Potential Implications of Hyperoside on Oxidative Stress-Induced Human Diseases: A Comprehensive Review

Figures & data

Figure 1 The outline of review.

Table 1 Original Plants and Parts

Num	Plants	Parts	Reference
1	Cuscuta chinensis var. chinensis	Seeds	[30,31]
2	Fagopyrum tataricum (L.) Gaertn. (Common Buckwheat)	Hull	[32]
3	Dioscorea esculenta (Lour.) Burkill (Sweet Potato)	Storage root	[33]
4	Hypericum hircinum subsp. majus (Aiton) N.Robson	Plants	[34]
5	Crataegus pinnatifida Bunge (Hawthorn)	Fruit Leaf	[35,36]
6	Carpobrotus edulis (L.) N.E.Br.	Fruit	[37]
7	Crataegus azarolus L.	Leaf	[38]
8	Hypericum reflexum L.f.	Blossom	[39]
9	Hypericum canariense L.
10	Hypericum grandifolium Choisy
11	Maytenus royleana Cufod.	Leaf	[40]
12	Eschweilera nana Miers	Leaf	[41]
13	Rosa rugosa Thunb. (Family Rosaceae)	Flower	[42]
14	Flaveria bidentis (L.) Kuntze	Leaf	[43]
15	Eleutherococcus senticosus Maxim.	Root	[44]
16	Apocynum venetum L.	Leaf	[44]
17	Polygonum aviculare L.	Aerial part	[45]
18	Hypericum ascyron L.	Aerial part	[46]
19	Euphorbia characias subsp. wulfenii (Hoppe ex W.D.J.Koch) Radcl.-Sm.	Aerial part	[47]
20	Hypericum perforatum L. (St. John’swort)	Seed Aerial part	[48,49]
21	Hypericum annulatum Moris	Seed	[48]
22	Chrysanthemum morifolium Ramat.	Flower	[50]
23	Arbutus unedo L.	Leaf	[51]

Figure 2 Structure and structure–activity of hyperoside. Chemical structural formula of hyperoside (a), Spatial structure diagram of hyperoside (b).

