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Food Science and Human Wellness 2024, 13(3): 1390-1401 https://doi.org/10.26599/FSHW.2022.9250117
Research Article | Open Access | Issue | Published: 08 February 2024

Mannogalactoglucan from mushrooms protects pancreatic islets via restoring UPR and promotes insulin secretion in T1DM mice

Show Author's Information Ting Liu,,  Si Chen,  Yunhe Qu,  Lujuan Zheng,  Xiaoxuan Yang,  Shuhan Men,  Yuanning Wang,  Hanrui Ma,  Yifa Zhou,  Yuying Fan( )
Engineering Research Center of Glycoconjugates, Ministry of Education, Jilin Provincial Key Laboratory of Chemistry and Biology of Changbai Mountain Natural Drugs, School of Life Sciences, Northeast Normal University, Changchun 130024, China

Peer review under responsibility of Tsinghua University Press.

Keywords:
Insulin secretion, Mannogalactoglucan, Mushroom, Insulin synthesis, Pancreatic islets, Unfolded protein response (UPR), Type 1 diabetes mellitus (T1DM)
Cite this article:
Liu T, Chen S, Qu Y, et al. Mannogalactoglucan from mushrooms protects pancreatic islets via restoring UPR and promotes insulin secretion in T1DM mice. Food Science and Human Wellness, 2024, 13(3): 1390-1401. https://doi.org/10.26599/FSHW.2022.9250117
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Abstract Full text About this article

Type 1 diabetes mellitus (T1DM) lacks insulin secretion due to autoimmune deficiency of pancreatic β-cells. Protecting pancreatic islets and enhancing insulin secretion has been therapeutic approaches. Mannogalactoglucan is the main type of polysaccharide from natural mushroom, which has potential medicinal prospects. Nevertheless, the antidiabetic property of mannogalactoglucan in T1DM has not been fully elucidated. In this study, we obtained the neutral fraction of alkali-soluble Armillaria mellea polysaccharide (AAMP-N) with the structure of mannogalactoglucan from the fruiting body of A. mellea and investigated the potential therapeutic value of AAMP-N in T1DM. We demonstrated that AAMP-N lowered blood glucose and improved diabetes symptoms in T1DM mice. AAMP-N activated unfolded protein response (UPR) signaling pathway to maintain ER protein folding homeostasis and promote insulin secretion in vivo. Besides that, AAMP-N promoted insulin synthesis via upregulating the expression of transcription factors, increased Ca2+ signals to stimulate intracellular insulin secretory vesicle transport via activating calcium/calmodulin-dependent kinase II (CamkII) and cAMP/PKA signals, and enhanced insulin secretory vesicle fusion with the plasma membrane via vesicle-associated membrane protein 2 (VAMP2). Collectively, these studies demonstrated that the therapeutic potential of AAMP-N on pancreatic islets function, indicating that mannogalactoglucan could be natural nutraceutical used for the treatment of T1DM.


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About this article

Mannogalactoglucan from mushrooms protects pancreatic islets via restoring UPR and promotes insulin secretion in T1DM mice

Show Author's information Ting Liu,, Si Chen, Yunhe Qu, Lujuan Zheng, Xiaoxuan Yang, Shuhan Men, Yuanning Wang, Hanrui Ma, Yifa Zhou, Yuying Fan( )
Engineering Research Center of Glycoconjugates, Ministry of Education, Jilin Provincial Key Laboratory of Chemistry and Biology of Changbai Mountain Natural Drugs, School of Life Sciences, Northeast Normal University, Changchun 130024, China

Peer review under responsibility of Tsinghua University Press.

Abstract

Type 1 diabetes mellitus (T1DM) lacks insulin secretion due to autoimmune deficiency of pancreatic β-cells. Protecting pancreatic islets and enhancing insulin secretion has been therapeutic approaches. Mannogalactoglucan is the main type of polysaccharide from natural mushroom, which has potential medicinal prospects. Nevertheless, the antidiabetic property of mannogalactoglucan in T1DM has not been fully elucidated. In this study, we obtained the neutral fraction of alkali-soluble Armillaria mellea polysaccharide (AAMP-N) with the structure of mannogalactoglucan from the fruiting body of A. mellea and investigated the potential therapeutic value of AAMP-N in T1DM. We demonstrated that AAMP-N lowered blood glucose and improved diabetes symptoms in T1DM mice. AAMP-N activated unfolded protein response (UPR) signaling pathway to maintain ER protein folding homeostasis and promote insulin secretion in vivo. Besides that, AAMP-N promoted insulin synthesis via upregulating the expression of transcription factors, increased Ca2+ signals to stimulate intracellular insulin secretory vesicle transport via activating calcium/calmodulin-dependent kinase II (CamkII) and cAMP/PKA signals, and enhanced insulin secretory vesicle fusion with the plasma membrane via vesicle-associated membrane protein 2 (VAMP2). Collectively, these studies demonstrated that the therapeutic potential of AAMP-N on pancreatic islets function, indicating that mannogalactoglucan could be natural nutraceutical used for the treatment of T1DM.

