Polyphosphate, Zn2+ and high molecular weight kininogen modulate individual reactions of the contact pathway of blood clotting
dc.contributor.author | Wang, Yuqi | |
dc.contributor.author | Ivanov, Ivan | |
dc.contributor.author | Smith, Stephanie A. | |
dc.contributor.author | Gailani, David | |
dc.contributor.author | Morrissey, James H. | |
dc.date.accessioned | 2020-01-13T15:14:43Z | |
dc.date.available | WITHHELD_12_MONTHS | |
dc.date.available | 2020-01-13T15:14:43Z | |
dc.date.issued | 2019-12 | |
dc.identifier.citation | Wang, Yuqi; Ivanov, Ivan; Smith, Stephanie A.; Gailani, David; Morrissey, James H. (2019). "Polyphosphate, Zn2+ and high molecular weight kininogen modulate individual reactions of the contact pathway of blood clotting." Journal of Thrombosis and Haemostasis 17(12): 2131-2140. | |
dc.identifier.issn | 1538-7933 | |
dc.identifier.issn | 1538-7836 | |
dc.identifier.uri | https://hdl.handle.net/2027.42/152988 | |
dc.description.abstract | BackgroundInorganic polyphosphate modulates the contact pathway of blood clotting, which is implicated in thrombosis and inflammation. Polyphosphate polymer lengths are highly variable, with shorter polymers (approximately 60‐100 phosphates) secreted from human platelets, and longer polymers (up to thousands of phosphates) in microbes. We previously reported that optimal triggering of clotting via the contact pathway requires very long polyphosphates, although the impact of shorter polyphosphate polymers on individual proteolytic reactions of the contact pathway was not interrogated.Objectives and methodsWe conducted in vitro measurements of enzyme kinetics to investigate the ability of varying polyphosphate sizes, together with high molecular weight kininogen and Zn2+, to mediate four individual proteolytic reactions of the contact pathway: factor XII autoactivation, factor XII activation by kallikrein, prekallikrein activation by factor XIIa, and prekallikrein autoactivation.ResultsThe individual contact pathway reactions were differentially dependent on polyphosphate length. Very long‐chain polyphosphate was required to support factor XII autoactivation, whereas platelet‐size polyphosphate significantly accelerated the activation of factor XII by kallikrein, and the activation of prekallikrein by factor XIIa. Intriguingly, polyphosphate did not support prekallikrein autoactivation. We also report that high molecular weight kininogen was required only when kallikrein was the enzyme (ie, FXII activation by kallikrein), whereas Zn2+ was required only when FXII was the substrate (ie, FXII activation by either kallikrein or FXIIa). Activation of prekallikrein by FXIIa required neither Zn2+ nor high molecular weight kininogen.ConclusionsPlatelet polyphosphate and Zn2+ can promote subsets of the reactions of the contact pathway, with implications for a variety of disease states. | |
dc.publisher | Wiley Periodicals, Inc. | |
dc.subject.other | blood coagulation factors | |
dc.subject.other | thrombosis | |
dc.subject.other | prekallikrein | |
dc.subject.other | polyphosphates | |
dc.subject.other | zinc | |
dc.title | Polyphosphate, Zn2+ and high molecular weight kininogen modulate individual reactions of the contact pathway of blood clotting | |
dc.type | Article | |
dc.rights.robots | IndexNoFollow | |
dc.subject.hlbsecondlevel | Internal Medicine and Specialties | |
dc.subject.hlbtoplevel | Health Sciences | |
dc.description.peerreviewed | Peer Reviewed | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/152988/1/jth14612_am.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/152988/2/jth14612-sup-0001-FigS1-S5.pdf | |
