Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-17T03:21:33.138Z Has data issue: false hasContentIssue false
  • English
  • Français

Evaluation of In Situ Antiaging Activity in Saccharomyces cerevisiae BY611 Yeast Cells Treated with Polyalthia longifolia Leaf Methanolic Extract (PLME) Using Different Microscopic Approaches: A Morphology-Based Evaluation

Published online by Cambridge University Press:  09 March 2022

Manisekaran Hemagirri  and
Sreenivasan Sasidharan Open the ORCID record for Sreenivasan Sasidharan [Opens in a new window]
Manisekaran Hemagirri
Affiliation:
Institute for Research in Molecular Medicine, Universiti Sains Malaysia, 11800 USM, Pulau Pinang, Malaysia
Sreenivasan Sasidharan*
Affiliation:
Institute for Research in Molecular Medicine, Universiti Sains Malaysia, 11800 USM, Pulau Pinang, Malaysia
*
*Corresponding author: Sreenivasan Sasidharan, E-mail: [email protected]
Get access

Abstract

Polyalthia longifolia is known for its anti-oxidative properties, which might contribute to the antiaging action. Hence, the current research was conducted to evaluate the antiaging activity of P. longifolia leaf methanolic extract (PLME) in a yeast model based on morphology using microscopic approaches. Saccharomyces cerevisiae BY611 strain yeast cells were treated with 1.00 mg/mL of PLME. The antiaging activity was assessed by determining the replicative lifespan, total lifespan, vacuole morphology by light microscopy, extra-morphology by scanning (SEM), and intra-morphology by transmission (TEM) electron microscopy. The findings demonstrated that PLME treatment significantly accelerated the replicative and total lifespan of the yeast cells. PLME treatment also delays the formation of large apoptotic-like type 3 yeast cell vacuoles. The untreated yeast cells demonstrated aging morphology via SEM analysis, such as shrinking, regional invaginations, and wrinkled cell surface. The TEM analysis revealed the quintessential aging intracellular morphology such as swollen, wrinkled, or damaged vacuole formation of the circular endoplasmic reticulum, a rupture in the nuclear membrane, fragmentation of the nucleus, and complete damaged cytoplasm. Decisively, the present study revealed the vital role of PLME in the induction of antiaging activity in a yeast model using three microscopic approaches—SEM, TEM, and bright-field light microscope.

Keywords

antiaginglight microscopePolyalthia longifoliascanning electron microscopytransmission electron microscopyyeast
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 28 , Issue 3 , June 2022 , pp. 767 - 779
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press on behalf of the Microscopy Society of America