Keywords: Insulin secretion, Mannogalactoglucan, Mushroom, Insulin synthesis, Pancreatic islets, Unfolded protein response (UPR), Type 1 diabetes mellitus (T1DM)

References(66)

[1]

J. Ilonen, J. Lempainen, R. Veijola, The heterogeneous pathogenesis of type 1 diabetes mellitus, Nat. Rev. Endocrinol. 15 (2019) 635-650. https://doi.org/10.1038/s41574-019-0254-y.
DOI Google Scholar
[2]

M.L. Marcovecchio, R.N. Dalton, D. Daneman, et al., A new strategy for vascular complications in young people with type 1 diabetes mellitus, Nat.Rev. Endocrinol. 15 (2019) 429-435. https://doi.org/10.1038/s41574-019-0198-2.
DOI Google Scholar
[3]

G.G. Nair, E.S. Tzanakakis, M. Hebrok, Emerging routes to the generation of functional β-cells for diabetes mellitus cell therapy, Nat. Rev. Endocrinol. 16 (2020) 506-518. https://doi.org/10.1038/s41574-020-0375-3.
DOI Google Scholar
[4]

B. Leibiger, K. Wahlander, P.O. Berggren, et al., Glucose-stimulated insulin biosynthesis depends on insulin-stimulated insulin gene transcription, J. Biol.Chem. 275 (2000) 30153-30156. https://doi.org/10.1074/jbc.M005216200.
DOI Google Scholar
[5]

H.W. Davidson, (Pro) Insulin processing: a historical perspective, Cell Biochem. Biophys. 40 (2004) 143-158. https://doi.org/10.1385/cbb:40:3:143.
DOI Google Scholar
[6]

I.X. Zhang, J. Ren, S. Vadrevu, et al., ER stress increases store-operated Ca2+ entry (SOCE) and augments basal insulin secretion in pancreatic β cells, J. Biol. Chem. 295 (2020) 5685-5700. https://doi.org/10.1074/jbc.RA120.012721.
DOI Google Scholar
[7]

N. Rachdaoui, Insulin: the friend and the foe in the development of type 2 diabetes mellitus, Int. J. Mol. Sci. 21 (2020) 1770. https://doi.org/10.3390/ijms21051770.
DOI Google Scholar
[8]

D. Mao, X.Y. Tian, D. Mao, et al., A polysaccharide extract from the medicinal plant Maidong inhibits the IKK-NF-κB pathway and IL-1 beta-induced islet inflammation and increases insulin secretion, J. Biol. Chem. 295 (2020) 12573-12587. https://doi.org/10.1074/jbc.RA120.014357.
DOI Google Scholar
[9]

T. Szkudelski, K. Szkudelska, The relevance of AMP-activated protein kinase in insulin-secreting β cells: a potential target for improving β cell function?, J. Physiol. Biochem. 75 (2019) 423-432. https://doi.org/10.1007/s13105-019-00706-3.
DOI Google Scholar
[10]

S. Yang, Y. Qu, J. Chen, et al., Bee pollen polysaccharide from Rosa rugosa Thunb. (Rosaceae) promotes pancreatic β-cell proliferation and insulin secretion, Front. Pharmacol. 12 (2021) 688073. https://doi.org/10.3389/fphar.2021.688073.
DOI Google Scholar
[11]

F. Zhang, D. Ma, W. Zhao, et al., Obesity-induced overexpression of miR-802 impairs insulin transcription and secretion, Nat. Commun. 11 (2020) 1822. https://doi.org/10.1038/s41467-020-15529-w.
DOI Google Scholar
[12]

C.J. Chang, C.S. Lin, C.C. Lu, et al., Ganoderma lucidum reduces obesity in mice by modulating the composition of the gut microbiota, Nat. Commun. 6(2015) 7489. https://doi.org/10.1038/ncomms8489.
DOI Google Scholar
[13]

