Role of heparanase in sepsis‑related acute kidney injury (Review)
- Authors:
- Jian-Chun Li
- Lin-Jun Wang
- Fei Feng
- Ting-Ting Chen
- Wen-Gui Shi
- Li-Ping Liu
-
Affiliations: The First Clinical Medical College of Lanzhou University, Lanzhou, Gansu 730000, P.R. China, Cuiying Biomedical Research Center, The Second Hospital of Lanzhou University, Lanzhou, Gansu 730000, P.R. China, Department of Emergency, The First Hospital of Lanzhou University, Lanzhou, Gansu 730000, P.R. China - Published online on: June 26, 2023 https://doi.org/10.3892/etm.2023.12078
- Article Number: 379
-
Copyright: © Li et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
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 |
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|
Lameire NH, Bagga A, Cruz D, De Maeseneer J, Endre Z, Kellum JA, Liu KD, Mehta RL, Pannu N, Van Biesen W and Vanholder R: .: Acute kidney injury: An increasing global concern. Lancet. 382:170–179. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Hoste EA and Schurgers M: Epidemiology of acute kidney injury: How big is the problem? Crit Care Med. 36 (4 Suppl):S146–S151. 2008.PubMed/NCBI View Article : Google Scholar | |
|
Susantitaphong P, Cruz DN, Cerda J, Abulfaraj M, Alqahtani F, Koulouridis I and Jaber BL: Acute Kidney Injury Advisory Group of the American Society of Nephrology. World incidence of AKI: A meta-analysis. Clin J Am Soc Nephrol. 8:1482–1493. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Ronco C, Bellomo R and Kellum JA: Acute kidney injury. Lancet. 394:1949–1964. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Kellum JA, Chawla LS, Keener C, Singbartl K, Palevsky PM, Pike FL, Yealy DM, Huang DT and Angus DC: ProCESS and ProGReSS-AKI Investigators. The effects of alternative resuscitation strategies on acute kidney injury in patients with septic shock. Am J Respir Crit Care Med. 193:281–287. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Mayeux PR and MacMillan-Crow LA: Pharmacological targets in the renal peritubular microenvironment: Implications for therapy for sepsis-induced acute kidney injury. Pharmacol Ther. 134:139–155. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Lygizos MI, Yang Y, Altmann CJ, Okamura K, Hernando AA, Perez MJ, Smith LP, Koyanagi DE, Gandjeva A, Bhargava R, et al: Heparanase mediates renal dysfunction during early sepsis in mice. Physiol Rep. 1(e00153)2013.PubMed/NCBI View Article : Google Scholar | |
|
Zhang Y, Huang H, Liu W, Liu S, Wang XY, Diao ZL, Zhang AH, Guo W, Han X, Dong X and Katilov O: Endothelial progenitor cells-derived exosomal microRNA-21-5p alleviates sepsis-induced acute kidney injury by inhibiting RUNX1 expression. Cell Death Dis. 12(335)2021.PubMed/NCBI View Article : Google Scholar | |
|
Kellum JA and Lameire N: KDIGO AKI Guideline Work Group. Diagnosis, evaluation, and management of acute kidney injury: A KDIGO summary (Part 1). Crit Care. 17(204)2013.PubMed/NCBI View Article : Google Scholar | |
|
Singer M, Deutschman CS, Seymour CW, Shankar-Hari M, Annane D, Bauer M, Bellomo R, Bernard GR, Chiche JD, Coopersmith CM, et al: The Third International Consensus Definitions for Sepsis and Septic Shock (Sepsis-3). JAMA. 315:801–810. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Bonventre JV and Yang L: Cellular pathophysiology of ischemic acute kidney injury. J Clin Invest. 121:4210–4221. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Schrier RW, Wang W, Poole B and Mitra A: Acute renal failure: Definitions, diagnosis, pathogenesis, and therapy. J Clin Invest. 114:5–14. 2004.PubMed/NCBI View Article : Google Scholar | |
