8,630
Views
71
CrossRef citations to date
0
Altmetric
Review Article

Extracellular vesicles in type 2 diabetes mellitus: key roles in pathogenesis, complications, and therapy

ORCID Icon, , , ORCID Icon, ORCID Icon & ORCID Icon
Article: 1625677 | Received 22 Aug 2018, Accepted 28 May 2019, Published online: 14 Jun 2019

References

  • Punthakee Z, Goldenberg R, Katz P. Definition, classification and diagnosis of diabetes, prediabetes and metabolic syndrome. Can J Diabetes. 2018;42:10–14.
  • Jia G, Whaley-Connell A, Sowers JR. Diabetic cardiomyopathy: A hyperglycaemia- and insulin-resistance-induced heart disease. Diabetologia. 2018;61:21–28.
  • Schena FP, Gesualdo L. Pathogenetic mechanisms of diabetic nephropathy. J Am Soc Nephrol. 2005;16:30–33.
  • Tang Y, Zhang MJ, Hellmann J, et al. Proresolution therapy for the treatment of delayed healing of diabetic wounds. Diabetes. 2013;62:618–627.
  • Stitt AW, Curtis TM, Chen M, et al. The progress in understanding and treatment of diabetic retinopathy. Prog Retin Eye Res. 2016;51:156–186.
  • Saedi E, Gheini MR, Faiz F, et al. Diabetes mellitus and cognitive impairments. World J Diabetes. 2016;7:412–422.
  • Park Y, Colditz GA. Diabetes and adiposity: a heavy load for cancer. Lancet Diabetes Endocrinol. 2018;6:82–83.
  • World Health Organization. Global report on diabetes. Working Papers; 2016.
  • Cho NH, Shaw JE, Karuranga S, et al. Idf diabetes atlas: global estimates of diabetes prevalence for 2017 and projections for 2045. Diabetes Res Clin Pract. 2018;138:271–281.
  • American Diabetes Association. (2) classification and diagnosis of diabetes: standards of medical care in diabetes-2018. Diabetes Care. 2018;41:13–27.
  • Weyer C, Bogardus C, Mott DM, et al. The natural history of insulin secretory dysfunction and insulin resistance in the pathogenesis of type 2 diabetes mellitus. J Clin Invest. 1999;104:787–794.
  • Nomura S, Suzuki M, Katsura K, et al. Platelet-derived microparticles may influence the development of atherosclerosis in diabetes mellitus. Atherosclerosis. 1995;116:235–240.
  • Sabatier F, Darmon P, Hugel B, et al. Type 1 and type 2 diabetic patients display different patterns of cellular microparticles. Diabetes. 2002;51:2840–2845.
  • Mocharla P, Briand S, Giannotti G, et al. Angiomir-126 expression and secretion from circulating cd34(+) and cd14(+) pbmcs: role for proangiogenic effects and alterations in type 2 diabetics. Blood. 2013;121:226–236.
  • Mathiyalagan P, Liang Y, Kim D, et al. Angiogenic mechanisms of human cd34(+) stem cell exosomes in the repair of ischemic hindlimb. Circ Res. 2017;120:1466–1476.
  • Fry CS, Kirby TJ, Kosmac K, et al. Myogenic progenitor cells control extracellular matrix production by fibroblasts during skeletal muscle hypertrophy. Cell Stem Cell. 2017;20:56–69.
  • Song H, Li X, Zhao Z, et al. Reversal of osteoporotic activity by endothelial cell-secreted bone targeting and biocompatible exosomes. Nano Lett. 2019;19:3040–3048.
  • Flaherty SE 3rd, Grijalva A, Xu X, et al. A lipase-independent pathway of lipid release and immune modulation by adipocytes. Science. 2019;363:989–993.
  • Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164:1226–1232.
  • Shao H, Im H, Castro CM, et al. New technologies for analysis of extracellular vesicles. Chem Rev. 2018;118:1917–1950.
  • Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell. 1983;33:967–978.
  • Kowal J, Tkach M, Thery C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol. 2014;29:116–125.
  • Van Niel G, D’angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19:213–228.
  • Ostrowski M, Carmo NB, Krumeich S, et al. Rab27a and rab27b control different steps of the exosome secretion pathway. Nat Cell Biol. 2010;12:19–30.
