Activity of Selected Group of Monoterpenes in Alzheimer’s Disease Symptoms in Experimental Model Studies—A Non-Systematic Review
Abstract
:1. Introduction
2. Pathophysiology of Alzheimer’s Disease
2.1. β-Amyloid
2.2. Tau Protein
2.3. Oxidative Stress
2.4. Inflammation
2.5. Apolipoprotein E
2.6. The Cholinergic System
2.7. Glutamatergic System
3. Therapeutic Potential of Monoterpenes for Alzheimer’s Disease
3.1. Outline of Mechanisms Involved in the Anti-AD Action of Monoterpenes and Monoterpenoids
3.2. Monoterpenes and Monoterpenoids in the Treatment of AD—Possible Mechanisms of Action
3.3. Iridoids in the Treatment of AD
3.4. Secoiridoids in the Treatment of AD
4. Memory and Learning Improvement
4.1. In Vitro and In Silico Studies Results
4.2. In Vivo Studies Results
5. Anxiolytic Effects
6. Insomnia
Monoterpenes
7. Outline of Polyphenols and Essential Oils Rich in Monoterpenes and Polyphenols Revealing Neuroprotective Effect
7.1. In Vitro Studies Results
7.2. In Vivo Studies Results
8. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
Abbreviations
Aβ | amyloid β |
ABCA-1 | ATP-binding cassette transporter-A1 |
ACh | acetylcholine |
AChE | acetylcholinesterase |
AD | Alzheimer’s disease |
AICD | intracellular domain CTFβ |
AMPK | AMP-activated protein kinase |
ApoE | apolipoprotein E |
APP | amyloid β precursor protein |
BACE1 | β-secretase 1 |
BBB | blood-brain barrier |
BChE | butyrylcholinesterase |
BDNF | brain-derived neurotrophic factor |
ChAT | choline acetyltrasferase |
COX | cyclooxygenase |
ECE | endothelin converting enzymes |
ER | endoplasmic reticulum |
ERK | extracellular signal–regulated kinase |
CREB | cAMP-response element binding protein |
GAD | generalized anxiety disorder |
GAP-43 | growth associated protein 43 |
GFAP | glial fibrillary acidic protein |
GLP-1R | glucagon-like peptide-1 receptor |
GLT-1 | glutamine transporter-1 |
GLUT-1 | glucose transporter-1 |
GPx | glutathione peroxidase |
GSHPx | glutathione peroxidase |
GSH-ST | glutathione S-transferase |
HFO | hogh fat diet |
hptau | hyperphosphorylated tau protein |
IDE | insulin degrading enzyme |
IκB | nuclear factor of kappa light polypeptide gene enhancer in B-cells inhibitor |
IL-1 | interleukin-1 |
JNK | c-Jun N-terminal kinase |
LC3II | lysosomal cysteine protease 3II |
LRP-1 | lipoprotein receptor-related protein 1 |
mAChR | muscarinic acetylcholine receptors |
MAPK | mitogen-activated protein kinase |
mTOR | mammalian target of rapamycin |
nAChR | nicotinic acetylcholine receptors |
NEP | neprilysin |
NF-κB | nuclear factor kappa light chain enhancer of activated B cells |
NFTs | neurofibrillary tangles |
NGF | nerve growth factor |
NMDA | N-methyl-D-aspartic acid |
NOS | nitric oxide synthase |
PGE | prostaglandin |
PHF | paired helical filaments |
PKC | protein kinase C |
PS | presenilin |
PSD-95 | postsynaptic density protein 95 |
PTEN | phosphatase and tensin homolog |
RAGE | receptor for advanced glycation endproducts |
ROS | reactive oxygen species |
SERT | serotonin transporter |
SNAP-25 | synaptosomal nerve-associated protein-25 |
SOD | superoxide dismutase |
SWS | slow wave sleep |
TACE | α-secretase |
TNF | tumor necrozing factor |
TrkB | tropomyosin receptor kinase B |
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Monoterpene | In Vivo Model | Type of Test | Administration of Compound | Observations | Possible Mechanism of Action | References |
---|---|---|---|---|---|---|
thymol | Wistar Rats impaired with intrahippocampal injection of amyloid or intraperitoneal injection of scopolamine | Morris water maze task | intraperitoneally; 0.5, 1, or 2 mg/kg | Improvement cognitive functions; reversed negative effect of Aβ and scopolamine | Antioxidant and anti-inflammatory activity of thymol | [146] |
carvacrol | Wistar Rats impaired with intrahippocampal injection of amyloid or intraperineal injection of scopolamine | Morris water maze task | intraperitoneally; 0.5, 1, or 2 mg/kg | Improvement cognitive functions; reversed negative effect of Aβ and scopolamine | Antioxidant and anti-inflammatory activity of carvacrol | [146] |
