574
Views
0
CrossRef citations to date
0
Altmetric
Chronic Kidney Disease and Progression

Research progress on the role of extracellular vesicles in the pathogenesis of diabetic kidney disease

&
Article: 2352629 | Received 01 Mar 2024, Accepted 02 May 2024, Published online: 20 May 2024

References

  • Samsu N. Diabetic nephropathy: challenges in pathogenesis, diagnosis, and treatment. Biomed Res Int. 2021;2021:1–11. Published 2021 Jul 8. doi:10.1155/2021/1497449.
  • Alicic RZ, Rooney MT, Tuttle KR. Diabetic kidney disease: challenges, progress, and possibilities. Clin J Am Soc Nephrol. 2017;12(12):2032–2045. doi:10.2215/CJN.11491116.
  • Tuttle KR, Agarwal R, Alpers CE, et al. Molecular mechanisms and therapeutic targets for diabetic kidney disease. Kidney Int. 2022;102(2):248–260. doi:10.1016/j.kint.2022.05.012.
  • Zoja C, Xinaris C, Macconi D. Diabetic nephropathy: novel molecular mechanisms and therapeutic targets. Front Pharmacol. 2020;11:586892. Published 2020 Dec 21. doi:10.3389/fphar.2020.586892.
  • Liu H, Feng J, Tang L. Early renal structural changes and potential biomarkers in diabetic nephropathy. Front Physiol. 2022;13:1020443. Published 2022 Nov 8. doi:10.3389/fphys.2022.1020443.
  • Tiwary M, Milder TY, Stocker SL, et al. Sodium-glucose co-transporter 2 inhibitor therapy: use in chronic kidney disease and adjunctive sodium restriction. Intern Med J. 2022;52(10):1666–1676. doi:10.1111/imj.15727.
  • Choi JG, Winn AN, Skandari MR, et al. First-line therapy for type 2 diabetes with sodium-glucose cotransporter-2 inhibitors and glucagon-like peptide-1 receptor agonists: a cost-effectiveness study. Ann Intern Med. 2022;175(10):1392–1400. doi:10.7326/M21-2941.
  • Lu Y, Liu D, Feng Q, et al. Diabetic nephropathy: perspective on extracellular vesicles. Front Immunol. 2020;11:943. Published 2020 Jun 3. doi:10.3389/fimmu.2020.00943.
  • Doyle LM, Wang MZ. Overview of extracellular vesicles, their origin, composition, purpose, and methods for exosome isolation and analysis. Cells. 2019;8(7):727. doi:10.3390/cells8070727.
  • Sykaras AG, Christofidis K, Politi E, et al. Exosomes on endometrial cancer: a biomarkers treasure trove? Cancers (Basel). 2022;14(7):1733. doi:10.3390/cancers14071733.
  • Kalluri R, LeBleu VS. The biology, function, and biomedical applications of exosomes. Science. 2020;367(6478):eaau6977. doi:10.1126/science.aau6977.
  • Toh WS, Lai RC, Zhang B, et al. MSC exosome works through a protein-based mechanism of action. Biochem Soc Trans. 2018;46(4):843–853. doi:10.1042/BST20180079.
  • Henne WM, Buchkovich NJ, Emr SD. The ESCRT pathway. Dev Cell. 2011;21(1):77–91. doi:10.1016/j.devcel.2011.05.015.
  • Colombo M, Raposo G, Théry C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30(1):255–289. doi:10.1146/annurev-cellbio-101512-122326.
  • Zhang Y, Bi J, Huang J, et al. Exosome: a review of its classification, isolation techniques, storage, diagnostic and targeted therapy applications. Int J Nanomedicine. 2020;15:6917–6934. Published 2020 Sep 22. doi:10.2147/IJN.S264498.
  • Migliano SM, Teis D. ESCRT and membrane protein ubiquitination. Prog Mol Subcell Biol. 2018;57:107–135.
  • Tran PHL, Xiang D, Tran TTD, et al. Exosomes and nanoengineering: a match made for precision therapeutics. Adv Mater. 2020;32(18):e1904040.