Table 2 Pharmacologic Effects

Num	Classification	Materials	Dose	Mechanism	Reference
1	Anti-oxidant	Saccharomyces Cerevisiae	5, 20 mg/L	Decreased LPO and the level of ROS	[60]
2		Human Spermatozoa	-	Decreased the level of LPO	[61]
3		PC12 cell	100 μg/mL	Inhibition the shrinking and apoptosis induced by H2O2 and TBHP	[62]
			160 μg/mL
4		ECV304 cells	128 μM	Increased SIRT1, inhibition the translocation of Bax	[63]
5		B16 melanoma cells	18.2 μM	Inhibition the expression of tyrosinase and oxidative stress-induced melanogenesis	[64]
6		B16 cells	5, 10, 50 μM	Against RS, ^• O2, NO ^•, ONOO ^−, enhance the GSH/GSSG ratio, inhibited oxidative stress-induced melanogenesis	[65]
7		MT3C3-E1 cells	5, 10, 50 μmol/L	Decreased the expression of p-JNK and p-p38, regulated the MAPK-mediated responses	[66]
8		SH-SY5Y Cells	0.25, 0.5, 1, 2 μM	Upregulation of Nrf2 and HO-1, activation of Nrf2/HO-1 signaling	[67]
9		L02 cell	10, 50, 100, 200, 500, 800 μM	Upregulation of HO-1 via the regulation of MAPK-dependent Keap1–Nrf2–ARE signaling pathway	[68]
10		Female Wistar rats	-	Increased transcription of CAT and GSH	[69]
11		V79-4 cells	5 μM	Downregulation of ROS, induction of catalase and glutathione peroxidase activities	[70]
12	Cardiovascular protective effect	H9C2 cells	1, 10, 50, 100 μM	Upregulated miR-138, inhibited the expression of MLK3 and Lnc2 to inhibit apoptosis	[71]
		Male C57BL/6 mice	10, 50, 100, 200 mg/kg
13		RAW 264.7 cells	10, 30, 100 μM	Inhibited the iNOS protein expression	[72]
14		HUVECs	10, 20, 50 μM	Reduced IL-1β, IL-8, TF, ICAM1, VCAM1, activated autophagy and suppressed mTOR/S6K and TLR/Myd88/NF-κB signaling	[73]
15		HUVECs	5, 10, 25 μM	Increased Bcl-2, decreased Bax, induced phosphorylation of ERK1/2	[74]
16		HUVECs, mice	5, 10, 20, 50 μM	Blocked HG-induced vascular inflammation via inhibition of NF-κB	[75]
17		HUVECs, mice	5, 10, 20, 50 μM	Inhibition of the HMGB1 signaling pathway	[76]
18		VSMCs, male C57BL/6N mice	5 μM in vitro 40 mg/kg in vivo	Upregulation of Nur77, inhibited both cell proliferation of VSMCs in vitro and carotid artery ligation-induced neointimal formation in vivo	[28]
19		VSMCs	10, 25, 50, 100 μg/mL	Inhibited oxLDL-induced LOX1 expression, ERK activation and cell proliferation via the regulation of oxLDL-LOX1-ERK pathway	[77]
20		Male SD rats	1–100 μM	Endothelium-dependent and endothelium-independent mechanisms	[78]
21		Male adult SD rats	50 μM	Activation of ERK-dependent signal pathway	[79]
22		Male KM mice	9, 18, 36 mg/kg	Upregulated autophagy, suppressed NLRP1 inflammation pathway	[80]
23		NRCMs, Male C57/BL6 mice	1, 5, 10 μM	Inhibition of the AKT signal pathway	[81]
24		H9C2 cells, Adult male Wistar rats	10 μM 100, 200 mg/kg	Attenuating myocardial apoptosis and inducing autophagy	[82]
25	Anti-inflammation	HT22 cells	20 μM	Alleviates the level of IL-1β, IL-6, IL-8, TNF-α, ROS, MDA, Bax, and caspase-3; increases the expression of CAT, SOD, GSH, Bcl-2, BDNF, TrkB, and NGF. Alleviated LPS-induced inflammation, oxidative stress, and apoptosis by upregulating SIRT1 to activate Wnt/β-catenin and sonic hedgehog pathways.	[83]
26		Rat peritoneal macrophages	100 μM	Inhibited NO production via inhibition of expression of iNOS by attenuation of p44/p42 MAPK, p38 MAPK and JNK	[84]
27		Chondrocytes, Male C57BL/6 mice	10, 20, 40 μM; 20 mg/kg	Suppression of PI3K/AKT/NF-κB and MAPK pathways Enhanced Nrf2/HO-1	[85]
28		HK-2 cells	10, 50, 100 μM	Activation of miR-499a-5p/NRIP1 signal pathway	[86]
29		Male SD rats, BMSCs	40 μg/mL	Activation of NF-κB pathway to proliferation and osteogenic differentiation	[87]
30		Mouse peritoneal macrophages	5 μM	Inhibition of TNF-α, IL-6, NO production, NF-κB activation	[25]
31	Antidepressant effect	C6 glioblastoma cells	1 μM	Reduced β2-adrenergic sensitivity	[88]
32		C6 glioblastoma cells	1 μM	Reduction in β2-AR density in plasma membrane and decrease in corresponding downstream signaling	[89]
33		PC12 cells	2.5, 5, 10 μg/mL	Decreased Ca^2+, upregulation of CREB and BNDF through the cAMP-CREB signal pathway	[90]