dc.description.bitstreamurl | https://deepblue.lib.umich.edu/bitstream/2027.42/152988/3/jth14612.pdf | |
dc.identifier.doi | 10.1111/jth.14612 | |
dc.identifier.source | Journal of Thrombosis and Haemostasis | |
dc.identifier.citedreference | Bernardo MM, Day DE, Halvorson HR, Olson ST, Shore JD. Surface‐independent acceleration of factor XII activation by zinc ions. II. Direct binding and fluorescence studies. J Biol Chem. 1993; 268: 12477 – 12483. | |
dc.identifier.citedreference | Hojima Y, Pierce JV, Pisano JJ. Plant inhibitors of serine proteinases: Hageman factor fragment, kallikreins, plasmin, thrombin, factor Xa, trypsin, and chymotrypsin. Thromb Res. 1980; 20: 163 – 171. | |
dc.identifier.citedreference | Chong GL, Reeck GR. Interaction of trypsin, beta‐factor XIIa, and plasma kallikrein with a trypsin inhibitor isolated from barley seeds: a comparison with the corn inhibitor of activated Hageman factor. Thromb Res. 1987; 48: 211 – 221. | |
dc.identifier.citedreference | Smith SA, Mutch NJ, Baskar D, Rohloff P, Docampo R, Morrissey JH. Polyphosphate modulates blood coagulation and fibrinolysis. Proc Natl Acad Sci USA. 2006; 103: 903 – 908. | |
dc.identifier.citedreference | Smith SA, Gajsiewicz JM, Morrissey JH. Ability of polyphosphate and nucleic acids to trigger blood clotting: some observations and caveats. Front Med. 2018; 5: 107. | |
dc.identifier.citedreference | Verhoef JJ, Barendrecht AD, Nickel KF, et al. Polyphosphate nanoparticles on the platelet surface trigger contact system activation. Blood. 2017; 129: 1707 – 1717. | |
dc.identifier.citedreference | Caen J, Wu Q. Hageman factor, platelets and polyphosphates: early history and recent connection. J Thromb Haemost. 2010; 8: 1670 – 1674. | |
dc.identifier.citedreference | Erickson HP. Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy. Biol Proced Online. 2009; 11: 32 – 51. | |
dc.identifier.citedreference | Bolesch DG, Keasling JD. Polyphosphate binding and chain length recognition of Escherichia coli exopolyphosphatase. J Biol Chem. 2000; 275: 33814 – 33819. | |
dc.identifier.citedreference | Gansler J, Jaax M, Leiting S, et al. Structural requirements for the procoagulant activity of nucleic acids. PLoS ONE. 2012; 7: e50399. | |
dc.identifier.citedreference | Stavrou E, Schmaier AH. Factor XII: what does it contribute to our understanding of the physiology and pathophysiology of hemostasis & thrombosis. Thromb Res. 2010; 125: 210 – 215. | |
dc.identifier.citedreference | Vu TT, Fredenburgh JC, Weitz JI. Zinc: an important cofactor in haemostasis and thrombosis. Thromb Haemost. 2013; 109: 421 – 430. | |
dc.identifier.citedreference | Herwald H, Morgelin M, Svensson HG, Sjöbring U. Zinc‐dependent conformational changes in domain D5 of high molecular mass kininogen modulate contact activation. Eur J Biochem. 2001; 268: 396 – 404. | |
dc.identifier.citedreference | Hasan AA, Cines DB, Herwald H, Schmaier AH, Muller‐Esterl W. Mapping the cell binding site on high molecular weight kininogen domain 5. J Biol Chem. 1995; 270: 19256 – 19261. | |
dc.identifier.citedreference | DeLa Cadena RA, Colman RW. The sequence HGLGHGHEQQHGLGHGH in the light chain of high molecular weight kininogen serves as a primary structural feature for zinc‐dependent binding to an anionic surface. Protein Sci. 1992; 1: 151 – 160. | |
dc.identifier.citedreference | Gajsiewicz JM, Smith SA, Morrissey JH. Polyphosphate and RNA differentially modulate the contact pathway of blood clotting. J Biol Chem. 2017; 292: 1808 – 1814. | |
dc.identifier.citedreference | Kleniewski J. Plasma high molecular weight kininogen concentration in health and in chosen impairments of haemostasis. Evidence that plasmin uncovers a new antigenic site in high molecular weight kininogen. Thromb Haemost. 1979; 42: 1046 – 1055. | |
