Please wait a minute...

中国生物工程杂志

China Biotechnology
China Biotechnology  2018, Vol. 38 Issue (6): 70-76    DOI: 10.13523/j.cb.20180610
    
The Role of FoxO1 in the Impaired Metabolic Flexibility and Decompensation Progress of Pancreatic Beta Cell
Lin-jing FENG1,Yang YV1,Hong-wei DU1,2,**()
1 School of Basic Medical Sciences, Jilin University, Changchun 130021, China
2 The First Hospital of Jilin University, Changchun 130021, China
Download: HTML   PDF(1047KB) HTML
Export: BibTeX | EndNote (RIS)      

Abstract  

It is well known that glucose and fatty acids are key metabolic substrates for pancreatic β-cells. Pancreatic β-cells secrete insulin by glucose stimulating to keep blood glucose levels within a homeostatic range. When insulin resistance occurs, β-cells metabolic flexibility has become the first victim of pancreatic β-cells dysfunction. Compensation to decompensation of pancreatic β-cells is the key for the development of obesity insulin resistance to type 2 diabetes. Nuclear transcription factor FoxO1 (forkhead box O1) belongs to the Fox family, which is widely expressed in pancreatic β-cells. FoxO1 is a key regulator of the insulin-signaling pathway, and is reported to play important roles in pancreatic β-cells differentiation, proliferation, apoptosis and stress resistance. In view of the key role of FoxO1 in the maintenance of pancreatic β-cells function, an overview focused on the role of FoxO1 in the impaired metabolic flexibility and decompensation progress of pancreatic beta cells is provided.



Key wordsPancreatic β-cells      FoxO1      Metabolic flexibility      Decompensation      Obesity      T2DM     
Received: 03 January 2018      Published: 06 July 2018
ZTFLH:  R967  
Corresponding Authors: Hong-wei DU     E-mail: dhw_101@126.com
Cite this article:

Lin-jing FENG,Yang YV,Hong-wei DU. The Role of FoxO1 in the Impaired Metabolic Flexibility and Decompensation Progress of Pancreatic Beta Cell. China Biotechnology, 2018, 38(6): 70-76.

URL:

https://manu60.magtech.com.cn/biotech/10.13523/j.cb.20180610     OR     https://manu60.magtech.com.cn/biotech/Y2018/V38/I6/70

