Cite this paper:
Zhongshan ZHANG, Xiaomei WANG, Yongliang PAN, Zhanqi WANG, Zhengshun WEN, Feng LIU, Genxiang MAO. Pyropia haitanensis polysaccharide extends lifespan by inhibiting protein aggregation in Caenorhabditis elegans[J]. Journal of Oceanology and Limnology, 2021, 39(2): 705-713

Pyropia haitanensis polysaccharide extends lifespan by inhibiting protein aggregation in Caenorhabditis elegans

Zhongshan ZHANG1, Xiaomei WANG1, Yongliang PAN1, Zhanqi WANG1, Zhengshun WEN2, Feng LIU3, Genxiang MAO4
1 Key Laboratory of Vector Biology and Pathogen Control of Zhejiang Province, Huzhou University, Huzhou Central Hospital, Huzhou 313000, China;
2 Zhejiang Provincial Engineering Technology Research Center of Marine Biomedical Products, School of Food Science and Pharmaceutics, Zhejiang Ocean University, Zhoushan 316022, China;
3 CAS Key Laboratory of Marine Ecology and Environmental Sciences, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
4 Zhejiang Provincial Key Lab of Geriatrics, Department of Geriatrics, Zhejiang Hospital, Hangzhou 310013, China
Abstract:
Pyropia haitanensis polysaccharide (LP) have been found for having many excellent functions such as anti-aging. Using Caenorhabditis elegans models, we evaluated the anti-aging activity of LP by observing the lifespan, reproduction, pharyngeal pumping, stress response, quantitative fluorescence of polyglutamic acid, and nuclear localization of DAF-16 of worms. The results reveal that LP could extend the adult lifespan of wild-type and polyQ nematodes, indicating a connection of its anti-aging benefit with the toxicity-suppressing effect. The number of polyglutamic acid aggregates in high concentration groups decreased by 24.39% (P<0.05) to the control. The high-dose group strongly induced DAF-16 nuclear translocation over intermediate and cytosolic localizations compared with the control (P<0.001). Therefore, we believe that LP could extend the lifespan and reduce the protein aggregation in C. elegans through nuclear DAF-16::GFP expression.
Key words:    Pyropia haitanensis|polysaccharide|protein aggregation|Caenorhabditis elegans   
Received: 2020-02-14   Revised: 2020-04-13
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Articles by Zhongshan ZHANG
Articles by Xiaomei WANG
Articles by Yongliang PAN
Articles by Zhanqi WANG
Articles by Zhengshun WEN
Articles by Feng LIU
Articles by Genxiang MAO
References:
Anandan R, Ganesan B, Obulesu T, Mathew S, Asha K K, Lakshmanan P T, Zynudheen A A. 2013. Antiaging effect of dietary chitosan supplementation on glutathionedependent antioxidant system in young and aged rats. Cell Stress and Chaperones, 18(1):121-125, https://doi.org/10.1007/s12192-012-0354-2.
Bhatia S, Sharma K, Bera T. 2015. Structural characterization and pharmaceutical properties of porphyran. Asian Journal of Pharmaceutics, 9(2):93-101, https://doi.org/10.4103/0973-8398.154698.
Brignull H R, Moore F E, Tang S J, Morimoto R I. 2006. Polyglutamine proteins at the pathogenic threshold display neuron-specific aggregation in a pan-neuronal Caenorhabditis elegans model. Journal of Neuroscience, 26(29):7 597-7 606, https://doi.org/10.1523/JNEUROSCI.0990-06.2006.
Burkewitz K, Choe K, Strange K. 2011. Hypertonic stress induces rapid and widespread protein damage in C. elegans. American Journal of Physiology-Cell Physiology, 301(3):C566-C576, https://doi.org/10.1152/ajpcell.00030.2011.
Cohen E, Dillin A. 2008. The insulin paradox:aging, proteotoxicity and neurodegeneration. Nature Reviews Neuroscience, 9(10):759-767, https://doi.org/10.1038/nrn2474.
Cypser J R, Tedesco P, Johnson T E. 2006. Hormesis and aging in Caenorhabditis elegans. Experimental Gerontology, 41(10):935-939, https://doi.org/10.1016/j.exger.2006.09.004.