S.R.A. Usuldin, W. Wan-Mohtar, Z. Ilham, et al., In vivo toxicity of bioreactor-grown biomass and exopolysaccharides from Malaysian tiger milk mushroom mycelium for potential future health applications, Sci. Rep. 11 (2021) 23079. https://doi.org/10.1038/s41598-021-02486-7.
DOI Google Scholar
[14]

Z. Gao, D. Kong, W. Cai, et al., Characterization and anti-diabetic nephropathic ability of mycelium polysaccharides from Coprinus comatus, Carbohydr. Polym. 251 (2021) 117081. https://doi.org/10.1016/j.carbpol.2020.117081.
DOI Google Scholar
[15]

H.R. Yang, L.H. Chen, Y.J. Zeng, Structure, antioxidant activity and in vitro hypoglycemic activity of a polysaccharide purified from Tricholoma matsutake, Foods 10 (2021) 2184. https://doi.org/10.3390/foods10092184.
DOI Google Scholar
[16]

Y. Liu, Y. Liu, M. Zhang, et al., Structural characterization of a polysaccharide from Suillellus luridus and its antidiabetic activity via Nrf2/HO-1 and NF-κB pathways, Int. J. Biol. Macromol. 162 (2020) 935-945. https://doi.org/10.1016/j.ijbiomac.2020.06.212.
DOI Google Scholar
[17]

T. Sang, C. Guo, D. Guo, et al., Suppression of obesity and inflammation by polysaccharide from sporoderm-broken spore of Ganoderma lucidum via gut microbiota regulation, Carbohydr. Polym. 256 (2021) 117594. https://doi.org/10.1016/j.carbpol.2020.117594.
DOI Google Scholar
[18]

S.D.S. Milhorini, F.R. Smiderle, S.M.P. Biscaia, et al., Fucogalactan from the giant mushroom Macrocybe titans inhibits melanoma cells migration, Carbohydr. Polym. 190 (2018) 50-56. https://doi.org/10.1016/j.carbpol.2018.02.063.
DOI Google Scholar
[19]

M. Zavadinack, D. de Lima Bellan, J.L. da Rocha Bertage, et al., An α-D-galactan and a β-D-glucan from the mushroom Amanita muscaria: structural characterization and antitumor activity against melanoma, Carbohydr.Polym. 274 (2021) 118647. https://doi.org/10.1016/j.carbpol.2021.118647.
DOI Google Scholar
[20]

S. Yang, J. Yan, L. Yang, et al., Alkali-soluble polysaccharides from mushroom fruiting bodies improve insulin resistance, Int. J. Biol. Macromol.126 (2019) 466-474. https://doi.org/10.1016/j.ijbiomac.2018.12.251.
DOI Google Scholar
[21]

B.K. Mani, N. Puzziferri, Z. He, et al., LEAP2 changes with body mass and food intake in humans and mice, J. Clin. Invest. 129 (2019) 3909-3923. https://doi.org/10.1172/JCI125332.
DOI Google Scholar
[22]

Y. Liu, Z. Yang, D. Kong, et al., Metformin ameliorates testicular damage in male mice with streptozotocin-induced type 1 diabetes through the PK2/PKR pathway, Oxid. Med. Cell Longev. 2019 (2019) 5681701. https://doi.org/10.1155/2019/5681701.
DOI Google Scholar
[23]

B.T. Lobingier, R. Huttenhain, K. Eichel, et al., An approach to spatiotemporally resolve protein interaction networks in living cells, Cell 169 (2017) 350-360. https://doi.org/10.1016/j.cell.2017.03.022.
DOI Google Scholar
[24]

X. Li, H. Gong, S. Yang, et al., Pectic bee pollen polysaccharide from Rosa rugosa alleviates diet-induced hepatic steatosis and insulin resistance via induction of AMPK/mTOR-mediated autophagy, Molecules 22 (2017) 699. https://doi.org/10.3390/molecules22050699.
DOI Google Scholar
[25]

I. Laidmae, A. Aints, R. Uibo, Growth of MIN-6 cells on salmon fibrinogen scaffold improves insulin secretion, Pharmaceutics 14 (2022) 941. https://doi.org/10.3390/pharmaceutics14050941.
DOI Google Scholar
[26]

D. Nasteska, N.H.F. Fine, F.B. Ashford, et al., PDX1LOW MAFALOW β-cells contribute to islet function and insulin release, Nat. Commun. 12 (2021) 674. https://doi.org/10.1038/s41467-020-20632-z.
DOI Google Scholar
[27]