  • Wolf P. The nature and significance of platelet products in human plasma. Br J Haematol. 1967;13:269–288.
  • Akers JC, Gonda D, Kim R, et al. Biogenesis of extracellular vesicles (ev): exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies. J Neurooncol. 2013;113:1–11.
  • Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255–289.
  • FaW C, Brisson AR, Buzas EI, et al. Methodological guidelines to study extracellular vesicles. Circ Res. 2017;120:1632–1648.
  • Gardiner C, Di Vizio D, Sahoo S, et al. Techniques used for the isolation and characterization of extracellular vesicles: results of a worldwide survey. J Extracell Vesicles. 2016;5:32945.
  • Mateescu B, Kowal EJ, Van Balkom BW, et al. Obstacles and opportunities in the functional analysis of extracellular vesicle rna - an isev position paper. J Extracell Vesicles. 2017;6:1286095.
  • Yamamoto CM, Murakami T, Oakes ML, et al. Uromodulin mrna from urinary extracellular vesicles correlate to kidney function decline in type 2 diabetes mellitus. Am J Nephrol. 2018;47:283–291.
  • Musante L, Tataruch D, Gu D, et al. Proteases and protease inhibitors of urinary extracellular vesicles in diabetic nephropathy. J Diabetes Res. 2015;2015:1–14.
  • Ravida A, Musante L, Kreivi M, et al. Glycosylation patterns of kidney proteins differ in rat diabetic nephropathy. Kidney Int. 2015;87:963–974.
  • Musante L, Tataruch DE, Holthofer H. Use and isolation of urinary exosomes as biomarkers for diabetic nephropathy. Front Endocrinol (Lausanne). 2014;5:149.
  • Karimi N, Cvjetkovic A, Jang SC, et al. Detailed analysis of the plasma extracellular vesicle proteome after separation from lipoproteins. Cell Mol Life Sci. 2018;75:2873–2886.
  • Liga A, Vliegenthart AD, Oosthuyzen W, et al. Exosome isolation: A microfluidic road-map. Lab Chip. 2015;15:2388–2394.
  • Reategui E, Van Der Vos KE, Lai CP, et al. Engineered nanointerfaces for microfluidic isolation and molecular profiling of tumor-specific extracellular vesicles. Nat Commun. 2018;9:175.
  • Liu C, Xu X, Li B, et al. Single-exosome-counting immunoassays for cancer diagnostics. Nano Lett. 2018;18:4226–4232.
  • Tian Y, Ma L, Gong M, et al. Protein profiling and sizing of extracellular vesicles from colorectal cancer patients via flow cytometry. ACS Nano. 2018;12:671–680.
  • Shen W, Guo K, Adkins GB, et al. A single extracellular vesicle (ev) flow cytometry approach to reveal ev heterogeneity. Angew Chem Int Ed Engl. 2018;57:15675–15680.
  • Sodar BW, Kittel A, Paloczi K, et al. Low-density lipoprotein mimics blood plasma-derived exosomes and microvesicles during isolation and detection. Sci Rep. 2016;6:24316.
  • Thery C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (misev2018): a position statement of the international society for extracellular vesicles and update of the misev2014 guidelines. J Extracell Vesicles. 2018;7:1535750.
  • Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016;113:968–977.
  • Jeppesen DK, Fenix AM, Franklin JL, et al. Reassessment of exosome composition. Cell. 2019;177:428–445.
  • Valadi H, Ekstrom K, Bossios A, et al. Exosome-mediated transfer of mrnas and micrornas is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654–659.
  • Maas SLN, Breakefield XO, Weaver AM. Extracellular vesicles: unique intercellular delivery vehicles. Trends Cell Biol. 2017;27:172–188.
  • Chen C, Zong S, Wang Z, et al. Visualization and intracellular dynamic tracking of exosomes and exosomal mirnas using single molecule localization microscopy. Nanoscale. 2018;10:5154–5162.
  • Truman-Rosentsvit M, Berenbaum D, Spektor L, et al. Ferritin is secreted via 2 distinct nonclassical vesicular pathways. Blood. 2018;131:342–352.
