The Role of Adipose Tissue-derived Exosomes in Chronic Metabolic Disorders

Rui He , Yong Chen

Current Medical Science ›› 2024, Vol. 44 ›› Issue (3) : 463 -474.

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Current Medical Science ›› 2024, Vol. 44 ›› Issue (3) : 463 -474. DOI: 10.1007/s11596-024-2902-2
Review

The Role of Adipose Tissue-derived Exosomes in Chronic Metabolic Disorders

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Abstract

Excessive fat deposition in obese subjects promotes the occurrence of metabolic diseases, such as type 2 diabetes mellitus (T2DM), cardiovascular diseases, and non-alcoholic fatty liver disease (NAFLD). Adipose tissue is not only the main form of energy storage but also an endocrine organ that not only secretes adipocytokines but also releases many extracellular vesicles (EVs) that play a role in the regulation of whole-body metabolism. Exosomes are a subtype of EVs, and accumulating evidence indicates that adipose tissue exosomes (AT Exos) mediate crosstalk between adipose tissue and multiple organs by being transferred to targeted cells or tissues through paracrine or endocrine mechanisms. However, the roles of AT Exos in crosstalk with metabolic organs remain to be fully elucidated. In this review, we summarize the latest research progress on the role of AT Exos in the regulation of metabolic disorders. Moreover, we discuss the potential role of AT Exos as biomarkers in metabolic diseases and their clinical application.

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Rui He, Yong Chen. The Role of Adipose Tissue-derived Exosomes in Chronic Metabolic Disorders. Current Medical Science, 2024, 44(3): 463-474 DOI:10.1007/s11596-024-2902-2

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References

[1]

TziomalosK, AthyrosVG, KaragiannisA, et al.. Endothelial dysfunction in metabolic syndrome: prevalence, pathogenesis and management. Nutr Metab Cardiovasc Dis, 2010, 20(2): 140-146

[2]

OuchiN, ParkerJL, LugusJJ, et al.. Adipokines in inflammation and metabolic disease. Nat Rev Immunol, 2011, 11(2): 85-97

[3]

SaltielAR, OlefskyJM. Inflammatory mechanisms linking obesity and metabolic disease. J Clin Invest, 2017, 127(1): 1-4

[4]

SternJH, RutkowskiJM, SchererPE. Adiponectin, Leptin, and Fatty Acids in the Maintenance of Metabolic Homeostasis through Adipose Tissue Crosstalk. Cell Metab, 2016, 23(5): 770-784

[5]

WeisbergSP, McCannD, DesaiM, et al.. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest, 2003, 112(12): 1796-1808

[6]

LiY, SoosTJ, LiX, et al.. Protein kinase C Theta inhibits insulin signaling by phosphorylating IRS1 at Ser(1101). J Biol Chem, 2004, 279(44): 45304-45307

[7]

MatsuzawaY, FunahashiT, NakamuraT. The concept of metabolic syndrome: contribution of visceral fat accumulation and its molecular mechanism. J Atheroscler Thromb, 2011, 18(8): 629-639

[8]

PekgorS, DuranC, BerberogluU, et al.. The Role of Visceral Adiposity Index Levels in Predicting the Presence of Metabolic Syndrome and Insulin Resistance in Overweight and Obese Patients. Metab Syndr Relat Disord, 2019, 17(5): 296-302

[9]

ChenY, PfeiferA. Brown Fat-Derived Exosomes: Small Vesicles with Big Impact. Cell Metab, 2017, 25(4): 759-760

[10]

CocucciE. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol, 2015, 25(6): 364-372

[11]

ZhangY, ShiL, MeiH, et al.. Inflamed macrophage microvesicles induce insulin resistance in human adipocytes. Nutr Metab (Lond), 2015, 12: 21

[12]

ThomouT, MoriMA, DreyfussJM, et al.. Adipose-derived circulating miRNAs regulate gene expression in other tissues. Nature, 2017, 542(7642): 450-455

[13]

ZhaoH, ShangQ, PanZ, et al.. Exosomes From Adipose-Derived Stem Cells Attenuate Adipose Inflammation and Obesity Through Polarizing M2 Macrophages and Beiging in White Adipose Tissue. Diabetes, 2018, 67(2): 235-247