34		Male Albino Swiss mice	0.94 mg/kg, 3.75 mg/kg	Mediated by monoaminergic system and the upregulation of BDNF level	[91]
35		Adult male CF1 mice, Male Wistar rats	10, 20, 40 mg/kg(i.p.) or 20 and 40 mg/kg(P.O.) in mice, 1.8 mg/kg/day (P.O.) in rats	D2-like receptor activation	[26]
36		Male ICR mice	10, 20, 30 mg/kg	Be related to the serotoninergic system including 5-HT2A, 5-HT2 receptor	[92]
37		Adult male SD rats	5, 10, 15 mg/kg	Regulation on hypothalamus- pituitary- adrenal (HPA) axis activity	[93]
38		ICR mice	-	Promoted the level of NE and 5-HT in brain and decreased the activity of MAO	[94]
39	Neuroprotective effect	Primary cortical neuron	2.5, 5, 10, 20 μM	Inhibited PI3K/Akt/Bad/Bclxl-regulated mitochondrial apoptotic pathway	[95]
40		Primary cortical neuron	10 μM	Inhibited the activation of NF-κB, lessened the expression of iNOS, ameliorated ERK, JNK and Bcl-2 family-related apoptotic signaling pathway	[29]
41		PC12 cells	10, 50, 100 μM	Inhibited ROS, the activation of caspase-3 and PARP to inhibit apoptosis	[96]
42		ICR mice	2.5 mg/kg	Inhibited AchE activity	[97]
43		SD rats	25, 50, 100 mg/kg	Upregulated the level of H2S, decreased the synthesis and release of NO	[98]
44		C57BL /6J mice (CSE^+/+, CSE^−/−)	25, 50, 100 mg/kg	Upregulation of cystathionine γ-lyase (CES)-H2S signal pathway	[99]
45		SD rats	1, 10, 100 μM	Upregulation of H2S, activation of KCa and opening KCa channels, blocked Ca^2+ influx	[100]
46		Male SD rats	10, 20, 40 mg/kg	Promote the anti-oxidant activity of SOD and CAT to alleviate oxidative stress injury	[101]
47	Anti-breast cancer	4T1 cells, MCF-7 cells, Balb/c mice	25, 50, 100 μM in vitro 50 mg/kg in vivo	Inhibition of NF-κB signal pathway, activation of Bax-caspase 3 axis to promote ROS induced apoptosis	[102]
48		MDA-MB-231 cells	5, 10, 50, 100 μg/mL	Blocking TLR4-mediated pro-survival and inflammatory cytokine expression to promote the sensitivity of breast cancer cells to paclitaxel	[103]
49	Anti-lung cancer	A549 cells, Balb/c-nude mice	15, 20, 25 μM in vitro 15, 20, 25 mg/kg in vivo	Activation of caspase-3 to motivate apoptosis and inactivation of NF-κB to inhibit inflammatory	[104]
50		A549 cells	10, 50, 100 μM	Upregulation of AMPK signal pathway and HO-1 expression to suppressed the survival and proliferation of A549 cells	[105]
51		A549 cells	10, 50, 100 μM	Upregulated apoptosis via activation of the p38 MAPK- and JNK-induced mitochondrial death pathway	[106]
52		A549 cells, H466 cells, C57BL/6J mice	–	Upregulated the expression of p38 MAPK, caspase 3, caspase 9, cleaved caspase 3, cleaved caspase 9 and Bax, downregulated the expression of Cu/Zn SOD, CAT, Nrf2, NQO1, HO-1 and Bcl-2	[107]
53		A549 cells	10, 20, 50, 100, 200, 400 μg/mL	Inhibited the process of G1/S phase to inhibit proliferation	[108]
54		NCI-H1975 cells, PC-9 cells, Nude male mice	30, 60, 90, 120, 150 μM in vitro, 25 mg/kg in vivo	Upregulation of FoxO1 via CCAT1 to inhibit proliferation and induce apoptosis	[109]
55		A549 cells	0.5, 1, 2 mM	Induced autophagy through inhibiting the Akt/mTOR/p70S6K signal pathway, induced apoptosis	[110]
56		H1975 cells, A549 cells, male Balb/c nude mice	20, 40, 60, 80, 100 μg/mL	Inhibited NF-κB transcriptional activity, caspase-9/caspase 3 activation, cell cycle arrest and suppression of cell proliferation	[111]
57		A549 cells	1, 2, 5 μM	Upregulation of Akt/PI3K and p38 MAPK signal pathway, downregulation of nm23-H1, MTA1, TIMP-2 and MMP-2	[112]
58	Anti-pancreatic cancer	PANC-1 cells, BxPC-3 cells, Female nude Balb/c mice	100, 300, 500 μM in vitro 20 mg/kg in vivo	Promote Bax/Bcl-2 and Bax/Bcl-xL ratios and inhibit NF-κB activation, promoted of apoptosis and suppressed of proliferation	[113]
59	Anti-osteocarcinoma	ARP cells, H929 cells MC3T3-E1 cells, Raw264.7 cells	0.05, 5 μM	Promoted osteoblastogenesis and suppressed osteoclastogenesis, thus improving the bone marrow microenvironment to inhibit MM cell proliferation	[114]
60		U2OS cells, MG63 cells	150 μg/mL	Activation of TGF-β signal pathway to induce G0/G1 arrest to inhibit cell proliferation	[115]
61	Anti-uterine cancer	Hela cells, C33-A cells	0.25, 0.5, 1, 2, 4, 8 μM	Downregulation of C-MYC gene expression	[116]
