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Review

The role of tissue inhibitors of metalloproteinases in microvascular endothelial cell barrier dysfunction during sepsis

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Pages 1-12 | Published online: 07 May 2019

References

  • Singer M, Deutschman CS, Seymour CW, et al. The third international consensus definitions for sepsis and septic shock (Sepsis-3). JAMA. 2016;315(8):801.
  • Genga KR, Russell JA. Update of sepsis in the intensive care unit. J Innate Immun. 2017;9(5):441–455.
  • Yende S, Austin S, Rhodes A, et al. Long-term quality of life among survivors of severe sepsis: analyses of two international trials. Crit Care Med. 2016;44(8):1461–1467.
  • Barichello T, Sayana P, Giridharan VV, et al. Long-term cognitive outcomes after sepsis: a translational systematic review. Mol Neurobiol. Epub 2018 Apr 23.
  • Sagy M, Al-Qaqaa Y, Kim P. Definitions and pathophysiology of sepsis. Curr Probl Pediatr Adolesc Health Care. 2013;43(10):260–263.
  • Duque GA, Descoteaux A. Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol. 2014;5:491.
  • Sullivan JS, Kilpatrick L, Costarino AT, Lee SC, Harris MC. Correlation of plasma cytokine elevations with mortality rate in children with sepsis. J Pediatr. 1992;120(4):510–515.
  • Nathan C, Ding A. Nonresolving inflammation. Cell. 2010;140(6):871–882.
  • Otto GP, Sossdorf M, Claus RA, et al. The late phase of sepsis is characterized by an increased microbiological burden and death rate. Critical Care. 2011;15(4):R183.
  • van Vught LA, Klein Klouwenberg PMC, Spitoni C, et al. Incidence, risk factors, and attributable mortality of secondary infections in the intensive care unit after admission for sepsis. JAMA. 2016;315(14):1469.
  • Souza ACP, Yuen PST, Star RA. Microparticles: markers and mediators of sepsis-induced microvascular dysfunction, immunosuppression, and AKI. Kidney Int. 2015;87(6):1100–1108.
  • Wallez Y, Huber P. Endothelial adherens and tight junctions in vascular homeostasis, inflammation and angiogenesis. Biochim Biophys Acta. 2008;1778(3):794–809.
  • Bhattacharya J, Matthay MA. Regulation and repair of the alveolar-capillary barrier in acute lung injury. Annu Rev Physiol. 2013;75(1):593–615.
  • Dejana E, Orsenigo F, Lampugnani MG. The role of adherens junctions and VE-cadherin in the control of vascular permeability. J Cell Sci. 2008;121(13):2115–2122.
  • Weksler BB, Subileau EA, Perrière N, et al. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. Faseb J. 2005;19(13):1872–1874.
  • Anderson JM. Molecular structure of tight junctions and their role in epithelial transport. News Physiol Sci. 2001;16:126–130.
  • Rodrigues SF, Granger DN. Blood cells and endothelial barrier function. Tissue Barriers. 2015;3(1–2):e978720.
  • Giancotti FG, Ruoslahti E. Integrin signaling. Science. 1999;285(5430):1028–1033.
  • Frantz C, Stewart KM, Weaver VM. The extracellular matrix at a glance. J Cell Sci. 2010;123(24):4195–4200.
  • Souza-Fernandes AB, Pelosi P, Rocco PRM. Bench-to-bedside review: the role of glycosaminoglycans in respiratory disease. Critical Care. 2006;10(6):237.
  • Sukriti S, Tauseef M, Yazbeck P, Mehta D. Mechanisms regulating endothelial permeability. Pulm Circ. 2014;4(4):535–551.
  • Pober JS, Min W, Bradley JR. Mechanisms of endothelial dysfunction, injury, and death. Annu Rev Pathol Mech Dis. 2009;4(1):71–95.
  • Lee KS, Jin SM, Kim HJ, Lee YC. Matrix metalloproteinase inhibitor regulates inflammatory cell migration by reducing ICAM-1 and VCAM-1 expression in a murine model of toluene diisocyanate-induced asthma. J Allergy Clin Immunol. 2003;111(6):1278–1284.