[14]

YingW, RiopelM, BandyopadhyayG, et al.. Adipose Tissue Macrophage-Derived Exosomal miRNAs Can Modulate In Vivo and In Vitro Insulin Sensitivity. Cell, 2017, 171(2): 372-384.e12

[15]

TheryC, WitwerKW, AikawaE, 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(1): 1535750

[16]

MartinezMC, AndriantsitohainaR. Extracellular Vesicles in Metabolic Syndrome. Circ Res, 2017, 120(10): 1674-1686

[17]

MallociM, PerdomoL, VeerasamyM, et al.. Extracellular Vesicles: Mechanisms in Human Health and Disease. Antioxid Redox Signal, 2019, 30(6): 813-856

[18]

DurcinM, FleuryA, TailleboisE, et al.. Characterisation of adipocyte-derived extracellular vesicle subtypes identifies distinct protein and lipid signatures for large and small extracellular vesicles. J Extracell Vesicles, 2017, 6(1): 1305677

[19]

BatemanRM, SharpeMD, JaggerJE, et al.. 36th International Symposium on Intensive Care and Emergency Medicine: Brussels, Belgium. 15–18 March 2016. Crit Care, 2016, 20(Suppl2): 94

[20]

KranendonkME, de KleijnDP, KalkhovenE, et al.. Extracellular vesicle markers in relation to obesity and metabolic complications in patients with manifest cardiovascular disease. Cardiovasc Diabetol, 2014, 13: 37

[21]

DengZB, PoliakovA, HardyRW, et al.. Adipose tissue exosome-like vesicles mediate activation of macrophage-induced insulin resistance. Diabetes, 2009, 58(11): 2498-2505

[22]

LazarI, ClementE, DauvillierS, et al.. Adipocyte Exosomes Promote Melanoma Aggressiveness through Fatty Acid Oxidation: A Novel Mechanism Linking Obesity and Cancer. Cancer Res, 2016, 76(14): 4051-4057

[23]

IacominoG, RussoP, StillitanoI, et al.. Circulating microRNAs are deregulated in overweight/obese children: preliminary results of the I.Family study. Genes Nutr, 2016, 11: 7

[24]

GuayC, RegazziR. Circulating microRNAs as novel biomarkers for diabetes mellitus. Nat Rev Endocrinol, 2013, 9(9): 513-521

[25]

OrtegaFJ, MercaderJM, Moreno-NavarreteJM, et al.. Profiling of circulating microRNAs reveals common microRNAs linked to type 2 diabetes that change with insulin sensitization. Diabetes Care, 2014, 37(5): 1375-1383

[26]

AmosseJ, DurcinM, MallociM, et al.. Phenotyping of circulating extracellular vesicles (EVs) in obesity identifies large EVs as functional conveyors of macrophage migration inhibitory factor. Mol Metab, 2018, 18: 134-142

[27]

LeeJE, MoonPG, LeeIK, et al.. Proteomic Analysis of Extracellular Vesicles Released by Adipocytes of Otsuka Long-Evans Tokushima Fatty (OLETF) Rats. Protein J, 2015, 34(3): 220-235

[28]

SELA, MagerI, BreakefieldXO, et al.. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov, 2013, 12(5): 347-357

[29]

MinciacchiVR, FreemanMR, Di VizioD. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol, 2015, 40: 41-51

[30]

D’Souza-SchoreyC, SchoreyJS. Regulation and mechanisms of extracellular vesicle biogenesis and secretion. Essays Biochem, 2018, 62(2): 125-133

[31]

HessvikNP, LlorenteA. Current knowledge on exosome biogenesis and release. Cell Mol Life Sci, 2018, 75(2): 193-208

[32]

WillmsE, CabanasC, MagerI, et al.. Extracellular Vesicle Heterogeneity: Subpopulations, Isolation Techniques, and Diverse Functions in Cancer Progression. Front Immunol, 2018, 9: 738

[33]

KahlertC, KalluriR. Exosomes in tumor microenvironment influence cancer progression and metastasis. J Mol Med (Berl), 2013, 91(4): 431-437