S. Li, N.P. Shah, Antioxidant and antibacterial activities of sulphated polysaccharides from Pleurotus eryngii and Streptococcus thermophilus ASCC 1275, Food Chem. 165 (2014) 262-270. https://doi.org/10.1016/j.foodchem.2014.05.110.
DOI Google Scholar
[28]

J. Yan, L. Zhu, Y. Qu, et al., Analyses of active antioxidant polysaccharides from four edible mushrooms, Int. J. Biol. Macromol. 123 (2019) 945-956. https://doi.org/10.1016/j.ijbiomac.2018.11.079.
DOI Google Scholar
[29]

Z.R. Li, R.B. Jia, J. Wu, et al., Sargassum fusiforme polysaccharide partly replaces acarbose against type 2 diabetes in rats, Int. J. Biol. Macromol. 170(2021) 447-458. https://doi.org/10.1016/j.ijbiomac.2020.12.126.
DOI Google Scholar
[30]

K. Dhatariya, Blood ketones: measurement, interpretation, limitations, and utility in the management of diabetic ketoacidosis, Rev. Diabet. Stud. 13(2016) 217-225. https://doi.org/10.1900/RDS.2016.13.217.
DOI Google Scholar
[31]

A. Almanza, A. Carlesso, C. Chintha, et al., Endoplasmic reticulum stress signalling-from basic mechanisms to clinical applications, FEBS J. 286(2019) 241-278. https://doi.org/10.1111/febs.14608.
DOI Google Scholar
[32]

N. Babaya, M. Nakayama, H. Moriyama, et al., A new model of insulin-deficient diabetes: male NOD mice with a single copy of Ins1 and no Ins2, Diabetologia 49 (2006) 1222-1228. https://doi.org/10.1007/s00125-006-0241-4.
DOI Google Scholar
[33]

H. Moriyama, N. Abiru, J. Paronen, et al., Evidence for a primary islet autoantigen (preproinsulin 1) for insulitis and diabetes in the nonobese diabetic mouse, Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 10376-10381. https://doi.org/10.1073/pnas.1834450100.
DOI Google Scholar
[34]

S.K. Chakrabarti, R.G. Mirmira, Transcription factors direct the development and function of pancreatic β cells, Trends Endocrinol. Metab. 14 (2003) 78-84. https://doi.org/10.1016/s1043-2760(02)00039-5.
DOI Google Scholar
[35]

J. Li, J. Cantley, J.G. Burchfield, et al., DOC2 isoforms play dual roles in insulin secretion and insulin-stimulated glucose uptake, Diabetologia 57(2014) 2173-2182. https://doi.org/10.1007/s00125-014-3312-y.
DOI Google Scholar
[36]

P.M. Heister, T. Powell, A. Galione, Glucose and NAADP trigger elementary intracellular β-cell Ca2+ signals, Sci. Rep. 11 (2021) 10714. https://doi.org/10.1038/s41598-021-88906-0.
DOI Google Scholar
[37]

P.K. Dadi, N.C. Vierra, A. Ustione, et al., Inhibition of pancreatic β-cell Ca2+/calmodulin-dependent protein kinase II reduces glucose-stimulated calcium influx and insulin secretion, impairing glucose tolerance, J. Biol. Chem. 289 (2014) 12435-12445. https://doi.org/10.1074/jbc.M114.562587.
DOI Google Scholar
[38]

O. Dyachok, Y. Isakov, J. Sagetorp, et al., Oscillations of cyclic AMP in hormone-stimulated insulin-secreting β-cells, Nature 439 (2006) 349-352. https://doi.org/10.1038/nature04410.
DOI Google Scholar
[39]

T. Mochida, H. Ueno, N. Tsubooka-Yamazoe, et al., Insulin-deficient diabetic condition upregulates the insulin-secreting capacity of human induced pluripotent stem cell-derived pancreatic endocrine progenitor cells after implantation in mice, Diabetes 69 (2020) 634-646. https://doi.org/10.2337/db19-0728.
DOI Google Scholar
[40]

S. Yang, Y. Meng, J. Yan, et al., Polysaccharide-enriched fraction from Amillariella mellea fruiting body improves insulin resistance, Molecules 24(2018) 46. https://doi.org/10.3390/molecules24010046.
DOI Google Scholar
[41]