62		RL952 cells	10, 20, 100 μM	Induced apoptosis through mitochondria-dependent and death receptor-dependent apoptotic pathways	[117]
63		SKOV-3 cells, HO-8901 cells	50, 100 μM	Overexpression of PGRMC1 enhanced the autophagy and apoptosis induced by hyperoside	[118]
64	Anti-liver cancer	HepG2 cells	10, 20, 50 nM	Upregulation of p53/caspase signal pathway to induce apoptosis and inhibit proliferation	[119]
65		HepG2 cells	5, 10, 20, 40, 80 μM	Inhibiting the BMP-7 dependent-PI3K/AKT pathway to suppress cell proliferation	[120]
66		CBRH-7919 cells, Balb/c nude mice	1, 1.25, 5, 20, 60 μg/mL in vitro, 6 mg/kg in vivo	Upregulation of caspase 3 and caspase 9 induced apoptosis to inhibit liver cancer in vitro and vivo	[59]
67	Anti-skin cancer	A431 cells, A432 cells, HS-4 cells, female mice	1, 5, 10, 25, 50, 100 μM in vitro, 8.16 μM in vivo	Inhibition of PI3K/Akt/mTOR/p38MAPK signal pathway and activation of AMPK to inhibit cell proliferation and induced apoptosis and autophagy	[121]
68	Anti-prostate cancer	PC3 cells	-	Reduced the expression of miR-21 to inhibit cell growth and metastasis	[122]
70	Anti-renal cancer	786-O cells	-	Downregulation of ROS to induce caspase-3 cleavage and PARP cleavage, decreased miR-27A and induced ZBTB10 and downregulated Sp1, Sp3 and Sp4	[123]
71	Anti-colon cancer	SW620 human colorectal cancer cells	12.5, 25, 50 μM	Upregulation of p21, p53 to induce G2/M phase arrest and apoptosis	[124]
72		HT-29 human colon cancer cells	100, 200 μM	Activation of mitochondria-dependent apoptotic pathway	[125]
73	Anti-thyroid cancer	SW579 cells	5, 10, 20 μg/mL	Upregulated the expression of Fas and FasL mRNAs, downregulated the expression of the survivin protein	[126]
74	Antiviral effect	HepG2.2.15 cells, Peking ducklings	0.2, 0.1, 0.05, 0.025, 0.0125 g/L in vitro 0.02, 0.05, 0.1 g/kg/d in vivo	Hyperoside showed an anti-HBV effect both in vitro and in vivo	[127]
75		HepG2.2.15 cells	50 μg/mL	Hyperoside showed an anti-HBV effect both in vitro	[128]
76		Huh-7 cells	-	Hyperoside from Nymphaea alba extracts showed anti-HCV effect	[129]
77	Hepatoprotective effect	L02 cells, C57BL/6 mice	5, 10, 20 μM in vitro 25, 50, 100 mg/kg in vivo	Activated Nrf2 to downregulate LDH and ALT	[130]
78		Male Balb/c mice, L02 cells	50, 100 mg/kg in vivo 50, 100, 200 μM in vitro	Activated ERK1/2-Crm1 pathway to promote the nuclear export of Bach 1 to upregulate Nrf2 binding to ARE	[131]
79		Male ICR mice	100 mg/kg	Upregulation of HO-1 and Nrf2, downregulation of iNOS, COX2, TNF-α	[132]
80		Female Wistar rats	-	Increased transcription of CAT and GSH to show an antioxidant effect	[69]
81		L02 cells, Male SD rats	100 μM in vitro 15, 30, 60 mg/kg in vivo	Reduced PHLPP2 expression, activated AKT phosphorylation, induced GSK-3β phosphorylation, increased Nrf2 translocation, promoted HO-1 expression	[133]
82		C57BL/6 mice, Nr4A1 knockout mice	50 mg/kg	Upregulation of Nr4A1 expression to macrophage polarization and HFD-induced NAFLD progression	[134]
83		Male Wistar rats	100, 200 mg/kg	Inhibiting the activation of TGF-β1/Smad pathway	[135]
84	Allergic reactions	HMC-1 cells	100, 160 μg/mL	Inhibited the level of TSLP by downregulation of intracellular calcium/RIP2/caspase 1/NF-κB signal	[136]
85		RBL-2H3 cells	0.35 μM	Hyperoside could covalently modify with Bovine β-Lactoglobulin	[137]
86	Anticoagulant activity	HUVECs ICR mice	0.5, 1, 2, 5, 10, 20, 50 μM in vitro, 2.3 mg/kg in vivo	Prolonged APTT and PT and inhibited the activities of thrombin and FXa, inhibited production of thrombin and FXa, inhibited TNF-α induced production of PAI-1	[138]
87	Herb-drug inhibitory effect	Human liver microsomes	0.5, 1, 2, 5 μM	Selectively inhibited CYP2D6	[139]
88	Treat chronic kidney disease	SD rats	-	Reduction in CaOx formation	[140]
89		SD rats Male SDT rats	2.5, 5, 10 μg/mL	Inhibited the interaction between PDGF-BB and PDGFR-β	[141]
90		SD male rats NRK-52E cells	20 mg/kg/d in vivo 5, 10, 15 μg/mL	Inhibited AMPK-ULK1 signaling-mediated autophagy to attenuate renal aging and injury	[142]