[34]

van NielG, D’AngeloG, RaposoG. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol, 2018, 19(4): 213-228

[35]

SchmidtO, TeisD. The ESCRT machinery. Curr Biol, 2012, 22(4): R116-R120

[36]

ColomboM, MoitaC, van NielG, et al.. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci, 2013, 126: 5553-5565Pt 24

[37]

HoshinoD, KirkbrideKC, CostelloK, et al.. Exosome secretion is enhanced by invadopodia and drives invasive behavior. Cell Rep, 2013, 5(5): 1159-1168

[38]

HemlerME. Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu Rev Cell Dev Biol, 2003, 19: 397-422

[39]

Perez-HernandezD, Gutierrez-VazquezC, JorgeI, et al.. The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes. J Biol Chem, 2013, 288(17): 11649-11661

[40]

Lopez-MonteroI, MonroyF, VelezM, et al.. Ceramide: from lateral segregation to mechanical stress. Biochim Biophys Acta, 2010, 1798(7): 1348-1356

[41]

ElsherbiniA, BieberichE. Ceramide and Exosomes: A Novel Target in Cancer Biology and Therapy. Adv Cancer Res, 2018, 140: 121-154

[42]

BlancL, VidalM. New insights into the function of Rab GTPases in the context of exosomal secretion. Small GTPases, 2018, 9(1–2): 95-106

[43]

LiuJ, ZhangY, TianY, et al.. Integrative biology of extracellular vesicles in diabetes mellitus and diabetic complications. Theranostics, 2022, 12(3): 1342-1372

[44]

HartwigS, De FilippoE, GoddekeS, et al.. Exosomal proteins constitute an essential part of the human adipose tissue secretome. Biochim Biophys Acta Proteins Proteom, 2019, 1867(12): 140172

[45]

ClementE, LazarI, AttaneC, et al.. Adipocyte extracellular vesicles carry enzymes and fatty acids that stimulate mitochondrial metabolism and remodeling in tumor cells. EMBO J, 2020, 39(3): e102525

[46]

TrajkovicK, HsuC, ChiantiaS, et al.. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science, 2008, 319(5867): 1244-1247

[47]

SubraC, GrandD, LaulagnierK, et al.. Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J Lipid Res, 2010, 51(8): 2105-2120

[48]

GaoY, QinY, WanC, et al.. Small Extracellular Vesicles: A Novel Avenue for Cancer Management. Front Oncol, 2021, 11: 638357

[49]

ZakharovaL, SvetlovaM, FominaAF. T cell exosomes induce cholesterol accumulation in human monocytes via phosphatidylserine receptor. J Cell Physiol, 2007, 212(1): 174-181

[50]

KalluriR, LeBleuVS. The biology, function, and biomedical applications of exosomes. Science, 2020, 367(6478): eaau6977

[51]

GarciaNA, Ontoria-OviedoI, Gonzalez-KingH, et al.. Glucose Starvation in Cardiomyocytes Enhances Exosome Secretion and Promotes Angiogenesis in Endothelial Cells. PLoS One, 2015, 10(9): e0138849

[52]

ZhangY, LiuY, LiuH, et al.. Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci, 2019, 9: 19

[53]

KowalJ, ArrasG, ColomboM, et al.. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A, 2016, 113(8): E968-E977

[54]

ValadiH, EkstromK, BossiosA, et al.. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol, 2007, 9(6): 654-659

[55]

BellinghamSA, ColemanBM, HillAF. Small RNA deep sequencing reveals a distinct miRNA signature released in exosomes from prion-infected neuronal cells. Nucleic Acids Res, 2012, 40(21): 10937-10949

[56]

HuangX, YuanT, TschannenM, et al.. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics, 2013, 14: 319

[57]

JonasS, IzaurraldeE. Towards a molecular understanding of microRNA-mediated gene silencing. Nat Rev Genet, 2015, 16(7): 421-433

[58]

LeeRC, FeinbaumRL, AmbrosV. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell, 1993, 75(5): 843-854

[59]

TreiberT, TreiberN, MeisterG. Regulation of microRNA biogenesis and its crosstalk with other cellular pathways. Nat Rev Mol Cell Biol, 2019, 20(1): 5-20