M. Kleinert, C. Clemmensen, S.M. Hofmann, et al., Animal models of obesity and diabetes mellitus, Nat. Rev. Endocrinol. 14 (2018) 140-162. https://doi.org/10.1038/nrendo.2017.161.
DOI Google Scholar
[42]

U.G. Bhat, V. Ilievski, T.G. Unterman, et al., Porphyromonas gingivalis lipopolysaccharide upregulates insulin secretion from pancreatic β cell line MIN6, J. Periodontol. 85 (2014) 1629-1636. https://doi.org/10.1902/jop.2014.140070.
DOI Google Scholar
[43]

R. Lazarenko, J. Geisler, D. Bayliss, et al., D-Chiro-inositol glycan stimulates insulin secretion in pancreatic β cells, Mol. Cell Endocrinol. 387(2014) 1-7. https://doi.org/10.1016/j.mce.2014.02.004.
DOI Google Scholar
[44]

P. Seedevi, A. Ramu Ganesan, M. Moovendhan, et al., Anti-diabetic activity of crude polysaccharide and rhamnose-enriched polysaccharide from G. lithophila on streptozotocin (STZ)-induced in Wistar rats, Sci. Rep. 10(2020) 556. https://doi.org/10.1038/s41598-020-57486-w.
DOI Google Scholar
[45]

P. Li, Y. Chen, L. Luo, et al., Immunoregulatory effect of Acanthopanax trifoliatus (L.) Merr. polysaccharide on T1DM mice, Drug Des. Devel. Ther.15 (2021) 2629-2639. https://doi.org/10.2147/DDDT.S309851.
DOI Google Scholar
[46]

G. Lu, F. Rausell-Palamos, J. Zhang, et al., Dextran sulfate protects pancreatic β-cells, reduces autoimmunity, and ameliorates type 1 diabetes, Diabetes 69 (2020) 1692-1707. https://doi.org/10.2337/db19-0725.
DOI Google Scholar
[47]

X. Zhou, Y. Xu, G. Yang, et al., Increased galectin-1 expression in muscle of Astragalus polysaccharide-treated type 1 diabetic mice, J. Nat. Med. 65(2011) 500-507. https://doi.org/10.1007/s11418-011-0527-9.
DOI Google Scholar
[48]

L. Pan, H. Weng, H. Li, et al., Therapeutic effects of bupleurum polysaccharides in streptozotocin induced diabetic mice, PLoS One 10 (2015) e0133212. https://doi.org/10.1371/journal.pone.0133212.
DOI Google Scholar
[49]

J. Wang, W. Hu, L. Li, et al., Antidiabetic activities of polysaccharides separated from Inonotus obliquus via the modulation of oxidative stress in mice with streptozotocin-induced diabetes, PLoS One 12 (2017) e0180476. https://doi.org/10.1371/journal.pone.0180476.
DOI Google Scholar
[50]

P. Kanikarla-Marie, S.K. Jain, Hyperketonemia and ketosis increase the risk of complications in type 1 diabetes, Free Radic. Biol. Med. 95 (2016) 268-277. https://doi.org/10.1016/j.freeradbiomed.2016.03.020.
DOI Google Scholar
[51]

G.S. Sahin, H. Lee, F. Engin, An accomplice more than a mere victim: the impact of β-cell ER stress on type 1 diabetes pathogenesis, Mol. Metab. 54(2021) 101365. https://doi.org/10.1016/j.molmet.2021.101365.
DOI Google Scholar
[52]

R.B. Sharma, H.V. Landa-Galvan, L.C. Alonso, Living dangerously:protective and harmful ER stress responses in pancreatic β-cells, Diabetes 70(2021) 2431-2443. https://doi.org/10.2337/dbi20-0033.
DOI Google Scholar
[53]

Q. Zhang, W. Chen, B. Zhang, et al., Central role of TRAP1 in the ameliorative effect of oleanolic acid on the mitochondrial-mediated and endoplasmic reticulum stress-excitated apoptosis induced by ochratoxin A, Toxicology 450 (2021) 152681. https://doi.org/10.1016/j.tox.2021.152681.
DOI Google Scholar
[54]

W. Peng, Y. Wu, Z. Peng, et al., Cyanidin-3-glucoside improves the barrier function of retinal pigment epithelium cells by attenuating endoplasmic reticulum stress-induced apoptosis, Food Res. Int. 157 (2022) 111313. https://doi.org/10.1016/j.foodres.2022.111313.
DOI Google Scholar
[55]

