Volume 20 Issue 12
Dec.  2022
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WANG Li-yao, WANG Bing-kun, LI Wen, A-RI-FU A-yi-mai-li-ka, BAI Tian-yu, XU Meng, SU Li-bo. Advances in pathogenesis of protein disulfide isomerase in thrombotic disease[J]. Chinese Journal of General Practice, 2022, 20(12): 2114-2118. doi: 10.16766/j.cnki.issn.1674-4152.002782
Citation: WANG Li-yao, WANG Bing-kun, LI Wen, A-RI-FU A-yi-mai-li-ka, BAI Tian-yu, XU Meng, SU Li-bo. Advances in pathogenesis of protein disulfide isomerase in thrombotic disease[J]. Chinese Journal of General Practice, 2022, 20(12): 2114-2118. doi: 10.16766/j.cnki.issn.1674-4152.002782

Advances in pathogenesis of protein disulfide isomerase in thrombotic disease

doi: 10.16766/j.cnki.issn.1674-4152.002782
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 BJ2019026

  • Received Date: 2022-06-08
    Available Online: 2023-02-07
  • Protein disulfide isomerase (PDI), the prototypical member of the PDI family, is encoded by the prolyl 4-hydroxylase subunit beta (P4HB) gene and is the β subunit of the P4H protein, so it is also called P4HB. It is mainly found in the endoplasmic reticulum (ER) and plays an important role in pathophysiological processes by promoting correct protein folding through enzymatic activity and molecular chaperone function. Related studies on PDI in China and abroad have explored the mechanisms of action in diseases, such as cancer and neurodegenerative diseases. In addition to its key role in ER, the role of cell surface PDI in initiating the thrombosis process is particularly prominent. PDI can be rapidly secreted from activated platelets and endothelial cells at the site of vascular injury to promote platelet activation and fibrin formation and mediate the activation of coagulation factor, its release and the coagulation pathway. Inhibition of PDI with antibodies or small-molecule inhibitors may prevent thrombosis. Given the important role of extracellular PDI in the regulation of thrombosis, scholars should aim to understand the pathogenic mechanism of PDI thrombotic disease. Efforts are ongoing to identify extracellular PDI substrates that participate in the network pathway between PDI and thrombosis. In this paper, we summarise our current understanding of the mechanism of PDI-mediated thrombosis, discusses the research progress in blocking thrombosis by targeted PDI and provide new ideas for further exploration of the application of this substance in the prevention and treatment of thrombotic diseases.

     

