Abstract
Mannosylerythritol lipids have drawn attention to cosmetic and pharmaceutical industries due to their non-toxicity and excellent biological interactions with human skin, particularly with the deepest epidermal layer. Lamellar liquid crystal structure, formed by MEL-B, is an interesting feature due to its similarity to the stratum corneum molecular arrangement and cell signaling events involved in the deregulation of the cancerous cell membrane. Thus, this work aimed to evaluate the cytotoxicity of commercial mannosylerythritol lipids-B in murine melanoma, fibroblast, and human erythrocytes cells. Cytotoxic effect was more pronounced on the tumor cells from 20 µg/mL, reducing cell viability by 65%, whereas fibroblast and human erythrocytes cells were more resistant to glycolipid treatment. Fluorescence microscopy and flow cytometer proved that mannosylerythritol lipids-B is an apoptosis inducer in tumor cells related to reactive oxygen species generation.
References
Adu, S. A., Naughton, P. J., Marchant, R., & Banat, I. M. (2020). Microbial biosurfactants in cosmetic and personal skincare pharmaceutical formulations. Pharmaceutics, 12, 1099. https://doi.org/10.3390/pharmaceutics12111099.
Aggarwal, V., Tuli, H. S., Varol, A., Thakral, F., Yerer, M. B., Sak, K., Varol, M., Jain, A., Khan, M. A., & Sethi, G. (2019). Role of reactive oxygen species in cancer progression: Molecular mechanisms and recent advancements. Biomolecules, 9(11), 735. https://doi.org/10.3390/biom9110735.
Albanese, A., Tang, P. S., & Chan, W. C. (2012). The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annual Review of Biomedical Engineering, 14, 1–16. https://doi.org/10.1146/annurev-bioeng-071811-150124.
Bae, I. H., Lee, E. S., Yoo, J. W., Lee, S. H., Ko, J. Y., Kim, Y. J., Lee, T. R., Kim, D. Y., & Lee, C. S. (2019). Mannosylerythritol lipids inhibit melanogenesis via suppressing ERK-CREB-MiTF-tyrosinase signalling in normal human melanocytes and a three-dimensional human skin equivalent. Experimental Dermatology, 28, 738–741. https://doi.org/10.1111/exd.13836
Bae, I. H., Lee, S. H., Oh, S., Choi, H., Marinho, P. A., Yoo, J. W., Ko, J. Y., Lee, E. S., Lee, T. R., Lee, C. S., & Kim, D. Y. (2019). Mannosylerythritol lipids ameliorate ultraviolet A-induced aquaporin-3 downregulation by suppressing c-Jun N-terminal kinase phosphorylation in cultured human keratinocytes. The Korean Journal of Physiology and Pharmacology, 23, 113–120. https://doi.org/10.4196/kjpp.2019.23.2.113.
Binot, C., Sadoc, J. F., & Chouard, O. H. (2018). Oncogenesis, lipids rafts and liquid crystals: A nanoscopic supplementary field for applied researches and a new hope of advances in cancer. Heliyon, 4, e00687. https://doi.org/10.1016/j.heliyon.2018.e00687
Biswas, S. K. (2016). Does the interdependence between oxidative stress and inflammation explain the antioxidant paradox? Oxidative Medicine and Cellular Longevity. 2016. https://doi.org/10.1155/2016/5698931.
Choi, J., Reipa, V., Hitchins, V. M., Goering, P. L., & Malinauskas, R. A. (2011). Physicochemical characterization and in vitro hemolysis evaluation of silver nanoparticles. Toxicological Sciences, 123, 133–143. https://doi.org/10.1093/toxsci/kfr149.
Coelho, A. L. S., Feuser, P. E., Carciofi, B. A. M., Andrade, C. J., & Oliveira, D. (2020). Mannosylerythritol lipids: Antimicrobial and biomedical properties. Applied Microbiology and Biotechnology, 104, 2297–2318. https://doi.org/10.1007/s00253-020-10354-z.
Collins, A., Dušinská, M., Franklin, M., Somorovská, M., Petrovská, H., Duthie, S., Fillion, L., Panayiotidis, M., Rašlová, K., & Vaughan, N. (1997). Comet assay in human biomonitoring studies: Reliability, validation, and applications. Environmental and Molecular Mutagenesis, 30, 139–146. https://doi.org/10.1002/(SICI)1098-2280(1997)30:2%3c139::AID-EM6%3e3.0.CO;2-I.
Fan, L., Li, H., Niu, Y., & Chen, Q. (2016). Characterization and inducing melanoma cell apoptosis activity of mannosylerythritol lipids-A produced from Pseudozyma aphidis. PLoS ONE, 11, e0148198. https://doi.org/10.1371/journal.pone.0148198.
