Protective and therapeutic effect of heparin in acute pancreatitis

Journal of Physiology and Pharmacology

Volumn 59, Issue SUPPL. 4, 2008, Pages 103-125

  Ceranowicz, P ^a   Dembinski, Artur ^a   Warzecha, Z ^a   Dembinski, M ^a   Cieszkowski, J ^a   Rembiasz, K ^a   Konturek, S J ^a   Kusnierz Cabala, B ^a   Tomaszewska, R ^a   Pawlik, W W ^a  

^a JAGIELLONIAN UNIVERSITY MEDICAL COLLEGE   (Poland)

Author keywords

Activated partial thromboplastin time; Interleukin 1 ; Ischemia reperfusion induced pancreatitis; Pancreatic damage; Plasma lipase activity

Indexed keywords

BIOCHEMICAL MARKER; D DIMER; HEPARIN; HEPARINUM; INTERLEUKIN 1BETA; UNCLASSIFIED DRUG;

ACUTE PANCREATITIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; DISEASE SEVERITY; DNA SYNTHESIS; MALE; MICROANGIOPATHY; NONHUMAN; PANCREAS BLOOD FLOW; PARTIAL THROMBOPLASTIN TIME; RAT; REGENERATION; REPERFUSION;

ACUTE DISEASE; ANIMALS; ANTICOAGULANTS; BLOOD FLOW VELOCITY; DISEASE MODELS, ANIMAL; HEPARIN; MALE; MICROCIRCULATION; PANCREAS; PANCREATITIS; RATS; RATS, WISTAR; REPERFUSION INJURY;

EID: 53549103031     PISSN: 08675910     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (85)

