Anti‑inflammatory role of Prunus persica L. Batsch methanol extract on lipopolysaccharide‑stimulated glial cells

Seo,Kyoung Hee; Choi,So   Young; Jin,Yeonsun; Son,Heebin; Kang,Young   Sun; Jung,Seung   Hyo; Kim,Yong‑In; Eum,Sangmi; Bach,Tran   The; Yoo,Hee   Min; Whang,Wan   Kyunn; Jung,Sun‑Young; Kang,Wonku; Ko,Hyun   Myung; Lee,Sung   Hoon

doi:10.3892/mmr.2020.11016

Anti‑inflammatory role of Prunus persica L. Batsch methanol extract on lipopolysaccharide‑stimulated glial cells

Authors:
- Kyoung Hee Seo
- So Young Choi
- Yeonsun Jin
- Heebin Son
- Young Sun Kang
- Seung Hyo Jung
- Yong‑In Kim
- Sangmi Eum
- Tran The Bach
- Hee Min Yoo
- Wan Kyunn Whang
- Sun‑Young Jung
- Wonku Kang
- Hyun Myung Ko
- Sung Hoon Lee
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Affiliations: College of Pharmacy, Chung‑Ang University, Seoul 06974, Republic of Korea, Department of Biomedical Science and Technology, Konkuk University, Seoul 05029, Republic of Korea, Department of Medicine, Research Institute of Medical Science, Konkuk University School of Medicine, Chungju 27478, Republic of Korea, International Biological Material Research Center, Korea Research Institute of Bioscience and Biotechnology, Daejeon 34141, Republic of Korea, Department of Botany, Institute of Ecology and Biological Resources, Vietnam Academy of Science and Technology, Cau Giay, Hanoi 10000, Vietnam, Center for Bioanalysis, Korea Research Institute of Standards and Science, Daejeon 34113, Republic of Korea, Pharmaceutical Botany Laboratory, College of Pharmacy, Chung‑Ang University, Seoul 06974, Republic of Korea, Department of Life Science, College of Science and Technology, Woosuk University, Chungcheongbuk 27841, Republic of Korea
Published online on: March 10, 2020 https://doi.org/10.3892/mmr.2020.11016
Pages: 2030-2040
Copyright: © Seo et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Glial cells are the resident immune cells of the central nervous system. Reactive glial cells release inflammatory mediators that induce neurotoxicity or aggravate neurodegeneration. Regulation of glial activation is crucial for the initiation and progression of neuropathological conditions. Constituents of the peach tree (Prunus persica L. Batsch), which has a global distribution, have been found to exert therapeutic effects in pathological conditions, such as rashes, eczema and allergies. However, the therapeutic potential of its aerial parts (leaves, fruits and twigs) remains to be elucidated. The present study aimed to evaluate the anti‑inflammatory role of P. persica methanol extract (PPB) on lipopolysaccharide (LPS)‑stimulated glial cells. High‑performance liquid chromatography coupled with tandem mass spectrometry analysis showed that PPB contained chlorogenic acid and catechin, which have antioxidant properties. Western blot and reverse transcription polymerase chain reaction results indicated that PPB reduced the transcription of various proinflammatory enzymes (nitric oxide synthase and cyclooxygenase‑2) and cytokines [tumor necrosis factor‑α, interleukin (IL)‑1β and IL‑6] in LPS‑stimulated BV2 cells. In addition, PPB inhibited the activation of NF‑κB and various mitogen‑activated protein kinases required for proinflammatory mediator transcription. Finally, nitrite measurement and immunocytochemistry results indicated that PPB also suppressed nitrite production and NF‑κB translocation in LPS‑stimulated primary astrocytes. Thus, PPB may be used as a potential therapeutic agent for neurodegenerative diseases and neurotoxicity via the suppression of glial cell activation.