Fan H C, Ho L I, Chi C S, Chen S J, Peng G S, Chan T M, Lin S Z, Harn H J. 2014. Polyglutamine (PolyQ) diseases:genetics to treatments. Cell Transplantation, 23(4-5):441-458, https://doi.org/10.3727/096368914X678454.
Gan L. 2007. Therapeutic potential of sirtuin-activating compounds in Alzheimer's disease. Drug News & Perspectives, 20(4):233, https://doi.org/10.1358/dnp. 2007.20.4.1101162.
Garcia S M, Casanueva M O, Silva M V, Amaral M D, Morimoto R I. 2007. Neuronal signaling modulates protein homeostasis in Caenorhabditis elegans post-synaptic muscle cells. Genes & Development, 21(22):3 006-3 016, https://doi.org/10.1101/gad.1575307.
Gong G P, Zhao J X, Wang C J, Wei M, Dang T T, Deng Y N, Sun J, Song S, Huang L J, Wang Z F. 2018. Structural characterization and antioxidant activities of the degradation products from Porphyra haitanensis polysaccharides. Process Biochemistry, 74:185-193, https://doi.org/10.1016/j.procbio.2018.05.022.
Gusella J F, MacDonald M E. 2006. Huntington's disease:seeing the pathogenic process through a genetic lens. Trends in Biochemical Sciences, 31(9):533-540, https://doi.org/10.1016/j.tibs.2006.06.009.
Hsu A L, Murphy C T, Kenyon C. 2003. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science, 300(5622):1 142-1 145, https://doi.org/10.1126/science.1083701.
Huangfu J F, Liu J, Sun Z, Wang M F, Jiang Y, Chen Z Y, Chen F. 2013. Antiaging effects of astaxanthin-rich alga Haematococcus pluvialis on fruit flies under oxidative stress. Journal of Agricultural and Food Chemistry, 61(32):7 800-7 804, https://doi.org/10.1021/jf402224w.
Jeon H, Cha D S. 2016. Anti-aging properties of Ribes fasciculatum in Caenorhabditis elegans. Chinese Journal of Natural Medicines, 14(5):335-342, https://doi.org/10.3724/SP.J.1009.2016.00335.
Jin L, Song Q R, Zhang W L, Geng B, Cai J. 2019. Roles of long noncoding RNAs in aging and aging complications. Biochimica et Biophysica Acta (BBA)-Molecular Basis of Disease, 1865(7):1 763-1 771, https://doi.org/10.1016/j.bbadis.2018.09.021.
Kandasamy S, Khan W, Evans F D, Critchley A T, Zhang J Z, Fitton J H, Stringer D N, Gardiner V A, Prithiviraj B. 2014. A fucose containing polymer-rich fraction from the brown alga Ascophyllum nodosum mediates lifespan increase and thermal-tolerance in Caenorhabditis elegans, by differential effects on gene and protein expression. Food & Function, 5(2):275-284, https://doi.org/10.1039/C3FO60050E.
Kim D K, Cho K W, Ahn W J, Perez-Acuña D, Jeong H, Lee H J, Lee S J. 2017. Cell-to-cell transmission of polyglutamine aggregates in C. elegans. Experimental Neurobiology, 26(6):321-328, https://doi.org/10.5607/en.2017.26.6.321.
Kim D K, Jeon H, Cha D S. 2014. 4-Hydroxybenzoic acidmediated lifespan extension in Caenorhabditis elegans. Journal of Functional Foods, 7:630-640, https://doi.org/10.1016/j.jff.2013.12.022.
Large E E, Padmanabhan R, Watkins K L, Campbell R F, Xu W, McGrath P T. 2017. Modeling of a negative feedback mechanism explains antagonistic pleiotropy in reproduction in domesticated Caenorhabditis elegans strains. PLoS Genetics, 13(5):e1006769, https://doi.org/10.1371/journal.pgen.1006769.