1. Lasson A, Ohlsson K. Consumptive coagulopathy, fibrinolysis and protease-antiprotease interactions during acute human pancreatitis. Thromb Res 1986; 41: 167-183.
2. Salomone T, Tosi P, Palareti G et al. Coagulative disorders in human acute pancreatitis: role for the D-dimer. Pancreas 2003; 26: 111-116.
3. Agarwal N, and Pitchumoni CS. Acute pancreatitis: a multisystem disease. Gastroenterologist 1993; 1: 115-128
4. Esmon CT, Taylor FB Jr, Snow TR. Inflammation and coagulation: linked processes potentially regulated through a common pathway mediated by protein C. Thromb Haemost 1991; 66: 160-165.
5. Esmon CT. Possible involvement of cytokines in diffuse intravascular coagulation and thrombosis. Baillieres Best Pract Res Clin Haematol 1999; 12: 343-359.
6. Bowman WC, Rand MJ. The blood: drugs affecting coagulation, fibrinolysis, haematopoiesis and functioning of blood cells. In Textbook of Pharmacology, WC Bowman, MJ Rand (eds). Oxford, London, Edinburgh, Melbourne, Blackwell Scientific Publication, 1980, pp. 21.15-21.16.
7. Finotti P, Manente S. Heparin-induced structural and functional alteration s of bovine trypsin. Biochim Biophys Acta 1994; 1207: 80-87.
8. Nobar SM, Guy-Crotte O, Rabaud M, Bieth JG. Inhibition of human pancreatic proteinases by human plasma alpha2-antiplasmin and antithrombin. Biol Chem 2004; 385: 423-427.
9. Struss D, Storck J, Zimmermann RE. The inhibition of thrombin and chymotrypsin by heparin-cofactor II. Trombin Res 1992; 68: 45-56.
10. Wolosowicz N, Prokopowicz J, Gabryelewicz A. The inhibitory effect of heparin on trypsinogen activation with enterokinase. Acta Hepatogastroenterol (Stuttg) 1977; 24: 367-371.
11. Gabryelewicz A, Kosidlo S, Prokopowicz J, Podkowicz K. Does heparin modify protease-antiprotease balance in acute experimental pancreatitis in rats. Hepatogastroenterology 1986; 33: 79-82.
12. Seta T, Noguchi Y, Shimada T, Shikata S, Fukui T. Treatment of acute pancreatitis with protease inhibitors: a meta-analysis. Eur J Gastroenterol Hepatol 2004; 16: 1287-1293.
13. Perretti M, Page CP. Heparin and inflammation: a new use for an old GAG? Gut 2000; 47: 14-15.
14. Gaffney A, Gaffney P. Rheumatoid arthritis and heparin. Br J Rheumatol 1996; 35: 808-809.
15. Bowler SD, Smith SM, Lavercombe PS. Heparin inhibits the immediate response to antigen in the skin and lungs of allergic subjects. Am Rev Respir Dis 1993; 147: 160-163.
16. Dwarakanath AD, Yu LG, Brookers C, Pryce D, Rhodes JM. 'Sticky' neutrophils, pathergic arthritis, and response to heparin in pyoderma gangrenosum complicating ulcerative colitis. Gut 1995; 37: 585-588.
17. Salas A, Sans M, Soriano A et al., Heparin attenuates TNF-alpha induced inflammatory response through a CD11b dependent mechanism. Gut 2000; 47: 88-96.
18. Lever R, Hoult JR, Page CP. The effects of heparin and related molecules upon the adhesion of human polymorphonuclear leucocytes to vascular endothelium in vitro. Br J Pharmacol 2000; 129: 533-540.
19. Tyrrell DJ, Horne AP, Holme KR, Preus JM, Page CP. Heparin in inflammation: potential therapeutic applications beyond anticoagulation. Adv Pharmacol 1999; 46: 151-208.
20. Lever R, Lo WT, Faraidoun M et al. Size-fractionated heparins have differential effects on human neutrophil function in vitro. Br J Pharmacol 2007; 151: 837-843.
21. Hornebeck W, Lafuma C, Robert L, Moczar M, Moczar E. Heparin and its derivatives modulate serine proteinases (SERPS) serine proteinase inhibitors (SERPINS) balance. Physiopathological relevance. Pathol Res Pract 1994; 190: 895-902.
22. Sissi C, Lucatello L, Naggi A, Torri G, Palumbo M. Interactions of low-molecular-weight semisynthetic sulfated heparins with human leukocyte elastase and human cathepsin G. Biochem Pharmacol 2006; 71: 2887-2893.