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1	González-Scarano F and Baltuch G: Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci. 22:219–240. 1999. View Article : Google Scholar : PubMed/NCBI
2	Maragakis NJ and Rothstein JD: Mechanisms of disease: Astrocytes in neurodegenerative disease. Nat Clin Pract Neurol. 2:679–689. 2006. View Article : Google Scholar : PubMed/NCBI
3	Prinz M and Priller J: Microglia and brain macrophages in the molecular age: From origin to neuropsychiatric disease. Nat Rev Neurosci. 15:300–312. 2014. View Article : Google Scholar : PubMed/NCBI
4	Liu B and Hong JS: Role of microglia in inflammation-mediated neurodegenerative diseases: Mechanisms and strategies for therapeutic intervention. J Pharmacol Exp Ther. 304:1–7. 2003. View Article : Google Scholar : PubMed/NCBI
5	Sanchez Guajardo V, Tentillier N and Romero Ramos M: The relation between α-synuclein and microglia in Parkinson's disease: Recent developments. Neuroscience. 302:47–58. 2015. View Article : Google Scholar : PubMed/NCBI
6	Keren Shaul H, Spinrad A, Weiner A, Matcovitch Natan O, Dvir Szternfeld R, Ulland TK, David E, Baruch K, Lara Astaiso D, Toth B, et al: A unique microglia type associated with restricting development of Alzheimer's disease. Cell. 169:1276–1290. 2017. View Article : Google Scholar : PubMed/NCBI
7	Kim DC, Lee DS, Ko W, Kim KW, Kim HJ, Yoon CS, Oh H and Kim YC: Heme oxygenase-1-inducing activity of 4-methoxydalbergione and 4′-hydroxy-4-methoxydalbergione from Dalbergia odorifera and their anti-inflammatory and cytoprotective effects in murine hippocampal and BV2 microglial cell line and primary rat microglial cells. Neurotox Res. 33:337–352. 2018. View Article : Google Scholar : PubMed/NCBI
8	Liddelow SA, Guttenplan KA, Clarke LE, Bennett FC, Bohlen CJ, Schirmer L, Bennett ML, Münch AE, Chung WS, Peterson TC, et al: Neurotoxic reactive astrocytes are induced by activated microglia. Nature. 541:481–487. 2017. View Article : Google Scholar : PubMed/NCBI
9	Dong Y and Benveniste EN: Immune function of astrocytes. Glia. 36:180–190. 2001. View Article : Google Scholar : PubMed/NCBI
10	Wang X, Yang L, Yang L, Xing F, Yang H, Qin L, Lan Y, Wu H, Zhang B, Shi H, et al: Gypenoside IX suppresses p38 MAPK/Akt/NFκB signaling pathway activation and inflammatory responses in astrocytes stimulated by proinflammatory mediators. Inflammation. 40:2137–2150. 2017. View Article : Google Scholar : PubMed/NCBI
11	Zhang J, Benveniste H, Klitzman B and Piantadosi CA: Nitric oxide synthase inhibition and extracellular glutamate concentration after cerebral ischemia/reperfusion. Stroke. 26:298–304. 1995. View Article : Google Scholar : PubMed/NCBI
12	Law A, Gauthier S and Quirion R: Say NO to Alzheimer's disease: The putative links between nitric oxide and dementia of the Alzheimer's type. Brain Res Brain Res Rev. 35:73–96. 2001. View Article : Google Scholar : PubMed/NCBI
13	Block ML, Zecca L and Hong JS: Microglia-mediated neurotoxicity: Uncovering the molecular mechanisms. Nat Rev Neurosci. 8:57–69. 2007. View Article : Google Scholar : PubMed/NCBI
14	Jung WK, Lee DY, Park C, Choi YH, Choi I, Park SG, Seo SK, Lee SW, Yea SS, Ahn SC, et al: Cilostazol is anti-inflammatory in BV2 microglial cells by inactivating nuclear factor-kappaB and inhibiting mitogen-activated protein kinases. Br J Pharmacol. 159:1274–1285. 2010. View Article : Google Scholar : PubMed/NCBI
15	Wilms H, Sievers J, Rickert U, Rostami-Yazdi M, Mrowietz U and Lucius R: Dimethylfumarate inhibits microglial and astrocytic inflammation by suppressing the synthesis of nitric oxide, IL-1beta, TNF-alpha and IL-6 in an in-vitro model of brain inflammation. J Neuroinflammation. 7:302010. View Article : Google Scholar : PubMed/NCBI
16	Liu D, Wang Z, Liu S, Wang F, Zhao S and Hao A: Anti-inflammatory effects of fluoxetine in lipopolysaccharide (LPS)-stimulated microglial cells. Neuropharmacology. 61:592–599. 2011. View Article : Google Scholar : PubMed/NCBI