[60]

GyorgyB, SzaboTG, PasztoiM, et al.. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci, 2011, 68(16): 2667-2688

[61]

Thery C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol, 2006,Chapter 3:Unit 3.22

[62]

LaulagnierK, JavaletC, HemmingFJ, et al.. Amyloid precursor protein products concentrate in a subset of exosomes specifically endocytosed by neurons. Cell Mol Life Sci, 2018, 75(4): 757-773

[63]

KamerkarS, LeBleuVS, SugimotoH, et al.. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature, 2017, 546(7659): 498-503

[64]

VargasA, ZhouS, Ethier-ChiassonM, et al.. Syncytin proteins incorporated in placenta exosomes are important for cell uptake and show variation in abundance in serum exosomes from patients with preeclampsia. FASEB J, 2014, 28(8): 3703-3719

[65]

EscreventeC, KellerS, AltevogtP, et al.. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer, 2011, 11: 108

[66]

HeusermannW, HeanJ, TrojerD, et al.. Exosomes surf on filopodia to enter cells at endocytic hot spots, traffic within endosomes, and are targeted to the ER. J Cell Biol, 2016, 213(2): 173-184

[67]

PradaI, AminL, FurlanR, et al.. A new approach to follow a single extracellular vesicle-cell interaction using optical tweezers. Biotechniques, 2016, 60(1): 35-41

[68]

TianT, ZhuYL, ZhouYY, et al.. Exosome uptake through clathrin-mediated endocytosis and macropinocytosis and mediating miR-21 delivery. J Biol Chem, 2014, 289(32): 22258-22267

[69]

VillarroyaF, CereijoR, VillarroyaJ, et al.. Brown adipose tissue as a secretory organ. Nat Rev Endocrinol, 2017, 13(1): 26-35

[70]

GuilhermeA, VirbasiusJV, PuriV, et al.. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol, 2008, 9(5): 367-377

[71]

CreweC, JoffinN, RutkowskiJM, et al.. An Endothelial-to-Adipocyte Extracellular Vesicle Axis Governed by Metabolic State. Cell, 2018, 175(3): 695-708.e613

[72]

CildirG, AkincilarSC, TergaonkarV. Chronic adipose tissue inflammation: all immune cells on the stage. Trends Mol Med, 2013, 19(8): 487-500

[73]

TilgH, MoschenAR. Adipocytokines: mediators linking adipose tissue, inflammation and immunity. Nat Rev Immunol, 2006, 6(10): 772-783

[74]

MenY, YelickJ, JinS, et al.. Exosome reporter mice reveal the involvement of exosomes in mediating neuron to astroglia communication in the CNS. Nat Commun, 2019, 10(1): 4136

[75]

PegtelDM, GouldSJ. Exosomes. Annu Rev Biochem, 2019, 88: 487-514

[76]

BebelmanMP, SmitMJ, PegtelDM, et al.. Biogenesis and function of extracellular vesicles in cancer. Pharmacol Ther, 2018, 188: 1-11

[77]

KalluriR. The biology and function of exosomes in cancer. J Clin Invest, 2016, 126(4): 1208-1215

[78]

MathieuM, Martin-JaularL, LavieuG, et al.. Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nat Cell Biol, 2019, 21(1): 9-17

[79]

AokiN, Jin-noS, NakagawaY, et al.. Identification and characterization of microvesicles secreted by 3T3-L1 adipocytes: redox- and hormone-dependent induction of milk fat globule-epidermal growth factor 8-associated microvesicles. Endocrinology, 2007, 148(8): 3850-3862

[80]

KranendonkME, VisserenFL, van BalkomBW, et al.. Human adipocyte extracellular vesicles in reciprocal signaling between adipocytes and macrophages. Obesity (Silver Spring), 2014, 22(5): 1296-1308

[81]

ConnollyKD, GuschinaIA, YeungV, et al.. Characterisation of adipocyte-derived extracellular vesicles released pre- and post-adipogenesis. J Extracell Vesicles, 2015, 4: 29159

[82]