23. Ewangelista V, Piccardoni P, Maugeri N, De Gaetano G, Cerletti C. Inhibition by heparin of platelet activation induced by neutrophil-derived cathepsin G. Eur J Pharmacol 1992; 216: 401-405.
24. Dobosz M, Wajda Z, Hac S et al. Heparin and nitric oxide treatment in experimental acute pancreatitis in rats. Forum (Genova) 1998; 8: 303-310.
25. Dobosz M, Mionkowska L, Hac S, Dobrowolski S, Dymeczki D, Wajda Z. Heparin improves organ microcirculatory disturbances in caerulein-induced acute pancreatitis in rats. World J Gastroenterol 2004; 10: 2553-2556.
26. Gabryelewicz A, Niewiarowski S, Prokopowicz J, Chlebowski J. Heparin and protease inhibitors in the prevention of experimental acute pancreatic necrosis in dogs. Digestion 1969; 2: 7-16.
27. Qiu F, Lu XS, Huang YK. Effect of low molecular weight heparin on pancreatic microcirculation in severe acute pancreatitis in a rodent model. Chin Med J 2007; 120: 2260-2263.
28. Rabenstein T, Roggenbuck S, Framke B et al.. Complications of endoscopic sphincterotomy: can heparin prevent acute pancreatitis after ERCP? Gastrointest Endosc 2002; 55: 476-483.
29. Barkay O, Niv E, Santo E, Bruck R, Hallak A, Konikoff FM. Low-dose heparin for the prevention of post-ERCP pancreatitis: a randomized placebo-controlled trial. Surg Endosc 2008; 2(9): 1971-1976.
30. Rabenstein T, Fischer B, Wiessner S et al. Low-molecular-weight heparin does not prevent acute post-ERCP pancreatitis. Gastrointest Endosc 2004; 59: 606-613.
31. Stewart JE, Schotz MC. Release of lipoprotein lipase activity from isolated fat cells. II. Effect of heparin. J Biol Chem 1974; 249: 904-907.
32. Alagözlü H, Cindoruk M, Karakan T, Unal S. Heparin and insulin in the treatment of hypertriglyceridemia-induced severe acute pancreatitis. Dig Dis Sci 2006; 51: 931-933.
33. Kyriakidis AV, Raitsiou B, Sakagianni A et al. Management of acute severe hyperlipidemic pancreatitis. Digestion 2006; 73: 259-264.
34. Jain P, Rai RR, Udawat H, Nijhawan S, Mathur A. Insulin and heparin in treatment of hypertriglyceridemia-induced pancreatitis. World J Gastroenterol 2007; 13: 2642-2643.
35. Eikelboom JW, Hirsh J. Monitoring unfractionated heparin with the aPTT: time for a fresh look. Thromb Haemost 2006; 96: 547-552.
36. Dembinski A, Warzecha Z, Ceranowicz P et al. Pancreatic damage and regeneration in the course of ischemia-induced acute pancreatitis in rats. J Physiol Pharmacol 2001; 52: 221-236.
37. Konturek SJ, Szlachcic A, Dembinski A, Warzecha Z, Jaworek J, Stachura J. Nitric oxide in pancreatic secretion and hormone-induced pancreatitis in rats. Int J Pancreatol 1994; 15: 19-28.
38. Dembinski A, Warzecha Z, Ceranowicz P et al. Effect of ischemic preconditioning on pancreatic regeneration and pancreatic expression of vascular endothelial growth factor and platelet-derived growth factor-A in ischemia/reperfusion-induced pancreatitis. J Physiol Pharmacol 2006; 57: 39-58.
39. Warzecha Z, Dembinski A, Ceranowicz P et al. Influence of ischemic preconditioning on blood coagulation, fibrinolytic activity and pancreatic repair in the course of caerulein-induced acute pancreatitis in rats. J Physiol Pharmacol 2007; 58: 303-319.
40. Warzecha Z, Dembiñski A, Ceranowicz P et al. Immunohistochemical expression of FGF-2, PDGF-A, VEGF and TGF beta RII in the pancreas in the course of ischemia/reperfusion-induced acute pancreatitis. J Physiol Pharmacol 2004; 55: 791-810.
41. Frossard JL, Past CM. Experimental acute pancreatitis: new insight into the pathophysiology. Front Biosci 2002; 7: d275-d287.
42. Norman JG, Fink GW, Denham W et al. Tissue-specific cytokine production during experimental acute pancreatitis. A probable mechanism for distant organ dysfunction. Dig Dis Sci 1997; 42: 1783-1788.
43. Dinarello CA. Interleukin-1 and interleukin-1 antagonism. Blood 1991; 77: 1625-1652.