|
Schmidt C, Steinke T, Moritz S, Graf BM and Bucher M: Acute renal failure and sepsis: Just an organ dysfunction due to septic multiorgan failure? Anaesthesist. 59:682–699. 2010.PubMed/NCBI View Article : Google Scholar : (In German). | |
|
Maiden MJ, Otto S, Brealey JK, Finnis ME, Chapman MJ, Kuchel TR, Nash CH, Edwards J and Bellomo R: Structure and function of the kidney in septic shock. A prospective controlled experimental study. Am J Respir Crit Care Med. 194:692–700. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Lerolle N, Nochy D, Guérot E, Bruneval P, Fagon JY, Diehl JL and Hill G: Histopathology of septic shock induced acute kidney injury: Apoptosis and leukocytic infiltration. Intensive Care Med. 36:471–478. 2010.PubMed/NCBI View Article : Google Scholar | |
|
Peerapornratana S, Manrique-Caballero CL, Gómez H and Kellum JA: Acute kidney injury from sepsis: Current concepts, epidemiology, pathophysiology, prevention and treatment. Kidney Int. 96:1083–1099. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Poston JT and Koyner JL: Sepsis associated acute kidney injury. BMJ. 364(k4891)2019.PubMed/NCBI View Article : Google Scholar | |
|
Gomez H, Ince C, De Backer D, Pickkers P, Payen D, Hotchkiss J and Kellum JA: A unified theory of sepsis-induced acute kidney injury: Inflammation, microcirculatory dysfunction, bioenergetics, and the tubular cell adaptation to injury. Shock. 41:3–11. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Bateman RM, Sharpe MD, Jagger JE and Ellis CG: Sepsis impairs microvascular autoregulation and delays capillary response within hypoxic capillaries. Crit Care. 19(389)2015.PubMed/NCBI View Article : Google Scholar | |
|
Ye C, Kawasaki M, Nakano K, Ohnishi T, Watanabe E, Oda S, Nakada TA and Haneishi H: Acquisition and analysis of microcirculation image in septic model rats. Sensors (Basel). 22(8471)2022.PubMed/NCBI View Article : Google Scholar | |
|
Ince C: The microcirculation is the motor of sepsis. Crit Care. 9 (Suppl 4):S13–S19. 2005.PubMed/NCBI View Article : Google Scholar | |
|
Joffre J, Hellman J, Ince C and Ait-Oufella H: Endothelial responses in sepsis. Am J Respir Crit Care Med. 202:361–370. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Anniss AM and Sparrow RL: Variable adhesion of different red blood cell products to activated vascular endothelium under flow conditions. Am J Hematol. 82:439–445. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Ishikawa K, Calzavacca P, Bellomo R, Bailey M and May CN: Effect of selective inhibition of renal inducible nitric oxide synthase on renal blood flow and function in experimental hyperdynamic sepsis. Crit Care Med. 40:2368–2375. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Heemskerk S, Pickkers P, Bouw MP, Draisma A, van der Hoeven JG, Peters WH, Smits P, Russel FG and Masereeuw R: Upregulation of renal inducible nitric oxide synthase during human endotoxemia and sepsis is associated with proximal tubule injury. Clin J Am Soc Nephrol. 1:853–862. 2006.PubMed/NCBI View Article : Google Scholar | |
|
Inkinen N, Pettilä V, Lakkisto P, Kuitunen A, Jukarainen S, Bendel S, Inkinen O, Ala-Kokko T and Vaara ST: FINNAKI Study Group. Association of endothelial and glycocalyx injury biomarkers with fluid administration, development of acute kidney injury, and 90-day mortality: Data from the FINNAKI observational study. Ann Intensive Care. 9(103)2019.PubMed/NCBI View Article : Google Scholar | |
|
