11):1349–1355

    PubMed  CAS  Google Scholar 

  149. Yan SD, Zhu H, Zhu A, Golabek A, Du H et al (2000) Receptor-dependent cell stress and amyloid accumulation in systemic amyloidosis. Nat Med 6(6):643–651

    PubMed  CAS  Google Scholar 

  150. Christenson K, Bjorkman L, Tangemo C, Bylund J (2008) Serum amyloid A inhibits apoptosis of human neutrophils via a P2X7-sensitive pathway independent of formyl peptide receptor-like 1. J Leukoc Biol 83(1):139–148

    PubMed  CAS  Google Scholar 

  151. Niemi K, Teirila L, Lappalainen J, Rajamaki K, Baumann MH et al (2011) Serum amyloid A activates the NLRP3 inflammasome via P2X7 receptor and a cathepsin B-sensitive pathway. J Immunol 186(11):6119–6128

    PubMed  CAS  Google Scholar 

  152. Baranova IN, Bocharov AV, Vishnyakova TG, Kurlander R, Chen Z et al (2010) CD36 is a novel serum amyloid A (SAA) receptor mediating SAA binding and SAA-induced signaling in human and rodent cells. J Biol Chem 285(11):8492–8506

    PubMed  CAS  Google Scholar 

  153. Miller YI, Viriyakosol S, Binder CJ, Feramisco JR, Kirkland TN et al (2003) Minimally modified LDL binds to CD14, induces macrophage spreading via TLR4/MD-2, and inhibits phagocytosis of apoptotic cells. J Biol Chem 278(3):1561–1568

    PubMed  CAS  Google Scholar 

  154. Bae YS, Lee JH, Choi SH, Kim S, Almazan F et al (2009) Macrophages generate reactive oxygen species in response to minimally oxidized low-density lipoprotein: Toll-like receptor 4- and spleen tyrosine kinase-dependent activation of NADPH oxidase 2. Circ Res 104(2):210–218

    PubMed  CAS  Google Scholar 

  155. Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H et al (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116(11):3015–3025

    PubMed  CAS  Google Scholar 

  156. Scheibner KA, Lutz MA, Boodoo S, Fenton MJ, Powell JD et al (2006) Hyaluronan fragments act as an endogenous danger signal by engaging TLR2. J Immunol 177(2):1272–1281

    PubMed  CAS  Google Scholar 

  157. Termeer C, Benedix F, Sleeman J, Fieber C, Voith U et al (2002) Oligosaccharides of Hyaluronan activate dendritic cells via Toll-like receptor 4. J Exp Med 195(1):99–111

    PubMed  CAS  Google Scholar 

  158. Johnson GB, Brunn GJ, Kodaira Y, Platt JL (2002) Receptor-mediated monitoring of tissue well-being via detection of soluble heparan sulfate by Toll-like receptor 4. J Immunol 168(10):5233–5239

    PubMed  CAS  Google Scholar 

  159. Cheng C, Tsuneyama K, Kominami R, Shinohara H, Sakurai S et al (2005) Expression profiling of endogenous secretory receptor for advanced glycation end products in human organs. Mod Pathol 18(10):1385–1396

    PubMed  CAS  Google Scholar 

  160. Babelova A, Moreth K, Tsalastra-Greul W, Zeng-Brouwers J, Eickelberg O et al (2009) Biglycan, a danger signal that activates the NLRP3 inflammasome via Toll-like and P2X receptors. J Biol Chem 284(36):24035–24048

    PubMed  CAS  Google Scholar 

  161. Schaefer L, Babelova A, Kiss E, Hausser HJ, Baliova M et al (2005) The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Invest 115(8):2223–2233

    PubMed  CAS  Google Scholar 

  162. Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S et al (2009) Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 457(7225):102–106

    PubMed  CAS  Google Scholar 

  163. Kariko K, Ni H, Capodici J, Lamphier M, Weissman D (2004) mRNA is an endogenous ligand for Toll-like receptor 3. J Biol Chem 279(13):12542–12550

    PubMed  CAS  Google Scholar 

  164. Vollmer J, Tluk S, Schmitz C, Hamm S, Jurk M et al (2005) Immune stimulation mediated by autoantigen binding sites within small nuclear RNAs involves Toll-like receptors 7 and 8. J Exp Med 202(11):1575–1585

    PubMed  CAS  Google Scholar 

  165. Leadbetter EA, Rifkin IR, Hohlbaum AM, Beaudette BC, Shlomchik MJ et al (2002) Chromatin–IgG complexes activate B cells by dual engagement of IgM and Toll-like receptors. Nature 416(6881):603–607

    PubMed  CAS  Google Scholar 

  166. Abbracchio MP, Burnstock G, Boeynaems JM, Barnard EA, Boyer JL et al (2006) International Union of Pharmacology LVIII: update on the P2Y G protein-coupled nucleotide receptors: from molecular mechanisms and pathophysiology to therapy. Pharmacol Rev 58(3):281–341

    PubMed  CAS  Google Scholar 

  167. Jarvis MF, Khakh BS (2009) ATP-gated P2X cation-channels. Neuropharmacology 56(1):208–215

    PubMed  CAS  Google Scholar 

  168. Nonaka M, Fukumoto A, Ogihara N, Pawankar R, Sakanushi A et al (2007) Expression of MCP-4 by TLR ligand-stimulated nasal polyp fibroblasts. Acta Otolaryngol 127(12):1304–1309

    PubMed  CAS  Google Scholar 

  169. Chen CI, Schaller-Bals S, Paul KP, Wahn U, Bals R (2004) Beta-defensins and LL-37 in bronchoalveolar lavage fluid of patients with cystic fibrosis. J Cyst Fibros 3(1):45–50

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by funding from the Research Foundation Flanders (FWO); research project Nr. G.0641.10 to KVC, a Concerted Research Action project (01G01009) from the Special Research Fund of Ghent University, and the Interuniversity Attraction Poles Program -Belgian Science Policy, P7/30.

Author information

Authors and Affiliations

  1. Upper Airways Research Laboratory, Department of Otorhinolaryngology, Ghent University Hospital, De Pintelaan 185, 9000, Ghent, Belgium

    Koen Van Crombruggen, Fenila Jacob, Nan Zhang & Claus Bachert

Authors
  1. Koen Van Crombruggen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fenila Jacob
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Claus Bachert
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Koen Van Crombruggen.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Van Crombruggen, K., Jacob, F., Zhang, N. et al. Damage-associated molecular patterns and their receptors in upper airway pathologies. Cell. Mol. Life Sci. 70, 4307–4321 (2013). https://doi.org/10.1007/s00018-013-1356-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-013-1356-7

Keywords

Search

Navigation