Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Oncology Letters
      • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Biomedical Reports
      • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • Information for Authors
    • Information for Reviewers
    • Information for Librarians
    • Information for Advertisers
    • Conferences
  • Language Editing
Spandidos Publications Logo
  • About
    • About Spandidos
    • Aims and Scopes
    • Abstracting and Indexing
    • Editorial Policies
    • Reprints and Permissions
    • Job Opportunities
    • Terms and Conditions
    • Contact
  • Journals
    • All Journals
    • Biomedical Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Experimental and Therapeutic Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Epigenetics
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Functional Nutrition
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Molecular Medicine
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • International Journal of Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Medicine International
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular and Clinical Oncology
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Molecular Medicine Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Letters
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • Oncology Reports
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
    • World Academy of Sciences Journal
      • Information for Authors
      • Editorial Policies
      • Editorial Board
      • Aims and Scope
      • Abstracting and Indexing
      • Bibliographic Information
      • Archive
  • Articles
  • Information
    • For Authors
    • For Reviewers
    • For Librarians
    • For Advertisers
    • Conferences
  • Language Editing
Login Register Submit
  • This site uses cookies
  • You can change your cookie settings at any time by following the instructions in our Cookie Policy. To find out more, you may read our Privacy Policy.

    I agree
Search articles by DOI, keyword, author or affiliation
Search
Advanced Search
presentation
Experimental and Therapeutic Medicine
Join Editorial Board Propose a Special Issue
Print ISSN: 1792-0981 Online ISSN: 1792-1015
Journal Cover
August-2023 Volume 26 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

Journals

International Journal of Molecular Medicine

International Journal of Molecular Medicine

International Journal of Molecular Medicine is an international journal devoted to molecular mechanisms of human disease.

International Journal of Oncology

International Journal of Oncology

International Journal of Oncology is an international journal devoted to oncology research and cancer treatment.

Molecular Medicine Reports

Molecular Medicine Reports

Covers molecular medicine topics such as pharmacology, pathology, genetics, neuroscience, infectious diseases, molecular cardiology, and molecular surgery.

Oncology Reports

Oncology Reports

Oncology Reports is an international journal devoted to fundamental and applied research in Oncology.

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine

Experimental and Therapeutic Medicine is an international journal devoted to laboratory and clinical medicine.

Oncology Letters

Oncology Letters

Oncology Letters is an international journal devoted to Experimental and Clinical Oncology.

Biomedical Reports

Biomedical Reports

Explores a wide range of biological and medical fields, including pharmacology, genetics, microbiology, neuroscience, and molecular cardiology.

Molecular and Clinical Oncology

Molecular and Clinical Oncology

International journal addressing all aspects of oncology research, from tumorigenesis and oncogenes to chemotherapy and metastasis.

World Academy of Sciences Journal

World Academy of Sciences Journal

Multidisciplinary open-access journal spanning biochemistry, genetics, neuroscience, environmental health, and synthetic biology.

International Journal of Functional Nutrition

International Journal of Functional Nutrition

Open-access journal combining biochemistry, pharmacology, immunology, and genetics to advance health through functional nutrition.

International Journal of Epigenetics

International Journal of Epigenetics

Publishes open-access research on using epigenetics to advance understanding and treatment of human disease.

Medicine International

Medicine International

An International Open Access Journal Devoted to General Medicine.

Journal Cover
August-2023 Volume 26 Issue 2

Full Size Image

Sign up for eToc alerts
Recommend to Library

  • Article
  • Citations
    • Cite This Article
    • Download Citation
    • Create Citation Alert
    • Remove Citation Alert
    • Cited By
  • Similar Articles
    • Related Articles (in Spandidos Publications)
    • Similar Articles (Google Scholar)
    • Similar Articles (PubMed)
  • Download PDF
  • Download XML
  • View XML
Review Open Access

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
  • View Affiliations / Copyright

    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
    Copyright: © Li et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
  • Article Number: 379
    |
    Published online on: June 26, 2023
       https://doi.org/10.3892/etm.2023.12078
  • Expand metrics +
Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )
Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )
Cited By (CrossRef): 0 citations Loading Articles...