  • Lindenbergh MFS, Stoorvogel W. Antigen presentation by extracellular vesicles from professional antigen-presenting cells. Annu Rev Immunol. 2018;36:435–459.
  • Crewe C, Joffin N, Rutkowski JM, et al. An endothelial-to-adipocyte extracellular vesicle axis governed by metabolic state. Cell. 2018;175:695–708.
  • Nocera AL, Mueller SK, Stephan JR, et al. Exosome swarms eliminate airway pathogens and provide passive epithelial immunoprotection through nitric oxide. J Allergy Clin Immunol. 2019;143:1525–1535.
  • Sardar Sinha M, Ansell-Schultz A, Civitelli L, et al. Alzheimer’s disease pathology propagation by exosomes containing toxic amyloid-beta oligomers. Acta Neuropathol. 2018;136:41–56.
  • Pavlyukov MS, Yu H, Bastola S, et al. Apoptotic cell-derived extracellular vesicles promote malignancy of glioblastoma via intercellular transfer of splicing factors. Cancer Cell. 2018;34:119–135.
  • Nabet BY, Qiu Y, Shabason JE, et al. Exosome rna unshielding couples stromal activation to pattern recognition receptor signaling in cancer. Cell. 2017;170:352–366.
  • Chen G, Huang AC, Zhang W, et al. Exosomal pd-l1 contributes to immunosuppression and is associated with anti-pd-1 response. Nature. 2018;560:382–386.
  • Freeman DW, Noren Hooten N, Eitan E, et al. Altered extracellular vesicle concentration, cargo, and function in diabetes. Diabetes. 2018;67:2377–2388.
  • Olefsky JM, Glass CK. Macrophages, inflammation, and insulin resistance. Annu Rev Physiol. 2010;72:219–246.
  • Tateya S, Kim F, Tamori Y. Recent advances in obesity-induced inflammation and insulin resistance. Front Endocrinol (Lausanne). 2013;4:93.
  • Deng Z, Poliakov A, Hardy RW, et al. Adipose tissue exosome-like vesicles mediate activation of macrophage-induced insulin resistance. Diabetes. 2009;58:2498–2505.
  • Kranendonk ME, Visseren FL, Van Balkom BW, et al. Human adipocyte extracellular vesicles in reciprocal signaling between adipocytes and macrophages. Obesity. 2014;22:1296–1308.
  • Zhang Y, Mei H, Chang X, et al. Adipocyte-derived microvesicles from obese mice induce m1 macrophage phenotype through secreted mir-155. J Mol Cell Biol. 2016;8:505–517.
  • Song M, Han L, Chen FF, et al. Adipocyte-derived exosomes carrying sonic hedgehog mediate m1 macrophage polarization-induced insulin resistance via ptch and pi3k pathways. Cell Physiol Biochem. 2018;48:1416–1432.
  • Kranendonk ME, Visseren FL, Van Herwaarden JA, et al. Effect of extracellular vesicles of human adipose tissue on insulin signaling in liver and muscle cells. Obesity. 2015;22:2216–2223.
  • Zhang Y, Shi L, Mei H, et al. Inflamed macrophage microvesicles induce insulin resistance in human adipocytes. Nutr Metab (Lond). 2015;12:1–14.
  • 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;171:372–384.
  • Yu Y, Du H, Wei S, et al. Adipocyte-derived exosomal mir-27a induces insulin resistance in skeletal muscle through repression of pparγ. Theranostics. 2018;8:2171–2188.
  • Wang L, Zhang B, Zheng W, et al. Exosomes derived from pancreatic cancer cells induce insulin resistance in c2c12 myotube cells through the pi3k/akt/foxo1 pathway. Sci Rep. 2017;7:5384.
  • Yuasa T, Amo-Shiinoki K, Ishikura S, et al. Sequential cleavage of insulin receptor by calpain 2 and γ-secretase impairs insulin signalling. Diabetologia. 2016;59:2711–2721.
  • Ce H, Pe S. Tgf-beta1-induced epithelial-to-mesenchymal transition and therapeutic intervention in diabetic nephropathy. Am J Nephrol. 2010;31:68–74.
  • Delić D, Eisele C, Schmid R, et al. Urinary exosomal mirna signature in type II diabetic nephropathy patients. Plos One. 2016;11:e0150154.