HuangXY, ChenJX, RenY, et al.. Exosomal miR-122 promotes adipogenesis and aggravates obesity through the VDR/SREBF1 axis. Obesity (Silver Spring), 2022, 30(3): 666-679

[83]

YaoF, YuY, FengL, et al.. Adipogenic miR-27a in adipose tissue upregulates macrophage activation via inhibiting PPARgamma of insulin resistance induced by high-fat diet-associated obesity. Exp Cell Res, 2017, 355(2): 105-112

[84]

PanY, HuiX, HooRLC, et al.. Adipocyte-secreted exosomal microRNA-34a inhibits M2 macrophage polarization to promote obesity-induced adipose inflammation. J Clin Invest, 2019, 129(2): 834-849

[85]

FlahertySE3rd, GrijalvaA, XuX, et al.. A lipase-independent pathway of lipid release and immune modulation by adipocytes. Science, 2019, 363(6430): 989-993

[86]

FedorenkoA, LishkoPV, KirichokY. Mechanism of fatty-acid-dependent UCP1 uncoupling in brown fat mitochondria. Cell, 2012, 151(2): 400-413

[87]

NedergaardJ, GolozoubovaV, MatthiasA, et al.. UCP1: the only protein able to mediate adaptive non-shivering thermogenesis and metabolic inefficiency. Biochim Biophys Acta, 2001, 1504(1): 82-106

[88]

LiuJ, WangY, LinL. Small molecules for fat combustion: targeting obesity. Acta Pharm Sin B, 2019, 9(2): 220-236

[89]

ChouchaniET, KazakL, SpiegelmanBM. New Advances in Adaptive Thermogenesis: UCP1 and Beyond. Cell Metab, 2019, 29(1): 27-37

[90]

LeeYH, PetkovaAP, MottilloEP, et al.. In vivo identification of bipotential adipocyte progenitors recruited by beta3-adrenoceptor activation and high-fat feeding. Cell Metab, 2012, 15(4): 480-491

[91]

ChenY, BuyelJJ, HanssenMJ, et al.. Exosomal microRNA miR-92a concentration in serum reflects human brown fat activity. Nat Commun, 2016, 7: 11420

[92]

BoutensL, StienstraR. Adipose tissue macrophages: going off track during obesity. Diabetologia, 2016, 59(5): 879-894

[93]

RussoL, LumengCN. Properties and functions of adipose tissue macrophages in obesity. Immunology, 2018, 155(4): 407-417

[94]

ChenY, SiegelF, KipschullS, et al.. miR-155 regulates differentiation of brown and beige adipocytes via a bistable circuit. Nat Commun, 2013, 4: 1769

[95]

YingW, GaoH, Dos ReisFCG, et al.. MiR-690, an exosomal-derived miRNA from M2-polarized macrophages, improves insulin sensitivity in obese mice. Cell Metab, 2021, 33(4): 781-790

[96]

AnY, LinS, TanX, et al.. Exosomes from adipose-derived stem cells and application to skin wound healing. Cell Prolif, 2021, 54(3): e12993

[97]

BuzzettiR, ZampettiS, MaddaloniE. Adult-onset autoimmune diabetes: current knowledge and implications for management. Nat Rev Endocrinol, 2017, 13(11): 674-686

[98]

KakleasK, SoldatouA, KarachaliouF, et al.. Associated autoimmune diseases in children and adolescents with type 1 diabetes mellitus (T1DM). Autoimmun Rev, 2015, 14(9): 781-797

[99]

AbdiR, FiorinaP, AdraCN, et al.. Immunomodulation by mesenchymal stem cells: a potential therapeutic strategy for type 1 diabetes. Diabetes, 2008, 57(7): 1759-1767

[100]

VolarevicV, ArsenijevicN, LukicML, et al.. Concise review: Mesenchymal stem cell treatment of the complications of diabetes mellitus. Stem Cells, 2011, 29(1): 5-10

[101]

VolarevicV, Al-QahtaniA, ArsenijevicN, et al.. Interleukin-1 receptor antagonist (IL-1Ra) and IL-1Ra producing mesenchymal stem cells as modulators of diabetogenesis. Autoimmunity, 2010, 43(4): 255-263

[102]