Gustot T: Multiple organ failure in sepsis: Prognosis and role of systemic inflammatory response. Curr Opin Crit Care. 17:153–159. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Zhu J, Zhang Y, Shi L, Xia Y, Zha H, Li H and Song Z: RP105 protects against ischemic and septic acute kidney injury via suppressing TLR4/NF-κB signaling pathways. Int Immunopharmacol. 109(108904)2022.PubMed/NCBI View Article : Google Scholar | |
|
Krivan S, Kapelouzou A, Vagios S, Tsilimigras DI, Katsimpoulas M, Moris D, Aravanis CV, Demesticha TD, Schizas D, Mavroidis M, et al: Increased expression of Toll-like receptors 2, 3, 4 and 7 mRNA in the kidney and intestine of a septic mouse model. Sci Rep. 9(4010)2019.PubMed/NCBI View Article : Google Scholar | |
|
Kawai T and Akira S: Signaling to NF-kappaB by Toll-like receptors. Trends Mol Med. 13:460–469. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Kawai T and Akira S: TLR signaling. Semin Immunol. 19:24–32. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Leemans JC, Stokman G, Claessen N, Rouschop KM, Teske GJ, Kirschning CJ, Akira S, van der Poll T, Weening JJ and Florquin S: Renal-associated TLR2 mediates ischemia/reperfusion injury in the kidney. J Clin Invest. 115:2894–2903. 2005.PubMed/NCBI View Article : Google Scholar | |
|
El-Achkar TM, Huang X, Plotkin Z, Sandoval RM, Rhodes GJ and Dagher PC: Sepsis induces changes in the expression and distribution of Toll-like receptor 4 in the rat kidney. Am J Physiol Renal Physiol. 290:F1034–F1043. 2006.PubMed/NCBI View Article : Google Scholar | |
|
Fani F, Regolisti G, Delsante M, Cantaluppi V, Castellano G, Gesualdo L, Villa G and Fiaccadori E: Recent advances in the pathogenetic mechanisms of sepsis-associated acute kidney injury. J Nephrol. 31:351–359. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Zafrani L, Gerotziafas G, Byrnes C, Hu X, Perez J, Lévi C, Placier S, Letavernier E, Leelahavanichkul A, Haymann JP, et al: Calpastatin controls polymicrobial sepsis by limiting procoagulant microparticle release. Am J Respir Crit Care Med. 185:744–755. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Stark K and Massberg S: Interplay between inflammation and thrombosis in cardiovascular pathology. Nat Rev Cardiol. 18:666–682. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Benedetti C, Waldman M, Zaza G, Riella LV and Cravedi P: COVID-19 and the Kidneys: An update. Front Med (Lausanne). 7(423)2020.PubMed/NCBI View Article : Google Scholar | |
|
Toro J, Manrique-Caballero CL and Gómez H: Metabolic reprogramming and host tolerance: A novel concept to understand sepsis-associated AKI. J Clin Med. 10(4184)2021.PubMed/NCBI View Article : Google Scholar | |
|
Wilson DF: Oxidative phosphorylation: Regulation and role in cellular and tissue metabolism. J Physiol. 595:7023–7038. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Waltz P, Carchman E, Gomez H and Zuckerbraun B: Sepsis results in an altered renal metabolic and osmolyte profile. J Surg Res. 202:8–12. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Zhang D, Qi B, Li D, Feng J, Huang X, Ma X, Huang L, Wang X and Liu X: Phillyrin relieves lipopolysaccharide-induced AKI by protecting against glycocalyx damage and inhibiting inflammatory responses. Inflammation. 43:540–551. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Vlodavsky I, Singh P, Boyango I, Gutter-Kapon L, Elkin M, Sanderson RD and Ilan N: Heparanase: From basic research to therapeutic applications in cancer and inflammation. Drug Resist Updat. 29:54–75. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Goldberg R, Meirovitz A, Hirshoren N, Bulvik R, Binder A, Rubinstein AM and Elkin M: Versatile role of heparanase in inflammation. Matrix Biol. 32:234–240. