Heparin and structurally related polymers attenuate eotaxin-1 (CCL11) release from human airway smooth muscle

British Journal of Pharmacology

Volumn 154, Issue 4, 2008, Pages 833-842

  Kanabar, V ^a,b   Page, C P ^b   Simcock, D E ^a   Karner, C ^a   Mahn, K ^a   O'Connor, B J ^a   Hirst, S J ^a,c  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c MONASH UNIVERSITY   (Australia)

Author keywords

Airway smooth muscle; Asthma; Eotaxin 1; Glycosaminoglycan; Heparin; Inflammation

Indexed keywords

EOTAXIN; GLYCOSAMINOGLYCAN; HEPARIN; INTERLEUKIN 13; LOW MOLECULAR WEIGHT HEPARIN;

ACETYLATION; AIRWAY SMOOTH MUSCLE; ANTICOAGULATION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; ASTHMA; CELL STIMULATION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; HUMAN; HUMAN CELL; INFLAMMATION; MAST CELL; MEDIATOR RELEASE; MOLECULAR SIZE; PRIORITY JOURNAL; SMOOTH MUSCLE FIBER; SULFATION;

ADULT; AGED; ANIONS; ANTI-INFLAMMATORY AGENTS; ANTICOAGULANTS; CELLS, CULTURED; CHEMOKINE CCL11; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HEPARIN; HEPARIN, LOW-MOLECULAR-WEIGHT; HUMANS; INTERLEUKIN-13; MALE; MIDDLE AGED; MOLECULAR WEIGHT; MYOCYTES, SMOOTH MUSCLE; SULFATES;

EID: 44949167500     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1038/bjp.2008.109     Document Type: Article

References (50)