  • Ludwig N, Whiteside TL, Reichert TE. Challenges in exosome isolation and analysis in health and disease. Int J Mol Sci. 2019;20(19):4684. Published 2019 Sep 21. doi:10.3390/ijms20194684.
  • Zhou LI, Lv T, Zhang Q, et al. The biology, function and clinical implications of exosomes in lung cancer. Cancer Lett. 2017;407:84–92. doi:10.1016/j.canlet.2017.08.003.
  • Skotland T, Sandvig K, Llorente A. Lipids in exosomes: current knowledge and the way forward. Prog Lipid Res. 2017;66:30–41. doi:10.1016/j.plipres.2017.03.001.
  • Chopra N, Dutt Arya B, Jain N, et al. Biophysical characterization and drug delivery potential of exosomes from human wharton’s jelly‑derived mesenchymal stem cells. ACS Omega. 2019;4(8):13143–13152. doi:10.1021/acsomega.9b01180.
  • Zhuoyang Y, Yan T, Jing Y, et al. The role of exosomes in adult neurogenesis: implications for neurodegenerative diseases. Neural Regen Res. 2024;19(2):282–288. doi:10.4103/1673-5374.379036.
  • Jia L, Huang X, Peng H, et al. Pregnancy-specific beta-1-glycoprotein 1-enriched exosomes are involved in the regulation of vascular endothelial cell function during pregnancy. Placenta. 2023;139:138–147. doi:10.1016/j.placenta.2023.06.014.
  • Hong Y, Heo J, Kang S, et al. Exosome-mediated delivery of gga-miR-20a-5p regulates immune response of chicken macrophages by targeting IFNGR2, MAPK1, MAP3K5, and MAP3K14. Anim Biosci. 2023;36(6):851–860. doi:10.5713/ab.22.0373.
  • Wang KH, Ding DC. The role and applications of exosomes in gynecological cancer: a review. Cell Transplant. 2023;32:9636897231195240. doi:10.1177/09636897231195240.
  • Chen C, Wang C, Hu C, et al. Normoalbuminuric diabetic kidney disease. Front Med. 2017;11(3):310–318. doi:10.1007/s11684-017-0542-7.
  • Mulder S, Hamidi H, Kretzler M, et al. An integrative systems biology approach for precision medicine in diabetic kidney disease. Diabetes Obes Metab. 2018;20(Suppl 3):6–13. doi:10.1111/dom.13416.
  • Gudehithlu KP, Garcia-Gomez I, Vernik J, et al. In diabetic kidney disease urinary exosomes better represent kidney specific protein alterations than whole urine. Am J Nephrol. 2015;42(6):418–424. doi:10.1159/000443539.
  • Wang G, Szeto CC. Quantification of gene expression in urinary sediment for the study of renal diseases. Nephrology (Carlton). 2007;12(5):494–499. doi:10.1111/j.1440-1797.2007.00836.x.
  • Sinha N, Kumar V, Puri V, et al. Urinary exosomes: potential biomarkers for diabetic nephropathy. Nephrology (Carlton). 2020;25(12):881–887. doi:10.1111/nep.13720.
  • Lv LL, Cao YH, Pan MM, et al. CD2AP mRNA in urinary exosome as biomarker of kidney disease. Clin Chim Acta. 2014;428:26–31. doi:10.1016/j.cca.2013.10.003.
  • Zhao Y, Shen A, Guo F, et al. Urinary exosomal MiRNA-4534 as a novel diagnostic biomarker for diabetic kidney disease. Front Endocrinol (Lausanne). 2020;11:590. Published 2020 Aug 28. doi:10.3389/fendo.2020.00590.
  • Feng Y, Zhong X, Ni HF, et al. Urinary small extracellular vesicles derived CCL21 mRNA as biomarker linked with pathogenesis for diabetic nephropathy. J Transl Med. 2021;19(1):355. Published 2021 Aug 17. doi:10.1186/s12967-021-03030-x.
  • Wang J, Tao Y, Zhao F, et al. Expression of urinary exosomal miRNA-615-3p and miRNA-3147 in diabetic kidney disease and their association with inflammation and fibrosis. Ren Fail. 2023;45(1):2121929.