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Goldberg R, Rubinstein AM, Gil N, Hermano E, Li JP, van der Vlag J, Atzmon R, Meirovitz A and Elkin M: Role of heparanase-driven inflammatory cascade in pathogenesis of diabetic nephropathy. Diabetes. 63:4302–4313. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Goldshmidt O, Zcharia E, Abramovitch R, Metzger S, Aingorn H, Friedmann Y, Schirrmacher V, Mitrani E and Vlodavsky I: Cell surface expression and secretion of heparanase markedly promote tumor angiogenesis and metastasis. Proc Natl Acad Sci USA. 99:10031–10036. 2002.PubMed/NCBI View Article : Google Scholar | |
|
Parish CR, Freeman C, Ziolkowski AF, He YQ, Sutcliffe EL, Zafar A, Rao S and Simeonovic CJ: Unexpected new roles for heparanase in type 1 diabetes and immune gene regulation. Matrix Biol. 32:228–233. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Meirovitz A, Goldberg R, Binder A, Rubinstein AM, Hermano E and Elkin M: Heparanase in inflammation and inflammation-associated cancer. FEBS J. 280:2307–2319. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Levey AS and James MT: Acute kidney injury. Ann Intern Med. 167:ITC66–ITC80. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Masola V, Zaza G, Onisto M, Lupo A and Gambaro G: Impact of heparanase on renal fibrosis. J Transl Med. 13(181)2015.PubMed/NCBI View Article : Google Scholar | |
|
Rosenfeldt MT and Ryan KM: The multiple roles of autophagy in cancer. Carcinogenesis. 32:955–963. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Bishop JR, Schuksz M and Esko JD: Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature. 446:1030–1037. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Bernfield M, Götte M, Park PW, Reizes O, Fitzgerald ML, Lincecum J and Zako M: Functions of cell surface heparan sulfate proteoglycans. Annu Rev Biochem. 68:729–777. 1999.PubMed/NCBI View Article : Google Scholar | |
|
Goldshmidt O, Nadav L, Aingorn H, Irit C, Feinstein N, Ilan N, Zamir E, Geiger B, Vlodavsky I and Katz BZ: Human heparanase is localized within lysosomes in a stable form. Exp Cell Res. 281:50–62. 2002.PubMed/NCBI View Article : Google Scholar | |
|
van den Hoven MJ, Rops AL, Vlodavsky I, Levidiotis V, Berden JH and van der Vlag J: Heparanase in glomerular diseases. Kidney Int. 72:543–548. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Gaskin SM, Soares Da Costa TP and Hulett MD: Heparanase: Cloning, function and regulation. Adv Exp Med Biol. 1221:189–229. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Masola V, Bellin G, Gambaro G and Onisto M: Heparanase: A multitasking protein involved in extracellular matrix (ECM) remodeling and intracellular events. Cells. 7(236)2018.PubMed/NCBI View Article : Google Scholar | |
|
Sanderson RD, Elkin M, Rapraeger AC, Ilan N and Vlodavsky I: Heparanase regulation of cancer, autophagy and inflammation: new mechanisms and targets for therapy. FEBS J. 284:42–55. 2017.PubMed/NCBI View Article : Google Scholar | |
|
