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Food Science and Human Wellness 2023, 12(5): 1618-1625 https://doi.org/10.1016/j.fshw.2023.02.009
Research Article | Open Access | Issue | Published: 21 March 2023

Lycium ruthenicum Murr. treatment attenuates APPswE/PS1ΔE9 mouse model-like mitochondrial dysfunction in Slc25a46 knockout mouse model

Show Author's Information Min Wanga,1,  Tianxiong Xua,1,  Li Gaoa,  Chujun Huanga,  Piao Xua,  Congcong Gonga,  William Kwame Amakyea,  Linfeng Liaoa,  Maojin Yaob,  Jiaoyan Rena( )
School of Food Science and Engineering, South China University of Technology, Guangzhou 510641, China
Guangzhou Institute of Respiratory Disease & China State Key Laboratory of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou 510182, China

1 These authors contributed equally to this work.

Peer review under responsibility of KeAi Communications Co., Ltd.

Keywords:
Alzheimer's disease, Ageing, Mitochondria dysfunction, Slc25a46 knockout mouse, Lycium ruthenicum Murr.
Cite this article:
Wang M, Xu T, Gao L, et al. Lycium ruthenicum Murr. treatment attenuates APPswE/PS1ΔE9 mouse model-like mitochondrial dysfunction in Slc25a46 knockout mouse model. Food Science and Human Wellness, 2023, 12(5): 1618-1625. https://doi.org/10.1016/j.fshw.2023.02.009
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Abstract Full text About this article

Mitochondrial dysfunction is proposed to be substantially associated with ageing and ageing-related diseases like Alzheimer's disease (AD). However, it is unclear whether different mouse models with mitochondrial-related diseases have similar changes in mitochondrial morphology of the same tissues. Moreover, whether similarities in mitochondrial morphology can be a suitable marker for screening and/or discovering mitochondrial-protective substances remains unknown. Mitochondria morphology in different tissues of a novel mitochondrial outer membrane protein Slc25a46 knockout mouse and a traditional APPSWE/PS1ΔE9 transgenic mouse were examined using transmission electron microscope (TEM). Both young Slc25a46 knockout mice and aged APPSWE/PS1ΔE9 mice models showed similar mitochondrial damage in cerebellum tissues. The results indicated that different mitochondrial-related diseases shared similar alteration and defects in mitochondrial morphology. Furthermore, Lycium ruthenicum Murr. extract, a bioactive food substance with cognition-improving property, could effectively improve muscle strength and increase body weight in the Slc25a46 knockout mice. These findings suggest that mitochondrial morphology defects in mice models, particularly in the mitochondrial compartment, represent a unified and effective marker for screening and validating natural product-derived functional substances with mitochondrial protective properties. It also holds potential application in mitochondrial-impaired senile neurodegenerative diseases, especially in AD.


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About this article

Lycium ruthenicum Murr. treatment attenuates APPswE/PS1ΔE9 mouse model-like mitochondrial dysfunction in Slc25a46 knockout mouse model

Show Author's information Min Wanga,1, Tianxiong Xua,1, Li Gaoa, Chujun Huanga, Piao Xua, Congcong Gonga, William Kwame Amakyea, Linfeng Liaoa, Maojin Yaob, Jiaoyan Rena( )
School of Food Science and Engineering, South China University of Technology, Guangzhou 510641, China
Guangzhou Institute of Respiratory Disease & China State Key Laboratory of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou 510182, China

1 These authors contributed equally to this work.

Peer review under responsibility of KeAi Communications Co., Ltd.

Abstract

Mitochondrial dysfunction is proposed to be substantially associated with ageing and ageing-related diseases like Alzheimer's disease (AD). However, it is unclear whether different mouse models with mitochondrial-related diseases have similar changes in mitochondrial morphology of the same tissues. Moreover, whether similarities in mitochondrial morphology can be a suitable marker for screening and/or discovering mitochondrial-protective substances remains unknown. Mitochondria morphology in different tissues of a novel mitochondrial outer membrane protein Slc25a46 knockout mouse and a traditional APPSWE/PS1ΔE9 transgenic mouse were examined using transmission electron microscope (TEM). Both young Slc25a46 knockout mice and aged APPSWE/PS1ΔE9 mice models showed similar mitochondrial damage in cerebellum tissues. The results indicated that different mitochondrial-related diseases shared similar alteration and defects in mitochondrial morphology. Furthermore, Lycium ruthenicum Murr. extract, a bioactive food substance with cognition-improving property, could effectively improve muscle strength and increase body weight in the Slc25a46 knockout mice. These findings suggest that mitochondrial morphology defects in mice models, particularly in the mitochondrial compartment, represent a unified and effective marker for screening and validating natural product-derived functional substances with mitochondrial protective properties. It also holds potential application in mitochondrial-impaired senile neurodegenerative diseases, especially in AD.