  • Kuebler WM, Wittenberg C, Lee WL, et al. Thrombin stimulates albumin transcytosis in lung microvascular endothelial cells via activation of acid sphingomyelinase. Am J Physiol Lung Cell Mol Physiol. 2016;310(8):L720–L732.
  • Wang L, Mehta S, Ahmed Y, Wallace S, Pape MC, Gill SE. Differential mechanisms of septic human pulmonary microvascular endothelial cell barrier dysfunction depending on the presence of neutrophils. Front Immunol. 2018;9:9.
  • Rahimi N. Defenders and challengers of endothelial barrier function. Front Immunol. 2017;8:1847.
  • Giannotta M, Trani M, Dejana E. VE-Cadherin and endothelial adherens junctions: active guardians of vascular integrity. Dev Cell. 2013;26(5):441–454.
  • Mehta D, Ravindran K, Kuebler WM. Novel regulators of endothelial barrier function. Am J Physiol Lung Cell Mol Physiol. 2014;307(12):L924–L935.
  • Dreymueller D, Uhlig S, Ludwig A. ADAM-family metalloproteinases in lung inflammation: potential therapeutic targets. Am J Physiol Lung Cell Mol Physiol. 2015;308(4):L325–L343.
  • Flemming S, Burkard N, Renschler M, et al. Soluble VE-cadherin is involved in endothelial barrier breakdown in systemic inflammation and sepsis. Cardiovasc Res. 2015;107(1):32–44.
  • Lakhan SE, Kirchgessner A, Tepper D, Leonard A, Aidan L. Matrix metalloproteinases and blood-brain barrier disruption in acute ischemic stroke. Front Neurol. 2013;4:32.
  • Nagase H, Woessner JF. Matrix metalloproteinases. J Biol Chem. 1999;274(31):21491–21494.
  • Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci. 2002;115(19):3719–3727.
  • Stetler-Stevenson WG. Matrix metalloproteinases in angiogenesis: a moving target for therapeutic intervention. J Clin Invest. 1999;103(9):1237–1241.
  • Dreymueller D, Pruessmeyer J, Groth E, Ludwig A. The role of ADAM-mediated shedding in vascular biology. Eur J Cell Biol. 2012;91(6–7):472–485.
  • Dreymueller D, Martin C, Kogel T, et al. Lung endothelial ADAM17 regulates the acute inflammatory response to lipopolysaccharide. EMBO Mol Med. 2012;4(5):412–423.
  • Brew K, Nagase H. The tissue inhibitors of metalloproteinases (TIMPs): an ancient family with structural and functional diversity. Biochim Biophys Acta – Mol Cell Res. 2010;1803(1):55–71.
  • Masciantonio MG, Lee CKS, Arpino V, Mehta S, Gill SE. Chapter Three – the balance between metalloproteinases and TIMPs: critical regulator of microvascular endothelial cell function in health and disease. In: Khalil RABT. Matrix Metalloproteinases and Tissue Remodeling in Health and Disease: Cardiovascular Remodeling. Vol 147. Academic Press; 2017:101–131.
  • Murphy G. Tissue inhibitors of metalloproteinases. Genome Biol. 2011;12(11):233.
  • Vaalamo M, Leivo T, Saarialho-Kere U. Differential expression of tissue inhibitors of metalloproteinases (TIMP-1, -2, -3, and -4) in normal and aberrant wound healing. Hum Pathol. 1999;30(7):795–802.
  • Ashcroft GS, Herrick SE, Tarnuzzer RW, Horan MA, Schultz GS, Ferguson MWJ. Human ageing impairs injury-inducedin vivo expression of tissue inhibitor of matrix metalloproteinases (TIMP)-1 and -2 proteins and mRNA. J Pathol. 1997;183(2):169–176.
  • Stetler-Stevenson WG. Tissue inhibitors of metalloproteinases in cell signaling: metalloproteinase-independent biological activities. Sci Signal. 2008;1(27):re6.
  • Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res. 2006;69(3):562–573.
  • Johnson JL. Metalloproteinases in atherosclerosis. Eur J Pharmacol. 2017;816(June):93–106.
  • Kelwick R, Desanlis I, Wheeler GN, Edwards DR. The ADAMTS (A Disintegrin and Metalloproteinase with Thrombospondin motifs) family. Genome Biol. 2015;16(1):113.