Sprague-Dawley rats with memory impairment and neuroinflammation gained by lipopolysaccharide injected into the lateral ventricle | Object recognition task; Morris water maze test | Intraperitoneally; 25 mg/kg, 100 mg/kg | Memory improvement; significantly attenuation of induced defects in cognitive functions | Attenuation of expression of inflammatory factors in the brain (interleukin-1β, taumor necrosis factor-α, cyclooxygenase-2). Increasing expression of brain-derived neurotropic factor mRNA and decrease expression of Toll-like receptor 4 mRNA. | [147] | |
Male Wistar rats with memory impairment obtained by lead acetate drinking water | Morris water maze test | Orally; 25,50, and 100 mg/kg | Improvement of memory and learning | Decreasing lipid peroxidation and oxidation stress by improvement of activity of antioxidant enzymes (SOD, CAT, GPx) | [148] | |
linalool | C57BL/6J mice model anesthetized and stereotypically injected aggregated Aβ into hippocampus | Morris water maze test; passive avoidance test | intraperitoneally; 100 mg/kg | Cognitive improvement effect without negative influence on locomotor activity | Decreasing of apoptosis and oxidative stress induced by Aβ depending on Nrf2/HO-1 pathway | [104] |
Homozygous triple transgenic AD model (3xTg-AD) and nontransgenic (Non-Tg) mice | Morris water maze test | Orally, 25 mg/kg | reversion of cognitive and emotional deficits | antioxidant activity; decreasing of β-amyloid level | [102] | |
limonene | WKY and SHRsp rats with ischemia induced by occlusion of right middle cerebral artery—evaluation of influence of limonene on memory after stroke | Morris water maze test; novel object recognition test | Intraperitoneally; 20 mg/kg | protection against memory impairment | antioxidant effects through increasing SOD and CAT activities, decreasing MDA levels, increasing GSH levels and decreasing ROS levels. | [149] |
α-pinene | scopolamine-induced memory deficit in C57BL/6 mice | Morris water maze test; passive avoidance test | Intraperitoneally; 10 mg/kg | memory enhancing activity and learning improvement | regulation of expression of proteins related to synthesis of acetylcholine and antioxidant defense system | [150] |
α-terpinene | female Wistar rats | inhibitory avoidance task; | Orally; 0.5, 0.75 and 1.0 mL/kg | memory impairment | altering activity of enzymes responsible for neuronal plasticity and hydrolysis of ADP and ATP | [151] |
Essential Oils and Main Chemical Compounds | Method of Administration | Dosage | In Vivo Model | Anxiety Model | Observed Effect, Main Results | Reference |
---|---|---|---|---|---|---|
α-pinene, camphene, β-pinene, β-phellandrene (Abies sachalinensis) | i.p. Inhalation | 0.6 g/kg body weight 3.6 mg/l air | Mouse | Elevated plus-maze test (EPM) | i.p. administration did not produce an anxiolytic-like effect, albeit, a significant anxiolytic-like effect was observed after inhalation. The influence of the way of administration on the distribution of the main compounds was then analyzed. The anxiolytical effect is suspected to be due to the achievement of adequate levels in the brain after inhalation | [176] |
fragranol, fragranyl acetate, γ-terpinene, thymol, eugenol (Achillea umbellata) | p.o. | 50, 100 and 150 mg/kg | Mouse | Light/Dark transition test | The applied EO showed antianxiety properties (increased time spent in the light compartment and decreased time spent in the dark in a dose-dependent manner), but these are very likely signs of intoxication and not of possible beneficial effects of the plant volatiles. | [177] |
p-cymene, 1,8-cineole, terpinen-4-ol, limonene (Alpinia zerumbet) | Inhalation | 0.087 ppm, 0.87 ppm and 8.7 ppm for 90 min | Mouse | Elevated plus-maze test | 0.087 and 8.7 ppm of EO obviously showed anxiolytic-like activity. | [178] |
limonene, β-pinene, β-myrcene, sabinene (Citrus aurantium) | p.o. | 1, 5, 10, 50 mg/kg for 30 min or 14-day repeated (1, 5, 10 mg/kg/day) | Mouse | Light/Dark Box Test | The anxiolytic-like activity observed after acute (5 mg/kg) or 14-day repeated (1 mg/kg/day) dosing was mediated by the serotonergic system (5-HT1A receptors). The obtained results suggest that the EO does not function through the GABA-benzodiazepine receptor complex | [179] |
limonene, β-pinene, β-myrcene, sabinene (Citrus aurantium) | p.o. | 0.5 and 1.0 g/kg | Mouse | Elevated plus-maze test | EPM results suggest the anxiolytic effect of the EO. | [180] |
limonene, β-pinene, β-myrcene, sabinene (Citrus aurantium) | p.o. | Acutely pretreated at 1, 5, 10 or 50 mg/kg and 1, 5 or 10 mg/kg/day for 14 days | Mouse | Light/Dark Box test | The EO possesses a significant anxiolytic-like effect, and the present results strongly suggest the involvement of 5- HT1A-receptors. | [179] |