dc.identifier.citedreference | Moreno‐Sanchez D, Hernandez‐Ruiz L, Ruiz FA, Docampo R. Polyphosphate is a novel pro‐inflammatory regulator of mast cells and is located in acidocalcisomes. J Biol Chem. 2012; 287: 28435 – 28444. | |
dc.identifier.citedreference | Kumble KD, Kornberg A. Inorganic polyphosphate in mammalian cells and tissues. J Biol Chem. 1995; 270: 5818 – 5822. | |
dc.identifier.citedreference | Marx G, Korner G, Mou X, Gorodetsky R. Packaging zinc, fibrinogen, and factor XIII in platelet a‐granules. J Cell Physiol. 1993; 156: 437 – 442. | |
dc.identifier.citedreference | Schmaier AH. Plasma prekallikrein: its role in hereditary angioedema and health and disease. Front Med. 2018; 5: 3. | |
dc.identifier.citedreference | Shariat‐Madar Z, Mahdi F, Schmaier AH. Recombinant prolylcarboxypeptidase activates plasma prekallikrein. Blood. 2004; 103: 4554 – 4561. | |
dc.identifier.citedreference | Moreira CR, Schmaier AH, Mahdi F, da Motta G, Nader HB, Shariat‐Madar Z. Identification of prolylcarboxypeptidase as the cell matrix‐associated prekallikrein activator. FEBS Lett. 2002; 523: 167 – 170. | |
dc.identifier.citedreference | Brown MR, Kornberg A. The long and short of it – polyphosphate, PPK and bacterial survival. Trends Biochem Sci. 2008; 33: 284 – 290. | |
dc.identifier.citedreference | Wu Y. Contact pathway of coagulation and inflammation. Thromb J. 2015; 13: 17. | |
dc.identifier.citedreference | Schmaier AH. The contact activation and kallikrein/kinin systems: pathophysiologic and physiologic activities. J Thromb Haemost. 2016; 14: 28 – 39. | |
dc.identifier.citedreference | Griffin JH. Role of surface in surface‐dependent activation of Hageman factor (blood coagulation factor XII). Proc Natl Acad Sci USA. 1978; 75: 1998 – 2002. | |
dc.identifier.citedreference | Samuel M, Pixley RA, Villanueva MA, Colman RW, Villanueva GB. Human factor XII (Hageman factor) autoactivation by dextran sulfate. Circular dichroism, fluorescence, and ultraviolet difference spectroscopic studies. J Biol Chem. 1992; 267: 19691 – 19697. | |
dc.identifier.citedreference | Long AT, Kenne E, Jung R, Fuchs TA, Renné T. Contact system revisited: an interface between inflammation, coagulation, and innate immunity. J Thromb Haemost. 2016; 14: 427 – 437. | |
dc.identifier.citedreference | Tans G, Rosing J, Berrettini M, Lämmle B, Griffin JH. Autoactivation of human plasma prekallikrein. J Biol Chem. 1987; 262: 11308 – 11314. | |
dc.identifier.citedreference | Bouma BN, Griffin JH. Human blood coagulation factor XI. Purification, properties, and mechanism of activation by activated factor XII. J Biol Chem. 1977; 252: 6432 – 6437. | |
dc.identifier.citedreference | Schulze‐Topphoff U, Prat A, Bader M, Zipp F, Aktas O. Roles of the kallikrein/kinin system in the adaptive immune system. Int Immunopharmacol. 2008; 8: 155 – 160. | |
dc.identifier.citedreference | Foley JH, Conway EM. Cross talk pathways between coagulation and inflammation. Circul Res. 2016; 118: 1392 – 1408. | |
dc.identifier.citedreference | Ratnoff OD, Colopy JE. A familial hemorrhagic trait associated with a deficiency of a clot‐promoting fraction of plasma. J Clin Invest. 1955; 34: 602 – 613. | |
dc.identifier.citedreference | Lämmle B, Wuillemin WA, Huber I, et al. Thromboembolism and bleeding tendency in congenital factor XII deficiency–a study on 74 subjects from 14 Swiss families. Thromb Haemost. 1991; 65: 117 – 121. | |
dc.identifier.citedreference | Kokoye Y, Ivanov I, Cheng Q, et al. A comparison of the effects of factor XII deficiency and prekallikrein deficiency on thrombus formation. Thromb Res. 2016; 140: 118 – 124. | |
