Effect of Sorbic Acid on the Induction of Static Growth Inhibition in Mouse Mastocytoma P-815 Cells
Main Article Content
Abstract
Sorbic acid and its salts are commonly used as preservatives because of their ability to inhibit the growth of molds, yeasts, and fungi without causing bacterial death. Despite several investigations on sorbic acid-induced static growth inhibition of microorganisms, its implications in mammals remain unexplored. This study investigated the effect of sorbic acid on the growth of mouse mastocytoma P-815 cells (P-815 cells) in culture medium. Our findings indicated that sorbic acid induced static growth inhibition, with optimal results achieved when P-815 cells were exposed to 2.5 mM sorbic acid for at least 48 h, starting approximately 20 h after administration. Notably, the same static growth inhibition by sorbic acid was observed in human promyelocytic leukemia cells but not in mouse bone marrow mast cells. Sorbic acid-induced static growth inhibition increased the number of cells in the G1 and G2 phases and decreased the number of cells in the S phase, demonstrating that sorbic acid affects the cell cycle's G1/S and G2/M transitions. When P-815 cells synchronized at the G1 phase of the cell cycle were treated with sorbic acid, the onset of the cell population was noticeably delayed, whereas S-phase cells revealed almost no delay. The cellular amount of sorbic acid 10 h post-administration was higher in the acidic medium (pH 7.0) than in the medium (pH 7.4), which can be attributed to the inhibition of extracellular release of sorbic acid. Verapamil, a modulator of P-glycoprotein, and sodium azide, an inhibitor of ATP synthesis, inhibited intracellular accumulation of sorbic acid. This suggests that P-glycoprotein plays a role in regulating the intracellular levels of sorbic acid. Administration of sorbic acid led to an increase in intracellular calcium concentration ([Ca2+]i), which was suppressed by co-administration with verapamil. Sorbic acid administration decreased the [Ca2+]i levels, which were elevated by thapsigargin, an inhibitor of Ca2+-ATPase in the ER. This inhibitory effect was observed regardless of whether thapsigargin was administered before or after treatment. This is the first study to report that sorbic acid has a static growth inhibitory effect, causing stagnation in the G1 phase in animal cancer cells such as P-815 cells. The primary mechanism involves suppression of thapsigargin-induced intracellular Ca2+ release from Ca2+ stores in the ER.
Keywords:
sorbic acid, static growth inhibition, mastocytoma P-815 cells, cell cycle dependency, intracellular Ca2 concentration
Article Details
How to Cite
OKADA, Yasuyo et al.
Effect of Sorbic Acid on the Induction of Static Growth Inhibition in Mouse Mastocytoma P-815 Cells.
Medical Research Archives, [S.l.], v. 12, n. 9, sep. 2024.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/5642>. Date accessed: 23 nov. 2024.
doi: https://doi.org/10.18103/mra.v12i9.5642.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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23. Stratford M, Anslow PA. Evidence that sorbic acid does not inhibit yeast as a classic weak acid preservative. Lett Appl Microbiol. 1998;27(4):203-6. doi: 10.101046/j.1472-765x.1998.00424.x.
24. Bracy D, Holyoak CD, Coote PJ. Comparison of the inhibitory effect of sorbic acid and amphotericin B on Saccharomyces cerevisiae: is growth inhibition dependent on reduced intracellular pH?. Appl Microbiol. 1998;85(6):1056-66. doi:10.1111/j.1365-2672.1998.tb05271.x.
25. Doyen D, Poet M, Jarretou G, Pisani DF, Tauc M, Cougnon M, Argentina M, Bouret Y, Counillon L. Intracellular pH control by membrane transport in mammalian cells. Insights into the selective advantages of functional redundancy. Front Mol Biosci. 2022:9:825028. doi:10.3389/fmolb.2022.825028.
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27. Okada Y, Ueyama K, Nishikawa J, semma M, Ichikawa A. Effect of 6-O-α-maltosyl-β cyclodextrin and its cholesterol inclusion complex on cellular cholesterol levels and ABCA1 and ABCG1 expression in mouse mastocytoma P-815 cells. Carbohydrate Res. 2012;357:68-74. doi:10.1016/j.carres.2012.04.019.