Keywords: Alzheimer's disease, Ageing, Mitochondria dysfunction, Slc25a46 knockout mouse, Lycium ruthenicum Murr.

References(45)

[1]
UN. 2019 World population prospects. (2019) 〈https://population.un.org/wpp/〉.
[2]

R. Zhang, Y. Lu, L. Shi, et al., Prevalence and patterns of multimorbidity among the elderly in China: a cross-sectional study using national survey data, BMJ Open 9 (2019) e024268. https://doi.org/10.1136/bmjopen-2018-024268.
DOI Google Scholar
[3]

Z. Guan, Z. Chen, S. Fu, et al., Progranulin administration attenuates β-amyloid deposition in the hippocampus of 5xfad mice through modulating bace1 expression and microglial phagocytosis, Front. Cell Neurosci. 14 (2020). https://doi.org/10.3389/fncel.2020.00260.
DOI Google Scholar
[4]

D.A. Chistiakov, I.A. Sobenin, V.V. Revin, et al., Mitochondrial aging and age-related dysfunction of mitochondria, Biomed. Res. Int. 2014 (2014) 238463. https://doi.org/10.1155/2014/238463.
DOI Google Scholar
[5]

H. Du, L. Guo, S. Yan, et al., Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model, Proc. Natl. Acad. Sci. U.S.A. 107 (2010) 18670-18675. https://doi.org/10.1073/pnas.1006586107.
DOI Google Scholar
[6]

S. Gallage, J. Gil, Mitochondrial dysfunction meets senescence, Trends Biochem. Sci. 41 (2016) 207-209. https://doi.org/10.1016/j.tibs.2016.01.005.
DOI Google Scholar
[7]

M.O. Hengartner, The biochemistry of apoptosis, Nature 407 (2000) 770-776. https://doi.org/10.1038/35037710.
DOI Google Scholar
[8]

J. Tang, A. Oliveros, M.H. Jang, Dysfunctional mitochondrial bioenergetics and synaptic degeneration in Alzheimer disease, Int. Neurourol. J. 23(Suppl 1) (2019). https://doi.org/10.5213/inj.1938036.018.
DOI Google Scholar
[9]

R.X. Santos, S.C. Correia, X. Wang, et al., Alzheimer's disease: diverse aspects of mitochondrial malfunctioning, Int. J. Clin. Exp. Pathol. 3 (2010) 570-581.
Google Scholar
[10]

M. Briga, S. Verhulst, What can long-lived mutants tell us about mechanisms causing aging and lifespan variation in natural environments? Exp. Gerontol. 71 (2015) 95-102. https://doi.org/10.1016/j.exger.2015.09.002.
DOI Google Scholar
[11]

R.C.G. Correa, R.M. Peralta, C.W.I. Haminiuk, et al., New phytochemicals as potential human anti-aging compounds: reality, promise, and challenges, Crit. Rev. Food Sci. Nutr. 58 (2018) 942-957. https://doi.org/10.1080/10408398.2016.1233860.
DOI Google Scholar
[12]

M. Chen, D. Kretzschmar, G. Verdile, et al., Animal models for the study of human disease, Models of Alzheimer's Disease (2013) 595-632. https://doi.org/10.1016/B978-0-12-415894-8.00025-7.
DOI Google Scholar
[13]

D. Pan, Q. Zhu, M.J. Conboy, et al., SnoN activates p53 directly to regulate aging and tumorigenesis, Aging Cell. 11(5) (2012) 902-911. https://doi.org/10.1111/j.1474-9726.2012.00857.x.
DOI Google Scholar
[14]

S.R. Kesler, P. Acton, V. Rao, et al., Functional and structural connectome properties in the 5xfad transgenic mouse model of Alzheimer's disease, Network Neurosci. (Cambridge, Mass.) (2018). https://doi.org/10.1162/netn_a_00048.
DOI Google Scholar
[15]

C. Lopez-Otin, M.A. Blasco, L. Partridge, et al., The hallmarks of aging, Cell 153 (2013) 1194-1217. https://doi.org/10.1016/j.cell.2013.05.039.
DOI Google Scholar
[16]

G. Pounis, S. Costanzo, R.D. Giuseppe, et al., Consumption of healthy foods at different content of antioxidant vitamins and phytochemicals and metabolic risk factors for cardiovascular disease in men and women of the Moli-sani study, Eur. J. Clin. Nutr. 67 (2013) 207-213. https://doi.org/10.1038/ejcn.2012.201.
DOI Google Scholar
[17]

W. Rizza, N. Veronese, L. Fontana, What are the roles of calorie restriction and diet quality in promoting healthy longevity? Ageing Res. Rev. 13 (2014) 38-45. https://doi.org/10.1016/j.arr.2013.11.002.
DOI Google Scholar
[18]