17	Boche D, Perry VH and Nicoll JA: Review: Activation patterns of microglia and their identification in the human brain. Neuropathol Appl Neurobiol. 39:3–18. 2013. View Article : Google Scholar : PubMed/NCBI
18	Recio MC, Andujar I and Rios JL: Anti-inflammatory agents from plants: Progress and potential. Curr Med Chem. 19:2088–2103. 2012. View Article : Google Scholar : PubMed/NCBI
19	Piotrowska H, Kucinska M and Murias M: Biological activity of piceatannol: Leaving the shadow of resveratrol. Mutat Res. 750:60–82. 2012. View Article : Google Scholar : PubMed/NCBI
20	Lee H, Kim YO, Kim H, Kim SY, Noh HS, Kang SS, Cho GJ, Choi WS and Suk K: Flavonoid wogonin from medicinal herb is neuroprotective by inhibiting inflammatory activation of microglia. FASEB J. 17:1943–1944. 2003. View Article : Google Scholar : PubMed/NCBI
21	Li FQ, Wang T, Pei Z, Liu B and Hong JS: Inhibition of microglial activation by the herbal flavonoid baicalein attenuates inflammation-mediated degeneration of dopaminergic neurons. J Neural Transm (Vienna). 112:331–347. 2005. View Article : Google Scholar : PubMed/NCBI
22	Suk K, Lee H, Kang SS, Cho GJ and Choi WS: Flavonoid baicalein attenuates activation-induced cell death of brain microglia. J Pharmacol Exp Ther. 305:638–645. 2003. View Article : Google Scholar : PubMed/NCBI
23	Park JS, Park EM, Kim DH, Jung K, Jung JS, Lee EJ, Hyun JW, Kang JL and Kim HS: Anti-inflammatory mechanism of ginseng saponins in activated microglia. J Neuroimmunol. 209:40–49. 2009. View Article : Google Scholar : PubMed/NCBI
24	He LF, Chen HJ, Qian LH, Chen GY and Buzby JS: Curcumin protects pre-oligodendrocytes from activated microglia in vitro and in vivo. Brain Res. 1339:60–69. 2010. View Article : Google Scholar : PubMed/NCBI
25	Li R, Huang YG, Fang D and Le WD: (−)-Epigallocatechin gallate inhibits lipopolysaccharide-induced microglial activation and protects against inflammation-mediated dopaminergic neuronal injury. J Neurosci Res. 78:723–731. 2004. View Article : Google Scholar : PubMed/NCBI
26	Choi DK, Koppula S and Suk K: Inhibitors of microglial neurotoxicity: Focus on natural products. Molecules. 16:1021–1043. 2011. View Article : Google Scholar : PubMed/NCBI
27	Shen H, Wang H, Wang L, Wang L, Zhu M, Ming Y, Zhao S, Fan J and Lai EY: Ethanol extract of root of Prunus persica inhibited the growth of liver cancer cell HepG2 by inducing cell cycle arrest and migration suppression. Evid Based Complement Alternat Med. 2017:82319362017. View Article : Google Scholar : PubMed/NCBI
28	Rho JR, Jun CS, Ha Y, Yoo MJ, Cui MX, Baek HS, Lim JA, Lee YH and Chai KY: Isolation and characterization of a new alkaloid from the seed of Prunus persica L. and its anti-inflammatory activity. Bull Korean Chem Soc. 28:1289–1293. 2007. View Article : Google Scholar
29	Lee JY and An BJ: Anti-oxidant and anti-inflammation activities of prunus persica flos. J Appl Biol Chem. 53:162–169. 2010. View Article : Google Scholar
30	Kwak CS, Yang J, Shin CY and Chung JH: Topical or oral treatment of peach flower extract attenuates UV-induced epidermal thickening, matrix metalloproteinase-13 expression and pro-inflammatory cytokine production in hairless mice skin. Nutr Res Pract. 12:29–40. 2018. View Article : Google Scholar : PubMed/NCBI
31	Shin TY, Park SB, Yoo JS, Kim IK, Lee HS, Kwon TK, Kim MK, Kim JC and Kim SH: Anti-allergic inflammatory activity of the fruit of prunus persica: Role of calcium and NF-kappaB. Food Chem Toxicol. 48:2797–2802. 2010. View Article : Google Scholar : PubMed/NCBI
32	Benmehdi H, Fellah K, Amrouche A, Memmou F, Malainine H, Dalile H and Siata W: Phytochemical study, antioxidant activity and kinetic behaviour of flavonoids fractions isolated from prunus persica L. Leaves. Asian J Chem. 29:132017. View Article : Google Scholar
33	Deb L, Gupta R, Dutta A, Yadav A, Bhowmik D and Kumar KS: Evaluation of antioxidant activity of aqueous fraction of Prunus persica L. aqueous extract. Der Pharmacia Sinica. 1:157–164. 2010.