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abudugupur, A, Mitsui, K, Yokota, S & Tsurugi, K (2002). An ARL1 mutation affected autophagic cell death in yeast, causing a defect in central vacuole formation. Cell Death Differ 9(2), 158–168.CrossRefGoogle ScholarPubMed
Armstrong, J (2010). Yeast vacuoles: More than a model lysosome. Trends Cell Biol 20, 580–585.CrossRefGoogle ScholarPubMed
Aufschnaiter, A & Büttner, S (2019). The vacuolar shapes of ageing: From function to morphology. Biochim Biophys Acta Mol Cell Res 1866(5), 957–970.CrossRefGoogle Scholar
Basisty, N, Meyer, JG & Schilling, B (2018). Protein turnover in aging and longevity. Proteomics 18, 1700108.CrossRefGoogle ScholarPubMed
Bernales, S, McDonald, KL & Walter, P (2006). Autophagy counterbalances endoplasmic expansion during the unfolded protein response. PLoS Biol 4(12), e423.CrossRefGoogle ScholarPubMed
Biriuzova, VI & Rapoport, AI (1978). Kriofraktograficheskoe issledovanie struktury drozhzhevykh kletok, nakhodiashchikhsia v anabioticheskom sostoianii [Cryofractographic study of the structure of yeast cells found in an anabiotic state]. Mikrobiologiia 47(2), 300–305.Google Scholar
Broach, JR, Pringle, JR & Jones, EW (1991). The Molecular and Cellular Biology of the Yeast Saccharomyces. Cold Spring Harbor: Cold Spring Harbor Laboratry Press.Google Scholar
Bryant, NJ & Stevens, TH (1998). Vacuole biogenesis in Saccharomyces cerevisiae: Protein transport pathways to the yeast vacuole. Microbiol Mol Biol Rev 62(1), 230–247.CrossRefGoogle Scholar
Carmona-Gutierrez, D, Eisenberg, T, Büttner, S, Meisinger, C, Kroemer, G & Madeo, F (2010). Apoptosis in yeast: Triggers, pathways, subroutines. Cell Death Differ 17(5), 763–773.CrossRefGoogle ScholarPubMed
Chang, Y, Kong, Q, Shan, X, Tian, G, Ilieva, H, Cleveland, DW, Rothstein, JD, Borchelt, DR, Wong, PC & Lin, CL (2008). Messenger RNA oxidation occurs early in disease pathogenesis and promotes motor neuron degeneration in ALS. PLoS ONE 3, e2849.CrossRefGoogle ScholarPubMed
de Duve, C (1973). Biochemical studies on the occurrence, biogenesis, and life history of mammalian peroxisomes. J Histochem Cytochem 21, 941–948.CrossRefGoogle ScholarPubMed
Denoth Lippuner, A, Julou, T & Barral, Y (2014). Budding yeast as a model organism to study the effects of age. FEMS Microbiol Rev 38(2), 300–325.CrossRefGoogle Scholar
Dhalaria, R, Verma, R, Kumar, D, Puri, S, Tapwal, A, Kumar, V, Nepovimova, E & Kuca, K (2020). Bioactive compounds of edible fruits with their anti-aging properties: A comprehensive review to prolong human life. Antioxidants (Basel) 9(11), 1123.CrossRefGoogle ScholarPubMed
Georgieva, M, Moyankova, D, Djilianov, D, Uzunova, K & Miloshev, G (2015). Methanol extracts from the resurrection plant Haberlea rhodopensis ameliorate cellular vitality in chronologically ageing Saccharomyces cerevisiae cells. Biogerontology 16(4), 461–472.Google ScholarPubMed
Ghosh, G, Kar, DM, Subudhi, BB & Mishra, SK (2010). Antihyperglycemic and antioxidant activity of stem bark of Polyalthia longifolia var. angustifolia. Der Pharmacia Lettre 2(2), 206–216.Google Scholar
Haguenau, F, Hawkes, PW, Hutchison, JL, Satiat-Jeunemaître, B, Simon, GT & Williams, DB (2003). Key events in the history of electron microscopy. Microsc Microanal 9(2), 96–138.CrossRefGoogle ScholarPubMed
Halliwell, B & Gutteridge, JMC (2007). Free Radicals in Biology and Medicine. Oxford, USA: University Press.Google Scholar
Hecht, KA, O'Donnell, AF & Brodsky, JL (2014). The proteolytic landscape of the yeast vacuole. Cell Logist 4(1), e28023.CrossRefGoogle ScholarPubMed
Henderson, KA & Hughes, AL (2014). Mother-daughter asymmetry of pH underlies aging and rejuvenation in yeast. eLife 3, e03504.CrossRefGoogle ScholarPubMed
Hoepfner, D, Schildknegt, D, Braakman, I, Philippsen, P & Tabak, HF (2005). Contribution of the endoplasmic reticulum to peroxisome formation. Cell 122, 85–95.CrossRefGoogle ScholarPubMed
Hofer, T, Badouard, C, Bajak, E, Ravanat, JL, Mattsson, A & Cotgreave, IA (2005). Hydrogen peroxide causes greater oxidation in cellular RNA than in DNA. Biol Chem 386, 333–337.CrossRefGoogle ScholarPubMed