limonene, β-pinene, β-myrcene, sabinene (Citrus aurantiu) | Inhalation | 1.0%, 2.5% and 5.0% for 7 min | Rat | Open-field test behavioral Social interaction test Elevated plus-maze test | The concentration of 2.5% increased both the time of the animals spent in the open arms of the EPM and the time of social interactions for rats. This was longer than that of the diazepam group (1.5 mg/kg i.p) and testifies to an anxiolytic-like effect. Results suggest a possible central action of EO | [181] |
limonene, geranyl acetate and trans-limonene-oxide (Citrus limon) | p.o. | 50, 100 and 150 mg/kg/day for 30 days | Mouse | Elevated plus-maze test | Dosage of EO was able to significantly increase the time of permanence and the number of entrances in the open arms, indicating a positive response. The study suggests anxiolytic effects of the used EO that might involve an action on benzodiazepine-type receptors. | [182] |
limonene, geranyl acetate and trans-limonene-oxide (Citrus limon) | Inhalation | 150 µL once a day for 2 weeks | Rat | Elevated plus-maze test | Long-term EO exposure (both male and female rats) increased anxiety in the plus-maze test, i.e., it reduced the time spent in the open arms. The obtained results indicate an anxiogenic-like effect. | [183] |
limonene, myrcene (Citrus sinensis) | Inhalation | 100, 200, 400 μL for 5 min | Rat | Elevated plus-maze test Light/Dark Box Test | All the used doses of the EO showed anxiolytic effects. To exclude the possibility that this result was due to non-specific effects of odor exposure, the rats’ response to Melaleuca alternifolia EO was also assessed. | [184] |
sabinene, 1,8-cineole, limonene, myrcene (Lantana camara) | Inhalation | 0.0004 and 0.04 mg for 60 min | Mouse | Open-field test | The administered EO significantly decreased locomotor activity in a dose-dependent manner. The reduction of locomotor activity may indicate anxiolytic effects. | [185] |
linalol, linalyl acetate, terpinene-4-ol, ocimene, cineole (Lavandula angustifolia) | Inhalation | 0.5%, 2.5%, 5.0% for 15 min | Mouse | Marble-burying test | The result of the study suggests that the perception of smells is not crucial for inducing the anxiolytic-like effect in normal and anosmic mice. | [161] |
linalol, linalyl acetate, terpinene-4-ol, ocimene, cineole (Lavandula angustifolia) | Inhalation | 4 µL/L air for 90 min | Mouse | Elevated plus-maze test | A similar anxiolytic-like effect was noticed in stressed and non-stressed mice | [186] |
linalol, linalyl acetate, terpinene-4-ol, ocimene, cineole (Lavandula angustifolia) | Inhalation | 1–5% for 15 min | Mouse | Marble-burying test Elevated plus-maze test | The anxiolytic-like effect of lavender oil may be mediated by serotonergic transmission, and the participation of the GABAA/BDZ complex is unlikely. Administering the oil by inhalation induced rats to reduce the number of marbles buried. This occurred at a dose that did not affect locomotor activity. 5% lavender EO attenuated the serotonin syndrome induced by 40 mg/kg fluoxetine plus 80 mg/kg 5-hydroxytryptophan. | [187] |
linalol, linalyl acetate, terpinene-4-ol, ocimene, cineole (Lavandula angustifolia) | Inhalation | Vaporized oil for 90 min | Mouse | Elevated plus-maze test | Olfactory stimulation is not necessarily required for lavender EO to show an anxiolytic action. An increase in hippocampal serotonin turn-over after lavender inhalation was, however, noticed. This enhanced the proposal of a serotonergic mediation of the anxiolytic-like effects of EO. | [188] |
linalol, linalyl acetate, terpinene-4-ol, ocimene, cineole (Lavandula angustifolia) | Inhalation | 0.1–1.0 mL for 30 min or 1 h | Rat | Open-field test | An anxiolytic-like effect was established. Higher doses had some effects on behavior similar to those of 10 mg/kg body weight chlordiazepoxide (CDP). Doses 0.5 mL–1.0 mL increased immobility. A sedative effect can also occur at the upper doses. | [189] |