  • Jia Y, Guan M, Zheng Z, et al. Mirnas in urine extracellular vesicles as predictors of early-stage diabetic nephropathy. J Diabetes Res. 2016;2016:1–10.
  • Wu X, Gao Y, Cui F, et al. Exosomes from high glucose-treated glomerular endothelial cells activate mesangial cells to promote renal fibrosis. Biol Open. 2016;5:484–491.
  • 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;7:9371.
  • Wang X, Huang W, Liu G, et al. Cardiomyocytes mediate anti-angiogenesis in type 2 diabetic rats through the exosomal transfer of mir-320 into endothelial cells. J Mol Cell Cardiol. 2014;74:139–150.
  • Davidson SM, Riquelme JA, Takov K, et al. Cardioprotection mediated by exosomes is impaired in the setting of type II diabetes but can be rescued by the use of non-diabetic exosomes in vitro. J Cell Mol Med. 2018;22:141–151.
  • Hu J, Wang S, Xiong Z, et al. Exosomal mst1 transfer from cardiac microvascular endothelial cells to cardiomyocytes deteriorates diabetic cardiomyopathy. Biochim Biophys Acta Mol Basis Dis. 2018;1864:3639–3649.
  • Mazzeo A, Beltramo E, Lopatina T, et al. Molecular and functional characterization of circulating extracellular vesicles from diabetic patients with and without retinopathy and healthy subjects. Exp Eye Res. 2018;176:69–77.
  • Huang C, Fisher KP, Hammer SS, et al. Plasma exosomes contribute to microvascular damage in diabetic retinopathy by activating the classical complement pathway. Diabetes. 2018;67:1639–1649.
  • Kamalden TA, Macgregor-Das AM, Kannan SM, et al. Exosomal microrna-15a transfer from the pancreas augments diabetic complications by inducing oxidative stress. Antioxid Redox Signal. 2017;27:913–930.
  • Liu C, Ge HM, Liu BH, et al. Targeting pericyte-endothelial cell crosstalk by circular rna-cpwwp2a inhibition aggravates diabetes-induced microvascular dysfunction. Proc Natl Acad Sci U S A. 2019;116:7455–7464.
  • Zhao H, Shang Q, Pan Z, et al. Exosomes from adipose-derived stem cells attenuate adipose inflammation and obesity through polarizing m2 macrophages and beiging in white adipose tissues. Diabetes. 2017;67:235–247.
  • Tsukita S, Yamada T, Takahashi K, et al. Micrornas 106b and 222 improve hyperglycemia in a mouse model of insulin-deficient diabetes via pancreatic β-cell proliferation. Ebiomedicine. 2017;15:163–172.
  • Sun Y, Shi H, Yin S, et al. Human mesenchymal stem cell derived exosomes alleviate type 2 diabetes mellitus by reversing peripheral insulin resistance and relieving beta-cell destruction. ACS Nano. 2018;12:7613–7628.
  • Geiger A, Walker A, Nissen E. Human fibrocyte-derived exosomes accelerate wound healing in genetically diabetic mice. Biochem Biophys Res Commun. 2015;467:303–309.
  • Chen CY, Rao SS, Ren L, et al. Exosomal dmbt1 from human urine-derived stem cells facilitates diabetic wound repair by promoting angiogenesis. Theranostics. 2018;8:1607–1623.
  • Li X, Xie X, Lian W, et al. Exosomes from adipose-derived stem cells overexpressing nrf2 accelerate cutaneous wound healing by promoting vascularization in a diabetic foot ulcer rat model. Exp Mol Med. 2018;50:29.
  • Tao SC, Rui BY, Wang QY, et al. Extracellular vesicle-mimetic nanovesicles transport lncrna-h19 as competing endogenous rna for the treatment of diabetic wounds. Drug Deliv. 2018;25:241–255.
  • Zhang J, Chen C, Hu B, et al. Exosomes derived from human endothelial progenitor cells accelerate cutaneous wound healing by promoting angiogenesis through erk1/2 signaling. Int J Biol Sci. 2016;12:1472–1487.
  • Li X, Jiang C, Zhao J. Human endothelial progenitor cells-derived exosomes accelerate cutaneous wound healing in diabetic rats by promoting endothelial function. J Diabetes Complications. 2016;30:986–992.
