Pollen Typhae total flavone improves insulin-induced glucose uptake through the β-arrestin-2-mediated signaling in C2C12 myotubes

Feng,Xiao-Tao; Wang,Tian-Zhan; Chen,Yi; Liu,Ji-Bo; Liu,Yi; Wang,Wen-Jian

doi:10.3892/ijmm.2012.1061

Pollen Typhae total flavone improves insulin-induced glucose uptake through the β-arrestin-2-mediated signaling in C2C12 myotubes

Authors:
- Xiao-Tao Feng
- Tian-Zhan Wang
- Yi Chen
- Ji-Bo Liu
- Yi Liu
- Wen-Jian Wang
View Affiliations

Affiliations: Institute of Chinese Integrative Medicine, Huashan Hospital, Fudan University, Shanghai, P.R. China, Department of Endocrinology, Longhua Hospital, Shanghai University of Chinese Medicine, Shanghai, P.R. China
Published online on: July 16, 2012 https://doi.org/10.3892/ijmm.2012.1061
Pages: 914-922

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Defects in insulin-stimulated glucose uptake in skeletal muscle result from the dysfunction of insulin signaling including the phosphatidylinositol-3 kinase (PI3K) pathway and a novel β-arrestin-2-mediated signaling, which leads to insulin resistance (IR). Pollen Typhae, a Chinese herb, has been used for thousands of years in traditional Chinese medicine, and has the potential to inhibit the development of IR. We have previously reported that Pollen Typhae total flavone (PTF), the extract from Pollen Typhae, ameliorates high-glucose- and high-insulin-induced impairment of glucose uptake in 3T3-L1 adipocytes, but the mechanisms remain unclear. The objective of this study was to investigate the effects of PTF on glucose uptake, and to explore the underlying mechanisms in C2C12 myotubes. PTF improved insulin-stimulated glucose uptake in a dose- and time-dependent manner in C2C12 myotubes, and prevented palmitate-induced IR. Furthermore, PTF enhanced the basal gene expression of Src and Akt2, elevated the protein expression of β-arrestin-2, Src and Akt, increased the phosphorylation of insulin receptor-β at Tyr1150/1151 and Akt at Thr308/Ser473 in an insulin-dependent manner, but had no effects on the protein expression of PI3K-p85 or the activity of PI3K. Inhibition of Src but not PI3K restrained PTF-induced phosphorylation of Akt and glucose uptake. Our findings indicate that PTF improves insulin-induced glucose uptake via the β-arrestin-2-mediated signaling in C2C12 myotubes.