[1]   Mugabo Y, Zhao S, Lamontagne J , et al. Metabolic fate of glucose and candidate signaling and excess-fuel detoxification pathways in pancreatic β-cells. Journal of Biological Chemistry, 2017,292(18):7407-7422.
doi: 10.1074/jbc.M116.763060 pmid: 28280244
[2]   Mulder H . Metabolic coupling in pancreatic beta cells: lipolysis revisited. Diabetologia, 2016,59(12):2510-2513.
doi: 10.1007/s00125-016-4111-4 pmid: 27660005
[3]   Zhang S , McMillan R P, Hulver M W , et al. Chickens from lines selected for high and low body weight show differences in fatty acid oxidation efficiency and metabolic flexibility in skeletal muscle and white adipose tissue. International Journal of Obesity, 2014,38(10):1374-1382.
doi: 10.1038/ijo.2014.8 pmid: 24441038
[4]   Bround M J, Wambolt R, Luciani D S , et al. Cardiomyocyte ATP production, metabolic flexibility, and survival require calcium flux through cardiac ryanodine receptors in vivo. Journal of Biological Chemistry, 2013,288(26):18975-18986.
doi: 10.1074/jbc.M112.427062 pmid: 3696672
[5]   Gopal K, Saleme B, Al Batran R , et al. FoxO1 regulates myocardial glucose oxidation rates via transcriptional control of pyruvate dehydrogenase kinase 4 expression. American Journal of Physiology Heart and Circulatory Physiology, 2017,313(3):H479-H490.
doi: 10.1152/ajpheart.00191.2017 pmid: 28687587
[6]   Kitamura T, Ido Kitamura Y . Role of FoxO proteins in pancreatic beta cells. Endocrine Journal, 2007,54(4):507-515.
doi: 10.1507/endocrj.KR-109 pmid: 17510498
[7]   Murtaza G, Khan A K, Rashid R , et al. FoxO transcriptional factors and long-term living. Oxidative Medicine and Cellular Longevity, 2017: 3494289.
doi: 10.1155/2017/3494289 pmid: 28894507
[8]   Kandula V, Kosuru R, Li H , et al. Forkhead box transcription factor 1: Role in the pathogenesis of diabetic cardiomyopathy. Cardiovascular Diabetology, 2016,15:44.
doi: 10.1186/s12933-016-0361-1 pmid: 4784400
[9]   Kim C G, Lee H, Gupta N , et al. Role of forkhead box Class O proteins in cancer progression and metastasis. Seminars in Cancer Biology, 2017.
doi: 10.1016/j.semcancer.2017.07.007 pmid: 28774834
[10]   Tsuchiya K, Ogawa Y . Forkhead box class O family member proteins: The biology and pathophysiological roles in diabetes. Journal of Diabetes Investigation, 2017,8(6):726-734.
doi: 10.1111/jdi.12651
[11]   Song M Y, Wang J, Ka S O , et al. Insulin secretion impairment in Sirt6 knockout pancreatic beta cells is mediated by suppression of the FoxO1-Pdx1-Glut2 pathway. Scientific Reports, 2016,6:30321.
doi: 10.1038/srep30321 pmid: 27457971
[12]   Xing Y Q, Li A, Yang Y , et al. The regulation of FOXO1 and its role in disease progression. Life Sciences, 2018,193(Supplement C):124-131.
doi: 10.1016/j.lfs.2017.11.030 pmid: 29158051
[13]   Goodpaster B H, Sparks L M . Metabolic flexibility in health and disease. Cell Metabolism, 2017,25(5):1027-1036
doi: 10.1016/j.cmet.2017.04.015 pmid: 28467922
[14]   Prentki M, Matschinsky F M, Madiraju S R . Metabolic signaling in fuel-induced insulin secretion. Cell Metabolism, 2013,18(2):162-185.
doi: 10.1016/j.cmet.2013.05.018 pmid: 23791483
[15]   Rutter G A, Pullen T J, Hodson D J , et al. Pancreatic β-cell identity, glucose sensing and the control of insulin secretion. Biochemical Journal, 2015,466(2):203-218.
doi: 10.1042/BJ20141384 pmid: 25697093
[16]   Haeusler R A, Hartil K, Vaitheesvaran B , et al. Integrated control of hepatic lipogenesis versus glucose production requires FoxO transcription factors. Nature Communications, 2014,5:5190.
doi: 10.1038/ncomms6190 pmid: 25307742
[17]   Talchai S C, Accili D . Legacy effect of FoxO1 in pancreatic endocrine progenitors on adult β-cell mass and function. Diabetes. 2015,64(8):2868-2879.
doi: 10.2337/db14-1696 pmid: 25784544
[18]   Lee S, Dong H H . FoxO integration of insulin signaling with glucose and lipid metabolism. Journal of Endocrinology, 2017,233(2):R67-R79.
doi: 10.1530/JOE-17-0002 pmid: 28213398