Levy M, Porat Y, Bacharach E, Shalev D E, Gazit E. 2008. Phenolsulfonphthalein, but not phenolphthalein, inhibits amyloid fibril formation:implications for the modulation of amyloid self-assembly. Biochemistry, 47(22):5 896-5 904, https://doi.org/10.1021/bi800043d.
Liang Z H, Yin D Z. 2010. Preventive treatment of traditional Chinese medicine as antistress and antiaging strategy. Rejuvenation Research, 13(2-3):248-252, https://doi.org/10.1089/rej.2009.0867.
Lin K, Hsin H, Libina N, Kenyon C. 2001. Regulation of the Caenorhabditis elegans longevity protein DAF-16 by insulin/IGF-1 and germline signaling. Nature Genetics, 28(2):139-145, https://doi.org/10.1038/88850.
Liu Q M, Xu S S, Li L, Pan T M, Shi C L, Liu H, Cao M J, Su W J, Liu G M. 2017. In vitro and in vivo immunomodulatory activity of sulfated polysaccharide from Porphyra haitanensis. Carbohydrate Polymers, 165:189-196, https://doi.org/10.1016/j.carbpol.2017.02.032.
Liu Y J, Geng L H, Zhang J J, Wang J, Zhang Q, Duan D L, Zhang Q B. 2018. Oligo-porphyran ameliorates neurobehavioral deficits in Parkinsonian mice by regulating the PI3K/Akt/Bcl-2 pathway. Marine Drugs, 16(3):82, https://doi.org/10.3390/md16030082.
Masoro E J. 2005. Overview of caloric restriction and ageing. Mechanisms of Ageing and Development, 126(9):913-922, https://doi.org/10.1016/j.mad.2005.03.012.
Mazzeo L E M, Dersh D, Boccitto M, Kalb R G, Lamitina T. 2012. Stress and aging induce distinct polyQ protein aggregation states. Proceedings of the National Academy of Sciences of the United States of America, 109(26):10 587-10 592, https://doi.org/10.1073/pnas.1108766109.
Monickaraj F, Aravind S, Nandhini P, Prabu P, Sathishkumar C, Mohan V, Balasubramanyam M. 2013. Accelerated fat cell aging links oxidative stress and insulin resistance in adipocytes. Journal of Biosciences, 38(1):113-122, https://doi.org/10.1007/s12038-012-9289-0.
Morley J F, Brignull H R, Weyers J J, Morimoto R I. 2002. The threshold for polyglutamine-expansion protein aggregation and cellular toxicity is dynamic and influenced by aging in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America, 99(16):10 417-10 422, https://doi.org/10.1073/pnas.152161099.
Pandey S, Tiwari S, Kumar A, Niranjan A, Chand J, Lehri A, Chauhan P S. 2018. Antioxidant and anti-aging potential of Juniper berry (Juniperus communis L.) essential oil in Caenorhabditis elegans model system. Industrial Crops and Products, 120:113-122, https://doi.org/10.1016/j.indcrop.2018.04.066.
Petrascheck M, Ye X L, Buck L B. 2007. An antidepressant that extends lifespan in adult Caenorhabditis elegans. Nature, 450(7169):553-556, https://doi.org/10.1038/nature05991.
Powers E T, Morimoto R I, Dillin A, Kelly J W, Balch W E. 2009. Biological and chemical approaches to diseases of proteostasis deficiency. Annual Review of Biochemistry, 78:959-991, https://doi.org/10.1146/annurev.biochem.052308.114844.
Powolny A A, Singh S V, Melov S, Hubbard A, Fisher A L. 2011. The garlic constituent diallyl trisulfide increases the lifespan of C. elegans via skn-1 activation. Experimental Gerontology, 46(6):441-452, https://doi.org/10.1016/j.exger.2011.01.005.
Sun C J, Wu F, Chen D D, Ge J B. 2018. Therapeutic effects of polysaccharides extracted from Porphyra yezoensis in rats with cerebral ischemia/reperfusion injury. Archives of Biological Sciences, 70(2):233-239, https://doi.org/10.2298/ABS170621039S.