  • Arpino V, Brock M, Gill SE. The role of TIMPs in regulation of extracellular matrix proteolysis. Matrix Biol. 2015;44–46:247–254.
  • Selman M, Ruiz V, Cabrera S. TIMP-1, -2, -3, and -4 in idiopathic pulmonary fibrosis. A prevailing nondegradative lung microenvironment? Am J Physiol Cell Mol Physiol. 2000;279(3):L562–L574.
  • Elkington PTG, Friedland JS. Matrix metalloproteinases in destructive pulmonary pathology. Thorax. 2006;61(3):259–266.
  • Gill SE, Huizar I, Bench EM, et al. Tissue inhibitor of metalloproteinases 3 regulates resolution of inflammation following acute lung injury. Am J Pathol. 2010;176(1):64–73.
  • Akahane T, Akahane M, Shah A, Connor CM, Thorgeirsson UP. TIMP-1 inhibits microvascular endothelial cell migration by MMP-dependent and MMP-independent mechanisms. Exp Cell Res. 2004;301(2):158–167.
  • Chen P, Mcguire JK, Hackman RC, et al. Tissue inhibitor of metalloproteinase-1 moderates airway re-epithelialization by regulating matrilysin activity. Am J Pathol. 2008;172(5):1256–1270.
  • Khokha R, Murthy A, Weiss A. Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat Rev Immunol. 2013;13(9):649–665.
  • Bernardo MM, Fridman R. TIMP-2 (tissue inhibitor of metalloproteinase-2) regulates MMP-2 (matrix metalloproteinase-2) activity in the extracellular environment after pro-MMP-2 activation by MT1 (membrane type 1)-MMP. Biochem J. 2003;374(3):739–745.
  • Black RA. TIMP3 checks inflammation. Nat Genet. 2004;36(9):934–935.
  • Mohammed FF, Smookler DS, Taylor SEM, et al. Abnormal TNF activity in Timp3 −/− mice leads to chronic hepatic inflammation and failure of liver regeneration. Nat Genet. 2004;36(9):969–977.
  • Borrell-Pagès M, Rojo F, Albanell J, Baselga J, Arribas J. TACE is required for the activation of the EGFR by TGF-α in tumors. Embo J. 2003;22(5):1114–1124.
  • Hamilton LM, Torres-Lozano C, Puddicombe SM, et al. The role of the epidermal growth factor receptor in sustaining neutrophil inflammation in severe asthma. Clin Exp Allergy. 2003;33(2):233–240.
  • Hashimoto G, Aoki T, Nakamura H, Tanzawa K, Okada Y. Inhibition of ADAMTS4 (aggrecanase-1) by tissue inhibitors of metalloproteinases (TIMP-1, 2, 3 and 4). FEBS Lett. 2001;494(3):192–195.
  • Troeberg L, Fushimi K, Scilabra SD, et al. The C-terminal domains of ADAMTS-4 and ADAMTS-5 promote association with N-TIMP-3. Matrix Biol. 2009;28(8):463–469.
  • Murphy AN, Unsworth EJ, Stetler-Stevenson WG. Tissue inhibitor of metalloproteinases-2 inhibits bFGF-induced human microvascular endothelial cell proliferation. J Cell Physiol. 1993;157(2):351–358.
  • Baker AH, Zaltsman AB, George SJ, Newby AC. Divergent effects of tissue inhibitor of metalloproteinase-1, -2, or -3 overexpression on rat vascular smooth muscle cell invasion, proliferation, and death in vitro. TIMP-3 promotes apoptosis. J Clin Invest. 1998;101(6):1478–1487.
  • Liu X-W, Bernardo MM, Fridman R, Kim H-RC, H-Rc K. Tissue inhibitor of metalloproteinase-1 protects human breast epithelial cells against intrinsic apoptotic cell death via the focal adhesion kinase/phosphatidylinositol 3-kinase and MAPK signaling pathway. Journal of Biological Chemistry. 2003;278(41):40364–40372.
  • Savarin C, Bergmann CC, Hinton DR, Stohlman SA. MMP-independent role of TIMP-1 at the blood brain barrier during viral encephalomyelitis. ASN Neuro. 2013;5(5):AN20130033.
  • Qi JH, Ebrahem Q, Moore N, et al. A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med. 2003;9(4):407–415.