1. Ammit AJ, Bekir SS, Johnson PR, Hughes JM, Armour CL, Black JL (1997). Mast cell numbers are increased in the smooth muscle of human sensitized isolated bronchi. Am J Respir Crit Care Med 155: 1123-1129.
2. Bode L, Murch S, Freeze HH (2006). Heparan sulfate plays a central role in a dynamic in vitro model of protein-losing enteropathy. J Biol Chem 281: 7809-7815.
3. Brightling CE, Bradding P, Symon FA, Holgate ST, Wardlaw AJ, Pavord ID (2002). Mast-cell infiltration of airway smooth muscle in asthma. N Engl J Med 346: 1699-1705.
4. Castellot JJ, Wong K, Herman B, Hoover RL, Albertini DF, Wright TC et al. (1985). Binding and internalization of heparin by vascular smooth muscle cells. J Cell Physiol 124: 13-20.
5. Casu B, Petitou M, Provasoli M, Sinay P (1988). Conformational flexibility: a new concept for explaining binding and biological properties of iduronic acid-containing glycosaminoglycans. Trends Biochem Sci 13: 221-225.
6. Chan V, Burgess JK, Ratoff JC, O'Connor BJ, Greenough A, Lee TH et al. (2006). Extracellular matrix regulates enhanced eotaxin-1 expression in asthmatic airway smooth muscle cells. Am J Respir Crit Care Med 174: 379-385.
7. de Paz JL, Moseman EA, Noti C, Polito L, von Andrian UH, Seeberger PH (2007). Profiling heparin-chemokine interactions using synthetic tools. ACS Chem Biol 2: 735-744.
8. Ellyard JI, Simson L, Bezos A, Johnston K, Freeman C, Parish CR (2007). Eotaxin-1 selectively binds heparin: an interaction that protects eotaxin from proteolysis and potentiates chemotactic activity in vivo. J Biol Chem 282: 15238-15247.
9. Fernandez-Botran R, Yan J, Justus DE (1999). Binding of interferon gamma by glycosaminoglycans: a strategy for localization and/or inhibition of its activity. Cytokine 11: 313-325.
10. Frevert CW, Kinsella MG, Vathanaprida C, Goodman RB, Baskin DG, Proudfoot A et al. (2003). Binding of interleukin-8 to heparan sulfate and chondroitin sulfate in lung tissue. Am J Respir Cell Mol Biol 28: 464-472.
11. Fryer A, Huang YC, Rao G, Jacoby D, Mancilla E, Whorton R et al. (1997). Selective O-desulfation produces non-anticoagulant heparin that retains pharmacological activity in the lung. J Pharmacol Exp Ther 282: 208-219.
12. Ghaffar O, Hamid Q, Renzi PM, Allakhverdi Z, Molet S, Hogg JC et al. (1999). Constitutive and cytokine-stimulated expression of eotaxin by human airway smooth muscle cells. Am J Respir Crit Care Med 159: 1933-1942.
13. Green WF, Konnaris K, Woolcock AJ (1993). Effect of salbutamol, fenoterol, and sodium cromoglycate on the release of heparin from sensitized human lung fragments challenged with Dermatophagoides pteronyssinus allergen. Am J Respir Cell Mol Biol 8: 518-521.
14. Grunig G, Warnock M, Wakil AE, Venkayya R, Brombacher F, Rennick DM et al. (1998). Requirement for IL-13 independently of IL-4 in experimental asthma. Science 282: 2261-2263.
15. Guyton JR, Rosenberg RD, Clowes AW, Karnovsky MJ (1980). Inhibition of rat arterial smooth muscle cell proliferation by heparin. In vivo studies with anticoagulant and nonanticoagulant heparin. Circ Res 46: 625-634.
16. Hirst SJ (2003). Regulation of airway smooth muscle cell immunomodulatory function: role in asthma. Respir Physiol Neurobiol 137: 309-326.
17. Hirst SJ, Hallsworth MP, Peng Q, Lee TH (2002). Selective induction of eotaxin release by interleukin-13 or interleukin-4 in human airway smooth muscle cells is synergistic with interleukin-1beta and is mediated by the interleukin-4 receptor alpha-chain. Am J Respir Crit Care Med 165: 1161-1171.
18. Hirst SJ, Twort CH, Lee TH (2000). Differential effects of extracellular matrix proteins on human airway smooth muscle cell proliferation and phenotype. Am J Respir Cell Mol Biol 23: 335-344.
19. Hoover RL, Rosenberg R, Haering W, Karnovsky MJ (1980). Inhibition of rat arterial smooth muscle cell proliferation by heparin. In vitro studies. Circ Res 47: 578-583.
20. Huang J, Olivenstein R, Taha R, Hamid Q, Ludwig M (1999). Enhanced proteoglycan deposition in the airway wall of atopic asthmatics. Am J Respir Crit Care Med 160: 725-729.
21. Huang SK, Xiao HQ, Kleine-Tebbe J, Paciotti G, Marsh DG, Lichtenstein LM et al. (1995). IL-13 expression at the sites of allergen challenge in patients with asthma. J Immunol 155: 2688-2694.
22. 2 inhibit DNA synthesis in human airway smooth muscle cells in culture. Am J Physiol 269: L514-L519.
23. Johnson Z, Kosco-Vilbois MH, Herren S, Cirillo R, Muzio V, Zaratin P et al. (2004). Interference with heparin binding and oligomerization creates a novel antiinflammatory strategy targeting the chemokine system. J Immunol 173: 5776-5785.
24. Jose PJ, Griffiths-Johnson DA, Collins PD, Walsh DT, Moqbel R, Totty NF et al. (1994). Eotaxin: a potent eosinophil chemoattractant cytokine detected in a guinea pig model of allergic airways inflammation. J Exp Med 179: 881-887.