This article is mentioned in:



Abstract

Sepsis‑related acute kidney injury (S‑AKI) is a common and significant complication of sepsis in critically ill patients, which can often only be treated with antibiotics and medications that reduce S‑AKI symptoms. The precise mechanism underlying the onset of S‑AKI is still unclear, thus hindering the development of new strategies for its treatment. Therefore, it is necessary to explore the pathogenesis of S‑AKI to identify biomarkers and therapeutic targets for its early diagnosis and treatment. Heparanase (HPA), the only known enzyme that cleaves the side chain of heparan sulfate, has been widely studied in relation to tumor metabolism, procoagulant activity, angiogenesis, inflammation and sepsis. It has been reported that HPA plays an important role in the progression of S‑AKI. The aim of the present review was to provide an overview of the function of HPA in S‑AKI and to summarize its underlying molecular mechanisms, including mediating inflammatory response, immune response, autophagy and exosome biogenesis. It is anticipated that emerging discoveries about HPA in S‑AKI will support HPA as a potential biomarker and therapeutic target to combat S‑AKI.
View Figures

Figure 1

Figure 2

View References

1 

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

2 

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

3 

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

4 

Ronco C, Bellomo R and Kellum JA: Acute kidney injury. Lancet. 394:1949–1964. 2019.PubMed/NCBI View Article : Google Scholar

5 

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

6 

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

7 

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

8 

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

9 

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

10 

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

11 

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

12 

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

13 

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).

14 

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

15 

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

16 

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

17 

Poston JT and Koyner JL: Sepsis associated acute kidney injury. BMJ. 364(k4891)2019.PubMed/NCBI View Article : Google Scholar

18 

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

19 

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

20 

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

21 

Ince C: The microcirculation is the motor of sepsis. Crit Care. 9 (Suppl 4):S13–S19. 2005.PubMed/NCBI View Article : Google Scholar

22 

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

23 

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

24 

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

25 

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

26 

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

27 

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

28 

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

29 

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

30 

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

31 

Kawai T and Akira S: TLR signaling. Semin Immunol. 19:24–32. 2007.PubMed/NCBI View Article : Google Scholar

32 

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

33 

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

34 

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

35 

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

36 

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

37 

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

38 

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

39 

Wilson DF: Oxidative phosphorylation: Regulation and role in cellular and tissue metabolism. J Physiol. 595:7023–7038. 2017.PubMed/NCBI View Article : Google Scholar

40 

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

41 

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

42 

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

43 

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

44 

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

45 

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

46 

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

47 

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

48 

Levey AS and James MT: Acute kidney injury. Ann Intern Med. 167:ITC66–ITC80. 2017.PubMed/NCBI View Article : Google Scholar

49 

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

50 

Rosenfeldt MT and Ryan KM: The multiple roles of autophagy in cancer. Carcinogenesis. 32:955–963. 2011.PubMed/NCBI View Article : Google Scholar

51 

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

52 

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

53 

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

54 

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

55 

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

56 

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

57 

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

58 

David G and Zimmermann P: Heparanase involvement in exosome formation. Adv Exp Med Biol. 1221:285–307. 2020.PubMed/NCBI View Article : Google Scholar

59 

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

60 

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

61 

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

62 

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

63 

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

64 

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

65 

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

66 

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

67 

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

68 

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

69 

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

70 

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

71 

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

72 

Xavier RJ and Podolsky DK: Unravelling the pathogenesis of inflammatory bowel disease. Nature. 448:427–434. 2007.PubMed/NCBI View Article : Google Scholar