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doi:10.1016/s0090-6980(98)00051-3.
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2. Bracey D, Holyoak CD, Coote PJ. Comparison of the inhibitory effect of sorbic acid and amphotericin B on Saccharomyces cerevisiae: is growth inhibition dependent on reduced intracellular pH?. J Appl Microbiol. 1998;85(6):1056–66. doi:10.1111/j.1365-2672.
3. Holyoak CD, Stratford M, McMullin Z, Cole MB, Crimmins K, Brown AJ, Coote PJ. Activity of the plasma membrane H+-ATPase and optimal glycolytic flux are required for rapid adaptation and growth of Saccharomyces cerevisiae in the presence of the weak-acid preservative sorbic acid. Appl Environ Microbiol. 1996;62(9):3158-64. doi:10.1128/aem.62.9.3158-3164.1996.
4. Sofos JN, Busta FF, Allen CE. Sodium nitrite and sorbic acid effects on Clostridium botulinum spore germination and total microbial growth in chicken frankfurter emulsions during temperature abuse. Appl Environ Microbiol. 1979;37(6):1103-9. doi:10.1128/aem.37.6.
5. Ronning IE, Frank HA. Growth inhibition of putrefactive anaerobe 3679 caused by stringent-type response induced by protonophoric activity of sorbic acid. Appl Environ Microbiol. 1987;53(5):1020-7. doi:10.1128/aem.53.5.1020-1027.1987.
6. Sun R, Vermeulen A, Devlieghere F. Modeling the combined effect of temperature, pH, acetic and lactic acid concentrations on the growth/no growth interface of acid-tolerant Bacillus spores. Int J Food Microbiol. 2021; 360:109419. doi: 10.1016/j.ijfoodmicro.
7. Wang Q, Peng Y, Chai L, Ding W. Antimicrobial effect of sorbic acid-loaded chitosan/ tripolyphosphate nanoparticles on Pseudomonas aeruginosa. Int J Biol Macromol. 2023; 226:1031-40. doi:10.1016/j.ijbiomac:2022.11.220.
8. Stratford M, Vallières C, Geoghegan IA, Archer DB, Avery SV. The preservative sorbic acid targets respiration, explaining the resistance of fermentative spoilage Yeast species. mSphere. 2020;5(3):e00273-20.
doi: 10.1128/mSphere.00273-20.
9. Stratford M, Nebe-von-Caron G, Steels H, Novodvorska M, Ueckert J, Archer DB. Weak-acid preservatives: pH and proton movements in the yeast Saccharomyces cerevisiae. Int J Food Microbiol. 2013;161(3):164-71. doi:10.1016/j.ijfoodmicro.2012.12.013.
10. Ullah A, Chandrasekaran G, Brul S, Smits GJ. Yeast adaptation to weak acids prevents futile energy expenditure. Front Microbiol. 2013;4:142. doi: 10.3389/fmicb.2013.00142.
11. Younes M, Aquilina G, Castle L, Engel KH, Fowler P, Jose M, Fernandez F, Fürst P, Gürtler R, Gundert-Remy U, Husøy T, Mennes W, Moldeus P, Oskarsson A, Shah R, Wölfle D, Lambré C, Christodoulidou A, Waalkens-Berendsen I. Opinion on the follow-up of the re-evaluation of sorbic acid (E200) and potassium sorbate (E202) as food additives. EFSA J. 2019;17(3):e05625. doi:10.2903/j.efsa.2019.5625.
12. Nemes D, Kovács R, Nagy F, Tóth Z, Herczegh P, Borbás A, Kelemen V, Pfliegler WP, Rebenku I, Hajdu PB, Fehér P, Ujhelyi Z, Fenyvesi F, Váradi J, Vecsernyés M, Bácskay II. Comparative biocompatibility and antimictobial studies of sorbic acid derivatives. Eur J Pharm Sci. 2020;143:105162. doi:10.1016/j.ejps.2019.105162.