linalol, linalyl acetate, terpinene-4-ol, ocimene, cineole (Lavandula angustifolia) | Inhalation | Refreshed three times daily with four drops of the EO by 24 h and 14 days | Gerbil | Elevated plus-maze test | Lavender EO inhalations have an anxiolytic profile in gerbils that is similar to that of the anxiolytic diazepam (1 mg/kg). Sex differences in protected head-dip (an ethological indicator of anxiety) was indicated–females showed a significant decrease in response to this test. Two-week exposure to the scent of lavender increased exploratory behavior in female gerbils, indicating a further decrease in anxiety in this sex. | [190] |
linalol, linalyl acetate, terpinene-4-ol, ocimene, cineole (Lavandula angustifolia) | Inhalation | 1 mL of 10% EO | Sheep | Reaction to stress (isolation) | Genetic differences in temperament determined whether lavender oil alleviates or exacerbates the behavioral and/or endocrine correlates of anxiety in sheep. Exposure of calm sheep to lavender oil i.a. decreased the agitation score and the plasma concentrations of cortisol prior to isolation, compared to control, and thus they exhibited anxiolytic-like effects. The parameters of the above-mentioned tests carried out on nervous sheep were opposite, lavender oil showed an anxiogenic effect. | [191] |
linalol, linalyl acetate, terpinene-4-ol, ocimene, cineole (Lavandula angustifolia) | p.o. | 1–30 mg/kg/day for 3 days | Mouse | Elevated plus-maze test | Anxiolytic-like effect was verified because the test mice showed an increase in open arms exploration in the elevated plus-maze compared to positive control (diazepam and pregablin). The results of the experiment suggest non-selective inhibition of voltage operated calcium channels as a mechanism of anxiolytic effect. | [162] |
linalol, linalyl acetate, terpinene-4-ol, ocimene, cineole (Lavandula angustifolia) | p.o. | 6-week-intake 80 mg/day | Human (adults with GAD) | Hamilton Anxiety Rating Scale (HAMA) total score, Double-blind, double-dummy, randomized, reference-controlled multicentre trial | The results suggest that silexan effectively ameliorates generalized anxiety at a comparable degree to that of lorazepam (0.5 mg/day) administration. | [192] |
linalol, linalyl acetate, terpinene-4-ol, ocimene, cineole (Lavandula angustifolia) | p.o. | 10-weeks-intake 80 mg/day | Human | Hamilton Anxiety Scale (HAMA), Double-blind, randomized, placebo-controlled multicentre trial | An anxiolytic effect was established. Symptoms of anxiety were reduced more explicitly in patients taking Silexan than that of those in the placebo group. Additionally, there was an improvement in the patients’ mental condition. | [167] |
geranial, neral, d-limonene, β-myrcene, α-terpinyl acetate (Litsea cubeba) | p.o. | 100, 300 and 500 mg/kg/day for 7 days | Mouse | Elevated plus-maze test | An anxiolytic effect was established. L. cubeba oil has a potent effect on the central nervous system of mice. | [193] |
thymol, γ-terpinene, trans-caryophyllene, β-selinene, p-cymene (Ocimum gratissimum) | Inhalation | 4.0 × 10−10 −4.0 × 10−1 mg for 60 min | Mouse | Light/Dark transition test | Inhalation of EO (at a concentration of 4.0 × 10−4 mg) showed anxiolytic potential and did not cause any deleterious effects on motor coordination. | [194] |
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Wojtunik-Kulesza, K.; Rudkowska, M.; Kasprzak-Drozd, K.; Oniszczuk, A.; Borowicz-Reutt, K. Activity of Selected Group of Monoterpenes in Alzheimer’s Disease Symptoms in Experimental Model Studies—A Non-Systematic Review. Int. J. Mol. Sci. 2021, 22, 7366. https://doi.org/10.3390/ijms22147366
Wojtunik-Kulesza K, Rudkowska M, Kasprzak-Drozd K, Oniszczuk A, Borowicz-Reutt K. Activity of Selected Group of Monoterpenes in Alzheimer’s Disease Symptoms in Experimental Model Studies—A Non-Systematic Review. International Journal of Molecular Sciences. 2021; 22(14):7366. https://doi.org/10.3390/ijms22147366
Chicago/Turabian StyleWojtunik-Kulesza, Karolina, Monika Rudkowska, Kamila Kasprzak-Drozd, Anna Oniszczuk, and Kinga Borowicz-Reutt. 2021. "Activity of Selected Group of Monoterpenes in Alzheimer’s Disease Symptoms in Experimental Model Studies—A Non-Systematic Review" International Journal of Molecular Sciences 22, no. 14: 7366. https://doi.org/10.3390/ijms22147366
APA StyleWojtunik-Kulesza, K., Rudkowska, M., Kasprzak-Drozd, K., Oniszczuk, A., & Borowicz-Reutt, K. (2021). Activity of Selected Group of Monoterpenes in Alzheimer’s Disease Symptoms in Experimental Model Studies—A Non-Systematic Review. International Journal of Molecular Sciences, 22(14), 7366. https://doi.org/10.3390/ijms22147366