WangJ, YiY, ZhuY, et al.. Effects of adipose-derived stem cell released exosomes on wound healing in diabetic mice. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi, 2020, 34(1): 124-131(Chinese)

[103]

LiX, XieX, LianW, 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(4): 1-14

[104]

BlazquezR, Sanchez-MargalloFM, de la RosaO, et al.. Immunomodulatory Potential of Human Adipose Mesenchymal Stem Cells Derived Exosomes on in vitro Stimulated T Cells. Front Immunol, 2014, 5: 556

[105]

MaJ, ZhangZ, WangY, et al.. Investigation of miR-126-3p loaded on adipose stem cell-derived exosomes for wound healing of full-thickness skin defects. Exp Dermatol, 2022, 31(3): 362-374

[106]

TogliattoG, DentelliP, GiliM, et al.. Obesity reduces the pro-angiogenic potential of adipose tissue stem cell-derived extracellular vesicles (EVs) by impairing miR-126 content: impact on clinical applications. Int J Obes (Lond), 2016, 40(1): 102-111

[107]

HeL, ZhuC, JiaJ, et al.. ADSC-Exos containing MALAT1 promotes wound healing by targeting miR-124 through activating Wnt/beta-catenin pathway. Biosci Rep, 2020, 40(5): BSR20192549

[108]

CooperDR, WangC, PatelR, et al.. Human Adipose-Derived Stem Cell Conditioned Media and Exosomes Containing MALAT1 Promote Human Dermal Fibroblast Migration and Ischemic Wound Healing. Adv Wound Care (New Rochelle), 2018, 7(9): 299-308

[109]

WuYL, LinZJ, LiCC, et al.. Adipose exosomal noncoding RNAs: Roles and mechanisms in metabolic diseases. Obes Rev, 2024, 25(6): e13740

[110]

ZhangY, TianZ, YeH, et al.. Emerging functions of circular RNA in the regulation of adipocyte metabolism and obesity. Cell Death Discov, 2022, 8(1): 268

[111]

SongM, HanL, ChenFF, 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(4): 1416-1432

[112]

TsaiS, Clemente-CasaresX, ReveloXS, et al.. Are obesity-related insulin resistance and type 2 diabetes autoimmune diseases?. Diabetes, 2015, 64(6): 1886-1897

[113]

CzechMP. Insulin action and resistance in obesity and type 2 diabetes. Nat Med, 2017, 23(7): 804-814

[114]

YounossiZM. Non-alcoholic fatty liver disease - A global public health perspective. J Hepatol, 2019, 70(3): 531-544

[115]

MziautH, HennigerG, GanssK, et al.. MiR-132 controls pancreatic beta cell proliferation and survival through Pten/Akt/Foxo3 signaling. Mol Metab, 2020, 31: 150-162

[116]

DusaulcyR, HandgraafS, VisentinF, et al.. miR-132-3p is a positive regulator of alpha-cell mass and is downregulated in obese hyperglycemic mice. Mol Metab, 2019, 22: 84-95

[117]

CuiX, YouL, ZhuL, et al.. Change in circulating microRNA profile of obese children indicates future risk of adult diabetes. Metabolism, 2018, 78: 95-105

[118]

Setyowati KarolinaD, SepramaniamS, TanHZ, et al.. miR-25 and miR-92a regulate insulin I biosynthesis in rats. RNA Biol, 2013, 10(8): 1365-1378

[119]

QianB, YangY, TangN, et al.. M1 macrophage-derived exosomes impair beta cell insulin secretion via miR-212-5p by targeting SIRT2 and inhibiting Akt/GSK-3beta/beta-catenin pathway in mice. Diabetologia, 2021, 64(9): 2037-2051

[120]

CioneE, CannataroR, GallelliL, et al.. Exosome microRNAs in Metabolic Syndrome as Tools for the Early Monitoring of Diabetes and Possible Therapeutic Options. Pharmaceuticals (Basel), 2021, 14(12): 1257

[121]

GesmundoI, PardiniB, GargantiniE, et al.. Adipocyte-derived extracellular vesicles regulate survival and function of pancreatic beta cells. JCI Insight, 2021, 6(5): e141962

[122]