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  • [1]
    KAJIHARA D, HON C C, ABDULLAH A N, et al. Analysis of splice variants of the human protein disulfide isomerase (P4HB) gene[J]. BMC Genomics, 2020, 21(1): 766. doi: 10.1186/s12864-020-07164-y
    [2]
    MATSUSAKI M, KANEMURA S, KINOSHITA M, et al. The protein disulfide isomerase family: From proteostasis to pathogenesis[J]. Biochim Biophys Acta Gen Subj, 2020, 1864(2): 129338. DOI: 10.1016/j.bbagen.2019.04.003.
    [3]
    GUYETTE J, EVANGELISTA B, TATULIAN S A, et al. Stability and conformational resilience of protein disulfide isomerase[J]. Biochemistry, 2019, 58(34): 3572-3584. doi: 10.1021/acs.biochem.9b00405
    [4]
    JHA V, KUMARI T, MANICKAM V, et al. ERO1-PDI redox signaling in health and disease[J]. Antioxid Redox Signal, 2021, 35(13): 1093-1115. doi: 10.1089/ars.2021.0018
    [5]
    XIONG B, JHA V, MIN J K, et al. Protein disulfide isomerase in cardiovascular disease[J]. Exp Mol Med, 2020, 52(3): 390-399. doi: 10.1038/s12276-020-0401-5
    [6]
    GIMENEZ M, VERÍSSIMO-FILHO S, WITTIG I, et al. Redox activation of Nox1 (NADPH oxidase 1) involves an intermolecular disulfide bond between protein disulfide isomerase and p47phox in vascular smooth muscle cells[J]. Arterioscler Thromb Vasc Biol, 2019, 39(2): 224-236. doi: 10.1161/ATVBAHA.118.311038
    [7]
    CHINNARAJ M, BARRIOS D A, FRIEDEN C, et al. Bioorthogonal chemistry enables single-molecule FRET measurements of catalytically active protein disulfide isomerase[J]. Chembiochem, 2021, 22(1): 134-138. doi: 10.1002/cbic.202000537
    [8]
    ESSEX D W, WU Y. Multiple protein disulfide isomerases support thrombosis[J]. Curr Opin Hematol, 2018, 25(5): 395-402. doi: 10.1097/MOH.0000000000000449
    [9]
    XU X L, CHIU J, CHEN S, et al. Pathophysiological roles of cell surface and extracellular protein disulfide isomerase and their molecular mechanisms[J]. Br J Pharmacol, 2021, 178(15): 2911-2930. doi: 10.1111/bph.15493
    [10]
    HIRAYAMA C, MACHIDA K, NOI K, et al. Distinct roles and actions of protein disulfide isomerase family enzymes in catalysis of nascent-chain disulfide bond formation[J]. iScience, 2021, 24(4): 102296. DOI: 10.1016/j.isci.2021.102296.
    [11]
    OKUMURA M, NOI K, INABA K. Visualization of structural dynamics of protein disulfide isomerase enzymes in catalysis of oxidative folding and reductive unfolding[J]. Curr Opin Struct Biol, 2021, 66: 49-57. doi: 10.1016/j.sbi.2020.10.004
    [12]
    MA Y S, FENG S, LIN L, et al. Protein disulfide isomerase inhibits endoplasmic reticulum stress response and apoptosis via its oxidoreductase activity in colorectal cancer[J]. Cell Signal, 2021, 86: 110076. DOI: 10.1016/j.cellsig.2021.110076.
    [13]
    GANGULY R, KHANAL S, MATHIAS A, et al. TSP-1 (thrombospondin-1) deficiency protects ApoE-/- mice against leptin-induced atherosclerosis[J]. Arterioscler Thromb Vasc Biol, 2021, 41(2): e112-e127.
    [14]
    ZHANG K J, LI M M, YIN L, et al. Role of thrombospondin-1 and thrombospondin-2 in cardiovascular diseases (Review)[J]. Int J Mol Med, 2020, 45(5): 1275-1293.
    [15]
    SHARDA A, FURIE B. Regulatory role of thiol isomerases in thrombus formation[J]. Expert Rev Hematol, 2018, 11(5): 437-448. doi: 10.1080/17474086.2018.1452612
    [16]
    CAPOZZI A, RⅡTANO G, RECALCHI S, et al. Effect of heparanase inhibitor on tissue factor overexpression in platelets and endothelial cells induced by anti-β2-GPI antibodies[J]. J Thromb Haemost, 2021, 19(9): 2302-2313. doi: 10.1111/jth.15417
    [17]
    TANAKA L Y, OLIVEIRA P V S, LAURINDO F R M. Peri/epicellular thiol oxidoreductases as mediators of extracellular redox signaling[J]. Antioxid Redox Signal, 2020, 33(4): 280-307. doi: 10.1089/ars.2019.8012
    [18]
    WEAVER J C, ULLAH I, QI M, et al. Free thiol β2-GPI (β-2-Glycoprotein-I) provides a link between inflammation and oxidative stress in atherosclerotic coronary artery disease[J]. Arterioscler Thromb Vasc Biol, 2020, 40(11): 2794-2804. doi: 10.1161/ATVBAHA.120.315156
    [19]
    KUMAR S, CHINNARAJ M, PLANER W, et al. An allosteric redox switch in domain V of β2-glycoprotein I controls membrane binding and anti-domain I autoantibody recognition[J]. J Biol Chem, 2021, 297(2): 100890. DOI: 10.1016/j.jbc.2021.100890.
    [20]
    ANSARI S A, PENDURTHI U R, RAO L V M. Role of cell surface lipids and thiol-disulphide exchange pathways in regulating the encryption and decryption of tissue factor[J]. Thromb Haemost, 2019, 119(6): 860-870. doi: 10.1055/s-0039-1681102
    [21]
    CHEN F W, ZHAO Z Z, ZHOU J S, et al. Protein disulfide isomerase enhances tissue factor-dependent thrombin generation[J]. Biochem Biophys Res Commun, 2018, 501(1): 172-177. doi: 10.1016/j.bbrc.2018.04.207
    [22]
    POPIELARSKI M, PONAMARCZUK H, STASIAK M, et al. P2Y12 receptor antagonists and AR receptor agonists regulates Protein Disulfide Isomerase secretion from platelets and endothelial cells[J]. Biochem Biophys Res Commun, 2020, 526(3): 756-763. doi: 10.1016/j.bbrc.2020.03.143
    [23]
    KAO C C, KUNG P H, TAI C J, et al. Juglone prevents human platelet aggregation through inhibiting Akt and protein disulfide isomerase[J]. Phytomedicine, 2021, 82: 153449. DOI: 10.1016/j.phymed.2020.153449.
    [24]
    MINEIRO M F, PATRICIO E S, S PEIXOTO Á, et al. Urate hydroperoxide oxidizes endothelial cell surface protein disulfide isomerase-A1 and impairs adherence[J]. Biochim Biophys Acta Gen Subj, 2020, 1864(3): 129481. DOI: 10.1016/j.bbagen.2019.129481.
    [25]
    PRZYBOROWSKI K, KURPINSKA A, WOJKOWSKA D, et al. Protein disulfide isomerase-A1 regulates intraplatelet reactive oxygen species-thromboxane A2-dependent pathway in human platelets[J]. J Thromb Haemost, 2022, 20(1): 157-169. doi: 10.1111/jth.15539
    [26]
    QIN R R, ZHU H, WANG F, et al. Platelet activation in diabetic mice models: The role of vascular endothelial cell-derived protein disulfide isomerase-mediated GP Ⅱb/Ⅲa receptor activation[J]. Aging (Albany NY), 2019, 11(16): 6358-6370.
    [27]
    WU Y, ESSEX D W. Vascular thiol isomerases in thrombosis: The yin and yang[J]. J Thromb Haemost, 2020, 18(11): 2790-2800. doi: 10.1111/jth.15019
    [28]
    ROSENBERG N, MOR-COHEN R, SHEPTOVITSKY V H, et al. Integrin-mediated cell adhesion requires extracellular disulfide exchange regulated by protein disulfide isomerase[J]. Exp Cell Res, 2019, 381(1): 77-85. doi: 10.1016/j.yexcr.2019.04.017
    [29]
    梁程辉, 陈丹, 廖馨源, 等. 蛋白质二硫键异构酶的结构及抑制剂研究进展[J]. 生物化学与生物物理进展, 2020, 47(7): 595-606. doi: 10.16476/j.pibb.2020.0065