Feuser, P. E., dos Santos, B. L., dos Santos Silva, M. C., da Cas, V. A., Fernandes, A. C., Ricci-Junior, E., Nele, M., Tedesco, A. C., Sayer, C., & de Araújo, P. H. H. (2015). Encapsulation of magnetic nanoparticles in poly (methyl methacrylate) by miniemulsion and evaluation of hyperthermia in U87MG cells. European Polymer Journal, 68, 355–365. https://doi.org/10.1016/j.eurpolymj.2015.04.029.
Feuser, P. E., Gaspar, P. C., Jacques, A. V., Tedesco, A. C., dos Santos Silva, M. C., Ricci-Júnior, E., Sayer, C., & de Araújo, P. H. H. (2016). Synthesis of ZnPc loaded poly (methyl methacrylate) nanoparticles via miniemulsion polymerization for photodynamic therapy in leukemic cells. Materials Science and Engineering C, 60, 458–466. https://doi.org/10.1016/j.msec.2015.11.063.
Fornaguera, C., Calderó, G., Mitjans, M., Vinardell, M. P., Solans, C., & Vauthier, C. (2015). Interactions of PLGA nanoparticles with blood components: protein adsorption, coagulation, activation of the complement system and hemolysis studies. Nanoescale, 7, 6045–6058. https://doi.org/10.1039/C5NR00733.
Galvani, N. C., Vilela, T. C., Domingos, A. C., Fagundes, M. Í., Bosa, L. M., Della Vechia, I. C., Scussel, R., Pereira, M., Steiner, B. T., Damiani, A. P., Chávez-Olórtegui, C., Andrade, V. M., & Machado-deÁvila, R. A. (2017). Genotoxicity evaluation induced by Tityus serrulatus scorpion venom in mice. Toxicon, 140, 132–138. https://doi.org/10.1016/j.toxicon.2017.10.024.
Govindarajan, M. (2018). Amphiphilic glycoconjugates as potential anticancer chemotherapeutics. European Journal of Medicinal Chemistry, 143, 1208–1253. https://doi.org/10.1016/j.ejmech.2017.10.015.
Gudiña, E. J., Rangarajan, V., Sen, R., & Rodrigues, L. R. (2013). Potential therapeutic applications of biosurfactants. Trends in Pharmacological Sciences, 34, 667–675. https://doi.org/10.1016/j.tips.2013.10.002.
Haque, F., Khan, M. A. S., & Al-Qurashi, N. (2021). ROS-mediated necrosis by glycolipid biosurfactants on lung, breast, and skin melanoma cells. Frontiers in Oncology, 11, 253. https://doi.org/10.3389/fonc2021622470.
Isoda, H., Kitamoto, D., Shinmoto, H., Matsumura, M., & Nakahara, T. (1997). Microbial extracellular glycolipid induction of differentiation and inhibition of the protein kinase C activity of human promyelocytic leukemia cell line HL60. Bioscience, Biotechnology, and Biochemistry, 61, 609–614. https://doi.org/10.1271/bbb.61.609.
Khazaei, Z., Ghorat, F., Jarrahi, A. M., Adineh, H. A., Sohrabivafa, M., & Goodarzi, E. (2019). Global incidence and mortality of skin cancer by histological subtype and its relationship with the human development index (HDI); an ecology study in 2018. World Cancer Research Journal, 6, e13.
Krishnaraj, C., Muthukumaran, P., Ramachandran, R., Balakumaran, M. D., & Kalaichelvan, P. T. (2014). Acalypha indica Linn: Biogenic synthesis of silver and gold nanoparticles and their cytotoxic effects against MDA-MB-231, human breast cancer cells. Biotechnology Reports, 4, 42–49. https://doi.org/10.1016/j.btre.2014.08.002.
Liou, G. Y., & Storz, P. (2010). Reactive oxygen species in cancer. Free Radical Research, 44, 479–496. https://doi.org/10.3109/10715761003667554.
Liu, Q., Das, M., Liu, Y., & Huang, L. (2018). Targeted drug delivery to melanoma. Advanced Drug Delivery Reviews, 127, 208–221. https://doi.org/10.1016/j.addr.2017.09.016.
Morita, T., Fukuoka, T., Imura, T., & Kitamoto, D. (2013). Production of mannosylerythritol lipids and their application in cosmetics. Applied Microbiology and Biotechnology, 97, 4691–4700. https://doi.org/10.1007/s0025301348581.
Morita, T., Ishibashi, Y., Hirose, N., Wada, K., Takahashi, M., Fukuoka, T., Imura, T., Sakai, H., Masahiko, A. B. E., & Dai Kitamoto, D. (2011). Production and characterization of a glycolipid biosurfactant, mannosylerythritol lipid B, from sugarcane juice by Ustilago scitaminea NBRC 32730. Bioscience, Biotechnology, and Biochemistry, 75(7), 1371–1376. https://doi.org/10.1271/bbb.110221.
Morita, T., Kitagawa, M., Suzuki, M., Yamamoto, S., Sogabe, A., Yanagidani, S., Imura, T., Fukuoka, T., & Kitamoto, D. (2009). A yeast glycolipid biosurfactant, mannosylerythritol lipid, shows potential moisturizing activity toward cultured human skin cells: the recovery effect of MEL-A on the SDS-damaged human skin cells. Journal of Oleo Science, 58, 639-642.l.
