Low anticoagulant heparin targets multiple sites of inflammation, suppresses heparin-induced thrombocytopenia, and inhibits interaction of RAGE with its ligands

American Journal of Physiology - Cell Physiology

Volumn 299, Issue 1, 2010, Pages

  Rao, Narayanam V ^a   Argyle, Brian ^a   Xu, Xiaoyu ^a   Reynolds, Paul R ^b   Walenga, Jeanine M ^c   Prechel, Margaret ^c   Prestwich, Glenn D ^a   MacArthur, Robert B ^d   Walters, Bradford B ^e   Hoidal, John R ^a   Kennedy, Thomas P ^a  

^a UNIVERSITY OF UTAH HEALTH SCIENCES CENTER   (United States)

^b BRIGHAM YOUNG UNIVERSITY   (United States)

^c LOYOLA UNIVERSITY CHICAGO   (United States)

^d Och Spine at New York Presbyterian Hospitals   (United States)

^e RTI HEALTH SOLUTIONS   (United States)

Author keywords

High mobility group box protein 1; Human research; P selectin; Receptor for advanced glycation end products; S100 calgranulins; Translational research

Indexed keywords

2 O, 3 O DESULFATED HEPARIN; ADVANCED GLYCATION END PRODUCT RECEPTOR; AZUROCIDIN; BOVINE SERUM ALBUMIN; CALGRANULIN; CATHEPSIN G; CD11B ANTIGEN; ELASTASE; HEPARIN; HEPARINOID; HIGH MOBILITY GROUP B1 PROTEIN; LIGAND; PADGEM PROTEIN; PLACEBO; UNCLASSIFIED DRUG; VASCULAR ADHESION PROTEIN 1;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTICOAGULATION; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG DOSE ESCALATION; FEMALE; HUMAN; HUMAN EXPERIMENT; INFLAMMATION; LEUKOCYTE ADHERENCE; LUNG METASTASIS; MALE; MELANOMA; MOUSE; NONHUMAN; NORMAL HUMAN; PNEUMONIA; PRIORITY JOURNAL; THROMBOCYTE ACTIVATION; THROMBOCYTOPENIA;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTICOAGULANTS; ANTITHROMBIN III; BLOOD COAGULATION; BLOOD COAGULATION TESTS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; FACTOR XIIA; FEMALE; GLYCOSYLATION END PRODUCTS, ADVANCED; HEPARIN; HMGB1 PROTEIN; HUMANS; INFUSIONS, INTRAVENOUS; INJECTIONS, INTRAVENOUS; INJECTIONS, SUBCUTANEOUS; LIGANDS; LUNG NEOPLASMS; MACROPHAGE-1 ANTIGEN; MALE; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NERVE GROWTH FACTORS; P-SELECTIN; PLATELET ACTIVATION; PLATELET FUNCTION TESTS; PNEUMONIA; RECEPTORS, IMMUNOLOGIC; RECOMBINANT PROTEINS; S100 PROTEINS; THROMBOCYTOPENIA; U937 CELLS;

BOVINAE; MUS;

EID: 77953772222     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00009.2010     Document Type: Article

References (50)