13. Aguilar F, Crebelli R, Domenico AD, Dusemund B, Frutos MJ, Galtier P, Gott D, Gundert-Remy U, Lambré C, Leblanc JC, Lindtner O, Moldeus P, Mortensen A, Mosesso P, Parent-Massin D, Oskarsson A, Stankovic I, Waalkens-Berendsen I, Woutersen RA, Wright M, Younes M. Scientific opinion on the re-evaluation of sorbic acid (E200), potassium sorbate (E202) and calcium sorbate (E203) as food additives. EFSA J. 2015;13(6):4144, 28pp. doi:10.2903/j.efsa.2015.4144.
14. Winkler C, Frick B, Schroecksnadel K, Schennach H, Fuchs D. Food preservatives such as sodium sulfite and sorbic acid suppress mitogen-stimulated peripheral blood mononuclear cells. Food Chem Toxicol. 2006;44(12):2003-7. doi:10.1016/j.fct.2006.06.019.
15. Munzer R, Guigas C, Renner HW. Re-examination of potassium and sodium sorbates for their possible genotoxic potential. Food Chem Toxicol. 1990;28(6):397-401. doi:10.1016/0278-6915(90)90085-2.
16. Ferrand C, Mark F, Cassand P, Saint Blanqut G. Mutagenicity and genotoxicity of sorbic acid-amine reaction products. Toxicol In Vitro. 2000;14(5):423-8. doi:10.1016/s0887-2333(00)00035-7.
17. Perez-Prior MT, Manso JA, del Pilasr Carcia-Santos M, Calle E, Casado J. Alkylating potential of potassium sorbate. J Agric Food Chem. 2005;53(26):10244-7. doi:10.1021/jf052152p.
18. Muller S, Sanders DA, Antonio MD, Matsis S, Riou JF, Rodriguez R, Balasubramanian S. Pyridostatin analogues promote telomere dysfunction and long-term growth inhibition in human cancer cells. Org Biomol Chem. 2012;10(32):6537-46. doi:10.1039/c2ob25830g.
19. Wiecek AJ, Cutty SJ, Kornai D, Parreno-Centteno M, Gourmet LE, Tagliazucchi GM, Jacobson DH, Zhang P, Xiong L, Bond GL, Barr AR, Secrier M. Genomic hallmarks and therapeutic implications of G0 cell cycle arrest in cancer. Genome Biology, 2023;24(1):128.
doi:10.1186/s13059-023-02963-4.
20. Ichikawa A, Negishi M, Tomita K, Ikegami S. Aphidicolin: A specific inhibitor of DNA synthesis in synchronous mastocytoma P-815 cells. Jpn J Pharmacol. 1980; 30(3): 301-8. doi:10.1254/jjp.30.301.
21. Ullah A, Orij R, Brul S, Smits GJ. Quantitative analysis of the modes of growth inhibition by weak acids in Saccharomyces cerevisiae. Appl Environ Microbiol. 2012;78(23):8377-87. doi:10:1128/AME.02126-12.
22. Zilberstein D, Agmon V, Schuldiner S, Paden E. Esherichia coli intracellular pH, membrane potential, and cell growth. J Bacteriol. 1984;158(1):246-52 doi:10.1128/jb.158.1.246-252.1984.
23. Stratford M, Anslow PA. Evidence that sorbic acid does not inhibit yeast as a classic weak acid preservative. Lett Appl Microbiol. 1998;27(4):203-6. doi: 10.101046/j.1472-765x.1998.00424.x.
24. Bracy D, Holyoak CD, Coote PJ. Comparison of the inhibitory effect of sorbic acid and amphotericin B on Saccharomyces cerevisiae: is growth inhibition dependent on reduced intracellular pH?. Appl Microbiol. 1998;85(6):1056-66. doi:10.1111/j.1365-2672.1998.tb05271.x.