    LIANG C H, CHEN D, LIAO X Y, et al. Progress in the structural studies and inhibitor development of protein disulfide isomerase[J]. Progress in Biochemistry and Biophysics, 2020, 47(7): 595-606. doi: 10.16476/j.pibb.2020.0065
    [30]
    张金, 李程, 韩笑蓉, 等. 抗磷脂综合征相关循环系统表现[J]. 中华全科医学, 2021, 19(9): 1557-1561. doi: 10.16766/j.cnki.issn.1674-4152.002111

    ZHANG J, LI C, HAN X R, et al. Circulatory system manifestations of antiphospholipid antibody syndrome[J]. Chinese Journal of General Practice, 2021, 19(9): 1557-1561. doi: 10.16766/j.cnki.issn.1674-4152.002111
    [31]
    WANG X, XUE G P, SONG M R, et al. Molecular basis of rutin inhibition of protein disulfide isomerase (PDI) by combined in silico and experimental methods[J]. RSC Adv, 2018, 8(33): 18480-18491. doi: 10.1039/C8RA02683A
    [32]
    CHEN D, LIU Y R, LIU P W, et al. Orally delivered rutin in lipid-based nano-formulation exerts strong antithrombotic effects by protein disulfide isomerase inhibition[J]. Drug Deliv, 2022, 29(1): 1824-1835. doi: 10.1080/10717544.2022.2083726
    [33]
    CHOI S S, PARK H R, LEE K A. A comparative study of rutin and rutin glycoside: Anti-oxidant activity, anti-inflammatory effect, effect on platelet aggregation and blood coagulation[J]. Antioxidants (Basel), 2021, 10(11): 1696. doi: 10.3390/antiox10111696
    [34]
    DUTTA A, DAHIYA A, VERMA S. Quercetin-3-rutinoside protects against gamma radiation inflicted hematopoietic dysfunction by regulating oxidative, inflammatory, and apoptotic mediators in mouse spleen and bone marrow[J]. Free Radic Res, 2021, 55(3): 230-245. doi: 10.1080/10715762.2021.1914334
    [35]
    WU H T, SU M L, JIN H, et al. Rutin-loaded silver nanoparticles with antithrombotic function[J]. Front Bioeng Biotechnol, 2020, 8: 598977. DOI: 10.3389/fbioe.2020.598977.
    [36]
    STAINER A R, SASIKUMAR P, BYE A P, et al. The metabolites of the dietary flavonoid quercetin possess potent antithrombotic activity, and interact with aspirin to enhance antiplatelet effects[J]. TH Open, 2019, 3(3): e244-e258. doi: 10.1055/s-0039-1694028
    [37]
    ZWICKER J I, SCHLECHTER B L, STOPA J D, et al. Targeting protein disulfide isomerase with the flavonoid isoquercetin to improve hypercoagulability in advanced cancer[J]. JCI Insight, 2019, 4(4): e125851. DOI: 10.1172/jci.insight.125851.
    [38]
    RAKSHIT S, SHUKLA P, VERMA A, et al. Protective role of rutin against combined exposure to lipopolysaccharide and D-galactosamine-induced dysfunctions in liver, kidney, and brain: Hematological, biochemical, and histological evidences[J]. J Food Biochem, 2021, 45(2): e13605. DOI: 10.1111/jfbc.13605.
    [39]
    HOLBROOK L M, KEETON S J, SASIKUMAR P, et al. Zafirlukast is a broad-spectrum thiol isomerase inhibitor that inhibits thrombosis without altering bleeding times[J]. Br J Pharmacol, 2021, 178(3): 550-563. doi: 10.1111/bph.15291
    [40]
    DUAN H X Y, ZHANG Q, LIU J, et al. Suppression of apoptosis in vascular endothelial cell, the promising way for natural medicines to treat atherosclerosis[J]. Pharmacol Res, 2021, 168: 105599. DOI: 10.1016/j.phrs.2021.105599.
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