Sutherland J E, Lindstrom S C, Nelson W A, Brodie J, Lynch M D J, Hwang M S, Choi H G, Miyata M, Kikuchi N, Oliveira M C, Farr T, Neefus C, Mols-Mortensen A, Milstein D, Müller K M. 2011. A new look at an ancient order:generic revision of the bangiales (Rhodophyta). Journal of Phycology, 47(5):1 131-1 151, https://doi.org/10.1111/j.1529-8817.2011.01052.x.
Wang H, Duennwald M L, Roberts B E, Rozeboom L M, Zhang Y L, Steele A D, Krishnan R, Su L J, Griffin D, Mukhopadhyay S, Hennessy E J, Weigele P, Blanchard B J, King J, Deniz A A, Buchwald S L, Ingram V M, Lindquist S, Shorter J. 2008. Direct and selective elimination of specific prions and amyloids by 4,5-dianilinophthalimide and analogs. Proceedings of the National Academy of Sciences of the United States of America, 105(20):7 159-7 164, https://doi.org/10.1073/pnas.0801934105.
Waterston R H, Brenner S. 1978. A suppressor mutation in the nematode acting on specific alleles of many genes. Nature, 275(5682):715-719, https://doi.org/10.1038/275715a0.
Wu M Y, Kang X, Wang Q, Zhou C Y, Mohan C, Peng A. 2017. Regulator of G protein signaling-1 modulates paraquat-induced oxidative stress and longevity via the insulin like signaling pathway in Caenorhabditis elegans. Toxicology Letters, 273:97-105, https://doi.org/10.1016/j.toxlet.2017.03.027.
Xu J, Jiang Y J, Wan L, Wang Q, Huang Z B, Liu Y M, Wu Y L, Chen Z Y, Liu X. 2017. Feeding recombinant E. coli with GST-mBmKTX fusion protein increases the fecundity and lifespan of Caenorhabditis elegans. Peptides, 89:1-8, https://doi.org/10.1016/j.peptides.2017.01.003.
Zhang H R, Pan N, Xiong S Q, Zou S L, Li H F, Xiao L Y, Cao Z J, Tunnacliffe A, Huang Z B. 2012. Inhibition of polyglutamine-mediated proteotoxicity by Astragalus membranaceus polysaccharide through the DAF-16/FOXO transcription factor in Caenorhabditis elegans. Biochemical Journal, 441(1):417-424, https://doi.org/10.1042/BJ20110621.
Zhang Z S, Wang X M, Lv F, Xie X C, Zhang S Y, Cai C E, Jia R, Pan Y L, Liu F. 2020. Anti-complementary activity of a degraded sulfated heterogalactan from red alga Pyropia haitanensis. International Journal of Biological Macromolecules, 147:527-533, https://doi.org/10.1016/j.ijbiomac.2020.01.045.
Zhao P, Niu J F, Huan L, Gu W H, Wu M J, Wang G C. 2019. Agar extraction from Pyropia haitanensis residue after the removal and purification of phycobiliproteins. Journal of Applied Phycology, 31(4):2 497-2 505, https://doi.org/10.1007/s10811-019-1735-z.
Zhao S X, Cheng Q, Peng Q, Yu X S, Yin X Q, Liang M, Ma C W, Huang Z B, Jia W Z. 2018. Antioxidant peptides derived from the hydrolyzate of purple sea urchin(Strongylocentrotus nudus) gonad alleviate oxidative stress in Caenorhabditis elegans. Journal of Functional Foods, 48:594-604, https://doi.org/10.1016/j.jff.2018.07.060.
Zhao T T, Zhang Q B, Qi H M, Zhang H, Niu X Z, Xu Z H, Li Z E. 2006. Degradation of porphyran from Porphyra haitanensis and the antioxidant activities of the degraded porphyrans with different molecular weight. International Journal of Biological Macromolecules, 38(1):45-50, https://doi.org/10.1016/j.ijbiomac.2005.12.018.
Zhou L, Wang L, Bai S J, Xing S, Li W N, Ma J F, Fu X Q. 2018. Knockdown of LMW-PTP enhances stress resistance in Caenorhabditis elegans. International Journal of Biological Macromolecules, 113:1 015-1 023, https://doi.org/10.1016/j.ijbiomac.2018.03.014.
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