David G and Zimmermann P: Heparanase involvement in exosome formation. Adv Exp Med Biol. 1221:285–307. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Simons M and Raposo G: Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol. 21:575–581. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Shteingauz A, Boyango I, Naroditsky I, Hammond E, Gruber M, Doweck I, Ilan N and Vlodavsky I: Heparanase enhances tumor growth and chemoresistance by promoting autophagy. Cancer Res. 75:3946–3957. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Schmidt EP, Overdier KH, Sun X, Lin L, Liu X, Yang Y, Ammons LA, Hiller TD, Suflita MA, Yu Y, et al: Urinary glycosaminoglycans predict outcomes in septic shock and acute respiratory distress syndrome. Am J Respir Crit Care Med. 194:439–449. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Masola V, Zaza G, Bellin G, Dall'Olmo L, Granata S, Vischini G, Secchi MF, Lupo A, Gambaro G and Onisto M: Heparanase regulates the M1 polarization of renal macrophages and their crosstalk with renal epithelial tubular cells after ischemia/reperfusion injury. FASEB J. 32:742–756. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Abassi Z, Hamoud S, Hassan A, Khamaysi I, Nativ O, Heyman SN, Muhammad RS, Ilan N, Singh P, Hammond E, et al: Involvement of heparanase in the pathogenesis of acute kidney injury: Nephroprotective effect of PG545. Oncotarget. 8:34191–34204. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Masola V, Zaza G, Gambaro G, Onisto M, Bellin G, Vischini G, Khamaysi I, Hassan A, Hamoud S, Nativ O, et al: Heparanase: A potential new factor involved in the renal epithelial mesenchymal transition (EMT) induced by ischemia/reperfusion (I/R) Injury. PLoS One. 11(e0160074)2016.PubMed/NCBI View Article : Google Scholar | |
|
Abu-Tayeh Suleiman H, Said S, Ali Saleh H, Gamliel-Lazarovich A, Haddad E, Minkov I, Zohar Y, Ilan N, Vlodavsky I, Abassi Z and Assady S: Heparanase increases podocyte survival and autophagic flux after adriamycin-induced injury. Int J Mol Sci. 23(12691)2022.PubMed/NCBI View Article : Google Scholar | |
|
Ilan N, Elkin M and Vlodavsky I: Regulation, function and clinical significance of heparanase in cancer metastasis and angiogenesis. Int J Biochem Cell Biol. 38:2018–2039. 2006.PubMed/NCBI View Article : Google Scholar | |
|
Parish CR, Freeman C and Hulett MD: Heparanase: A key enzyme involved in cell invasion. Biochim Biophys Acta. 1471:M99–M108. 2001.PubMed/NCBI View Article : Google Scholar | |
|
Secchi MF, Masola V, Zaza G, Lupo A, Gambaro G and Onisto M: Recent data concerning heparanase: Focus on fibrosis, inflammation and cancer. Biomol Concepts. 6:415–421. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Vlodavsky I, Beckhove P, Lerner I, Pisano C, Meirovitz A, Ilan N and Elkin M: Significance of heparanase in cancer and inflammation. Cancer Microenviron. 5:115–132. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Vreys V and David G: Mammalian heparanase: What is the message? J Cell Mol Med. 11:427–452. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Sanderson RD, Bandari SK and Vlodavsky I: Proteases and glycosidases on the surface of exosomes: Newly discovered mechanisms for extracellular remodeling. Matrix Biol. 75-76:160–169. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Xavier RJ and Podolsky DK: Unravelling the pathogenesis of inflammatory bowel disease. Nature. 448:427–434. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Belmiro CL, Souza HS, Elia CC, Castelo-Branco MT, Silva FR, Machado RL and Pavão MS: Biochemical and immunohistochemical analysis of glycosaminoglycans in inflamed and non-inflamed intestinal mucosa of patients with Crohn's disease. Int J Colorectal Dis. 20:295–304. 2005.PubMed/NCBI View Article : Google Scholar | |
|
Abassi Z and Goligorsky MS: Heparanase in acute kidney injury. Adv Exp Med Biol. 1221:685–702. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Axelsson J, Xu D, Kang BN, Nussbacher JK, Handel TM, Ley K, Sriramarao P and Esko JD: Inactivation of heparan sulfate 2-O-sulfotransferase accentuates neutrophil infiltration during acute inflammation in mice. Blood. 120:1742–1751. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Götte M: Syndecans in inflammation. FASEB J. 17:575–591. 2003.PubMed/NCBI View Article : Google Scholar | |