  • Han LL, Wang SH, Yao MY, et al. Urinary exosomal microRNA-145-5p and microRNA-27a-3p act as noninvasive diagnostic biomarkers for diabetic kidney disease. World J Diabetes. 2024;15(1):92–104. doi:10.4239/wjd.v15.i1.92.
  • Su J, Li SJ, Chen ZH, et al. Evaluation of podocyte lesion in patients with diabetic nephropathy: wilms’ tumor-1 protein used as a podocyte marker. Diabetes Res Clin Pract. 2010;87(2):167–175. doi:10.1016/j.diabres.2009.10.022.
  • Kalani A, Mohan A, Godbole MM, et al. Wilm’s tumor-1 protein levels in urinary exosomes from diabetic patients with or without proteinuria. PLoS One. 2013;8(3):e60177. doi:10.1371/journal.pone.0060177.
  • Guerrero-Hernandez A, Verkhratsky A. Calcium signalling in diabetes. Cell Calcium. 2014;56(5):297–301. doi:10.1016/j.ceca.2014.08.009.
  • Li T, Ci Liu T, Liu N, et al. Changes in urinary exosomal protein CALM1 may serve as an early noninvasive biomarker for diagnosing diabetic kidney disease. Clin Chim Acta. 2023;547:117466. doi:10.1016/j.cca.2023.117466.
  • Regmi A, Liu G, Zhong X, et al. Evaluation of serum microRNAs in patients with diabetic kidney disease: a nested case-controlled study and bioinformatics analysis. Med Sci Monit. 2019;25:1699–1708. Published 2019 Mar 5. doi:10.12659/MSM.913265.
  • Prattichizzo F, De Nigris V, Sabbatinelli J, et al. CD31+ extracellular vesicles from patients with type 2 diabetes shuttle a miRNA signature associated with cardiovascular complications. Diabetes. 2021;70(1):240–254. doi:10.2337/db20-0199.
  • Prattichizzo F, Matacchione G, Giuliani A, et al. Extracellular vesicle-shuttled miRNAs: a critical appraisal of their potential as nano-diagnostics and nano-therapeutics in type 2 diabetes mellitus and its cardiovascular complications. Theranostics. 2021;11(3):1031–1045. doi:10.7150/thno.51605.
  • Olivieri F, Prattichizzo F, Giuliani A, et al. miR-21 and miR-146a: the microRNAs of inflammaging and age-related diseases. Ageing Res Rev. 2021;70:101374. doi:10.1016/j.arr.2021.101374.
  • Kangas R, Pöllänen E, Rippo MR, et al. Circulating miR-21, miR-146a and fas ligand respond to postmenopausal estrogen-based hormone replacement therapy–a study with monozygotic twin pairs. Mech Ageing Dev. 2014;143-144:1–8. doi:10.1016/j.mad.2014.11.001.
  • Kidney disease: improving global outcomes (KDIGO) diabetes work group. KDIGO 2020 clinical practice guideline for diabetes management in chronic kidney disease. Kidney Int. 2020;98(4S):S1–S115.
  • da Silva Novaes A, Borges FT, Maquigussa E, et al. Influence of high glucose on mesangial cell-derived exosome composition, secretion and cell communication [published correction appears in sci rep. 2020 jan 29;10(1):1730]. Sci Rep. 2019;9(1):6270. Published 2019 Apr 18. doi:10.1038/s41598-019-42746-1.
  • Donate-Correa J, Luis-Rodríguez D, Martín-Núñez E, et al. Inflammatory targets in diabetic nephropathy. J Clin Med. 2020;9(2):458. Published 2020 Feb 7. doi:10.3390/jcm9020458.
  • Tian S, Chen SY. Macrophage polarization in kidney diseases. Macrophage (Houst). 2015;2(1):e679.
  • Arabpour M, Saghazadeh A, Rezaei N. Anti-inflammatory and M2 macrophage polarization-promoting effect of mesenchymal stem cell-derived exosomes. Int Immunopharmacol. 2021;97:107823. doi:10.1016/j.intimp.2021.107823.
  • Liu Y, Li X, Zhao M, et al. Macrophage-derived exosomes promote activation of NLRP3 inflammasome and autophagy deficiency of mesangial cells in diabetic nephropathy. Life Sci. 2023;330:121991. doi:10.1016/j.lfs.2023.121991.
