Modulation of the Plasma Kallikrein-Kinin System Proteins Performed by Heparan Sulfate Proteoglycans

Overview

Journal Front Physiol

Date 2017 Jul 27

PMID 28744223

Citations 9

Authors

Guacyara Motta

Ivarne L S Tersariol

Affiliations

Soon will be listed here.

Abstract

Human plasma kallikrein-kinin system proteins are related to inflammation through bradykinin. In the proximity of its target cells, high molecular weight kininogen (H-kininogen) is the substrate of plasma kallikrein, which releases bradykinin from H-kininogen. Heparan sulfate proteoglycans (HSPGs) play a critical role in either recruiting kinin precursors from the plasma, or in the assembly of kallikrein-kinin system components on the cell surface. Furthermore, HSPGs mediate the endocytosis and activation of H-kininogen and plasma prekallikrein. In the presence of HSPGs (Chinese hamster ovary cell, CHO-K1, wild type cells) both heparin and heparan sulfate strongly inhibit the H-kininogen interaction with the cell membrane. H-kininogen is internalized in endosomal acidic vesicles in CHO-K1 but not in CHO-745 cells (mutant cells deficient in glycosaminoglycan biosynthesis). The endocytosis process is lipid raft-mediated and is dependent on caveolae. Both types of CHO cells do not internalize bradykinin-free H-kininogen. At pH 7.35, bradykinin is released from H-kininogen on the surface of CHO-745 cells only by serine proteases; however, in CHO-K1 cells either serine or cysteine proteases are found to be involved. The CHO-K1 cell lysate contains different kininogenases. Plasma prekallikrein endocytosis in CHO-K1 cells is independent of H-kininogen, and also prekallikrein is not internalized by CHO-745 cells. Plasma prekallikrein cleavage/activation is independent of glycosaminoglycans but plasma kallikrein formation is more specific on H-kininogen assembled on the cell surface through glycosaminoglycans. In this mini-review, the importance of HSPGs in the regulation of plasma kallikrein-kinin system proteins is shown.

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References

ROCHA e SILVA M, BERALDO W, ROSENFELD G . Bradykinin, a hypotensive and smooth muscle stimulating factor released from plasma globulin by snake venoms and by trypsin. Am J Physiol. 1949; 156(2):261-73. DOI: 10.1152/ajplegacy.1949.156.2.261. View

Niemann C, Abrink M, Pejler G, Fischer R, Christensen E, Knight S . Neutrophil elastase depends on serglycin proteoglycan for localization in granules. Blood. 2007; 109(10):4478-86. DOI: 10.1182/blood-2006-02-001719. View

Lalmanach G, Naudin C, Lecaille F, Fritz H . Kininogens: More than cysteine protease inhibitors and kinin precursors. Biochimie. 2010; 92(11):1568-79. DOI: 10.1016/j.biochi.2010.03.011. View

Gozzo A, Motta G, Cruz-Silva I, Nunes V, Barros N, Carmona A . Heparin affects the interaction of kininogen on endothelial cells. Biochimie. 2011; 93(10):1839-45. DOI: 10.1016/j.biochi.2011.07.003. View

Kainulainen V, Wang H, Schick C, Bernfield M . Syndecans, heparan sulfate proteoglycans, maintain the proteolytic balance of acute wound fluids. J Biol Chem. 1998; 273(19):11563-9. DOI: 10.1074/jbc.273.19.11563. View

Li Y, Sun C, Yates E, Jiang C, Wilkinson M, Fernig D . Heparin binding preference and structures in the fibroblast growth factor family parallel their evolutionary diversification. Open Biol. 2016; 6(3). PMC: 4821243. DOI: 10.1098/rsob.150275. View

Page J, Colman R . Localization of distinct functional domains on prekallikrein for interaction with both high molecular weight kininogen and activated factor XII in a 28-kDa fragment (amino acids 141-371). J Biol Chem. 1991; 266(13):8143-8. View

Kaplan A . The bradykinin-forming cascade: a historical perspective. Chem Immunol Allergy. 2014; 100:205-13. DOI: 10.1159/000358739. View

Nunes G, Simoes A, Dyszy F, Shida C, Juliano M, Juliano L . Mechanism of heparin acceleration of tissue inhibitor of metalloproteases-1 (TIMP-1) degradation by the human neutrophil elastase. PLoS One. 2011; 6(6):e21525. PMC: 3121799. DOI: 10.1371/journal.pone.0021525. View

10.

Alvarez-Sabin J, Delgado P, Abilleira S, Molina C, Arenillas J, Ribo M . Temporal profile of matrix metalloproteinases and their inhibitors after spontaneous intracerebral hemorrhage: relationship to clinical and radiological outcome. Stroke. 2004; 35(6):1316-22. DOI: 10.1161/01.STR.0000126827.69286.90. View

11.

Couture R, Blaes N, Girolami J . Kinin receptors in vascular biology and pathology. Curr Vasc Pharmacol. 2014; 12(2):223-48. DOI: 10.2174/1570161112666140226121627. View

12.

Renne T, Muller-Esterl W . Cell surface-associated chondroitin sulfate proteoglycans bind contact phase factor H-kininogen. FEBS Lett. 2001; 500(1-2):36-40. DOI: 10.1016/s0014-5793(01)02570-4. View

13.

Stuardo M, Gonzalez C, Nualart F, Boric M, Corthorn J, Bhoola K . Stimulated human neutrophils form biologically active kinin peptides from high and low molecular weight kininogens. J Leukoc Biol. 2004; 75(4):631-40. DOI: 10.1189/jlb.1103546. View

14.

Rajgopal R, Bear M, Butcher M, Shaughnessy S . The effects of heparin and low molecular weight heparins on bone. Thromb Res. 2007; 122(3):293-8. DOI: 10.1016/j.thromres.2006.10.025. View

15.

Kolte D, Shariat-Madar Z . Plasma Kallikrein Inhibitors in Cardiovascular Disease: An Innovative Therapeutic Approach. Cardiol Rev. 2015; 24(3):99-109. DOI: 10.1097/CRD.0000000000000069. View

16.

Barros N, Puzer L, Tersariol I, Oliva M, Sampaio C, Carmona A . Plasma prekallikrein/kallikrein processing by lysosomal cysteine proteases. Biol Chem. 2004; 385(11):1087-91. DOI: 10.1515/BC.2004.141. View

17.

Bord S, Horner A, Hembry R, Reynolds J, Compston J . Distribution of matrix metalloproteinases and their inhibitor, TIMP-1, in developing human osteophytic bone. J Anat. 1997; 191 ( Pt 1):39-48. PMC: 1467657. DOI: 10.1046/j.1469-7580.1997.19110039.x. View

18.

Iozzo R, Cohen I, Grassel S, Murdoch A . The biology of perlecan: the multifaceted heparan sulphate proteoglycan of basement membranes and pericellular matrices. Biochem J. 1994; 302 ( Pt 3):625-39. PMC: 1137278. DOI: 10.1042/bj3020625. View

19.

Sahoo M, Del Barrio L, Miller M, Re F . Neutrophil elastase causes tissue damage that decreases host tolerance to lung infection with burkholderia species. PLoS Pathog. 2014; 10(8):e1004327. PMC: 4148436. DOI: 10.1371/journal.ppat.1004327. View

20.

Renne T, Dedio J, David G, Muller-Esterl W . High molecular weight kininogen utilizes heparan sulfate proteoglycans for accumulation on endothelial cells. J Biol Chem. 2000; 275(43):33688-96. DOI: 10.1074/jbc.M000313200. View