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Effects of Puerarin on the Ovariectomy-Induced Depressive-Like Behavior

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Effects of Puerarin on the Ovariectomy-Induced Depressive-Like Behavior molecules Article Effects of Puerarin on the Ovariectomy-Induced Depressive-Like Behavior in ICR Mice and Its Possible Mechanism of Action Ariyawan Tantipongpiradet 1, Orawan Monthakantirat 1, Onchuma Vipatpakpaiboon 1, Charinya Khampukdee 1 , Kaoru Umehara 2, Hiroshi Noguchi 2, Hironori Fujiwara 3, Kinzo Matsumoto 3, Nazim Sekeroglu 4 , Anake Kijjoa 5,* and Yaowared Chulikhit 1,* 1 Division of Pharmaceutical Chemistry, Faculty of Pharmaceutical Sciences, Khon Kaen University, Khon Kaen 40002, Thailand; [email protected] (A.T.); [email protected] (O.M.); [email protected] (O.V.); [email protected] (C.K.) 2 Department of Pharmacognosy, School of Pharmaceutical Sciences, University of Shizuoka, Yada 52-1, Shizuoka-shi, Shizuoka 422-8526, Japan; [email protected] (K.U.); [email protected] (H.N.) 3 Division of Medicinal Pharmacology, Institute of Natural Medicine, University of Toyama, 2630 Sugitani, Toyama 930-0194, Japan; [email protected] (H.F.); [email protected] (K.M.) 4 Department of Horticulture, Faculty of Agriculture, Killis 7 Aralik University, Killis 79000, Turkey; [email protected] 5 ICBAS-Instituto de Ciências Biomédicas Abel Salazar and CIIMAR, Rua de Jorge Viterbo Ferreira, 228, 4050-313 Porto, Portugal * Correspondence: [email protected] (A.K.); [email protected] (Y.C.); Tel.: +351-220428331 (A.K.) Received: 23 September 2019; Accepted: 11 December 2019; Published: 13 December 2019 Abstract: Daily treatment of ovariectomized (OVX) ICR mice with puerarin, a glycosyl isoflavone isolated from the root bark of Pueraria candollei var. mirifica, and 17β-estradiol attenuated ovariectomy-induced depression-like behavior, as indicated by a decrease in immobility times in the tail suspension test (TST) and the forced swimming test (FST), an increase in the uterine weight and volume, a decrease in serum corticosterone levels, and dose-dependently normalized the downregulated transcription of the brain-derived neurotrophic factor (BDNF) and estrogen receptor (Erβ and Erα) mRNAs. Like 17β-estradiol, puerarin also inhibited ovariectomy-induced suppression of neurogenesis in the dentate gyrus of the hippocampus (increased the number of doublecortin (DCX)-immunosuppressive cells). These results suggest that puerarin exerts antidepressant-like effects in OVX animals, possibly by attenuating the OVX-induced hyperactivation of the HPA axis and/or normalizing the downregulated transcription of BDNF and ER mRNA in the brain. Keywords: puerarin; Pueraria candollei var. mirifica; ovariectomy; forced swimming test; tail suspension test; neurogenesis 1. Introduction Physiological fluctuations of estrogen in women are an important factor that affects mood, behavior, and cognition during their lifespan. A sharp decline in estrogen levels, which occurs during the anestrus cycle and menopausal transition, post-menopause, and surgical menopause, causes the most significant alterations in mood and cognitive function [1,2]. Thus, females exposed to a state of estrogen deprivation are prone to a higher risk of neurological symptoms, such as anxiety, depression, and memory impairment, than males. Preclinical studies demonstrated that bilateral ovariectomy and aging make female rodents more susceptible to stressful stimuli than control animals, inducing emotional deficits such as anxiety and Molecules 2019, 24, 4569; doi:10.3390/molecules24244569 www.mdpi.com/journal/molecules Molecules 2020, 25, x FOR PEER REVIEW 2 of 16 MoleculesPreclinical2019, 24, 4569 studies demonstrated that bilateral ovariectomy and aging make female rodents2 of 15 more susceptible to stressful stimuli than control animals, inducing emotional deficits such as anxiety and depression. These symptoms can be reversed by supplementation with estrogen. A body of depression.evidence suggests These symptoms that such can estrogen be reversed replac by supplementationement therapy with(ERT) estrogen. can exert A body anxiolytic of evidence and suggestsantidepressant that such effects estrogen in menopausal replacement females therapy by (ERT) modulating can exert the anxiolytic hypothalamic–pituitary–adrenal and antidepressant effects in(HPA) menopausal axis functions females [3,4]. by modulating However, the the drawback hypothalamic–pituitary–adrenal of ERT is its adverse effects, (HPA) such axis as functions an increased [3,4]. However,risk of breast the drawbackand endometrial of ERT is cancers, its adverse as well effects, as suchthromboembolic as an increased events riskof [5,6]. breast Consequently, and endometrial the cancers,long-term as usage well of as ERT thromboembolic to ameliorate eventsemotional [5,6 ].and Consequently, cognitive deficits the has long-term