  • Qi JH, Anand-Apte B. Tissue inhibitor of metalloproteinase-3 (TIMP3) promotes endothelial apoptosis via a caspase-independent mechanism. Apoptosis. 2015;20(4):523–534.
  • Aird WC. Review article the role of the endothelium in severe sepsis and multiple organ dysfunction syndrome. 2003;101(10):3765–3777.
  • Yazdan-Ashoori P, Liaw P, Toltl L, et al. Elevated plasma matrix metalloproteinases and their tissue inhibitors in patients with severe sepsis. J Crit Care. 2011;26(6):556–565.
  • Hästbacka J, Linko R, Tervahartiala T, et al. Serum MMP-8 and TIMP-1 in critically ill patients with acute respiratory failure: TIMP-1 is associated with increased 90-day mortality. Anesth Analg. 2014;118(4):790-8.
  • Wang M, Zhang Q, Zhao X, Dong G, Li C. Diagnostic and prognostic value of neutrophil gelatinase-associated lipocalin, matrix metalloproteinase-9, and tissue inhibitor of matrix metalloproteinases-1 for sepsis in the Emergency Department: an observational study. Critical Care. 2014;18(6):634.
  • Lorente L, Martín MM, Solé-Violán J, et al. Association of sepsis-related mortality with early increase of TIMP-1/MMP-9 ratio. PLoS One. 2014;9(4):e94318.
  • Bojic S, Kotur-Stevuljevic J, Kalezic N, et al. Diagnostic value of matrix metalloproteinase-9 and tissue inhibitor of matrix metalloproteinase-1 in sepsis-associated acute kidney injury. Tohoku J Exp Med. 2015;237(2):103–109.
  • Mühl D, Nagy B, Woth G, et al. Dynamic changes of matrix metalloproteinases and their tissue inhibitors in severe sepsis. J Crit Care. 2011;26(6):550–555.
  • Bugno M, Witek B, Bereta J, Bereta M, Edwards DR, Kordula T. Reprogramming of TIMP-1 and TIMP-3 expression profiles in brain microvascular endothelial cells and astrocytes in response to proinflammatory cytokines. FEBS Lett. 1999;448(1):9–14.
  • Shastry S, Tyagi SC. Homocysteine induces metalloproteinase and shedding of β-1 integrin in microvessel endothelial cells. J Cell Biochem. 2004;93(1):207–213.
  • Arpino V, Mehta S, Wang L, et al. Tissue inhibitor of metalloproteinases 3-dependent microvascular endothelial cell barrier function is disrupted under septic conditions. American Journal of Physiology-Heart and Circulatory Physiology. 2016;310(11):H1455–H1467.
  • Shen Q, Lee ES, Pitts RL, Mh W, Yuan SY. Tissue inhibitor of metalloproteinase-2 regulates matrix metalloproteinase-2–mediated endothelial barrier dysfunction and breast cancer cell transmigration through lung microvascular endothelial cells. Mol Cancer Res. 2010;8(7):939–951.
  • Dollery CM, Mcewan JR, Wang M, Sang QA, Liu YE, Shi YE. TIMP-4 is regulated by vascular injury in rats. Circ Res. 1999;84(5):498–504.
  • Schrimpf C, Xin C, Campanholle G, et al. Pericyte TIMP3 and ADAMTS1 modulate vascular stability after kidney injury. J Am Soc Nephrol. 2012;23(5):868–883.
  • Schrimpf C, Koppen T, Duffield JS, et al. TIMP3 is regulated by pericytes upon shear stress detection leading to a modified endothelial cell response. Eur J Vasc Endovasc Surg. 2017;54(4):524–533.
  • Fujimoto M, Takagi Y, Aoki T, et al. Tissue inhibitor of metalloproteinases protect blood—brain barrier disruption in focal cerebral ischemia. J Cereb Blood Flow Metab. 2008;28(10):1674–1685.
  • Chen F, Ohashi N, Li W, Eckman C, Nguyen JH. Disruptions of occludin and claudin-5 in brain endothelial cells in vitro and in brains of mice with acute liver failure. Hepatology. 2009;50(6):1914–1923.
  • Menge T, Zhao Y, Zhao J. mesenchymal stem cells regulate blood brain barrier integrity in traumatic brain injury through production of the soluble factor TIMP3. Sci Transl Med. 2012;4(161):161ra150–161161.