A. Guiotto, A. Calderan, P. Ruzza, et al., Carnosine and carnosine-related antioxidants: a review, Curr. Med. Chem. 12 (2005) 2293-2315. https://doi.org/10.2174/0929867054864796.
DOI Google Scholar
[19]

C. Valls-Pedret, A. Sala-Vila, M. Serra-Mir, et al., Mediterranean diet and age-related cognitive decline: a randomized clinical trial, JAMA Intern. Med. 175(7) (2015). https://doi.org/10.1001/jamainternmed.2015.1668.
DOI Google Scholar
[20]

J. Zheng, C. Ding, L. Wang, et al., Anthocyanins composition and antioxidant activity of wild Lycium ruthenicum Murr. from qinghai-tibet plateau, Food Chem. 126(3) (2011) 859-865. https://doi.org/10.1016/j.foodchem.2010.11.052.
DOI Google Scholar
[21]

T. Wu, H. Lv, F. Wang, et al., Characterization of polyphenols from Lycium ruthenicum fruit by UPLC-Q-TOF/MS(E) and their antioxidant activity in Caco-2 cells, J. Agric. Food Chem. 64 (2016) 2280-2288. https://doi.org/10.1021/acs.jafc.6b00035.
DOI Google Scholar
[22]

P.H. Shih, Y.C. Chan, J.W. Liao, et al., Antioxidant and cognitive promotion effects of anthocyanin-rich mulberry (Morus atropurpurea L.) on senescence- accelerated mice and prevention of Alzheimer's disease, J. Nutr. Biochem. 21 (2010) 598-605. https://doi.org/10.1016/j.jnutbio.2009.03.008.
DOI Google Scholar
[23]

L. Gao, M. Wang, L. Liao, et al., A Slc25a46-/- mouse model simulating motor deficit, imbalance of redox system and mitochondria dysfunction during aging, J. Gerontol A. Biol. Sci. Med. Sci. Dec. 4 (2020). https://doi.org/10.1093/gerona/glaa306.
DOI Google Scholar
[24]

N.V. Shults, S.S. Kanovka, J.E.Ten Eyck, et al., Ultrastructural changes of the right ventricular myocytes in pulmonary arterial hypertension, J. Am. Heart Assoc. 8 (2019) e011227. https://doi.org/10.1161/JAHA.118.011227.
DOI Google Scholar
[25]

K. McAvoy, H. Kawamata, Glial mitochondrial function and dysfunction in health and neurodegeneration, Mol. Cell Neurosci. 101 (2019) 103417. https://doi.org/10.1016/j.mcn.2019.103417.
DOI Google Scholar
[26]

M.K. Singh-Bains, V. Linke, M.D.R. Austria, et al., Altered microglia and neurovasculature in the Alzheimer's disease cerebellum, Neurobiol. Dis. 132 (2019) 104589. https://doi.org/10.1016/j.nbd.2019.104589.
DOI Google Scholar
[27]

J.M.S. Perez Ortiz, H. Russell, Mitochondrial dysfunction in Alzheimer's disease: role in pathogenesis and novel therapeutic opportunities, Brit. J. Pharmacol. 176 (2018) 3489-3507. https://doi.org/10.1111/bph.14585.
DOI Google Scholar
[28]

J.B. Toledo, M. Arnold, G. Kastenmuller, et al., Metabolic network failures in Alzheimer's disease: a biochemical road map, Alzheimers Dement 13 (2017) 965-984. https://doi.org/10.1016/j.jalz.2017.01.020.
DOI Google Scholar
[29]

M. Xu, J. Feng, M. Tang, et al., Blocking retrograde axonal transport of autophagosomes contributes to sevoflurane-induced neuron apoptosis in APP/PS1 mice, Acta Neurol. Belg. 4 (2020). https://doi.org/10.1007/s13760-020-01359-6.
DOI Google Scholar
[30]

K. Richetin, M. Moulis, A. Millet, et al., Amplifying mitochondrial function rescues adult neurogenesis in a mouse model of Alzheimer's disease, Neurobiol. Dis. 102 (2017) 113-124. https://doi.org/10.1016/j.nbd.2017.03.002.
DOI Google Scholar
[31]

L. Massimi, N. Pieroni, L. Maugeri, et al., Assessment of plaque morphology in Alzheimer's mouse cerebellum using three-dimensional x-ray phase-based virtual histology, Sci. Rep. 10(1) (2020). https://doi.org/10.1038/s41598-020-68045-8.
DOI Google Scholar
[32]

Palmieri, Ferdinando. The mitochondrial transporter family SLC25: identification, properties and physiopathology, Mol. Aspects Med. 34 (2013) 465-484. https://doi.org/10.1016/j.mam.2012.05.005.
DOI Google Scholar
[33]