[19]   Kim-Muller J Y, Kim Y J, Fan J , et al. FoxO1 deacetylation decreases fatty acid oxidation in beta-cells and sustains insulin secretion in diabetes. Journal of Biological Chemistry, 2016,291(19):10162-10172.
doi: 10.1074/jbc.M115.705608 pmid: 26984405
[20]   Palmieri F . Mitochondrial transporters of the SLC25 family and associated diseases: a review. Journal of Inherited Metabolic Disease, 2014,37(4):565-575.
doi: 10.1007/s10545-014-9708-5 pmid: 24797559
[21]   Palmieri F . The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Archiv, 2004,447(5):689-709.
doi: 10.1007/s00424-003-1099-7 pmid: 14598172
[22]   Kim-Muller J Y, Zhao S, Srivastava S , et al. Metabolic inflexibility impairs insulin secretion and results in MODY-like diabetes in triple FoxO-deficient mice. Cell Metabolism, 2014,20(4):593-602.
doi: 10.1016/j.cmet.2014.08.012 pmid: 4192072
[23]   潘长玉 . 胰岛β细胞与胰岛素分泌--可塑性与失代偿 . 中华内分泌代谢杂志, 2009, 25(2): 2c-1-2c-3.
doi: 10.3760/cma.j.issn.1000-6699.2009.01.047
[23]   Pan C Y . Pancreatic β-cell and insulinsecretion--plasticity and decompensation. Chinese Journal of Endocrinology and Metabolism, 2009, 25(2): 2c-1-2c-3.
doi: 10.3760/cma.j.issn.1000-6699.2009.01.047
[24]   Salvi R, Abderrahmani A . Decompensation of β-cells in diabetes: When pancreatic-cells are on ICE(R). Journal of Diabetes Research, 2014,2014(3):768024.
[25]   Accili D, Talchai S C , Kim-Muller J Y, et al. When beta-cells fail: lessons from dedifferentiation. Diabetes, Obesity and Metabolism, 2016,18(Suppl 1):117-122.
doi: 10.1111/dom.12723 pmid: 27615140
[26]   Zhang T, Kim D H, Xiao X , et al. FoxO1 plays an important role in regulating beta-cell compensation for insulin resistance in male mice. Endocrinology, 2016,157(3):1055-1070.
doi: 10.1210/en.2015-1852 pmid: 26727107
[27]   Kobayashi M, Kikuchi O, Sasaki T , et al. FoxO1 as a double-edged sword in the pancreas: analysis of pancreas- and β-cell-specific FoxO1 knockout mice. American Journal of Physiology-Endocrinology and Metabolism, 2012,302(5):E603-E613.
[28]   Baba S, Ueno Y, Kikuchi T , et al. A limonoid kihadanin b from immature citrus unshiu peels suppresses adipogenesis through repression of the Akt-FOXO1-PPARγ axis in adipocytes. Journal of Agricultural and Food Chemistry, 2016,64(51):9607-9615.
doi: 10.1021/acs.jafc.6b04521 pmid: 27977180
[29]   Gupta D, Leahy A A, Monga N , et al. Peroxisome proliferator-activated receptor gamma (PPAR gamma) and its target genes are downstream effectors of FoxO1 protein in islet beta-cells: mechanism of beta-cell compensation and failure. Journal of Biological Chemistry, 2013,288(35):25440-25449.
doi: 10.1074/jbc.M113.486852
[30]   Panten U, Willenborg M, Schumacher K , et al. Acute metabolic amplification of insulin secretion in mouse islets is mediated by mitochondrial export of metabolites, but not by mitochondrial energy generation. Metabolism, 2013,62(10):1375-1386.
doi: 10.1016/j.metabol.2013.05.006 pmid: 23790612
[31]   MacDonald M J, Longacre M J, Langberg E C , et al. Decreased levels of metabolic enzymes in pancreatic islets of patients with type 2 diabetes. Diabetologia, 2009,52(6):1087-1091.
doi: 10.1007/s00125-009-1319-6 pmid: 2903059
[32]   Pachera N, Papin J, Zummo F P , et al. Heterozygous inactivation of plasma membrane Ca(2+)-ATPase in mice increases glucose-induced insulin release and beta cell proliferation, mass and viability. Diabetologia, 2015,58(12):2843-2850.
doi: 10.1007/s00125-015-3745-y
[33]   Kono T, Ahn G, Moss D R , et al. PPAR-gamma activation restores pancreatic islet SERCA2 levels and prevents beta-cell dysfunction under conditions of hyperglycemic and cytokine stress. Molecular Endocrinology, 2012,26(2):257-271.
doi: 10.1210/me.2011-1181
[34]   Hayes H L, Zhang L, Becker T C , et al. A Pdx-1-regulated soluble factor activates rat and human islet cell proliferation. Molecular and Cellular Biology, 2016,36(23):2918-2930.
doi: 10.1128/MCB.00103-16