Abbreviations: AchE, anti-acetyl-cholinesterase; Akt, Akt kinase; AMPK, adenosine monophosphate-activated protein kinase; APTT, activated partial thromboplastin time; ARE, antioxidant response element; BDNF, brain-derived neurotrophic factor; BMP-7, bone morphogenetic protein-7; CAT, catalase; CREB, cAMP response element binding protein; COX2, cyclooxygenase 2; ERK, extra cellular signal-regulated protein kinase; FoxO1, fork head box protein O1; GSH, reduced glutathione; GSK-3β, glycogen synthase kinase 3β; GSSG, Glutathione Oxidized; HBV, hepatitis B virus; HCV, hepatitis C virus; HFD, high-fat diet; HO-1, heme oxygenase-1; ICAM1, intercellular cell adhesion molecule-1; iNOS, inducible nitric oxide synthase; JNK, c-Jun N-terminal kinase; Keap1, kelch-like ECH-associated protein 1; LDH, lactate dehydrogenase; LPO, lipid peroxidation; LPS, lipopolysaccharide; MAO, monoamine oxidase; MTA1, Metastasis Associated 1; MAPK, mitogen-activated proteinkinase; MDA, malondialdehyde; MMP-2, matrix metalloproteinase 2; mTOR, mammalian target of rapamycin; NAFLD, non-alcoholic fatty liver disease; NGF, nerve growth factor; Nrf2, nuclear erythroid 2-related factor 2; NF-κB, nuclear factor kappa-B; NO, nitric oxide; NO^•, nitric oxide radical; NQO1, NAD(P)H quinone dehydrogenase 1; Nr4A1, nuclear receptor subfamily 4 group A member 1; ^•O₂, superoxide radical; ONOO⁻, peroxynitrite anion; PAI-1, Plasminogen activator inhibitor 1; PARP, poly-ADP-ribose-polymerase; PHLPP2, PH domain leucine-rich repeat protein phosphatase 2; PI3K, phosphatidylinositol 3-kinase; p-JNK, phosphorylated c-Jun N-terminal kinase; PGRMC1, progesterone receptor membrane component 1; PT, prothrombin time; RIP2, receptor-interacting protein 2; RS, reactive species; ROS, reactive oxygen species; PDGF-BB, platelet-derived growth factor-BB; PDGFR-β, platelet-derived growth factor-B receptor; SD, Sprague-Dawley; SIRT1, silent mating type information regulation 2 homolog-1; SOD, superoxide dismutase; TBHP, tert-butyl hydroperoxide; TNF-α, tumor necrosis factor-α; TIMP-2, Tissue inhibitors metalloproteinases; TrkB, Tyrosine Kinase receptor B; TGF-β, transforming growth factor beta; TLR4, toll-like receptor-4; TSLP, thymic stromal lymphopoietin; ULK1, unc-51-like kinase 1; VCAM1, vascular cell adhesion molecule-1.

Figure 3 The possible molecular mechanisms of hyperoside in anti-oxidant effect, anti-inflammatory effect, cardiovascular protective effects, anti-depressant effect, neuroprotective effect and hepatoprotective effect.

Figure 4 The possible molecular mechanisms of hyperoside in anti-cancer (breast, lung, pancreatic, skin, thyroid, renal, colon, liver, prostate and uterine).

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