Helicobacter pylori urease activates blood platelets through a lipoxygenase-mediated pathway

Journal of Cellular and Molecular Medicine

Volumn 14, Issue 7, 2010, Pages 2025-2034

  Wassermann, German E ^a   Olivera Severo, Deiber ^a   Uberti, Augusto F ^a   Carlini, Célia R ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Eicosanoids; Helicobacter pylori; Lipoxygenase; Platelet activation; Urease

Indexed keywords

LIPOXYGENASE; UREASE;

ARTICLE; ENZYMOLOGY; HELICOBACTER PYLORI; HUMAN; METABOLISM; PHYSIOLOGY; THROMBOCYTE ACTIVATION;

HELICOBACTER PYLORI; HUMANS; LIPOXYGENASES; PLATELET ACTIVATION; UREASE;

BACTERIA (MICROORGANISMS); CANAVALIA; GLYCINE MAX; HELICOBACTER PYLORI; ORYCTOLAGUS CUNICULUS; SPOROSARCINA PASTEURII;

EID: 77955171796     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2009.00901.x     Document Type: Article

References (52)

1. Dixon NE, Gazzola C, Blakeley RL. Jack bean urease (EC 3.5.1.5): a metalloenzyme. A simple biological role for nickel. J Amer Chem Soc. 1975, 97:4131-3.
2. Mobley HL, Island MD, Hausinger RP. Molecular biology of microbial ureases. Microbiol Rev. 1995, 59:451-80.
3. Follmer C. Insights into the role and structure of plant ureases. Phytochemistry. 2008, 69:18-28.
4. Sirko A, Brodzik R. Plant ureases: roles and regulation. Acta Biochim Pol. 2000, 47:1189-95.
5. Carlini CR, Polacco JC. Toxic properties of urease. Crop Sci. 2008, 48:1665-72.
6. Fischbach W, Chan AOO, Wong BCY. Helicobacter pylori and gastric malignancy. Helicobacter. 2005, 10:34-9.
7. Suzuki H, Marshall BJ, Hibi T. Overview: Helicobacter pylori and Extragastric Disease. Int J Hematol. 2006, 84:291-300.
8. Clyne M, Dolan B, Reeves EP. Bacterial factors that mediate colonization of the stomach and virulence of Helicobacter pylori. FEMS Microbiol Lett. 2007, 268:135-43.
9. Franco AT, Johnston E, Krishna U. Regulation of gastric carcinogenesis by helicobacter pylori virulence factors. Cancer Res. 2008, 68:379-87.
10. Suzuki H, Hibi T, Marshall BJ. Helicobacter pylori: present status and future prospects in Japan. J Gastroenterol 2007, 42:1-15.
11. Becker-Ritt AB, Martinelli AHS, Mitidieri S. Antifungal activity of plant and bacterial ureases. Toxicon. 2007, 50:971-83.
12. Carlini CR, Grossi-de-Sa MF. Plant toxic proteins with insecticidal properties. A review on their potentialities as bioinsecticides. Toxicon. 2002, 40:1515-39.
13. Follmer C, Real-Guerra R, Wasserman GE. Jackbean, soybean and Bacillus pasteurii ureases - Biological effects unrelated to ureolytic activity. Eur J Biochem. 2004, 271:1357-63.
14. Ferreira-DaSilva CT, Gombarovits MEC, Masuda H. Proteolytic activation of canatoxin, a plant toxic protein, by insect cathepsin-like enzymes. Arch Insect Biochem Physiol. 2000, 44:162-71.
15. Mulinari F, Staniscuaski F, Bertholdo-Vargas LR. Jaburetox-2Ec: an insecticidal peptide derived from an isoform of urease from the plant Canavalia ensiformis. Peptides. 2007, 28:2042-50.
16. Carlini CR, Guimaraes JA. Isolation and characterization of a toxic protein from Canavalia ensiformis (jack bean) seeds, distinct from concanavalin A. Toxicon. 1981, 19:667-75.
17. Follmer C, Barcellos GBS, Zingali RB. Canatoxin, a toxic protein from jack beans (Canavalia ensiformis), is a variant form of urease (EC 3.5.1.5): biological effects of urease independent of its ureolytic activity. Biochem J. 2001, 360:217-24.
18. Carlini CR, Guimaraes JA, Ribeiro JM. Platelet release reaction and aggregation induced by canatoxin, a convulsant protein: evidence for the involvement of the platelet lipoxygenase pathway. Br J Pharmacol. 1985, 84:551-60.
19. Barja-Fidalgo C, Guimaraes JA, Carlini CR. Lipoxygenase-mediated secretory effect of canatoxin, the toxic protein from Canavalia ensiformis seeds. Toxicon. 1991, 29:453-60.
20. Ghazaleh FA, Francischetti IM, Gombarovits ME. Stimulation of calcium influx and platelet activation by canatoxin: methoxyverapamil inhibition and downregulation by cGMP. Arch Biochem Biophys. 1997, 339:362-7.
21. Benjamin CF, Carlini CR, Barja-Fidalgo C. Pharmacological characterization of rat paw edema induced by canatoxin, the toxic protein from Canavalia ensiformis (jack bean) seeds. Toxicon. 1992, 30:879-85.
22. Barja-Fidalgo C, Guimaraes JA, Carlini CR. Canatoxin, a plant protein, induces insulin release from isolated pancreatic islets. Endocrinology. 1991, 128:675-9.
23. Olivera-Severo D, Wasserman GE, Carlini CR. Ureases display biological effects independent of enzymatic activity. Is there a connection to diseases caused by urease-producing bacteria. Braz J Med Biol Res. 2006, 39:851-61.
24. Alves EW, Ferreira AT, Ferreira CT. Effects of canatoxin on the Ca(2+)-ATPase of sarcoplasmic reticulum membranes. Toxicon. 1992, 30:1411-8.
