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Anti-Ageing Effect of Physalis Alkekengi Ethyl Acetate Layer on A

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Anti-Ageing Effect of Physalis Alkekengi Ethyl Acetate Layer on A International Journal of Molecular Sciences Article Anti-Ageing Effect of Physalis alkekengi Ethyl Acetate Layer on a d-galactose-Induced Mouse Model through the Reduction of Cellular Senescence and Oxidative Stress Kaiyue Sun * , Yingting Sun, Heyang Li, Dongyao Han, Yuting Bai, Rong Zhao and Zijiao Guo College of Animal Science and Veterinary Medicine, Shanxi Agricultural University, Taigu 030801, Shanxi, China; [email protected] (Y.S.); [email protected] (H.L.); [email protected] (D.H.); [email protected] (Y.B.); [email protected] (R.Z.); [email protected] (Z.G.) * Correspondence: [email protected] Received: 17 January 2020; Accepted: 4 March 2020; Published: 6 March 2020 Abstract: We aimed to study the effects of an ethyl acetate fraction of Physalis alkekengi (PAE) on d-galactose (d-gal)-induced senescence and the underlying mechanism. Firstly, analysis of the phytochemical composition revealed total flavonoids, total phenolics, total saponins, rutin, and luteolin contents of 71.72 2.99 mg rutin equivalents/g, 40.19 0.47 mg gallic acid equivalents/g, ± ± 128.13 1.04 mg oleanolic acid equivalents/g, 1.67 0.07 mg/g and 1.61 0.01 mg/g, respectively. ± ± ± The mice were treated with d-gal for six weeks, and from the fifth week, the mice were administered with PAE by gavage once a day for five weeks. We found significant d-gal-induced ageing-related changes, such as learning and memory impairment in novel object recognition and Y-maze, fatigue in weight-loaded forced swimming, reduced thymus coefficient, and histopathological injury of the liver, spleen, and hippocampus. The PAE effectively protected from such changes. Further evaluation showed that PAE decreased the senescence-associated β-galactosidase of the liver, spleen, and hippocampus, as well as the oxidative stress of the liver, plasma, and brain. The abundance of flavonoids, phenols, and saponins in PAE may have contributed to the above results. Overall, this study showed the potential application of PAE for the prevention or treatment of ageing-associated disorders. Keywords: Physalis alkekengi; learning and memory; exercise endurance; cellular senescence; oxidative stress 1. Introduction Ageing-related diseases are attracting widespread attention as the global population increases and human lifespan extends. By 2050, the proportion of the world’s population over 60 years old will reach 22% [1]. Ageing is an irreversible process characterized by various progressive bouts of degeneration of physiological functions. The morbidity and death rate of humans increase with ageing. Moreover, risk factors for humans increased with ageing to develop various chronic diseases, such as Alzheimer’s disease (AD) [2], fatigue [3], tumor suppression [4], type 2 diabetes, obesity [5], and cardiovascular disorders [6]. DNA damage and cellular senescence caused by free radicals are two primary mechanisms for age-related disease [7]. Furthermore, several studies have shown that reduction of cellular senescence could improve the healthspan [8] and ameliorate age-related diseases, such as hepatic steatosis [9], post-traumatic osteoarthritis [10], Parkinson’s disease [11], and AD [12]. The Food and Drug Administration have proved six substances for the anti-ageing clinical study; five are related to the reduction of senescent cells or senescence-associated secretory phenotype [13]. These conditions Int. J. Mol. Sci. 2020, 21, 1836; doi:10.3390/ijms21051836 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 18 Int. J. Mol. Sci. 2020, 21, 1836 2 of 18 reduction of senescent cells or senescence-associated secretory phenotype [13]. These conditions suggestsuggest thatthat senescentsenescent cellscells areare anan emergingemerging targettarget forfor ageing-relatedageing-related diseases,diseases, andand inhibitioninhibition ofof senescentsenescent cellscells couldcould delaydelay ageing.ageing. Some active compounds,compounds, such asas metformin,metformin, rapamycin,rapamycin, oror senolyticssenolytics thatthat targetedtargeted to to senescent senescent cells, cells, are are found found to to slow slow down down the the ageing-relative ageing-relative diseases, diseases, such such as cardiacas cardiac dysfunction, dysfunction, loss loss of of muscle muscle mass, mass, and and osteoporosis osteoporosis [14 [14–16–16].]. However, However, their their value value isis limitedlimited becausebecause ofof disadvantages,disadvantages, suchsuch asas hyperlipidemiahyperlipidemia andand fatiguefatigue [[1717,,1818].]. Thus, researchersresearchers areare activelyactively developingdeveloping novelnovel substancessubstances withwith goodgood eefficaciesfficacies andand fewfew sideside eeffectsffects [ 15[15].]