|
Carter NM, Ali S and Kirby JA: Endothelial inflammation: The role of differential expression of N-deacetylase/N-sulphotransferase enzymes in alteration of the immunological properties of heparan sulphate. J Cell Sci. 116(Pt 17):3591–3600. 2003.PubMed/NCBI View Article : Google Scholar | |
|
Uchimido R, Schmidt EP and Shapiro NI: The glycocalyx: A novel diagnostic and therapeutic target in sepsis. Crit Care. 23(16)2019.PubMed/NCBI View Article : Google Scholar | |
|
Becker BF, Jacob M, Leipert S, Salmon AH and Chappell D: Degradation of the endothelial glycocalyx in clinical settings: Searching for the sheddases. Br J Clin Pharmacol. 80:389–402. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Lupu F, Kinasewitz G and Dormer K: The role of endothelial shear stress on haemodynamics, inflammation, coagulation and glycocalyx during sepsis. J Cell Mol Med. 24:12258–12271. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Ponticelli C: Ischaemia-reperfusion injury: A major protagonist in kidney transplantation. Nephrol Dial Transplant. 29:1134–1140. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Bayam E, Kalçık M, Gürbüz AS, Yesin M, Güner A, Gündüz S, Gürsoy MO, Karakoyun S, Cerşit S, Kılıçgedik A, et al: The relationship between heparanase levels, thrombus burden and thromboembolism in patients receiving unfractionated heparin treatment for prosthetic valve thrombosis. Thromb Res. 171:103–110. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Masola V, Gambaro G, Tibaldi E, Brunati AM, Gastaldello A, D'Angelo A, Onisto M and Lupo A: Heparanase and syndecan-1 interplay orchestrates fibroblast growth factor-2-induced epithelial-mesenchymal transition in renal tubular cells. J Biol Chem. 287:1478–1488. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Jiang P and Mizushima N: Autophagy and human diseases. Cell Res. 24:69–79. 2014.PubMed/NCBI View Article : Google Scholar | |
|
He C and Klionsky DJ: Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet. 43:67–93. 2009.PubMed/NCBI View Article : Google Scholar | |
|
Singh R and Cuervo AM: Autophagy in the cellular energetic balance. Cell Metab. 13:495–504. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Melk A, Baisantry A and Schmitt R: The yin and yang of autophagy in acute kidney injury. Autophagy. 12:596–597. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Kim WY, Nam SA, Song HC, Ko JS, Park SH, Kim HL, Choi EJ, Kim YS, Kim J and Kim YK: The role of autophagy in unilateral ureteral obstruction rat model. Nephrology (Carlton). 17:148–159. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Zhang M, Sui W, Xing Y, Cheng J, Cheng C, Xue F, Zhang J, Wang X, Zhang C, Hao P and Zhang Y: Angiotensin IV attenuates diabetic cardiomyopathy via suppressing FoxO1-induced excessive autophagy, apoptosis and fibrosis. Theranostics. 11:8624–8639. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Jin H and Zhou S: The functions of heparanase in human diseases. Mini Rev Med Chem. 17:541–548. 2017.PubMed/NCBI View Article : Google Scholar | |
|
White E: Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer. 12:401–410. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Saiki S, Sasazawa Y, Imamichi Y, Kawajiri S, Fujimaki T, Tanida I, Kobayashi H, Sato F, Sato S, Ishikawa K, et al: Caffeine induces apoptosis by enhancement of autophagy via PI3K/Akt/mTOR/p70S6K inhibition. Autophagy. 7:176–187. 2011.PubMed/NCBI View Article : Google Scholar | |