25. Olivera-Severo D, Wassermann GE, Carlini CR. Bacillus pasteurii urease shares with plant ureases the ability to induce aggregation of blood platelets. Arch Biochem Biophys. 2006, 452:149-55.
26. Andrews RK, Gardiner EE, Shen Y. Platelet interactions in thrombosis. IUBMB Life. 2004, 56:13-8.
27. Ruggeri ZM, Mendolicchio GL. Adhesion mechanisms in platelet function. Circulation Res. 2007, 100:1673-85.
28. Gachet C, Hechler B, Leon C. Activation of ADP receptors and platelet function. Thromb Haemost. 1997, 78:271-5.
29. Belville JS, Bennett WF, Lynch G. A method for investigating the role of calcium in the shape change, aggregation and serotonin release of rat platelets. J Physiol. 1979, 297:289-97.
30. Blache D, Ciavatti M, Ojeda C. The effect of calcium channel blockers on blood platelet function especially calcium uptake. Biochim Biophys Acta. 1987, 923:401-12.
31. Moncada S, Vane JR. Arachidonic-acid metabolites and the interactions between platelets and blood-vessel walls. N Eng J Med. 1979, 300:1142-7.
32. Hawiger J. Mechanisms involved in platelet-vessel wall interaction. Thromb Haemost. 1995, 74:369-72.
33. Benveniste J, Chignard M, Lecouedic JP. Biosynthesis of Platelet-Activating Factor (Paf-acether) .2. Involvement of phospholipase-A2 in the formation of Paf-acether and lyso-Paf-acether from rabbit platelets. Thromb Res. 1982, 25:375-85.
34. McGee DJ, May CA, Garner RM. Isolation of Helicobacter pylori genes that modulate urease activity. J Bacteriol. 1999, 181:2477-84.
35. Weatherburn MW. Phenol-hypochlorite reaction for determination of ammonia. Anal Chem. 1967, 39:971-4.
36. Francischetti IMB, Ribeiro JMC, Champagne D. Purification, cloning, expression, and mechanism of action of a novel platelet aggregation inhibitor from the salivary gland of the blood-sucking bug, Rhodnius prolixus. J Biol Chem. 2000, 275:12639-50.
37. Coffey MJ, Jarvis GE, Gibbins JM. Platelet 12-lipoxygenase activation via glycoprotein VI - involvement of multiple signaling pathways in agonist control of H(P)ETE synthesis. Circulation Res. 2004, 94:1598-605.
38. Sekiya K, Okuda H, Arichi S. Selective inhibition of platelet lipoxygenase by esculetin. Biochim Biophys Acta. 1982, 713:68-72.
39. Kalvegren H, Andersson J, Grenegard M. Platelet activation triggered by Chlamydia pneumoniae is antagonized by 12-lipoxygenase inhibitors but not cyclooxygenase inhibitors. Eur J Pharmacol. 2007, 566:20-7.
40. Coffey MJ, Coles B, Locke M. Interactions of 12-lipoxygenase with phospholipase A(2) isoforms following platelet activation through the glycoprotein VI collagen receptor. FEBS Lett. 2004, 576:165-8.
41. Gawaz M, Langer H, May AE. Platelets in inflammation and atherogenesis. J Clin Invest. 2005, 115:3378-84.
42. Tobin NP, Henehan GT, Murphy RP. Helicobacter pylori-induced inhibition of vascular endothelial cell functions: a role for VacA-dependent nitric oxide reduction. Am J Physiol-Heart C. 2008, 295:H1403-13.
43. Manolakis A, Kapsoritakis AN, Potamianos SP. A review of the postulated mechanisms concerning the association of Helicobacter pylori with ischemic heart disease. Helicobacter. 2007, 12:287-97.
44. Corcoran PA, Atherton JC, Kerrigan SW. The effect of different strains of Helicobacter pylori on platelet aggregation. Can J Gastroenterol. 2007, 21:367-70.
45. Suzuki H, Mori M, Seto K. Polaprezinc attenuates the Helicobacter pylori-induced gastric mucosal leucocyte activation in Mongolian gerbils - a study using intravital videomicroscopy. Aliment Pharmacol Ther. 2001, 15:715-25.
46. Kalia N, Bardhan KD. Of blood and guts: association between Helicobacter pylori and the gastric microcirculation. J Gastroenterol Hepatol. 2003, 18:1010-7.
47. Byrne MF, Kerrigan SW, Corcoran PA. Helicobacter pylori binds von Willebrand factor and interacts with GPlb to induce platelet aggregation. Gastroenterology. 2003, 124:1846-54.
48. Wroblewski LE, Shen L, Ogden S. Helicobacter pylori dysregulation of gastric epithelial tight junctions by urease-mediated myosin II activation. Gastroenterology. 2009, 136:236-46.
49. Montecucco C, Papini E, de Bernard M. Molecular and cellular activities of Helicobacter pylori pathogenic factors. FEBS Lett. 1999, 452:16-21.
50. Icatlo FC, Goshima H, Kimura N. Acid-dependent adherence of Helicobacter pylori urease to diverse polysaccharides. Gastroenterology. 2000, 119:358-67.
51. Gobert AP, Mersey BD, Cheng YL. Cutting edge: urease release by Helicobacter pylori stimulates macrophage inducible nitric oxide synthase. J Immunol. 2002, 168:6002-6.
52. Harris PR, Mobley HL, Perez-Perez GI. Helicobacter pylori urease is a potent stimulus of mononuclear phagocyte activation and inflammatory cytokine production. Gastroenterology. 1996, 111:419-25.