1. Altinbas M, Coskun HS, Er O, Ozkan M, Eser B, Unal A, Cetin M, Soyuer S. A randomized clinical trial of combination chemotherapy with and without low-molecular-weight heparin in small cell lung cancer. J Thromb Haemost 2: 1266-1261, 2004.
2. Ashikari-Hada S, Habuchi H, Kariya Y, Itoh N, Reddi AH, Kimata K. Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library. J Biol Chem 279: 12346-12354, 2004.
3. Ashikari-Hada S, Habuchi H, Kariya Y, Kimata K. Heparin regulates vascular endothelial growth factor165-dependent mitogenic activity, tube formation, and its receptor phosphorylation of human endothelial cells. Comparison of the effects of heparin and modified heparins. J Biol Chem 280: 31508-31515, 2005.
4. Barker RL, Gundel RH, Gleich GJ, Checkel JL, Loegering DA, Pease LR, Hamann KJ. Acidic polyamino acids inhibit human eosinophil granule major basic protein toxicity. Evidence of a functional role for ProMBP. J Clin Invest 88: 798-805, 1991.
5. Borsig L, Wong R, Feramisco J, Nadeau DR, Varki NM, Varki A. Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis. Proc Natl Acad Sci USA 98: 3352-3357, 2001.
6. Borsig L, Wong R, Hynes RO, Varki NM, Varki A. Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proc Natl Acad Sci USA 99: 2193-2198, 2002.
7. Cardin A, Weintraub H. Molecular modeling of protein-glycosaminoglycan interactions. Arteriosclerosis 9: 21-32, 1989.
8. Chavakis T, Bierhaus A, Al-Fakhri N, Schneider D, Witte S, Linn T, Nagashima M, Morser J, Arnold B, Preissner KT, Nawroth PP. The pattern recognition receptor (RAGE) is a counterreceptor for leukocyte integrins: a novel pathway for inflammatory cell recruitment. J Exp Med 198: 1507-1515, 2003.
9. Cheng Y, Prusoff W. Relationship between the inhibition constant (K1) and the concentration of inhibitor which causes 50 per cent inhibition (IC50) of an enzymatic reaction. Biochem Pharmacol 22: 3099-3108, 1973.
10. Dudas B, Rose M, Cornelli U, Pavlovich A, Hanin I. Neuroprotective properties of glycosaminoglycans: potential treatment for neurodegenerative disorders. Neurodegener Dis 5: 200-205, 2008.
11. Diamond M, Alon R, Parkos C, Quinn M, Springer T. Heparin is an adhesive ligand for the leukocyte integrin Mac-1 (CD11b/CD1). J Cell Biol 130: 1473-1482, 1995.
12. Dattilo BM, Fritz G, Leclerc E, Kooi CW, Heizmann CW, Chazin WJ. The extracellular region of the receptor for advanced glycation end products is composed of two independent structural units. Biochemistry 46: 6957-6970, 2007.
13. Fryer AD, Jacoby DB. Function of pulmonary M2 muscarinic receptors in antigen-challenged guinea pigs is restored by heparin and poly-Lglutamate. J Clin Invest 90: 2292-2298, 1992.
14. Fryer A, Huang YC, Rao G, Jacoby D, Mancilla E, Whorton R, Piantadosi CA, Kennedy T, Hoidal J. Selective O-desulfation produces nonanticoagulant heparin that retains pharmacologic activity in the lung. J Pharmacol Exp Ther 282: 208-219, 1997.
15. Gautam N, Olofsson A, Herwald H, Iversen L, Lundgren-Akerlund E, Hedqvist P, Arfors KE, Glodgaard H, Lindbom L. Heparin-binding protein (HBP/CAP37): a missing link in neutrophil-evoked alteration of vascular permeability. Nat Med 2: 1123-1127, 2001.
16. Goldin A, Beckman JA, Schmidt AM, Creager MA. Advanced glycation end products. Sparking the development of diabetic vascular injury. Circulation 114: 597-605, 2006.
17. Hanford LE, Enghild JJ, Valnickova Z, Petersen SV, Schaefer LM, Schaefer TM, Reinhart TA, Oury TD. Purification and characterization of mouse soluble receptor for advanced glycation end products (sRAGE). J Biol Chem 279: 50019-50024, 2004.
18. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, Neurath MG, Slattery T, Beach D, McClary J, Nagahima M, Morser J, Stern D, Schmidt AM. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 97: 889-901, 1999.
19. Hori O, Brett J, Slattery T, Cao R, Zhang J, Chen J, Nagashima M, Lundh ER, Vijay S, Nitecki D, Morser J, Stern D, Schmidt AM. 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: 25752-25761, 1995.
20. Kakkar AK, Levine MN, Kadziola Z, Lemoine NR, Low V, Patel HK, Rustin G, Thomas M, Quigley M, Williamson RCH. Low molecular weight heparin, therapy with dalteparin, and survival in advanced cancer: The Fragmin Advanced Malignancy Outcome Study (FAMOUS). J Clin Oncol 22: 1944-1948, 2004.
21. Klerk CP, Smorenburg SM, Otten HM, Lensing AW, Prins MH, Piovella F, Prandoni P, Bos MM, Richel DJ, van Tienhoven G, Buuler HR. The effect of low molecular weight heparin on survival in patients with advanced malignancy. J Clin Oncol 23: 21230-2135, 2005.
22. Koenig A, Norgard-Sumnicht K, Linhardt R, Varki A. Differential interactions of heparin and heparan sulfate glycosaminoglycans with the selectins. Implications for the use of unfractionated and low molecular weight heparins as therapeutic agents. J Clin Invest 101: 877-889, 1998. (Pubitemid 28096085)
23. Leclerc E, Fritz G, Weibel M, Heizmann CW, Galichet A. S100B and S100A6 differentially modulate cell survival by interacting with distinct RAGE (receptor for advanced glycation end products) immunoglobulin domains. J Biol Chem 282: 31317-31331, 2006.
24. Lee AYY, Rickles FR, Julian JA, Gent M, Baker RI, Bowden C, Kakkar AK, Prins M, Levine NM. Randomized comparison of low molecular weight heparin and coumarin derivatives on the survival of patients with cancer and venous thromboembolism. J Clin Oncol 23: 2123-2129, 2005.
25. Lever R, Page CP. Novel drug development opportunities for heparin. Nat Rev Drug Disc 1: 140-148, 2002.
26. Matsumoto S, Yoshida T, Murata H, Harada S, Fujita N, Nakamura S, Yamamoto Y, Watanabe T, Yonekura H, Yamamoto H, Ohkubo T, Kobayashi Y. Solution structure of the variable-type domain of the receptor for advanced glycation end products: new insight into AGERAGE interaction. Biochemistry 47: 12299-12311, 2008.
27. McClean J. The thromboplastic action of cephalin. Am J Physiol 41: 250-257, 1916.
28. McEver R, Cummings R. Role of PSGL-1 binding to selectins in leukocyte recruitment. J Clin Invest 100: S97-103, 1997.
29. Myint KM, Yamamoto Y, Doi T, Kato I, Harashima A, Yonekura H, Watanabe T, Shinohara H, Takeuchi M, Tsuneyama K, Hashimoto N, Asano M, Takasawa S, Okamoto H, Yamamoto H. RAGE control of diabetic nephropathy in a mouse model. Effects of RAGE gene disruption and administration of low-molecular weight heparin. Diabetes 55: 2510-2522, 2006.
30. Ono K, Hattori H, Takeshita S, Kurita A, Ishihara M. Structural features in heparin that interact with VEGF165 and modulate its biological activity. Glycobiology 9: 705-711, 1999.
31. Orlova VV, Choi EY, Xie C, Chavakis E, Bierhaus A, Ihanus E, Ballantyne CM, Gahmberg CG, Bianchi ME, Nawroth PP, Chavakis T. A novel pathway way of HMGB1-mediated inflammatory cell recruitment that requires Mac-1 integrin. EMBO J 26: 1129-1139, 2007.
32. Patey SJ, Edwards EA, Yates EA, Turnbull JE. Heparin derivatives as inhibitors of BACE-1, the Alzheimer's beta-secretase, with reduced activity against factor Xa and other proteases. J Med Chem 49: 6129-6132, 2006.
33. Pham C. Neutrophil serine proteases: specific regulators of inflammation. Nat Rev Immunol 6: 541-550, 2006.