34	Prakash V, Rana S and Sagar A: Studies on analysis of antibacterial and antioxidant activity of Prunus persica (L.) Batsch. Int J Sci Nat. 8:54–58. 2017.
35	Zhao X, Zhang W, Yin X, Su M, Sun C, Li X and Chen K: Phenolic composition and antioxidant properties of different peach [Prunus persica (L.) Batsch] cultivars in China. Int J Mol Sci. 16:5762–5778. 2015. View Article : Google Scholar : PubMed/NCBI
36	McCarthy KD and de Vellis J: Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol. 85:890–902. 1980. View Article : Google Scholar : PubMed/NCBI
37	NIH, . Laboratory animal welfare. Special Edition of the NIH Guide for Grants and Contracts. NIH; Bethesda, MD, USA: pp. 85–23. 1985
38	Wrobel K, Claudio E, Segade F, Ramos S and Lazo PS: Measurement of cytotoxicity by propidium iodide staining of target cell DNA: Application to the quantification of murine TNF-alpha. J Immunol Methods. 189:243–249. 1996. View Article : Google Scholar : PubMed/NCBI
39	Baldwin AS Jr: The NF-kappaB and I kappaB proteins: New discoveries and insights. Annu Rev Immunol. 14:649–683. 1996. View Article : Google Scholar : PubMed/NCBI
40	Mankan AK, Lawless MW, Gray SG, Kelleher D and McManus R: NF- kappaB regulation: The nuclear response. J Cell Mol Med. 13:631–643. 2009. View Article : Google Scholar : PubMed/NCBI
41	Oh YT, Lee JY, Lee J, Kim H, Yoon KS, Choe W and Kang I: Oleic acid reduces lipopolysaccharide-induced expression of iNOS and COX-2 in BV2 murine microglial cells: Possible involvement of reactive oxygen species, p38 MAPK, and IKK/NF-kappaB signaling pathways. Neurosci Lett. 464:93–97. 2009. View Article : Google Scholar : PubMed/NCBI
42	Mander P and Brown GC: Nitric oxide, hypoxia and brain inflammation. Biochem Soc Trans. 32:1068–1069. 2004. View Article : Google Scholar : PubMed/NCBI
43	Pautz A, Art J, Hahn S, Nowag S, Voss C and Kleinert H: Regulation of the expression of inducible nitric oxide synthase. Nitric Oxide. 23:75–93. 2010. View Article : Google Scholar : PubMed/NCBI
44	Bishop Bailey D, Calatayud S, Warner TD, Hla T and Mitchell JA: Prostaglandins and the regulation of tumor growth. J Environ Pathol Toxicol Oncol. 21:93–101. 2002. View Article : Google Scholar : PubMed/NCBI
45	Singh AK and Jiang Y: How does peripheral lipopolysaccharide induce gene expression in the brain of rats? Toxicology. 201:197–207. 2004. View Article : Google Scholar : PubMed/NCBI
46	Banks WA and Robinson SM: Minimal penetration of lipopolysaccharide across the murine blood-brain barrier. Brain Behav Immun. 24:102–109. 2010. View Article : Google Scholar : PubMed/NCBI
47	Banks WA, Gray AM, Erickson MA, Salameh TS, Damodarasamy M, Sheibani N, Meabon JS, Wing EE, Morofuji Y, Cook DG and Reed MJ: Lipopolysaccharide-induced blood-brain barrier disruption: Roles of cyclooxygenase, oxidative stress, neuroinflammation, and elements of the neurovascular unit. J Neuroinflammation. 12:2232015. View Article : Google Scholar : PubMed/NCBI
48	Tarassishin L, Suh HS and Lee SC: LPS and IL-1 differentially activate mouse and human astrocytes: Role of CD14. Glia. 62:999–1013. 2014. View Article : Google Scholar : PubMed/NCBI
49	Panicker N, Saminathan H, Jin H, Neal M, Harischandra DS, Gordon R, Kanthasamy K, Lawana V, Sarkar S, Luo J, et al: Fyn kinase regulates microglial neuroinflammatory responses in cell culture and animal models of Parkinson's disease. J Neurosci. 35:10058–10077. 2015. View Article : Google Scholar : PubMed/NCBI
50	Kim YJ, Hwang SY and Han IO: Insoluble matrix components of glioma cells suppress LPS-mediated iNOS/NO induction in microglia. Biochem Biophys Res Commun. 347:731–738. 2006. View Article : Google Scholar : PubMed/NCBI