25. Doyen D, Poet M, Jarretou G, Pisani DF, Tauc M, Cougnon M, Argentina M, Bouret Y, Counillon L. Intracellular pH control by membrane transport in mammalian cells. Insights into the selective advantages of functional redundancy. Front Mol Biosci. 2022:9:825028. doi:10.3389/fmolb.2022.825028.
26. Quesada I, Chin WC, Verdugo P. ATP-independent luminal oscillations and release of Ca2+ and H+ from mast cell secretory granules:implication for signal transduction. Biophys J. 2003;85(2):963-70. doi:10.1016/S0006-3495(03)74535-4.
27. Okada Y, Ueyama K, Nishikawa J, semma M, Ichikawa A. Effect of 6-O-α-maltosyl-β cyclodextrin and its cholesterol inclusion complex on cellular cholesterol levels and ABCA1 and ABCG1 expression in mouse mastocytoma P-815 cells. Carbohydrate Res. 2012;357:68-74. doi:10.1016/j.carres.2012.04.019.
28. Ishiguro S, Takahashi N, Nemoto K, Negishi M, Ichikawa A. Potentiation of retinoic acid-induced differentiation of HL-60 cells by prostaglandin EP2 receptor. Prostaglandins Other Lipid Mediat. 1998;56(2-3):145-53.
doi:10.1016/s0090-6980(98)00051-3.
29. Tanaka S, Mikura S, Hashimoto E, Sugimoto Y, Ichikawa A. Ca2+ influx-mediated histamine synthesis and IL-6 release in mast cells activated by monomeric IgE. Eur J Immunol. 2005;35(2):460-8. doi:10.1002/eji.200425622.
30. Han DW, Lee MH, Kim HH, Hyon SH, Park JC. Epigallocatechin-3-gallate regulates cell growth, cell cycle and phosphorylated nuclear factor-kB in human dermal fibroblast. Acta Pharmacol Sin. 2011;32:637-46. doi:10.1038/aps.2011.17.
31. Horiyama S, Honda C, Suwa K, Okada Y, Semma M, Ichikawa A, Takayama M, Negative and positive ion mode LC/MS/MS for sample, selective analysis of sorbic acid. Chem Pharm Bull. 2010; 58(1): 106-9. doi:10.1248/cpb.58.106.
32. Thomas JA, Buchsbaum RN, Zimniak A, Racker E. Intracellular pH measurement in Ehrlichascites tumpr cells utilizing spectroscopic probes generated in situ. Biochemistry. 1979;18(11): 2210-18. doi:10.1021/bi00578a012.
33. Tanaka S, Takasu Y, Mikura S, Satoh N, Ichikawa A. Antigen-independent induction of histamine synthesis by immunoglobulin E in mouse bone marrow-derived mast cells. J Exp Med. 2002;196(2):229-35. doi:10.1084/jem.20012037.
34. Sharom, FJ. The P-glycoprotein efflux pump: how does it transport drugs? Membrane Biol. 1997;160:161-75. doi:10.1007/s002329900305.
35. Legend A, Cerrina J, Bonne C, Lockhart A, Benveniste J. Inhibition of rat mast cell degranulation by verapamil. Agents Actions. 1984;14(2):153-6. doi:10.1007/BF01966635.
36. Salmond CV, Kroll RG, Booth IR. The effect of food preservatives on the pH homeostasis in Escherichia coli. J Gen Microbiol. 1984;130:2845-50. doi: 10.1099/00221287-130-11-2845.
37. Schreiber R. Ca2+ signaling, intracellular pH and cell volume in cell proliferation. J Membr Biol. 2005;205(3):129-37. doi:10.1007/s00232-005-0778-z.
38. Holyak CD, Stratford M, McMulin Z, Cole MB, Klimmins K, Brown, AJ. Coote PJ. Activity of the plasma membrane H+-ATPase and optimal glycolytic flux are required for rapid adaptation and growth of Saccharomyces cerevisiae in the presence of the weak-acid preservative sorbic acid. Appl Environ Microbiol. 1996;62(9):3158-64. doi:10.1128/aem.62.9.3164.1996
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