dc.identifier.citedreference | Renné T, Pozgajová M, Grüner S, et al. Defective thrombus formation in mice lacking coagulation factor XII. J Exp Med. 2005; 202: 271 – 281. | |
dc.identifier.citedreference | Revenko AS, Gao D, Crosby JR, et al. Selective depletion of plasma prekallikrein or coagulation factor XII inhibits thrombosis in mice without increased risk of bleeding. Blood. 2011; 118: 5302 – 5311. | |
dc.identifier.citedreference | Kleinschnitz C, Stoll G, Bendszus M, et al. Targeting coagulation factor XII provides protection from pathological thrombosis in cerebral ischemia without interfering with hemostasis. J Exp Med. 2006; 203: 513 – 518. | |
dc.identifier.citedreference | Matafonov A, Leung PY, Gailani AE, et al. XII inhibition reduces thrombus formation in a primate thrombosis model. Blood. 2014; 123: 1739 – 1746. | |
dc.identifier.citedreference | Cheng Q, Tucker EI, Pine MS, et al. A role for factor XIIa‐mediated factor XI activation in thrombus formation in vivo. Blood. 2010; 116: 3981 – 3989. | |
dc.identifier.citedreference | Smith SA, Choi SH, Davis‐Harrison R, et al. Polyphosphate exerts differential effects on blood clotting, depending on polymer size. Blood. 2010; 116: 4353 – 4359. | |
dc.identifier.citedreference | Ruiz FA, Lea CR, Oldfield E, Docampo R. Human platelet dense granules contain polyphosphate and are similar to acidocalcisomes of bacteria and unicellular eukaryotes. J Biol Chem. 2004; 279: 44250 – 44257. | |
dc.identifier.citedreference | Brown MR, Kornberg A. Inorganic polyphosphate in the origin and survival of species. Proc Natl Acad Sci USA. 2004; 101: 16085 – 16087. | |
dc.identifier.citedreference | Kornberg A, Rao NN, Ault‐Riché D. Inorganic polyphosphate: a molecule of many functions. Annu Rev Biochem. 1999; 68: 89 – 125. | |
dc.identifier.citedreference | Morrissey JH. Polyphosphate: a link between platelets, coagulation and inflammation. Int J Hematol. 2012; 95: 346 – 352. | |
dc.identifier.citedreference | Smith SA, Baker CJ, Gajsiewicz JM, Morrissey JH. Silica particles contribute to the procoagulant activity of DNA and polyphosphate isolated using commercial kits. Blood. 2017; 130: 88 – 91. | |
dc.identifier.citedreference | Smith SA, Morrissey JH. Sensitive fluorescence detection of polyphosphate in polyacrylamide gels using 4′,6‐diamidino‐2‐phenylindol. Electrophoresis. 2007; 28: 3461 – 3465. | |
dc.identifier.citedreference | Levison PR, Tomalin G. Studies on the temperature‐dependent autoinhibition of human plasma kallikrein I. Biochem J. 1982; 205: 529 – 534. | |
dc.identifier.citedreference | Ivanov I, Matafonov A, Sun MF, et al. Proteolytic properties of single‐chain factor XII: a mechanism for triggering contact activation. Blood. 2017; 129: 1527 – 1537. | |
dc.identifier.citedreference | Chung DW, Fujikawa K, McMullen BA, Davie EW. Human plasma prekallikrein, a zymogen to a serine protease that contains four tandem repeats. Biochemistry. 1986; 25: 2410 – 2417. | |
dc.identifier.citedreference | Wallisch M, Tucker EI, Lorentz CU, et al. The anti‐factor XII antibody AB052 is antithrombotic without hemostatic impairment in a primate model of extracorporeal membrane oxygenation. Blood. 2017; 130: 236. | |
dc.identifier.citedreference | Røjkjaer R, Schousboe I. The surface‐dependent autoactivation mechanism of factor XII. Eur J Biochem. 1997; 243: 160 – 166. | |
dc.identifier.citedreference | Wu JW, Wu Y, Wang ZX. Kinetic analysis of a simplified scheme of autocatalytic zymogen activation. Eur J Biochem. 2001; 268: 1547 – 1553. | |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.