|
Ferro V, Dredge K, Liu L, Hammond E, Bytheway I, Li C, Johnstone K, Karoli T, Davis K, Copeman E and Gautam A: PI-88 and novel heparan sulfate mimetics inhibit angiogenesis. Semin Thromb Hemost. 33:557–568. 2007.PubMed/NCBI View Article : Google Scholar | |
|
Rabelink TJ, van den Berg BM, Garsen M, Wang G, Elkin M and van der Vlag J: Heparanase: Roles in cell survival, extracellular matrix remodelling and the development of kidney disease. Nat Rev Nephrol. 13:201–212. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Suchorska WM and Lach MS: The role of exosomes in tumor progression and metastasis (Review). Oncol Rep. 35:1237–1244. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Oosthuyzen W, Sime NE, Ivy JR, Turtle EJ, Street JM, Pound J, Bath LE, Webb DJ, Gregory CD, Bailey MA and Dear JW: Quantification of human urinary exosomes by nanoparticle tracking analysis. J Physiol. 591:5833–5842. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Petrik J and Seghatchian J: Big things from small packages: The multifaceted roles of extracellular vesicles in the components quality, therapy and infection. Transfus Apher Sci. 55:4–8. 2016.PubMed/NCBI View Article : Google Scholar | |
|
Conlan RS, Pisano S, Oliveira MI, Ferrari M and Mendes Pinto I: Exosomes as reconfigurable therapeutic systems. Trends Mol Med. 23:636–650. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Essandoh K, Yang L, Wang X, Huang W, Qin D, Hao J, Wang Y, Zingarelli B, Peng T and Fan GC: Blockade of exosome generation with GW4869 dampens the sepsis-induced inflammation and cardiac dysfunction. Biochim Biophys Acta. 1852:2362–2371. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Kanki M, Moriguchi A, Sasaki D, Mitori H, Yamada A, Unami A and Miyamae Y: Identification of urinary miRNA biomarkers for detecting cisplatin-induced proximal tubular injury in rats. Toxicology. 324:158–168. 2014.PubMed/NCBI View Article : Google Scholar | |
|
Viñas JL, Spence M, Porter CJ, Douvris A, Gutsol A, Zimpelmann JA, Campbell PA and Burns KD: micro-RNA-486-5p protects against kidney ischemic injury and modifies the apoptotic transcriptome in proximal tubules. Kidney Int. 100:597–612. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Sun J, Sun X, Chen J, Liao X, He Y, Wang J, Chen R, Hu S and Qiu C: microRNA-27b shuttled by mesenchymal stem cell-derived exosomes prevents sepsis by targeting JMJD3 and downregulating NF-κB signaling pathway. Stem Cell Res Ther. 12(14)2021.PubMed/NCBI View Article : Google Scholar | |
|
Zhang R, Zhu Y, Li Y, Liu W, Yin L, Yin S, Ji C, Hu Y, Wang Q, Zhou X, et al: Human umbilical cord mesenchymal stem cell exosomes alleviate sepsis-associated acute kidney injury via regulating microRNA-146b expression. Biotechnol Lett. 42:669–679. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Juan CX, Mao Y, Cao Q, Chen Y, Zhou LB, Li S, Chen H, Chen JH, Zhou GP and Jin R: Exosome-mediated pyroptosis of miR-93-TXNIP-NLRP3 leads to functional difference between M1 and M2 macrophages in sepsis-induced acute kidney injury. J Cell Mol Med. 25:4786–4799. 2021.PubMed/NCBI View Article : Google Scholar | |
|