KatayamaM, WiklanderOPB, FritzT, et al.. Circulating Exosomal miR-20b-5p Is Elevated in Type 2 Diabetes and Could Impair Insulin Action in Human Skeletal Muscle. Diabetes, 2019, 68(3): 515-526

[123]

FabbriniE, SullivanS, KleinS. Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology, 2010, 51(2): 679-689

[124]

LiD, SongH, ShuoL, et al.. Gonadal white adipose tissue-derived exosomal MiR-222 promotes obesity-associated insulin resistance. Aging (Albany NY), 2020, 12(22): 22719-22743

[125]

KoeckES, IordanskaiaT, SevillaS, et al.. Adipocyte exosomes induce transforming growth factor beta pathway dysregulation in hepatocytes: a novel paradigm for obesity-related liver disease. J Surg Res, 2014, 192(2): 268-275

[126]

EguchiA, LazicM, ArmandoAM, et al.. Circulating adipocyte-derived extracellular vesicles are novel markers of metabolic stress. J Mol Med (Berl), 2016, 94(11): 1241-1253

[127]

HeneghanHM, MillerN, McAnenaOJ, et al.. Differential miRNA expression in omental adipose tissue and in the circulation of obese patients identifies novel metabolic biomarkers. J Clin Endocrinol Metab, 2011, 96(5): E846-E850

[128]

ArgyropoulosC, WangK, McClartyS, et al.. Urinary microRNA profiling in the nephropathy of type 1 diabetes. PLoS One, 2013, 8(1): e54662

[129]

BaruttaF, TricaricoM, CorbelliA, et al.. Urinary exosomal microRNAs in incipient diabetic nephropathy. PLoS One, 2013, 8(11): e73798

[130]

de Gonzalo-CalvoD, van der MeerRW, RijzewijkLJ, et al.. Serum microRNA-1 and microRNA-133a levels reflect myocardial steatosis in uncomplicated type 2 diabetes. Sci Rep, 2017, 7(1): 47

[131]

DengL, HuangY, LiL, et al.. Serum miR-29a/b expression in gestational diabetes mellitus and its influence on prognosis evaluation. J Int Med Res, 2020, 48(9): 300060520954763

[132]

EissaS, MatboliM, AboushahbaR, et al.. Urinary exosomal microRNA panel unravels novel biomarkers for diagnosis of type 2 diabetic kidney disease. J Diabetes Complications, 2016, 30(8): 1585-1592

[133]

EissaS, MatboliM, BekhetMM. Clinical verification of a novel urinary microRNA panal: 133b, -342 and -30 as biomarkers for diabetic nephropathy identified by bioinformatics analysis. Biomed Pharmacother, 2016, 83: 92-99

[134]

WanS, WangJ, WangJ, et al.. Increased serum miR-7 is a promising biomarker for type 2 diabetes mellitus and its microvascular complications. Diabetes Res Clin Pract, 2017, 130: 171-179

[135]

FlowersE, AouizeratBE, AbbasiF, et al.. Circulating microRNA-320a and microRNA-486 predict thiazolidinedione response: Moving towards precision health for diabetes prevention. Metabolism, 2015, 64(9): 1051-1059

[136]

KarolinaDS, TavintharanS, ArmugamA, et al.. Circulating miRNA profiles in patients with metabolic syndrome. J Clin Endocrinol Metab, 2012, 97(12): E2271-E2276

[137]

ZbikowskiA, Blachnio-ZabielskaA, GalliM, et al.. Adipose-Derived Exosomes as Possible Players in the Development of Insulin Resistance. Int J Mol Sci, 2021, 22(14): 7427

[138]

LiM, KeQF, TaoSC, et al.. Fabrication of hydroxyapatite/chitosan composite hydrogels loaded with exosomes derived from miR-126-3p overexpressed synovial mesenchymal stem cells for diabetic chronic wound healing. J Mater Chem B, 2016, 4(42): 6830-6841

[139]

TaoSC, RuiBY, WangQY, et al.. Extracellular vesicle-mimetic nanovesicles transport LncRNA-H19 as competing endogenous RNA for the treatment of diabetic wounds. Drug Deliv, 2018, 25(1): 241-255

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