. PhysalisPhysalis alkekengi L. var. var. FranchetiiFranchetii, ,named named the the Chinese Chinese lantern, lantern, is an is anedible edible plant plant classified classified in the in theSolanaceae Solanaceae family. family. The Thecalyx calyx and fruit and fruitof P. ofalkekenP. alkekengigi L. var.L. franchetii var. franchetii (Mast.)(Mast.) MakinoMakino possesspossess a variety a varietyof properties, of properties, including including anti-inflammatory, anti-inflammatory, antimicrobial, antimicrobial, antitumor, antitumor, and anti and-diabetes anti-diabetes [19–23]. [19– The23]. Theethyl ethyl acetate acetate fraction fraction of P. of P.alkekengi alkekengi (PAE)(PAE) inhibited inhibited lipopolysaccharide lipopolysaccharide-induced-induced pro pro-inflammatory-inflammatory mediatorsmediators inin BV2BV2 cellscells [[2424]] andand demonstrateddemonstrated potentpotent memorymemory improvementimprovement inin scopolamine-inducedscopolamine-induced cognitivecognitive impairmentsimpairments through through anti-oxidative anti-oxidative stress stress [25 [25].]. However, However, PAE’s PAE’s effect effect on ageing on ageing has not has been not explored.been explored. In this In study, this westudy, used we a d -galactoseused a D-galactose (d-gal)-induced (D-gal) senescence-induced senescence mouse model mouse to observe model the to protectiveobserve the eff protectiveect of the PAE.effect of the PAE. 2.2. Results 2.1.2.1. Component Analysis of PAEPAE TheThe experimentalexperimental designdesign andand timelinetimeline areare shownshown inin FigureFigure1 1.. The The contents contents of of active active components components inin PAEPAE areare shownshown inin TableTable1 .1. The The total total flavonoid flavonoid content content (TFC), (TFC), total total phenolic phenolic content content (TPC), (TPC), and and total saponins content (TSC) were 71.72 2.99 mg rutin equivalents (REs)/g, 40.19 0.47 mg gallic total saponins content (TSC) were 71.72 ±± 2.99 mg rutin equivalents (REs)/g, 40.19 ±± 0.47 mg gallic acid equivalents (GAEs)/g and 128.13 1.04 mg oleanolic acid equivalents (OAEs)/g, respectively. acid equivalents (GAEs)/g and 128.13 ±± 1.04 mg oleanolic acid equivalents (OAEs)/g, respectively. The contents of rutin and luteolin in PAE were 1.67 0.07 mg/g and 1.61 0.01 mg/g, respectively, The contents of rutin and luteolin in PAE were 1.67 ±± 0.07 mg/g and 1.61 ±± 0.01 mg/g, respectively, calculatedcalculated byby high-performancehigh-performance liquidliquid chromatographychromatography (HPLC)(HPLC) and byby usingusing anan externalexternal standardstandard (Table(Table1 ,1, Figure Figure2). 2). Figure 1. Experimental design and timeline.The mice were treated with once-daily d-galactose (d-gal) (150Figure mg 1/kg). Experimental or saline by design subcutaneous and timeline injection.The for mice the were first sixtreated weeks. with From once the-daily fifth D week,-galactose the vitamin (D-gal) E(150 (VE) mg/kg) or Physalis or saline alkekengi by subcutaneous(PAE) groups wereinjection subjected for the to first VE (100six weeks. mg/kg) From or PAE the (at fifth doses week, of 3, the 10, 30vitamin mg/kg, E oral)(VE) onceor Physalis daily foralkekengi five weeks, (PAE) and groups the controlwere subjected group and to VE model (100 group mg/kg) were or PAE administered (at doses aof solvent 3, 10, 30 (2% mg/kg, ethanol oral) in oil,once oral) daily in for the five same weeks, way instead.and the control In the ninthgroup week, and model the behavior group were tests wereadministered investigated a solvent after PAE(2% administration.ethanol in oil, oral) NOR, in novel the same object way recognition; instead. WLFST,In the ninth weight-loaded week, the swimmingbehavior tests test. were investigated after PAE administration. NOR, novel object recognition; WLFST, weight-loaded swimming test. Table 1. The bioactive components of PAE. Bioactive Components Content TFC (mg REs/g PAE) 71.72 ± 2.99 TPC (mg GAEs/g PAE) 40.19 ± 0.47 TSC (mg OAEs / g PAE) 128.13 ± 1.04 Int. J. Mol. Sci. 2020, 21, 1836 3 of 18 Table 1. The bioactive components of PAE. Bioactive Components Content TFC (mg REs/g PAE) 71.72 2.99 ± TPC (mg GAEs/g PAE) 40.19 0.47 ± Int. J. Mol. Sci. 2020TSC, 21, (mgx FOR OAEs PEER/ REVIEWg PAE) 128.13 1.04 3 of 18 ± Rutin (mg/ g PAE) 1.67 0.07 ± Luteolin (mgRutin/g PAE) (mg/ g PAE) 1.67 ±1.62 0.07 0.01 ± TPC, Total phenolicLuteolin content; (mg/g TFC, PAE) Total flavonoid content; TSC,1.6 Total2 ±saponins 0.01 content. TPC, Total phenolic content; TFC, Total flavonoid content; TSC, Total saponins content. Figure 2. HPLC chromatogram of the ethyl acetate fraction of Physalis alkekengi.(A) HPLC analysis of Figure 2. HPLC chromatogram of the ethyl acetate fraction of Physalis alkekengi. (A) HPLC analysis of PAE, and (B) external standard. The peak 1, rutin (t’R =
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