44. Norman J, Franz M, Messina J et al. Interleukin-1 receptor antagonist decreases severity of experimental acute pancreatitis. Surgery 1995; 117: 648-655.
45. Laghi Pasini F, Pasqui Al, Ceccatelli L, Capecchi PL, Orrico A, Di Perri T. Heparin inhibition of polymorphonuclear leukocyte activation in vitro. A possible pharmacological approach to granulocyte-mediated vascular damage. Thromb Res 1984; 35: 527-537.
46. Brown RA, Lever R, Jones NA, Page CP. Effects of heparin and related molecules upon neutrophil aggregation and elastase release in vitro. Br J Pharmacol 2003; 139: 845-853.
47. Hochart H, Jenkins PV, Smith OP, White B. Low-molecular weight and unfractionated heparins induce a downregulation of inflammation: decreased levels of proinflammatory cytokines and nuclear factor-kappaB in LPS-stimulated human monocytes. Br J Haematol 2006; 133: 62-67.
48. Hecht I, Hershkoviz R, Shivtiel S et al. Heparin-disaccharide affects T cells: inhibition of NFkappaB activation, cell migration, and modulation of intracellular signaling. J Leukoc Biol 2004; 75: 1139-1146.
49. Dervenis C, Johnson CD, Bassi C et al. Diagnosis, objective assessment of severity, and management of acute pancreatitis. Santorini consensus conference. Int J Pancreatol 1999; 25: 195-210.
50. Keck T, Friebe V, Warshaw AL et al. Pancreatic proteases in serum induce leukocyte-endothelial adhesion and pancreatic microcirculatory failure. Pancreatology 2005; 5: 241-250.
51. Vollmar B, Menger MD. Microcirculatory dysfunction in acute pancreatitis. A new concept of pathogenesis involving vasomotion-associated arteriolar constriction and dilation. Pancreatology 2003; 3: 181-190.
52. Tripodi A, Mannucci PM. Markers of activated coagulation and their usefulness in the clinical laboratory. Clin Chem 1996; 42: 664-669.
53. Dembinski A, Warzecha Z, Ceranowicz P et al. Cannabinoids in acute gastric damage and pancreatitis. J Physiol Pharmacol 2006; 57(Suppl 5): 137-154.
54. Dembinski A, Warzecha Z, Ceranowicz P et al. Dual, time-dependent deleterious and protective effect of anandamide on the course of cerulein-induced acute pancreatitis. Role of sensory nerves. Eur J Pharmacol 2008; 591: 284-292.
55. Warzecha Z, Dembinski A, Ceranowicz P et al. Ischemic preconditioning of the hindlimb or kidney does not attenuate the severity of acute ischemia/reperfusion-induced pancreatitis in rats. J Physiol Pharmacol 2008; 59: 337-352.
56. Flint N, Cove FL, Evans GS. Heparin stimulates the proliferation of intestinal epithelial cells in primary culture. J Cell Sci 1994; 107: 401-411.
57. Burgess WH, Maciag T. The heparin-binding (fibroblast) growth factor family of proteins. Annu Rev Biochem 1989; 58: 575-606.
58. 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 2004; 279: 12346-12354.
59. Gitay-Goren H, Soker S, Vlodavski I, Neufeld G. The binding of vascular endothelial growth factor to its receptors is dependent on cell surface-associated heparin-like molecules. J Biol Chem 1992; 267: 6093-6098.
60. Higashiyama S, Abraham JA, Miller J, Fiddes JC, Klagsbrun M. A heparin-binding growth factor secreted by macrophage-like cells that is related to EGF. Science 1991; 251: 936-939.
61. Thompson S.A., Higashiyama S, Wood K et al. Characterization of sequences within heparin-binding EGF-like growth factor that mediate interaction with heparin. J Biol Chem 1994; 269: 2541-2549.
62. Muramatsu T, Muramatsu H. Glycosaminoglycan-binding cytokines as tumor markers. Proteomics 2008; 8: 3350-3359.
63. Rapraeger AC, Krufka A, Olwin BB. Requirement of heparan sulfate for bFGF-mediated fibroblast growth and myoblast differentiation. Science 1991; 252: 1705-1708.
64. Ornitz DM, Leder P. Ligand specificity and heparin dependence of fibroblast growth factor receptors 1 and 3. J Biol Chem 1992; 267: 16305-16311.