K.L. Lipson, S.G. Fonseca, S. Ishigaki, et al., Regulation of insulin biosynthesis in pancreatic β cells by an endoplasmic reticulum-resident protein kinase IRE1, Cell Metab. 4 (2006) 245-254. https://doi.org/10.1016/j.cmet.2006.07.007.
DOI Google Scholar
[56]

T. Xu, L. Yang, C. Yan, et al., The IRE1α-XBP1 pathway regulates metabolic stress-induced compensatory proliferation of pancreatic β-cells, Cell Res. 24 (2014) 1137-1140. https://doi.org/10.1038/cr.2014.55.
DOI Google Scholar
[57]

K. Lee, J.Y. Chan, C. Liang, et al., XBP1 maintains β cell identity, represses β-to-α cell transdifferentiation and protects against diabetic β cell failure during metabolic stress in mice, Diabetologia 65 (2022) 984-996. https://doi.org/10.1007/s00125-022-05669-7.
DOI Google Scholar
[58]

Y. Gao, D.J. Sartori, C.H. Li, et al., PERK is required in the adult pancreas and is essential for maintenance of glucose homeostasis, Mol. Cell. Biol. 32(2012) 5129-5139. https://doi.org/10.1128/Mcb.01009-12.
DOI Google Scholar
[59]

H.P. Harding, H. Zeng, Y. Zhang, et al., Diabetes mellitus and exocrine pancreatic dysfunction in perk−/− mice reveals a role for translational control in secretory cell survival, Mol. Cell 7 (2001) 1153-1163. https://doi.org/10.1016/s1097-2765(01)00264-7.
DOI Google Scholar
[60]

P. Zhang, B. McGrath, S. Li, et al., The PERK eukaryotic initiation factor 2 alpha kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas, Mol. Cell. Biol. 22(2002) 3864-3874. https://doi.org/10.1128/MCB.22.11.3864-3874.2002.
DOI Google Scholar
[61]

A.S.D. Wickramasinghe, P. Kalansuriya, A.P. Attanayake, Herbal medicines targeting the improved β-cell functions and β-cell regeneration for the management of diabetes mellitus, Evid. Based Complement Alternat. Med.2021 (2021) 2920530. https://doi.org/10.1155/2021/2920530.
DOI Google Scholar
[62]

Q.Y. Xiong, C. Yu, Y. Zhang, et al., Key proteins involved in insulin vesicle exocytosis and secretion, Biomed. Rep. 6 (2017) 134-139. https://doi.org/10.3892/br.2017.839.
DOI Google Scholar
[63]

S. Nagamatsu, Y. Nakamichi, T. Watanabe, et al., Localization of cellubrevin-related peptide, endobrevin, in the early endosome in pancreatic β cells and its physiological function in exo-endocytosis of secretory granules, J. Cell Sci. 114 (2001) 219-227. https://doi.org/10.1242/jcs.114.1.219.
DOI Google Scholar
[64]

T. Galli, T. Chilcote, O. Mundigl, et al., Tetanus toxin-mediated cleavage of cellubrevin impairs exocytosis of transferrin receptor-containing vesicles in CHO cells, J. Cell Biol. 125 (1994) 1015-1024. https://doi.org/10.1083/jcb.125.5.1015.
DOI Google Scholar
[65]

C. Yang, S. Mora, J.W. Ryder, et al., VAMP3 null mice display normal constitutive, insulin- and exercise-regulated vesicle trafficking, Mol. Cell Biol. 21 (2001) 1573-1580. https://doi.org/10.1128/MCB.21.5.1573-1580.2001.
DOI Google Scholar
[66]

S. Deng, L. Yang, K. Ma, et al., Astragalus polysaccharide improve the proliferation and insulin secretion of mouse pancreatic β cells induced by high glucose and palmitic acid partially through promoting miR-136-5p and miR-149-5p expression, Bioengineered 12 (2021) 9872-9884. https://doi.org/10.1080/21655979.2021.1996314.
DOI Google Scholar
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Received: 31 August 2022
Revised: 28 October 2022
Accepted: 17 November 2022
Published: 08 February 2024
Issue date: May 2024

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© 2024 Beijing Academy of Food Sciences. Publishing services by Tsinghua University Press.

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Acknowledgement

This research was funded by the National Natural Science Foundation of China (32371341, 31872674), the Scientific and Technologic Foundation of Jilin Province (20230202050NC), and the Fundamental Research Funds for the Central Universities (CGZH202206).

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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