  • Zhao J, Chen J, Zhu W, et al. Exosomal miR-7002-5p derived from highglucose-induced macrophages suppresses autophagy in tubular epithelial cells by targeting Atg9b. FASEB J. 2022;36(9):e22501.
  • Zhang Y, Le X, Zheng S, et al. MicroRNA-146a-5p-modified human umbilical cord mesenchymal stem cells enhance protection against diabetic nephropathy in rats through facilitating M2 macrophage polarization. Stem Cell Res Ther. 2022;13(1):171. Published 2022 Apr 27. doi:10.1186/s13287-022-02855-7.
  • Li Y, Liu J, Liao G, et al. Early intervention with mesenchymal stem cells prevents nephropathy in diabetic rats by ameliorating the inflammatory microenvironment. Int J Mol Med. 2018;41(5):2629–2639. doi:10.3892/ijmm.2018.3501.
  • Ma L, Wu F, Shao Q, et al. Baicalin alleviates oxidative stress and inflammation in diabetic nephropathy via Nrf2 and MAPK signaling pathway. Drug Des Devel Ther. 2021;15:3207–3221. Published 2021 Jul 21. doi:10.2147/DDDT.S319260.
  • Jha JC, Banal C, Chow BS, et al. Diabetes and kidney disease: role of oxidative stress. Antioxid Redox Signal. 2016;25(12):657–684. doi:10.1089/ars.2016.6664.
  • Hasegawa K, Wakino S, Yoshioka K, et al. Sirt1 protects against oxidative stress-induced renal tubular cell apoptosis by the bidirectional regulation of catalase expression. Biochem Biophys Res Commun. 2008;372(1):51–56. doi:10.1016/j.bbrc.2008.04.176.
  • Zeng S, Wu X, Chen X, et al. Hypermethylated in cancer 1 (HIC1) mediates high glucose induced ROS accumulation in renal tubular epithelial cells by epigenetically repressing SIRT1 transcription. Biochim Biophys Acta Gene Regul Mech. 2018;1861(10):917–927. doi:10.1016/j.bbagrm.2018.08.002.
  • Gao C, Wang B, Chen Q, et al. Serum exosomes from diabetic kidney disease patients promote pyroptosis and oxidative stress through the miR-4449/HIC1 pathway. Nutr Diabetes. 2021;11(1):33. Published 2021 Nov 3. doi:10.1038/s41387-021-00175-y.
  • Zeng LF, Xiao Y, Sun L. A glimpse of the mechanisms related to renal fibrosis in diabetic nephropathy. Adv Exp Med Biol. 2019;1165:49–79.
  • Mora C, Navarro JF. Inflammation and pathogenesis of diabetic nephropathy. Metabolism. 2004;53(2):265–266. doi:10.1016/j.metabol.2003.11.005.
  • Ma TT, Meng XM. TGF-β/smad and renal fibrosis. Adv Exp Med Biol. 2019;1165:347–364.
  • Wu XM, Gao YB, Cui FQ, et al. Exosomes from high glucose-treated glomerular endothelial cells activate mesangial cells to promote renal fibrosis. Biol Open. 2016;5(4):484–491. doi:10.1242/bio.015990.
  • Zhang Y, Qin X, Yang Y, et al. Ginkgo biloba extract attenuates cisplatin-induced renal interstitial fibrosis by inhibiting the activation of renal fibroblasts through down-regulating the HIF-1α/STAT3/IL-6 pathway in renal tubular epithelial cells. Phytomedicine. 2023;115:154809. doi:10.1016/j.phymed.2023.154809.
  • Tsai YC, Kuo MC, Hung WW, et al. Proximal tubule-derived exosomes contribute to mesangial cell injury in diabetic nephropathy via miR-92a-1-5p transfer. Cell Commun Signal. 2023;21(1):10. Published 2023 Jan 13. doi:10.1186/s12964-022-00997-y.
  • Bai S, Xiong X, Tang B, et al. Exosomal circ_DLGAP4 promotes diabetic kidney disease progression by sponging miR-143 and targeting ERBB3/NF-κB/MMP-2 axis. Cell Death Dis. 2020;11(11):1008. Published 2020 Nov 23. doi:10.1038/s41419-020-03169-3.