65. Kan M, Wang F, Xu J, Crabb JW, Hou J, McKeehan WL. An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science 1993; 259: 1918-1921.
66. Saksela O, Moscatelli D, Sommer A, Rifkin DB. Endothelial cell-derived heparan sulfate binds basic fibroblast growth factor and protects it from proteolytic degradation. J Cell Biol 1988; 107: 743-751.
67. Kiehne K, Otte JM, Folsch UR, Herzig KH. Growth factors in development and diseases of the exocrine pancreas. Pancreatology 2001; 1: 15-23.
68. Menke A, Yamaguchi H, Giehl K, Adler G. Hepatocyte growth factor and fibroblast growth factor 2 are overexpressed after cerulein-induced acute pancreatitis. Pancreas 1999; 18: 28-33.
69. Calvo EL, Bernatchez G, Pelletier G, Iovanna JL, Morisset J. Downregulation of IGF-I mRNA expression during postnatal pancreatic development and overexpression after subtotal pancreatectomy and acute pancreatitis in the rat pancreas. J Mol Endocrinol 1997; 18: 233-242.
70. Friess H, Lu Z, Riesle E et al. Enhanced expression of TGF-betas and their receptors in human acute pancreatitis. Ann Surg 1998; 227: 95-104.
71. Ebert M, Yokoyama M, Ishiwata T et al. Alteration of fibroblast growth factor and receptor expression after acute pancreatitis in humans. Pancreas 1999; 18: 240-246.
72. Warzecha Z, Dembinski A, Konturek PC, Ceranowicz P, Konturek SJ. Epidermal growth factor protects against pancreatic damage in cerulein-induced pancreatitis. Digestion 1999; 60: 314-323.
73. Dembinski A, Warzecha Z, Konturek PC et al. Epidermal growth factor accelerates pancreatic recovery after caerulein-induced pancreatitis. Eur J Pharmacol 2000; 398: 159-168.
74. Tomaszewska R, Dembiñski A, Warzecha Z, Ceranowicz P, Konturek SJ, Stachura J. The influence of epidermal growth factor on the course of ischemia-reperfusion induced pancreatitis in rats. J Physiol Pharmacol 2002; 53: 183-198.
75. Hosokawa M, Tsukada H, Fukuda F et al. Therapeutic effect of basic fibroblast growth factor on experimental pancreatitis in rat. Pancreas 2000; 20: 373-377.
76. Warzecha Z, Dembinski A, Konturek PC et al. Hepatocyte growth factor attenuates pancreatic damage in caerulein-induced pancreatitis in rats. Eur J Pharmacol 2001; 430: 113-121.
77. Warzecha Z, Dembinski A, Ceranowicz P et al. Inhibition of cyclooxygenase-2 reduces the protective effect of hepatocyte growth factor in experimental pancreatitis. Eur J Pharmacol 2004; 486: 107-119.
78. Warzecha Z, Dembinski A, Ceranowicz P et al. IGF-1 stimulates production of interleukin-10 and inhibits development of caerulein-induced pancreatitis. J Physiol Pharmacol 2003; 54: 575-590.
79. Wang X, Wang B, Wu J, Wang G. Beneficial effects of growth hormone on bacterial translocation during the course of acute necrotizing pancreatitis in rats. Pancreas 2001; 23: 148-156.
80. Dembinski A, Warzecha Z, Ceranowicz P et al. Ghrelin attenuates the development of acute pancreatitis in rat. J Physiol Pharmacol 2003; 54: 561-573.
81. Dembinski A, Warzecha Z, Ceranowicz P et al. Role of growth hormone and insulin-like growth factor-1 in the protective effect of ghrelin in ischemia/reperfusion-induced acute pancreatitis. Growth Horm IGF Res 2006; 16: 348-356.
82. Banks PA. Acute pancreatitis: medical and surgical management. Am J Gastroenterol 1994; 89(8 Suppl): S78-S85
83. Carnovale A, Rabitti PG, Manes G, Esposito P, Pacelli L, Uomo G. Mortality in acute pancreatitis: is it an early or a late event? JOP 2005; 6: 438-444.
84. Fu CY, Yeh CN, Hsu JT, Jan YY, Hwang TL. Timing of mortality in severe acute pancreatitis: experience from 643 patients. World J Gastroenterol 2007; 13: 1966-1969.
85. Takahashi H, Tsuda Y, Kobayashi M, Herndon DN, Suzuki F. CCL2 as a trigger of manifestations of compensatory anti-inflammatory response syndrome in mice with severe systemic inflammatory response syndrome. J Leukoc Biol 2006; 79: 789-796.