Hofer, T, Marzetti, E, Xu, J, Seo, AY, Gulec, S, Knutson, MD, Leeuwenburgh, C & Dupont-Versteegden, EE (2008). Increased iron content and RNA oxidative damage in skeletal muscle with aging and disuse atrophy. Exp Gerontol 43, 563–570.CrossRefGoogle ScholarPubMed
Hughes, AL & Gottschling, DE (2012). An early age increase in vacuolar pH limits mitochondrial function and lifespan in yeast. Nature 492, 261–265.CrossRefGoogle ScholarPubMed
Jones, EW, Webb, GC & Hiller, MA (1997). Biogenesis and function of the yeast vacuole. In Molecular Biology of the Yeast Saccharomyces cerevisiae, Pringle, JR, Broach, JR & Jones, EW (Eds.), Vol. III. pp. 363–469. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory PressGoogle Scholar
Jothy, SL, Aziz, A, Chen, Y & Sasidharan, S (2012). Antioxidant activity and hepatoprotective potential of Polyalthia longifolia and Cassia spectabilis leaves against paracetamol-induced liver injury. Evid Based Complement Alternat Med 2012, 561284.CrossRefGoogle ScholarPubMed
Jothy, SL, Chen, Y, Kanwar, JR & Sasidharan, S (2013). Evaluation of the genotoxic potential against H2O2-radical-mediated DNA damage and acute oral toxicity of standardized extract of Polyalthia longifolia leaf. Evid Based Complement Alternat Med 2013, 925380.CrossRefGoogle ScholarPubMed
Jothy, SL, Saito, T, Kanwar, JR, Chen, Y, Aziz, A, Yin-Hui, L & Sasidharan, S (2016). Radioprotective activity of Polyalthia longifolia standardized extract against X-ray radiation injury in mice. Phys Med 32, 150–161.CrossRefGoogle ScholarPubMed
Kaeberlein, M (2010). Lessons on longevity from budding yeast. Nature 464, 513–519.CrossRefGoogle ScholarPubMed
Katkar, KV, Suthar, AC & Chauhan, VS (2010). The chemistry, pharmacologic and therapeutic applications of Polyalthia longifolia. Pharmacogn Rev 4(7), 62–68.Google ScholarPubMed
Kuchitsu, K, Oh-hama, T, Tsuzuki, M & Miyachi, S (1987). Detection and characterization of acidic compartments (vacuoles) in Chlorella vulgaris 11 h cells by 31P-in vivo NMR spectroscopy and cytochemical techniques. Arch Microbiol 148, 83–87.CrossRefGoogle Scholar
Lasserre, JP, Dautant, A, Aiyar, RS, Kucharczyk, R, Glatigny, A, Tribouillard-Tanvier, D, Rytka, J, Blondel, M, Skoczen, N, Reynier, P, Pitayu, L, Rötig, A, Delahodde, A, Steinmetz, LM, Dujardin, G, Procaccio, V & di Rago, JP (2015). Yeast as a system for modeling mitochondrial disease mechanisms and discovering therapies. Dis Model Mech 8(6), 509–526.CrossRefGoogle ScholarPubMed
Li, SC & Kane, PM (2009). The yeast lysosome-like vacuole: Endpoint and crossroads. Biochim Biophys Acta Mol Cell Res 1793, 650–663.CrossRefGoogle ScholarPubMed
Liu, W, Li, L, Ye, H, Chen, H, Shen, W, Zhong, Y, Tian, T & He, H (2017). From saccharomyces cerevisiae to human: The important gene co-expression modules. Biomed Rep 7, 153–158.CrossRefGoogle ScholarPubMed
Longo, VD & Fabrizio, P (2002). Regulation of longevity and stress resistance: A molecular strategy conserved from yeast to humans? Cell Mol Life Sci 59(6), 903–908.CrossRefGoogle ScholarPubMed
Longo, VD, Shadel, GS, Kaeberlein, M & Kennedy, B (2012). Replicative and chronological aging in Saccharomyces cerevisiae. Cell Metab 16(1), 18–31.CrossRefGoogle ScholarPubMed
Marques, M, Mojzita, D, Amorim, MA, Almeida, T, Hohmann, S, Moradas-Ferreira, P & Costa, V (2006). The Pep4p vacuolar proteinase contributes to the turnover of oxidized proteins but PEP4 overexpression is not sufficient to increase chronological lifespan in Saccharomyces cerevisiae. Microbiology 152, 3595–3605.CrossRefGoogle Scholar
Minois, N, Frajnt, M, Wilson, C & Vaupel, JW (2005). Advances in measuring lifespan in the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A 102, 402–406.CrossRefGoogle ScholarPubMed
Molon, M, Panek, A, Molestak, E, Skoneczny, M, Tchorzewski, M & Wnuk, M (2018). Daughters of the budding yeast from old mothers have shorter replicative lifespans but not total lifespans. Are DNA damage and rDNA instability the factors that determine longevity? Cell Cycle 17, 1173–1187.CrossRefGoogle Scholar
Molon, M & Zebrowski, J (2017). Phylogenetic relationship and Fourier-transform infrared spectroscopy-derived lipid determinants of lifespan parameters in the Saccharomyces cerevisiae yeast. FEMS Yeast Res 17, fox031.Google ScholarPubMed