Lv LL, Feng Y, Wu M, Wang B, Li ZL, Zhong X, Wu WJ, Chen J, Ni HF, Tang TT, et al: Exosomal miRNA-19b-3p of tubular epithelial cells promotes M1 macrophage activation in kidney injury. Cell Death Differ. 27:210–226. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Thompson CA, Purushothaman A, Ramani VC, Vlodavsky I and Sanderson RD: Heparanase regulates secretion, composition, and function of tumor cell-derived exosomes. J Biol Chem. 288:10093–10099. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Roucourt B, Meeussen S, Bao J, Zimmermann P and David G: Heparanase activates the syndecan-syntenin-ALIX exosome pathway. Cell Res. 25:412–428. 2015.PubMed/NCBI View Article : Google Scholar | |
|
Bernfield M and Sanderson RD: Syndecan, a developmentally regulated cell surface proteoglycan that binds extracellular matrix and growth factors. Philos Trans R Soc Lond B Biol Sci. 327:171–186. 1990.PubMed/NCBI View Article : Google Scholar | |
|
Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, et al: Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol. 14:677–685. 2012.PubMed/NCBI View Article : Google Scholar | |
|
Bandari SK, Purushothaman A, Ramani VC, Brinkley GJ, Chandrashekar DS, Varambally S, Mobley JA, Zhang Y, Brown EE, Vlodavsky I and Sanderson RD: Chemotherapy induces secretion of exosomes loaded with heparanase that degrades extracellular matrix and impacts tumor and host cell behavior. Matrix Biol. 65:104–118. 2018.PubMed/NCBI View Article : Google Scholar | |
|
Cummings JJ, Shaw AD, Shi J, Lopez MG, O'Neal JB and Billings FT IV: Intraoperative prediction of cardiac surgery-associated acute kidney injury using urinary biomarkers of cell cycle arrest. J Thorac Cardiovasc Surg. 157:1545–1553.e5. 2019.PubMed/NCBI View Article : Google Scholar | |
|
Parikh CR, Thiessen-Philbrook H, Garg AX, Kadiyala D, Shlipak MG, Koyner JL, Edelstein CL, Devarajan P, Patel UD, Zappitelli M, et al: Performance of kidney injury molecule-1 and liver fatty acid-binding protein and combined biomarkers of AKI after cardiac surgery. Clin J Am Soc Nephrol. 8:1079–1088. 2013.PubMed/NCBI View Article : Google Scholar | |
|
Nakamura T, Sugaya T, Node K, Ueda Y and Koide H: Urinary excretion of liver-type fatty acid-binding protein in contrast medium-induced nephropathy. Am J Kidney Dis. 47:439–444. 2006.PubMed/NCBI View Article : Google Scholar | |
|
Mori K, Lee HT, Rapoport D, Drexler IR, Foster K, Yang J, Schmidt-Ott KM, Chen X, Li JY, Weiss S, et al: Endocytic delivery of lipocalin-siderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J Clin Invest. 115:610–621. 2005.PubMed/NCBI View Article : Google Scholar | |
|
Chen S, He Y, Hu Z, Lu S, Yin X, Ma X, Lv C and Jin G: Heparanase mediates intestinal inflammation and injury in a mouse model of sepsis. J Histochem Cytochem. 65:241–249. 2017.PubMed/NCBI View Article : Google Scholar | |
|
Kiyan Y, Tkachuk S, Kurselis K, Shushakova N, Stahl K, Dawodu D, Kiyan R, Chichkov B and Haller H: Heparanase-2 protects from LPS-mediated endothelial injury by inhibiting TLR4 signalling. Sci Rep. 9(13591)2019.PubMed/NCBI View Article : Google Scholar | |
|
McKenzie E, Tyson K, Stamps A, Smith P, Turner P, Barry R, Hircock M, Patel S, Barry E, Stubberfield C, et al: Cloning and expression profiling of Hpa2, a novel mammalian heparanase family member. Biochem Biophys Res Commun. 276:1170–1177. 2000.PubMed/NCBI View Article : Google Scholar | |
|
Pinhal MAS, Melo CM and Nader HB: The good and bad sides of heparanase-1 and heparanase-2. Adv Exp Med Biol. 1221:821–845. 2020.PubMed/NCBI View Article : Google Scholar | |
|
Bashkin P, Doctrow S, Klagsbrun M, Svahn CM, Folkman J and Vlodavsky I: Basic fibroblast growth factor binds to subendothelial extracellular matrix and is released by heparitinase and heparin-like molecules. Biochemistry. 28:1737–1743. 1989.PubMed/NCBI View Article : Google Scholar |