25. Joseph PA, Garg HG, Thompson BT, Liu X, Hales CA (1997). Influence of molecular weight, protein core and charge of native heparin fractions on pulmonary artery smooth muscle cell proliferation. Biochem Biophys Res Commun 241: 18-23.
26. Kanabar V, Hirst SJ, O'Connor BJ, Page CP (2005). Some structural determinants of the antiproliferative effect of heparin-like molecules on human airway smooth muscle. Br J Pharmacol 146: 370-377.
27. Kaur D, Saunders R, Berger P, Siddiqui S, Woodman L, Wardlaw A et al. (2006). Airway smooth muscle and mast cell-derived CC chemokine ligand 19 mediate airway smooth muscle migration in asthma. Am J Respir Crit Care Med 174: 1179-1188.
28. Kawashima H, Atarashi K, Hirose M, Hirose J, Yamada S, Sugahara K et al. (2002). Oversulphated chondroitin/dermatan sulphates containing GlcAb1/IdoAa1-3GalNAc (4,6-O-disulphate) interact with L- and P-selectin and chemokines. J Biol Chem 277: 12921-12930.
29. Kilfeather SA, Tagoe S, Perez AC, Okona-Mensa K, Matin R, Page CP (1995). Inhibition of serum-induced proliferation of bovine tracheal smooth muscle cells in culture by heparin and related glycosaminoglycans. Br J Pharmacol 114: 1442-1446.
30. Koyanagi S, Tanigawa N, Nakagawa H, Soeda S, Shimeno H (2003). Oversulphation of fucoidan enhances its anti-angiogenic and antitumor activities. Biochem Pharmacol 65: 173-179.
31. Kotsimbos TC, Ernst P, Hamid QA (1996). Interleukin-13 and interleukin-4 are coexpressed in atopic asthma. Proc Assoc Am Physicians 108: 368-373.
32. Kuschert GS, Coulin F, Power CA, Proudfoot AE, Hubbard RE, Hoogewerf AJ et al. (1999). Glycosaminoglycans interact selectively with chemokines and modulate receptor binding and cellular responses. Biochemistry 38: 12959-12968.
33. Lever R, Page CP (2002). Novel drug development opportunities for heparin. Nat Rev Drug Discov 1: 140-148.
34. Longas MO, Garg HG, Trinkle-Pereira JM, Hales CA (2003). Heparin antiproliferative activity on bovine pulmonary artery smooth muscle cells requires both N-acetylation and N-sulfonation. Carbohydr Res 338: 251-256.
35. Moore PE, Church TL, Chism DD, Panettieri RA, Shore SA (2002). IL-13 and IL-4 cause eotaxin release in human airway smooth muscle cells: a role for ERK. Am J Physiol Lung Cell Mol Physiol 282: L847-L853.
36. Mummery RS, Rider CC (2000). Characterization of the heparin-binding properties of IL-6. J Immunol 165: 5671-5679.
37. Page S, Ammit AJ, Black JL, Armour CL (2001). Human mast cell and airway smooth muscle cell interactions: implications for asthma. Am J Physiol Lung Cell Mol Physiol 281: L1313-L1323.
38. Panettieri RA (2002). Airway smooth muscle: an immunomodulatory cell. J Allergy Clin Immunol 110: S269-S274.
39. Rabenstein DL (2002). Heparin and heparan sulfate: structure and function. Nat Prod Rep 19: 312-331.
40. Robinson DS (2004). The role of the mast cell in asthma: induction of airway hyperresponsiveness by interaction with smooth muscle? J Allergy Clin Immunol 114: 58-65.
41. Rose MJ, Page C (2004). Glycosaminoglycans and the regulation of allergic inflammation. Curr Drug Targets Inflamm Allergy 3: 221-225.
42. Salek-Ardakani S, Arrand JR, Shaw D, Mackett M (2000). Heparin and heparan sulfate bind interleukin-10 and modulate its activity. Blood 96: 1879-1888.
43. Seeds EA, Horne AP, Tyrrell DJ, Page CP (1995). The effect of inhaled heparin and related glycosaminoglycans on allergen-induced eosinophil infiltration in guinea-pigs. Pulm Pharmacol 8: 97-105.
44. Tiozzo R, Cingi MR, Reggiani D, Andreoli T, Calandra S, Milani MR et al. (1993). Effect of the desulfation of heparin on its anticoagulant and antiproliferative activity. Thromb Res 70: 99-106.
45. Tiozzo R, Reggiani D, Cingi MR, Bianchini P, Osima B, Calandra S (1991). Effect of heparin derived fractions on the proliferation and protein synthesis of cells in culture. Thromb Res 62: 177-188.
46. Tyrrell DJ, Horne AP, Holme KR, Preuss JM, Page CP (1999). Heparin in inflammation: potential therapeutic applications beyond anticoagulation. Adv Pharm 46: 151-208.
47. Varma R, Varma RS (eds) (1983). Chemistry and metabolism of glycosaminoglycans and proteoglycans. In. Mucopolysaccharides. Glycosaminoglycans of Body Fluids in Health and Disease. Walter de Gruyter: Berlin. pp 3-48.
48. Windholz M, Budaveri S, Strountsos L, Fertig M (1976). The Merck Index, 9th edn. Merck Rahway: New Jersey, 387 pp.
49. Wright Jr TC, Castellot Jr JJ, Petitou M, Lormeau JC, Choay J, Karnovsky MJ (1989). Structural determinants of heparin's growth inhibitory activity. Interdependence of oligosaccharide size and charge. J Biol Chem 264: 1534-1542.
50. Zhu Z, Homer RJ, Wang Z, Chen Q, Geba GP, Wang J et al. (1999). Pulmonary expression of interleukin-13 causes inflammation, mucus hypersecretion, subepithelial fibrosis, physiologic abnormalities, and eotaxin production. J Clin Invest 103: 779-788.