73 

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

74 

Abassi Z and Goligorsky MS: Heparanase in acute kidney injury. Adv Exp Med Biol. 1221:685–702. 2020.PubMed/NCBI View Article : Google Scholar

75 

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

76 

Götte M: Syndecans in inflammation. FASEB J. 17:575–591. 2003.PubMed/NCBI View Article : Google Scholar

77 

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

78 

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

79 

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

80 

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

81 

Ponticelli C: Ischaemia-reperfusion injury: A major protagonist in kidney transplantation. Nephrol Dial Transplant. 29:1134–1140. 2014.PubMed/NCBI View Article : Google Scholar

82 

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

83 

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

84 

Jiang P and Mizushima N: Autophagy and human diseases. Cell Res. 24:69–79. 2014.PubMed/NCBI View Article : Google Scholar

85 

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

86 

Singh R and Cuervo AM: Autophagy in the cellular energetic balance. Cell Metab. 13:495–504. 2011.PubMed/NCBI View Article : Google Scholar

87 

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

88 

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

89 

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

90 

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

91 

White E: Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer. 12:401–410. 2012.PubMed/NCBI View Article : Google Scholar

92 

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

93 

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

94 

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

95 

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

96 

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

97 

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

98 

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

99 

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

100 

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

101 

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

102 

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

103 

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

104 

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

105 

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

106 

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

107 

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

108 

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

109 

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

110 

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

111 

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

112 

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

113 

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

114 

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

115 

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

116 

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

117 

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

118 

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

119 

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

Related Articles

  • Abstract
  • View
  • Download
  • Twitter
Copy and paste a formatted citation
Spandidos Publications style
Li J, Wang L, Feng F, Chen T, Shi W and Liu L: Role of heparanase in sepsis‑related acute kidney injury (Review). Exp Ther Med 26: 379, 2023.
APA
Li, J., Wang, L., Feng, F., Chen, T., Shi, W., & Liu, L. (2023). Role of heparanase in sepsis‑related acute kidney injury (Review). Experimental and Therapeutic Medicine, 26, 379. https://doi.org/10.3892/etm.2023.12078
MLA
Li, J., Wang, L., Feng, F., Chen, T., Shi, W., Liu, L."Role of heparanase in sepsis‑related acute kidney injury (Review)". Experimental and Therapeutic Medicine 26.2 (2023): 379.
Chicago
Li, J., Wang, L., Feng, F., Chen, T., Shi, W., Liu, L."Role of heparanase in sepsis‑related acute kidney injury (Review)". Experimental and Therapeutic Medicine 26, no. 2 (2023): 379. https://doi.org/10.3892/etm.2023.12078
Copy and paste a formatted citation
x
Spandidos Publications style
Li J, Wang L, Feng F, Chen T, Shi W and Liu L: Role of heparanase in sepsis‑related acute kidney injury (Review). Exp Ther Med 26: 379, 2023.
APA
Li, J., Wang, L., Feng, F., Chen, T., Shi, W., & Liu, L. (2023). Role of heparanase in sepsis‑related acute kidney injury (Review). Experimental and Therapeutic Medicine, 26, 379. https://doi.org/10.3892/etm.2023.12078
MLA
Li, J., Wang, L., Feng, F., Chen, T., Shi, W., Liu, L."Role of heparanase in sepsis‑related acute kidney injury (Review)". Experimental and Therapeutic Medicine 26.2 (2023): 379.
Chicago
Li, J., Wang, L., Feng, F., Chen, T., Shi, W., Liu, L."Role of heparanase in sepsis‑related acute kidney injury (Review)". Experimental and Therapeutic Medicine 26, no. 2 (2023): 379. https://doi.org/10.3892/etm.2023.12078
Follow us
  • Twitter
  • LinkedIn
  • Facebook
About
  • Spandidos Publications
  • Careers
  • Cookie Policy
  • Privacy Policy
How can we help?
  • Help
  • Live Chat
  • Contact
  • Email to our Support Team