51	Bhatt D and Ghosh S: Regulation of the NF-κB-mediated transcription of inflammatory genes. Front Immunol. 5:712014. View Article : Google Scholar : PubMed/NCBI
52	Lawrence T: The nuclear factor NF-kappaB pathway in inflammation. Cold Spring Harb Perspect Biol. 1:a0016512009. View Article : Google Scholar : PubMed/NCBI
53	Lu YC, Yeh WC and Ohashi PS: LPS/TLR4 signal transduction pathway. Cytokine. 42:145–151. 2008. View Article : Google Scholar : PubMed/NCBI
54	Korcheva V, Wong J, Corless C, Iordanov M and Magun B: Administration of ricin induces a severe inflammatory response via nonredundant stimulation of ERK, JNK, and P38 MAPK and provides a mouse model of hemolytic uremic syndrome. Am J Pathol. 166:323–339. 2005. View Article : Google Scholar : PubMed/NCBI
55	Da Silva J, Pierrat B, Mary JL and Lesslauer W: Blockade of p38 mitogen-activated protein kinase pathway inhibits inducible nitric-oxide synthase expression in mouse astrocytes. J Biol Chem. 272:28373–28380. 1997. View Article : Google Scholar : PubMed/NCBI
56	Xia Q, Hu Q, Wang H, Yang H, Gao F, Ren H, Chen D, Fu C, Zheng L, Zhen X, et al: Induction of COX-2-PGE2 synthesis by activation of the MAPK/ERK pathway contributes to neuronal death triggered by TDP-43-depleted microglia. Cell Death Dis. 6:e17022015. View Article : Google Scholar : PubMed/NCBI
57	Bhat NR, Zhang P, Lee JC and Hogan EL: Extracellular signal-regulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-α gene expression in endotoxin-stimulated primary glial cultures. J Neurosci. 18:1633–1641. 1998. View Article : Google Scholar : PubMed/NCBI
58	Abidi W, Jiménez S, Moreno MÁ and Gogorcena Y: Evaluation of antioxidant compounds and total sugar content in a nectarine [Prunus persica (L.) Batsch] progeny. Int J Mol Sci. 12:6919–6935. 2011. View Article : Google Scholar : PubMed/NCBI
59	Gasparotto J, Somensi N, Bortolin RC, Moresco KS, Girardi CS, Klafke K, Rabelo TK, Morrone Mda S, Vizzotto M and Raseira Mdo C: Effects of different products of peach (Prunus persica L. Batsch) from a variety developed in southern Brazil on oxidative stress and inflammatory parameters in vitro and ex vivo. J Clin Biochem Nutr. 55:110–119. 2014. View Article : Google Scholar : PubMed/NCBI
60	Lee JY and An BJ: Antioxidant and anti-inflammatory effects of fractions from Pruni persicae Flos. Korea J Herbol. 27:55–63. 2012. View Article : Google Scholar
61	Mei X, Zhou L, Zhang T, Lu B, Sheng Y and Ji L: Chlorogenic acid attenuates diabetic retinopathy by reducing VEGF expression and inhibiting VEGF-mediated retinal neoangiogenesis. Vascul Pharmacol. 101:29–37. 2018. View Article : Google Scholar : PubMed/NCBI
62	Kim M, Choi SY, Lee P and Hur J: Neochlorogenic acid inhibits lipopolysaccharide-induced activation and pro-inflammatory responses in BV2 microglial cells. Neurochem Res. 40:1792–1798. 2015. View Article : Google Scholar : PubMed/NCBI
63	Li N, Wang Y, Li X, Zhang H, Zhou D, Wang W, Li W, Zhang X, Li X, Hou Y and Meng D: Bioactive phenols as potential neuroinflammation inhibitors from the leaves of Xanthoceras sorbifolia Bunge. Bioorg Med Chem Lett. 26:5018–5023. 2016. View Article : Google Scholar : PubMed/NCBI
64	Kim CY, Lee C, Park GH and Jang JH: Neuroprotective effect of epigallocatechin-3-gallate against β-amyloid-induced oxidative and nitrosative cell death via augmentation of antioxidant defense capacity. Arch Pharm Res. 32:869–881. 2009. View Article : Google Scholar : PubMed/NCBI