Mortimer, RK & Johnston, JR (1959). Life span of individual yeast cells. Nature 183, 1751–1752.CrossRefGoogle ScholarPubMed
Nunomura, A, Moreira, PI, Castellani, RJ, Lee, HG, Zhu, X, Smith, MA & Perry, G (2012). Oxidative damage to RNA in aging and neurodegenerative disorders. Neurotox Res 22, 231–248.CrossRefGoogle ScholarPubMed
Ohtani, M, Saka, A, Sano, F, Ohya, Y & Morishita, S (2004). Development of image processing program for yeast cell morphology. J Bioinform Comput Biol 1(4), 695–709.CrossRefGoogle ScholarPubMed
Ohya, Y, Sese, J, Yukawa, M, Sano, F, Nakatani, Y, Saito, TL, Saka, A, Fukuda, T, Ishihara, S, Oka, S, Suzuki, G, Watanabe, M, Hirata, A, Ohtani, M, Sawai, H, Fraysse, N, Latgé, JP, François, JM, Aebi, M, Tanaka, S, Muramatsu, S, Araki, H, Sonoike, K, Nogami, S & Morishita, S (2005). High-dimensional and large-scale phenotyping of yeast mutants. Proc Natl Acad Sci U S A 102(52), 19015–19020.CrossRefGoogle ScholarPubMed
Pandey, KB & Rizvi, SI (2009). Plant polyphenols as dietary antioxidants in human health and disease. Oxid Med Cell Longev 2(5), 270–278.CrossRefGoogle ScholarPubMed
Pereira, C, Bessa, C & Saraiva, L (2012). Endocytosis inhibition during H2O2-induced apoptosis in yeast. FEMS Yeast Res 12, 755–760.CrossRefGoogle ScholarPubMed
Pretorius, A, Yamaguchi, T, Kübel, C, Kröger, R, Hommel, D & Rosenauer, A (2006). TEM analyses of wurtzite InGaN islands grown by MOVPE and MBE. Curr Top Solid State Phys 3(6), 1679–1682.Google Scholar
Schuck, S, Gallagher, CM & Walter, P (2014). ER-phagy mediates selective degradation of endoplasmic reticulum independently of the core autophagy machinery. J Cell Sci 127, 4078–4088.Google ScholarPubMed
Stadtländer, CTK-H (2007). Scanning electron microscopy and transmission electron microscopy of Mollicutes, challenges and opportunities. In Modern Research and Educational Topics in Microscopy, Méndez-Vilas, A & Díaz, J (Eds.), pp. 122–131. Badajoz, Spain: Formatex.Google Scholar
Starborg, T & Kadler, KE (2015). Serial block face-scanning electron microscopy, A tool for studying embryonic development at the cell–matrix interface. Birth Defects Res C Embryo Today 105(1), 9–18.CrossRefGoogle ScholarPubMed
Stępień, K, Wojdyła, D, Nowak, K & Mołoń, M (2020). Impact of curcumin on replicative and chronological aging in the Saccharomyces cerevisiae yeast. Biogerontology 21(1), 109–123.CrossRefGoogle ScholarPubMed
Unwin, PNT & Ennis, PD (1984). Two configurations of a channel-forming membrane protein. Nature 307, 609–613.CrossRefGoogle ScholarPubMed
Unwin, PNT & Zampighi, G (1980). Structure of the junction between communicating cells. Nature 283, 545–549.CrossRefGoogle ScholarPubMed
van Tendeloo, G, Bals, S, Van Aert, S, Verbeeck, J & Van Dyck, D (2012). Advanced electron microscopy for advanced materials. Adv Mater 24(42), 5655–5675.CrossRefGoogle ScholarPubMed
Venditti, P & Di Meo, S (2020). The role of reactive oxygen species in the life cycle of the mitochondrion. Int J Mol Sci 21(6), 2173.CrossRefGoogle ScholarPubMed
Vijayarathna, S (2016). Fundamental studies of the mechanism of action of Polyalthia longifolia polyphenolics in HeLa cells in relation to microRNA regulation, Dissertation. Universiti Sains Malaysia.Google Scholar
Vijayarathna, S, Oon, CE, Chen, Y, Kanwar, JR & Sasidharan, S (2017). Polyalthia longifolia methanolic leaf extracts (PLME) induce apoptosis, cell cycle arrest and mitochondrial potential depolarization by possibly modulating the redox status in hela cells. Biomed Pharmacother 89, 499–514.CrossRefGoogle ScholarPubMed
Yalcin, G & Lee, CK (2019). Recent studies on anti-aging compounds with Saccharomyces cerevisiae as a model organism. Transl Med Aging 3, 109–115.CrossRefGoogle Scholar
Zadrag, R, Bartosz, G & Bilinski, T (2008). Is the yeast a relevant model for aging of multicellular organisms? An insight-from the total lifespan of Saccharomyces cerevisiae. Curr Aging Sci 1(3), 159–165.CrossRefGoogle ScholarPubMed
Zakeri, Z, Bursch, W, Tenniswood, M & Lockson, RA (1995). Cell death: Programmed, apoptosis, necrosis, or other? Cell Death Differ 2, 87–96.Google ScholarPubMed