View Figures

View References

1.	AD BaronG BrechtelP WallaceSV EdelmanRates and tissue sites of non-insulin- and insulin-mediated glucose uptake in humansAm J Physiol255E769E77419883059816
2.	C FrøsigEA RichterImproved insulin sensitivity after exercise: focus on insulin signalingObesity (Silver Spring)17Suppl 3S15S20200919927140
3.	W YangJ LuJ WengPrevalence of diabetes among men and women in ChinaN Engl J Med36210901101201010.1056/NEJMoa090829220335585
4.	J FernandesIE LofgrenPrevalence of metabolic syndrome and individual criteria in college studentsJ Am Coll Health59313321201110.1080/07448481.2010.50808421308592
5.	BM BurgeringPJ CofferProtein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transductionNature376599602199510.1038/376599a07637810
6.	DR AlessiM AndjelkovicB CaudwellMechanism of activation of protein kinase B by insulin and IGF-1EMBO J156541655119968978681
7.	DD SarbassovDA GuertinSM AliDM SabatiniPhosphorylation and regulation of Akt/PKB by the rictor-mTOR complexScience30710981101200510.1126/science.110614815718470
8.	CM TaniguchiB EmanuelliCR KahnCritical nodes in signalling pathways: insights into insulin actionNat Rev Mol Cell Biol78596200610.1038/nrm183716493415
9.	E JacintoV FacchinettiD LiuSIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificityCell127125137200610.1016/j.cell.2006.08.03316962653
10.	T KadowakiInsights into insulin resistance and type 2 diabetes from knockout mouse modelsJ Clin Invest106459465200010.1172/JCI1083010953020
11.	K CusiK MaezonoA OsmanInsulin resistance differentially affects the PI3-kanase-and MAP kinase-mediated signaling in human muscleJ Clin Invest105311320200010.1172/JCI753510675357
12.	B LuanJ ZhaoH WuDeficiency of a β-arrestin-2 signal complex contributes to insulin resistanceNature457114611492009
13.	A MaretteJM RichardsonT RamlalAbundance, localization, and insulin-induced translocation of glucose transporters in red and white muscleAm J Physiol263C443C45219921514590
14.	T JiangY QiuInteraction between Src and a C-terminal proline-rich motif of Akt is required for Akt activationJ Biol Chem2781578915793200310.1074/jbc.M21252520012600984
15.	JM BeaulieuTD SotnikovaS MarionAn Akt/β-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behaviorCell1222612732005
16.	M LodeiroM TheodorpoulouM Pardoc-Src regulates Akt signaling in response to ghrelin via beta-arrestin signaling-independent and -dependent mechanismsPLoS One4e4686200910.1371/journal.pone.000468619262695
17.	A GibbsC GreenVM DoctorIsolation and anticoagulant properties of polysaccharides of Typha augustata and Daemonoropes speciesThromb Res3297108198310.1016/0049-3848(83)90021-X6658717
18.	J ZhaoCY ZhangDM XuThe antiatherogenic effects of components isolated from pollen typhaeThromb Res57957966199010.1016/0049-3848(90)90162-62116685
19.	S ChungS ParkCH YangUnsaturated fatty acids bind Myc-Max transcription factor and inhibit Myc-Max-DNA complex formationCancer Lett188153162200210.1016/S0304-3835(02)00455-X12406560
20.	F QinHX SunImmunosuppressive activity of Pollen Typhae ethanol extract on the immune responses in miceJ Ethnopharmacol102424429200510.1016/j.jep.2005.06.02716095855
21.	Y YangS WangS ZhangDetermination of flavonoids in pollen typhae (Puhuang) by HPCE and HPLCZhongguo Zhong Yao Za Zhi246826847031999(In Chinese)
22.	HF MaB LiuGY ZhangGC-MS analysis of the fatty components of Pollen Typhae before and after being carbonizedZhongguo Zhong Yao Za Zhi312002022006(In Chinese)
23.	SY LouY LiuWH ChenPollen Typhae total flavones inhibit expression of interleukin-6 in C2C12 skeletal muscle cells cultured with palmitateZhong Xi Yi Jie He Xue Bao64884922008(In Chinese)
24.	N OhkuraK TamuraA TanakaExperimental study on the hemostatc activity of Pollen Typhae: a traditional folk medicine used by external and oral applicationBlood Coagul Fibrinolysis22631636201110.1097/MBC.0b013e328349a22c21934490
25.	SY LouY LiuYY MaEffects of Yiqi Sanju Formula on non-alcoholic fatty liver disease: a randomized controlled trialZhong Xi Yi Jie He Xue Bao67937982008(In Chinese)
26.	CY HeWJ WangB LiClinical research of Yiqi Sanju Formula in treating central obese men at high risk of metabolic syndromeZhong Xi Yi Jie He Xue Bao52632672007(In Chinese)