  • Liu D, Liu F, Li Z, et al. HNRNPA1-mediated exosomal sorting of miR-483-5p out of renal tubular epithelial cells promotes the progression of diabetic nephropathy-induced renal interstitial fibrosis. Cell Death Dis. 2021;12(3):255. Published 2021 Mar 10. doi:10.1038/s41419-021-03460-x.
  • Yang B, Chen Y, Shi J. Exosome biochemistry and advanced nanotechnology for Next-Generation theranostic platforms. Adv Mater. 2019;31(2):e1802896.
  • Grange C, Bussolati B. Extracellular vesicles in kidney disease. Nat Rev Nephrol. 2022;18(8):499–513. doi:10.1038/s41581-022-00586-9.
  • Tung CW, Hsu YC, Shih YH, et al. Glomerular mesangial cell and podocyte injuries in diabetic nephropathy. Nephrology (Carlton). 2018;23 Suppl 4:32–37. doi:10.1111/nep.13451.
  • Barutta F, Bellini S, Gruden G. Mechanisms of podocyte injury and implications for diabetic nephropathy. Clin Sci (Lond). 2022;136(7):493–520. doi:10.1042/CS20210625.
  • Lu Z, Liu H, Song N, et al. METTL14 aggravates podocyte injury and glomerulopathy progression through N6-methyladenosine-dependent downregulating of Sirt1. Cell Death Dis. 2021;12(10):881. Published 2021 Sep 27. doi:10.1038/s41419-021-04156-y.
  • Li XZ, Jiang H, Xu L, et al. Sarsasapogenin restores podocyte autophagy in diabetic nephropathy by targeting GSK3β signaling pathway. Biochem Pharmacol. 2021;192:114675. doi:10.1016/j.bcp.2021.114675.
  • Zhang H, Yan Y, Hu Q, et al. LncRNA MALAT1/microRNA let-7f/KLF5 axis regulates podocyte injury in diabetic nephropathy [retracted in: life sci. 2023 apr 1;318:121420]. Life Sci. 2021;266:118794. doi:10.1016/j.lfs.2020.118794.
  • Guo F, Song Y, Wu L, et al. SUMO specific peptidase 6 regulates the crosstalk between podocytes and glomerular endothelial cells in diabetic kidney disease. Biochim Biophys Acta Mol Basis Dis. 2023;1869(5):166685. doi:10.1016/j.bbadis.2023.166685.
  • Wu X, Gao Y, Xu L, et al. Exosomes from high glucose-treated glomerular endothelial cells trigger the epithelial-mesenchymal transition and dysfunction of podocytes. Sci Rep. 2017;7(1):9371. Published 2017 Aug 24. doi:10.1038/s41598-017-09907-6.
  • Ling L, Tan Z, Zhang C, et al. CircRNAs in exosomes from high glucose-treated glomerular endothelial cells activate mesangial cells. Am J Transl Res. 2019;11(8):4667–4682.
  • Wang YY, Tang LQ, Wei W. Berberine attenuates podocytes injury caused by exosomes derived from high glucose-induced mesangial cells through TGFβ1-PI3K/AKT pathway. Eur J Pharmacol. 2018;824:185–192. doi:10.1016/j.ejphar.2018.01.034.
  • Marušić M, Paić M, Knobloch M, et al. NAFLD, insulin resistance, and diabetes mellitus type 2. Can J Gastroenterol Hepatol. 2021;2021:6613827–6613829. doi:10.1155/2021/6613827.
  • Lebovitz HE. Insulin resistance: definition and consequences. Exp Clin Endocrinol Diabetes. 2001;109(Suppl 2):S135–S148. doi:10.1055/s-2001-18576.
  • Artunc F, Schleicher E, Weigert C, et al. The impact of insulin resistance on the kidney and vasculature. Nat Rev Nephrol. 2016;12(12):721–737. doi:10.1038/nrneph.2016.145.