34. Prechel MM, McDonald MK, Jeske WP, Messmore HL, Walenga JM. Activation of platelets by heparin-induced thrombocytopenia antibodies in the serotonin release assay is not dependent on the presence of heparin. J Thromb Haemost 3: 2168-2175, 2005.
35. Rauova L, Zhai L, Kowalska A, Arepally GM, Cines DB, Poncz M. Role of platelet surface PF4 antigenic complexes in heparin-induced thrombocytopenia pathogenesis: diagnostic and therapeutic implications. Blood 107: 2346-2353, 2006.
36. Rauvala H, Pihlaskari R. Isolation and some characteristics of an adhesive factor of brain that enhances neurite outgrowth in central neurons. J Biol Chem 262: 16625-16635, 1987.
37. Rowe SM, Jackson PL, Liu G, Hardison M, Livraghi A, Solomon GM, McQuaid DB, Noerager BD, Gaggar A, Clancy JP, O'Neal W, Sorcher EJ, Abraham E, Blalock JE. Potential role of high-mobility group box 1 in cystic fibrosis airway disease. Am J Respir Crit Care Med 178: 822-831, 2008.
38. Samuel M, Pixley RA, Villanueva MA, Colman RW. Human factor XII (Hageman factor) autoactivation by dextran sulfate: circular dichroism, fluorescence, and ultraviolet difference spectroscopic studies. J Biol Chem 267: 19691-19697, 1992.
39. Schmidt AM, Vianna M, Gerlach M, Brett J, Ryan J, Kao J, Esposito C, Hegarty H, Hurley W, Clauss M, Wang F, Peng YCE, Tsang TC, Stern D. Isolation and characterization of two binding proteins for advanced glycosylation end products from bovine lung which are present on the endothelial cell surface. J Biol Chem 267: 14987-14997, 1992.
40. Schmidt AM, Yan SD, Yan SF, Stern DM. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 108: 949-955, 2001.
41. Silverberg M, Dunn JT, Garen L, Kaplan AP. Autoactivation of human Hageman factor. Demonstration using a synthetic substrate. J Biol Chem 255: 7281-7286, 1980. (Pubitemid 11245061)
42. Stevenson JL, Choi SH, Varki A. Differential metastasis inhibition by clinically relevant levels of heparins- correlation with selectin inhibition, not antithrombotic activity. Clin Cancer Res 11: 7003-7011, 2005.
43. Thourani VH, Brarr SS, Kennedy TP, Thornton LR, Watts JA, Ronson RS, Zhao ZQ, Sturrock AL, Hoidal JR, Vinten-Johansen J. Nonanticoagulant heparin inhibits NF-κB activation and attenuates myocardial reperfusion injury. Am J Physiol Heart Circ Physiol 278: H2084-H2093, 2000.
44. Walenga JM, Jeske WP, Prechel MM, Makhos M. Newer insights on the mechanism of heparin-induced thrombocytopenia. Semin Thromb Hemost 30, Suppl 1: 57-67, 2004.
45. Wang L, Brown JR, Varki A, Esko JD. Heparin's anti-inflammatory effects require glucosamine 6-O-sulfation and are mediated by blockade of L- and P-selectins. J Clin Invest 110: 127-136, 2001.
46. Weiler JM, Edens RE, Linhardt RJ, Kapelanski DP. Heparin and modified heparin inhibit complement activation in vivo. J Immunol 148: 3210-3215, 1992.
47. Weiss S. Tissue destruction by neutrophils. N Engl J Med 320: 365-376, 1989.
48. Westwood ME, Thornally PJ. Molecular characteristics of methylglyoxal-modified bovine and human serum albumins. Comparison with glucose-derived advanced glycation endproduct-modified serum albumins. J Protein Chem 14: 359-372, 1995.
49. Xie J, Burz DS, He W, Bronstein IB, Lednev I, Shekhtman A. Hexameric calgranulin C (S100A12) binds to the receptor for advanced glycated end products (RAGE) using symmetric hydrophobic target-binding patches. J Biol Chem 282: 4218-4231, 2007.
50. Xie J, Reverdatto S, Frolov A, Hoffmann R, Burz DS, Shekhtman A. Structural basis for pattern recognition by the receptor for advanced glycation end products (RAGE). J Biol Chem 282: 27255-27269, 2008.