[35]   Zhu Y, Liu Q, Zhou Z , et al. PDX1, Neurogenin-3, and MAFA: critical transcription regulators for beta cell development and regeneration. Stem Cell Research & Therapy, 2017,8:240.
doi: 10.1186/s13287-017-0694-z pmid: 5667467
[36]   Lv L, Chen H, Sun J , et al. PRMT1 promotes glucose toxicity-induced β cell dysfunction by regulating the nucleo-cytoplasmic trafficking of PDX-1 in a FOXO1-dependent manner in INS-1 cells. Endocrine, 2015,49(3):669-682.
doi: 10.1007/s12020-015-0543-8 pmid: 25874535
[37]   Huang T N, Hsueh Y P . Calcium/calmodulin-dependent serine protein kinase (CASK), a protein implicated in mental retardation and autism-spectrum disorders, interacts with T-Brain-1 (TBR1) to control extinction of associative memory in male mice. Journal of Psychiatry & Neuroscience: JPN, 2017,42(1):37-47.
pmid: 28234597
[38]   Wang Y, Lin H, Hao N , et al. Forkhead box O1 mediates defects in palmitate-induced insulin granule exocytosis by downregulation of calcium/calmodulin-dependent serine protein kinase expression in INS-1 cells. Diabetologia, 2015,58(6):1272-1281.
doi: 10.1007/s00125-015-3561-4 pmid: 25796372
[39]   郝娜娜, 王天元, 王尧 等. 钙/钙调蛋白依赖性丝氨酸蛋白激酶在胰岛素囊泡分泌过程中的作用. 中华糖尿病杂志, 2016,8(11):677-680.
doi: 10.3760/cma.j.issn.1674-5809.2016.11.009
[39]   Hao N N, Wang T Y, Wang Y , et al. Role of calcium/calmodulin-dependent serine protein kinase in insulin granules secretion. Chinese Journal of Diabetes, 2016,8(11):677-680.
doi: 10.3760/cma.j.issn.1674-5809.2016.11.009
[40]   Landry-Voyer A M, Bilodeau S, Bergeron D , et al. Human PDCD2L is an export substrate of CRM1 that associates with 40S ribosomal subunit precursors. Molecular and Cellular Biology, 2016,36(24):3019-3032.
doi: 10.1128/MCB.00303-16 pmid: 27697862
[41]   Kramer J, Granier C J, Davis S , et al. PDCD2 controls hematopoietic stem cell differentiation during development. Stem Cells and Development, 2013,22(1):58-72.
doi: 10.1089/scd.2012.0074 pmid: 22800338
[42]   Barboza N, Minakhina S, Medina D J , et al. PDCD2 functions in cancer cell proliferation and predicts relapsed leukemia. Cancer Biology & Therapy, 2013,14(6):546-555.
doi: 10.4161/cbt.24484 pmid: 3813571
[43]   Chen Q, Yan C, Yan Q, Feng L, Chen J, Qian K . The novel MGC13096 protein is correlated with proliferation. Cell Biochemistry and Function, 2008,26(2):141-145.
doi: 10.1002/cbf.1410 pmid: 17393540
[44]   Chen Q, Yan C Q, Liu F J , et al. Overexpression of the PDCD2-like gene results in inhibited TNF-[α] production in activated daudi cells. Human Immunology, 2008,69(4-5):259-265.
doi: 10.1016/j.humimm.2008.01.020 pmid: 18486760
[45]   Yin Y, Yong W, Yu J N , et al. Pdcd2l promotes palmitate-induced pancreatic beta-cell apoptosis as a FoxO1 target gene. PLOS ONE, 2016,11(11):e0166692.
doi: 10.1371/journal.pone.0166692 pmid: 27861641
[46]   Prentki M, Matschinsky Franz M, Madiraju SRM . Metabolic signaling in fuel-induced insulin secretion. Cell Metabolism, 2013,18(2):162-185.
doi: 10.1016/j.cmet.2013.05.018 pmid: 23791483
[47]   Talchai S C, Accili D . Legacy effect of foxo1 in pancreatic endocrine progenitors on adult β-cell mass and function. Diabetes, 2015,64(8):2868-2879.
doi: 10.2337/db14-1696 pmid: 25784544
[1] ZENG Xiang-Yi,PAN Jie. Progress on Autophagy Regulation of Browning of White Adipose Cells[J]. China Biotechnology, 2020, 40(6): 63-73.
[2] CHEN Qing-yu,WANG Xian-zhong,ZHANG Jiao-jiao. Application of Gene Technology in the Treatment of Type 2 Diabetes Mellitus[J]. China Biotechnology, 2020, 40(11): 73-81.
[3] LI Yan-wei, MA Yi, HAN Lei, XIAO Xing, DANG Shi-ying, WEN Tao, WANG De-hua, FAN Zhi-yong. A Preliminary Study on Fas Apoptosis Inhibitory Molecule FAIM 1 Inducing and Simple Obesity[J]. China Biotechnology, 2017, 37(6): 37-42.
[4] YIN Shuang, FENG Cui, ZHANG Chun, WANG Qi, WANG Jian, YU Rong, LIU Yong-dong, SU Zhi-guo. Preparation of Transferrin Conjugated Ciliary Neurotrophic Factor and Evaluation of Biological Activity[J]. China Biotechnology, 2016, 36(4): 43-49.