  • Guo SC, Tao SC, Yin WJ, et al. Exosomes derived from platelet-rich plasma promote the re-epithelization of chronic cutaneous wounds via activation of yap in a diabetic rat model. Theranostics. 2017;7:81–96.
  • Zhu LL, Huang X, Yu W, et al. Transplantation of adipose tissue-derived stem cell-derived exosomes ameliorates erectile function in diabetic rats. Andrologia. 2018;50:1–9.
  • Chen F, Zhang H, Wang Z, et al. Adipose-derived stem cell-derived exosomes ameliorate erectile dysfunction in a rat model of type 2 diabetes. J Sex Med. 2017;14:1084–1094.
  • Ouyang B, Xie Y, Zhang C, et al. Extracellular vesicles from human urine-derived stem cells ameliorate erectile dysfunction in a diabetic rat model by delivering proangiogenic microrna. Sex Med. 2019;7(2):241–250.
  • Nakano M, Nagaishi K, Konari N, et al. Bone marrow-derived mesenchymal stem cells improve diabetes-induced cognitive impairment by exosome transfer into damaged neurons and astrocytes. Sci Rep. 2016;6:24805.
  • Kalani A, Chaturvedi P, Maldonado C, et al. Dementia-like pathology in type-2 diabetes: a novel microrna mechanism. Mol Cell Neurosci. 2017;80:58–65.
  • Nagaishi K, Mizue Y, Chikenji T, et al. Mesenchymal stem cell therapy ameliorates diabetic nephropathy via the paracrine effect of renal trophic factors including exosomes. Sci Rep. 2016;6:34842.
  • Nagaishi K, Mizue Y, Chikenji T, et al. Umbilical cord extracts improve diabetic abnormalities in bone marrow-derived mesenchymal stem cells and increase their therapeutic effects on diabetic nephropathy. Sci Rep. 2017;7:8484.
  • Ebrahim N, Ahmed IA, Hussien NI, et al. Mesenchymal stem cell-derived exosomes ameliorated diabetic nephropathy by autophagy induction through the mtor signaling pathway. Cells. 2018;7:E226
  • Grange C, Tritta S, Tapparo M, et al. Stem cell-derived extracellular vesicles inhibit and revert fibrosis progression in a mouse model of diabetic nephropathy. Sci Rep. 2019;9:4468.
  • Wang X, Gu H, Wei H, et al. Hsp20-mediated activation of exosome biogenesis in cardiomyocytes improves cardiac function and angiogenesis in diabetic mice. Diabetes. 2016;65:3111–3128.
  • Luo Q, Guo D, Liu G, et al. Exosomes from mir-126-overexpressing adscs are therapeutic in relieving acute myocardial ischaemic injury. Cell Physiol Biochem. 2017;44:2105–2116.
  • Vandergriff A, Huang K, Shen D, et al. Targeting regenerative exosomes to myocardial infarction using cardiac homing peptide. Theranostics. 2018;8:1869–1878.
  • Mayourian J, Ceholski DK, Gorski PA, et al. Exosomal microrna-21-5p mediates mesenchymal stem cell paracrine effects on human cardiac tissue contractility. Circ Res. 2018;122:933–944.
  • Melo SA, Luecke LB, Christoph K, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523:177–182.
  • Hoshino A, Costa-Silva B, Shen TL, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527:329–335.
  • Tang MKS, Yue PYK, Ip PP, et al. Soluble e-cadherin promotes tumor angiogenesis and localizes to exosome surface. Nat Commun. 2018;9:2270.
  • Ela S, Mager I, Breakefield XO, et al. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov. 2013;12:347–357.
  • Kamerkar S, Lebleu VS, Sugimoto H, et al. Exosomes facilitate therapeutic targeting of oncogenic kras in pancreatic cancer. Nature. 2017;546:498–503.
  • Gao X, Ran N, Dong X, et al. Anchor peptide captures, targets, and loads exosomes of diverse origins for diagnostics and therapy. Sci Transl Med. 2018;10:1–14.
  • Fuhrmann G, Chandrawati R, Parmar PA, et al. Engineering extracellular vesicles with the tools of enzyme prodrug therapy. Adv Mater. 2018;30:e1706616.