  • Adeva-Andany MM, Fernández-Fernández C, Funcasta-Calderón R, et al. Insulin resistance is associated with clinical manifestations of diabetic kidney disease (glomerular hyperfiltration, albuminuria, and kidney function decline). Curr Diabetes Rev. 2022;18(7):e171121197998.
  • De Taeye BM, Novitskaya T, McGuinness OP, et al. Macrophage TNF-alpha contributes to insulin resistance and hepatic steatosis in diet-induced obesity. Am J Physiol Endocrinol Metab. 2007;293(3):E713–E725. doi:10.1152/ajpendo.00194.2007.
  • Mafi A, Aghadavod E, Mirhosseini N, et al. The effects of expression of different microRNAs on insulin secretion and diabetic nephropathy progression. J Cell Physiol. 2018;234(1):42–50. doi:10.1002/jcp.26895.
  • Ying W, Riopel M, Bandyopadhyay G, et al. Adipose tissue macrophage-derived exosomal miRNAs can modulate in vivo and in vitro insulin sensitivity. Cell. 2017;171(2):372–384.e12. doi:10.1016/j.cell.2017.08.035.
  • Zhang L, Li K, Liu X, et al. Repeated systemic administration of human adipose-derived stem cells attenuates overt diabetic nephropathy in rats. Stem Cells Dev. 2013;22(23):3074–3086. doi:10.1089/scd.2013.0142.
  • Wang Y, Liu J, Wang H, et al. Mesenchymal stem cell-derived exosomes ameliorate diabetic kidney disease through the NLRP3 signaling pathway. Stem Cells. 2023;41(4):368–383. doi:10.1093/stmcls/sxad010.
  • Ren P, Qian F, Fu L, et al. Adipose-derived stem cell exosomes regulate Nrf2/Keap1 in diabetic nephropathy by targeting FAM129B. Diabetol Metab Syndr. 2023;15(1):149. Published 2023 Jul 4. doi:10.1186/s13098-023-01119-5.
  • Lv J, Hao YN, Wang XP, et al. Bone marrow mesenchymal stem cell-derived exosomal miR-30e-5p ameliorates high-glucose induced renal proximal tubular cell pyroptosis by inhibiting ELAVL1. Ren Fail. 2023;45(1):2177082.
  • Cui C, Zang N, Song J, et al. Exosomes derived from mesenchymal stem cells attenuate diabetic kidney disease by inhibiting cell apoptosis and epithelial-to-mesenchymal transition via miR-424-5p. FASEB J. 2022;36(10):e22517.
  • Chen J, Chen J, Cheng Y, et al. Mesenchymal stem cell-derived exosomes protect beta cells against hypoxia-induced apoptosis via miR-21 by alleviating ER stress and inhibiting p38 MAPK phosphorylation. Stem Cell Res Ther. 2020;11(1):97. Published 2020 Mar 4. doi:10.1186/s13287-020-01610-0.
  • Ji JL, Shi HM, Li ZL, et al. Satellite cell-derived exosome-mediated delivery of microRNA-23a/27a/26a cluster ameliorates the renal tubulointerstitial fibrosis in mouse diabetic nephropathy. Acta Pharmacol Sin. 2023;44(12):2455–2468. doi:10.1038/s41401-023-01140-4.
  • Zhuang Y, Zheng H, Yang Y, et al. GABA alleviates high glucose-induced podocyte injury through dynamically altering the expression of macrophage M1/M2-derived exosomal miR-21a-5p/miR-25-3p. Biochem Biophys Res Commun. 2022;618:38–45. doi:10.1016/j.bbrc.2022.06.019.
  • Li X, Guo L, Chen J, et al. Intravenous injection of human umbilical cord-derived mesenchymal stem cells ameliorates not only blood glucose but also nephrotic complication of diabetic rats through autophagy-mediated anti-senescent mechanism. Stem Cell Res Ther. 2023;14(1):146. Published 2023 May 29. doi:10.1186/s13287-023-03354-z.
  • Wang Z, Sun W, Li R, et al. miRNA-93-5p in exosomes derived from M2 macrophages improves lipopolysaccharide-induced podocyte apoptosis by targeting toll-like receptor 4. Bioengineered. 2022;13(3):7683–7696. doi:10.1080/21655979.2021.2023794.