27.	Z ZhangHL XueY LiuWJ WangYi-Qi-Zeng-Min-Tang, a Chinese medicine, ameliorates insulin resistance in type 2 diabetic ratsWorld J Gastroenterol17987995201121448349
28.	YM HeWJ WangWH ChenEffects of Pollen Typhae total flavone on glucose and lipid metabolism in 3T3-L1 adipocytesZhong Xi Yi Jie He Xue Bao45935952006(In Chinese)
29.	EA KoulaouzidouN EconomidesP BeltesIn vitro evaluation of the cytotoxicity of ProRoot MTA and MTA AngelusJ Oral Sci50397402200810.2334/josnusd.50.39719106466
30.	B JiangY YangH JinAstragaloside IV attenuates lipolysis and improves insulin resistance induced by TNFalpha in 3T3-L1 adipocytesPhytother Res2214341439200810.1002/ptr.243418972582
31.	JJ SennToll-like receptor-2 is essential for the development of palmitate-induced insulin resistance in myotubesJ Biol Chem2812686526875200610.1074/jbc.M51330420016798732
32.	A XuH WangRL HooSelective elevation of adiponectin production by the natural compounds derived from a medicinal herb alleviates insulin resistance and glucose intolerance in obese miceEndocrinology150625633200910.1210/en.2008-099918927219
33.	GM ReavenRole of insulin resistance in human diseaseDiabetes3715951607198810.2337/diab.37.12.15953056758
34.	MF WhiteSE ShoelsonH KeutmannCR KahnA cascade of tyrosine autophosphorylation in the beta-subunit activates the phosphotransferase of the insulin receptorJ Biol Chem2632969298019882449432
35.	S GeorgeJJ RochfordC WolfrumA family with severe insulin resistance and diabetes due to a mutation in AKT2Science30413251328200410.1126/science.109670615166380
36.	P LauRL FitzsimmonsMA PearenHomozygous staggerer (sg/sg) mice display improved insulin sensitivity and enhanced glucose uptake in skeletal muscleDiabetologia5411691180201110.1007/s00125-011-2046-321279323
37.	M ChaoD ZouY ZhangImproving insulin resistance with traditional Chinese medicine in type 2 diabetic patientsEndocrine36268274200910.1007/s12020-009-9222-y19728183
38.	W XieL DuDiabetes is an inflammatory disease: evidence from traditional Chinese medicinesDiabetes Obes Metab13289301201110.1111/j.1463-1326.2010.01336.x21205111
39.	A DresnerD LaurentM MarcucciEffects of free fatty acids on glucose transport and IRS-1-associated phosphatidylinositol 3-kinase activityJ Clin Invest103253259199910.1172/JCI50019916137
40.	R BelfortL MandarinoS KashyapDose response effect of elevated plasma FFA on insulin signalingDiabetes5416401648200510.2337/diabetes.54.6.164015919784
41.	LM NeriP BorgattiS CapitaniAM MartelliThe nuclear phosphoinositide 3-kinase/AKT pathway: a new second messenger systemBiochim Biophys Acta15847380200210.1016/S1388-1981(02)00300-112385889
42.	X FengW WangJ LiuY Liuβ-Arrestins: multifunctional signaling adaptors in type 2 diabetesMol Biol Rep38251725282011
43.	VV GurevichEV GurevichThe structural basis of arrestin-mediated regulation of G protein coupled receptorPharmacol Ther110465502200610.1016/j.pharmthera.2005.09.00816460808
44.	B LiuY LuHPLC determination of two flavonoids in pollen Typhae (puhuang) and its different processed productsZhongguo Zhong Yao Za Zhi234024044471983(In Chinese)
45.	SL HwanqGC YenModulation of Akt, JNK, and p38 activation is involved in citrus flavonoid-mediated cytoprotection of PC12 cells challenged by hydrogen peroxideJ Agric Food Chem5725762582200910.1021/jf803360719222219
46.	SE ParkK SapkotaS KimKaempferol acts through mitogen-activated protein kinases and protein kinase B/AKT to elicit protection in a model of neuroinflammation in BV2 microglial cellsBr J Pharmacol16410081025201110.1111/j.1476-5381.2011.01389.x21449918
47.	XQ WangRQ YaoX LiuQuercetin protects oligodendrocyte precursor cells from oxygen/glucose deprivation injury in vitro via the activation of the PI3K/Akt signaling pathwayBrain Res Bull86277284201110.1016/j.brainresbull.2011.07.014
48.	UI IsaoI TakeshiH Jieβ-Arrestin-1 competitively inhibits insulin-induced ubiquitination and degradation of insulin receptor substrate 1Mol Cell Biol24892989372004
49.	X LiGS BaillieMD HouslayMdm2 directs the ubiquitination of beta-arrestin-sequestered cAMP phosphodiesterase-4D5J Biol Chem2841617016182200910.1074/jbc.M109.00807819372219
50.	L NoguésA SalcedoF Mayor JrP PenelaMultiple scaffolding functions of (beta)-arrestins in the degradation of G protein-coupled receptor kinase 2J Biol Chem28611651173201121081496