A.J. Abrams, R.B. Hufnagel, A. Rebelo, et al., Mutations in Slc25a46, encoding a UGO1-like protein, cause an optic atrophy spectrum disorder, Nat. Genet. 47 (2015). https://doi.org/10.1038/ng.3354.
DOI Google Scholar
[34]

G. Charlesworth, B. Balint, N.E. Mencacci, et al., Slc25a46 mutations underlie progressive myoclonic ataxia with optic atrophy and neuropathy, Mov. Disord. 31 (2016) 1249-1251. https://doi.org/10.1002/mds.26716.
DOI Google Scholar
[35]

Z. Li, Y. Peng, B.R. Hufnagel, et al., Loss of Slc25a46 causes neurodegeneration by affecting mitochondrial dynamics and energy production in mice, Hum. Mol. Genet. 26 (2017) 3776-3791. https://doi.org/10.1093/hmg/ddx262.
DOI Google Scholar
[36]

H. Chen, J.K. Mccaffery, D.C. Chan, Mitochondrial fusion protects against neurodegeneration in the cerebellum, Cell 130(3) (2007) 548-562. https://doi.org/10.1016/j.cell.2007.06.026.
DOI Google Scholar
[37]

C.L. Masters, D.J. Selkoe, Biochemistry of amyloid beta-protein and amyloid deposits in Alzheimer disease, CSH. Perspect. Med. 2 (2012) a006262. https://doi.org/10.1101/cshperspect.a006262.
DOI Google Scholar
[38]

M. Abate, A. Festa, M. Falco, et al., Mitochondria as playmakers of apoptosis, autophagy and senescence, Semin. Cell. Dev. Biol. 98 (2020) 139-153. https://doi.org/10.1016/j.semcdb.2019.05.022.
DOI Google Scholar
[39]

R. Quintana-Cabrera, C. Quirin, C. Glytsou, et al., The cristae modulator Optic atrophy 1 requires mitochondrial ATP synthase oligomers to safeguard mitochondrial function, Nat. Commun. 9 (2018) 3399. https://doi.org/10.1038/s41467-018-05655-x.
DOI Google Scholar
[40]

R.H. Swerdlow, J.M. Burns, S.M. Khan, The Alzheimer's disease mitochondrial cascade hypothesis: progress and perspectives, Biochim. Biophys. Acta. 1842 (2014) 1219-1231. https://doi.org/10.1016/j.bbadis.2013.09.010.
DOI Google Scholar
[41]

S. Vepsäläinen, H. Koivisto, E. Pekkarinen, et al., Anthocyanin-enriched bilberry and blackcurrant extracts modulate amyloid precursor protein processing and alleviate behavioral abnormalities in the APP/PS1 mouse model of Alzheimer's disease, J. Nutr. Biochem. 24 (2013) 360-370. https://doi.org/10.1016/j.jnutbio.2012.07.006.
DOI Google Scholar
[42]

S. Chen, H. Zhou, G. Zhang, et al., Anthocyanins from Lycium ruthenicum Murr. ameliorated d-galactose-induced memory impairment, oxidative stress, and neuroinflammation in adult rats, J. Agric. Food Chem. 67 (2019) 3140-3149. https://doi.org/10.1021/acs.jafc.8b06402.
DOI Google Scholar
[43]

A.S. Sousa, R.S. Guerra, I. Fonseca, et al., Financial impact of sarcopenia on hospitalization costs, Eur. J. Clin. Nutr. 70 (2016) 1046-1051. https://doi.org/10.1038/ejcn.2016.73.
DOI Google Scholar
[44]

B. Yan, L. Yao, A. Shi, et al., Investigation of the antifatigue effects of Korean Ginseng on professional athletes by gas chromatography-time-of-flight-mass spectrometry-based metabolomics, J. Aoac. Int. 3 (2019) 701-707. https://doi.org/10.5740/jaoacint.17-0220.
DOI Google Scholar
[45]

J. Zhang, D.S. Ji, S.H. Zhao, et al., Anti-aging effects of Lycium ruthenicum Murr. granules in Caenorhabditis elegans, Pak. J. Zool. 52 (2020). https://doi.org/10.17582/journal.pjz/20191016031055.
DOI Google Scholar
Publication history
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Publication history

Received: 16 January 2021
Revised: 18 February 2021
Accepted: 29 April 2021
Published: 21 March 2023
Issue date: September 2023

Copyright

© 2023 Beijing Academy of Food Sciences.

Acknowledgements

We thank Y. Zhang (Infinitus (China) Ltd., Guangzhou China) for providing the Lycium ruthenicum Murr. extracts. This work was supported by National Key R&D Program of China (2018YFD0901101); the Natural Science Foundation of Guangdong Province Research (2019A1515012230); Development Program in Key Areas of Guangdong Province (2019B020210002); the Fundamental Research Funds for the Central Universities (2019KZ01).

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This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

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