  • Koskivirta I, Rahkonen O, Mäyränpää M, et al. Tissue inhibitor of metalloproteinases 4 (TIMP4) is involved in inflammatory processes of human cardiovascular pathology. Histochem Cell Biol. 2006;126(3):335–342.
  • Rorive S, Lopez XM, Maris C, et al. TIMP-4 and CD63: new prognostic biomarkers in human astrocytomas. Mod Pathol. 2010;23(10):1418–1428.
  • Bauer H, Zweimueller-Mayer J, Steinbacher P, Lametschwandtner A, Bauer HC. The dual role of zonula occludens (ZO) proteins. J Biomed Biotechnol. 2010;2010(4):1–11.
  • Ichikawa-Tomikawa N, Sugimoto K, Satohisa S, Nishiura K, Chiba H. Possible involvement of tight junctions, extracellular matrix and nuclear receptors in epithelial differentiation. J Biomed Biotechnol. 2011;2011(2):1–10.
  • Liu J, Jin X, Liu KJ, Liu W. Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage. Journal of Neuroscience. 2012;32(9):3044–3057.
  • Sidibé A, Mannic T, Arboleas M, et al. Soluble VE-cadherin in rheumatoid arthritis patients correlates with disease activity: evidence for tumor necrosis factor α-induced VE-cadherin cleavage. Arthritis Rheum. 2012;64(1):77–87.
  • Schulz B, Pruessmeyer J, Maretzky T, et al. ADAM10 regulates endothelial permeability and T-cell transmigration by proteolysis of vascular endothelial cadherin. Circ Res. 2008;102(10):1192–1201.
  • Lominadze D, Roberts AM, Tyagi N, Moshal KS, Tyagi SC. Homocysteine causes cerebrovascular leakage in mice. Am J Physiol Heart Circ Physiol. 2006;290(3):H1206–H1213.
  • Passi A, Negrini D, Albertini R, de Luca G, Miserocchi G. Involvement of lung interstitial proteoglycans in development of hydraulic- and elastase-induced edema. Am J Physiol Lung Cell Mol Physiol. 1998;275(3):L631–L635.
  • Partridge CA, Jeffrey JJ, Malik AB. A 96-kDa gelatinase induced by TNF-alpha contributes to increased microvascular endothelial permeability. Am J Physiol Lung Cell Mol Physiol. 1993;265(5):L438–L447.
  • Mehta D, Malik AB. Signaling mechanisms regulating endothelial permeability. Physiol Rev. 2006;86(1):279–367.
  • Bruegmann E, Gruemmer R, Neulen J, Motejlek K. Regulation of soluble vascular endothelial growth factor receptor 1 secretion from human endothelial cells by tissue inhibitor of metalloproteinase 1. Mol Hum Reprod. 2009;15(11):749–756.
  • Ebrahem Q, Qi JH, Sugimoto M, et al. Increased neovascularization in mice lacking tissue inhibitor of metalloproteinases-3. Invest Ophthalmol Vis Sci. 2011;52(9):6117–6123.
  • Lee S-J, Tsang PS, M Diaz T, Wei B-Yang, Stetler-Stevenson WG. TIMP-2 modulates VEGFR-2 phosphorylation and enhances phosphodiesterase activity in endothelial cells. Lab Invest. 2010;90(3):374–382.
  • Singh R, Mason J, Lidington E, et al. Cytokine stimulated vascular cell adhesion molecule-1 (VCAM-1) ectodomain release is regulated by TIMP-3. Cardiovasc Res. 2005;67(1):39–49.
  • Ponnuchamy B, Khalil RA. Role of ADAMs in endothelial cell permeability: cadherin shedding and leukocyte rolling. Circ Res. 2008;102(10):1139–1142.
  • Sithu SD, English WR, Olson P, et al. Membrane-type 1-matrix metalloproteinase regulates intracellular adhesion molecule-1 (ICAM-1)-mediated monocyte transmigration. J Biol Chem. 2007;282(34):25010–25019.
  • Garton KJ, Gough PJ, Philalay J, et al. Stimulated shedding of vascular cell adhesion molecule 1 (VCAM-1) is mediated by tumor necrosis factor-alpha-converting enzyme (ADAM 17). J Biol Chem. 2003;278(39):37459–37464.