an obvious usage limitation of ERT toin amelioratewomen. Thus, emotional the search and cognitivefor new phytoestrogens, deficits has an obviouswith a weak limitation effect in on women. reproductive Thus, theorgans, search from for newnatural phytoestrogens, sources continues with to a weakbe an e importantffect on reproductive field of research. organs, from natural sources continues to be an importantPueraria fieldcandollei of research. var. mirifica is a medicinal plant used in Thai traditional medicine for its rejuvenatingPueraria and candollei estrogenicvar. mirificaeffects [7].is aFor medicinal this reason, plant this used plant in has Thai been traditional widely investigated medicine forfor itsits rejuvenatingconstituents and and pharmacological estrogenic effects activities. [7]. For this Peerakam reason, thiset al. plant [8] found has been that widelythe 95% investigated ethanol extract for itsof constituentsthis plant contained and pharmacological puerarin (1), as activities. a major Peerakamcompound, et and al. [ 8other] found isoflavonoids, that the 95% such ethanol as daidzin, extract ofdaidzein, this plant genistin, contained and pueraringenistein, (1 in), asaddition a major to compound, the phytoestrogens and other miroestrol isoflavonoids, and deoxymiroestrol. such as daidzin, daidzein,Suthon et genistin,al. [9] evaluated and genistein, the anti-osteoporotic in addition to effects the phytoestrogens of the crude extract miroestrol of P. and candollei deoxymiroestrol. var. mirifica Suthonand puerarin et al. [ 9(1]) evaluated in ovariectomized the anti-osteoporotic (OVX) mice e andffects found of the that crude only extract the crude of P. candolleiextract atvar. 50 mirificamg/kg and(body puerarin weight) ( 1per) in day ovariectomized caused a significant (OVX) miceincrease and in found the trabecular that only bone the crude mineral extract densities at 50 of mg tibia/kg (bodymetaphysis weight) when per compared day caused to a the significant control group. increase On in the the other trabecular hand, bonethe pharmacological mineral densities activities of tibia metaphysisof puerarin when(1) (Figure compared 1), a major to the isoflavonoid control group. from On P. the candollei other hand, var. mirifica the pharmacological, have been extensively activities ofinvestigated. puerarin (1 Puerarin) (Figure 1(),1) a has major been isoflavonoid widely used from in P.the candollei treatmentvar. ofmirifica diabetes,, have dyslipidemia, been extensively liver investigated.fibrosis, cardiovascular Puerarin (1 )diseases, has been neurotoxicity, widely used in and the treatmentAlzheimer’s of diabetes, disease dyslipidemia,[10]. This compound liver fibrosis, was cardiovascularalso found to diseases,exhibit neurotoxicity,various protective and Alzheimer’s effects against disease fever, [10]. Thishyperlipidemia, compound wasosteonecrosis, also found toinflammation, exhibit various and protective oxidative edamageffects against [10,11]. fever, Puerarin hyperlipidemia, (1) was also osteonecrosis, investigated for inflammation, its hypotensive and oxidativeeffects and damage mechanisms [10,11]. in Puerarin spontaneously (1) was alsohypert investigatedensive rats for [12]. its hypotensive The effect of eff puerarinects and mechanisms(1), isolated infrom spontaneously P. lobata, on hypertensive angiotensin rats II-induced [12]. The eaorticffect of aneurysm puerarin (1formation), isolated fromwas P.also lobata investigated, on angiotensin [13]. II-inducedAlthough puerarin aortic aneurysm (1) was formationreported for was its also antidepressant-lik investigated [13e]. effects Although in the puerarin chronic (1 )unpredictable was reported forstress-induced its antidepressant-like rats [14], its e effectsffects in on the depressive chronic unpredictable-like symptoms stress-induced and neurogenesis rats [in14 ],OVX its emice,ffects the on depressive-likeanimal model for symptoms menopause, and have neurogenesis never been in inve OVXstigated. mice, the Therefore, animal model the present for menopause, study aimed have to neverinvestigate been investigated.the effects of Therefore,puerarin (1 the) on present depressive-like study aimed behavior to investigate in OVX themice, eff asects well of puerarinas to elucidate (1) on depressive-likethe underlying behavior mechanisms in OVX relate mice,d asto wellHPA as axis to elucidate function, the using underlying 17β-estradiol mechanisms (2) as related a reference to HPA axishormone. function, Additionally, using 17β-estradiol the expressions (2) as a reference of mRNAs hormone. of estrogen Additionally, receptor the (ER expressionsα and ER ofβ), mRNAs brain- ofderived estrogen neurotrophic receptor (ER factorα and (BDNF), ERβ), brain-derived and doublecortin neurotrophic (DCX), which factor (BDNF),is an indicator/marker and doublecortin of (DCX),neurogenesis
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