Naughton, P. J., Marchant, R., Naughton, V., & Banat, I. M. (2019). Microbial biosurfactants: Current trends and applications in agricultural and biomedical industries. Journal of Applied Microbiology, 127, 12–28. https://doi.org/10.1111/jam.14243.
Onwosi, C. O., Aliyu, G. O., Onu, C. J., Chukwu, K. O., Ndukwe, J. K., & Igbokwe, V. C. (2021). Microbial-derived glycolipids in the sustainable formulation of biomedical and personal care products: A consideration of the process economics towards commercialization. Process Biochemistry, 100, 124–139. https://doi.org/10.1016/j.procbio202010001.
Perillo, B., Di Donato, M., Pezone, A., Di Zazzo, E., Giovannelli, P., Galasso, G., Castoria, G., Migliaccio, A. (2020). ROS in cancer therapy: the bright side of the moon. Experimental and Molecular Medicine, 1-12. https://doi.org/10.1038/s12276-020-0384-2.
Pisoschi, A. M., & Pop, A. (2015). The role of antioxidants in the chemistry of oxidative stress: A review. European Journal of Medicinal Chemistry, 97, 55–74. https://doi.org/10.1016/j.ejmech.2015.04.040.
Rofeal, M., & El-Malek, F. A. (2021). Valorization of lipopeptides biosurfactants as anticancer agents. International Journal of Peptide Research and Therapeutics, 27, 447–455. https://doi.org/10.1007/s10989020101058.
Sakr, E. A., Ahmed, H. A. E., & Saif, F. A. A. (2021). Characterization of low-cost glycolipoprotein biosurfactant produced by Lactobacillus plantarum 60 FHE isolated from cheese samples using food wastes through response surface methodology and its potential as antimicrobial, antiviral, and anticancer activities. International Journal of Biological Macromolecules, 170, 94–106. https://doi.org/10.1016/j.ijbiomac202012140.
Tice, R. R., Agurell, E., Anderson, D., Burlinson, B., Hartmann, A., Kobayashi, H., Mayamae, Y., Rojas, E., Ryu, J. C., & Sasaki, Y. F. (2000). Single cell gel/comet assay: Guidelines for in vitro and in vivo genetic toxicology testing. Environmental and Molecular Mutagenesis, 35, 206–221. https://doi.org/10.1002/(SICI)1098-2280(2000)35:3%3c206::AID-EM8%3e3.0.CO;2-J.
Tokudome, Y., & Tsukiji, H. (2020). Mannosylerythritol lipid B enhances the skin pemeability of the water-soluble compound calcein via OH stretching vibration changes. Colloids Interfaces, 4, 10. https://doi.org/10.3390/colloids4010010.
Upadhyay, P. R., Ho, T., & Abdel-Malek, Z. A. (2021). participation of keratinocyte and fibroblast derived factor in melanocyte homeostasis, the response to UV, and pigmentary disorders. Pigment Cell and Melanoma Research, 0, 1–15. https://doi.org/10.1111/pcmr.12985.
Worakitkanchanakul, W., Imura, T., Fukuoka, T., Morita, T., Sakai, H., Abe, M., Rujiravanit, R., Chavadej, S., Minamikawa, H., & Kitamoto, D. (2008). Aqueous-phase behavior and vesicle formation of natural glycolipid biosurfactant, mannosylerythritol lipid-B. Colloids and Surfaces B, 65, 106–112. https://doi.org/10.1016/j.colsurfb.2008.03.009.
Yamamoto, S., Morita, T., Fukuoka, T., Imura, T., Yanagidani, S., Sogabe, A., Kitamoto, D., & Kitagawa, M. (2012). The moisturizing effects of glycolipid biosurfactants, mannosylerythritol lipids, on human skin. Journal of Oleo Science, 61, 407–412. https://doi.org/10.5650/jos.61.407.
Zaragoza, A., Aranda, F. J., Espuny, M. J., Teruel, J. Á., Marqués, A., Manresa, A., & Ortiz, A. (2010). Hemolytic activity of a bacterial trehalose lipid biosurfactant produced by Rhodococcus sp. evidence for a colloid-osmotic mechanism. Langmuir, 26, 8567–8672. https://doi.org/10.1021/la904637k.
Zhao, X., Geltinger, C., Kishikawa, S., Ohshima, K., Murata, T., Nomura, N., Nakahara, T., & Yokoyama, K. K. (1999). Treatment of mouse melanoma cells with phorbol 12-myristate 13-acetate counteracts mannosylerythritol lipid-induced growth arrest and apoptosis. Cytotechnology, 33, 123–130. https://doi.org/10.1023/A:1008129616127.
Zhao, X., Murata, T., Ohno, S., Day, N., Song, J., Nomura, N., Nakahara, T., & Yokoyama, K. K. (2002). Protein kinase Cα plays a critical role in mannosylerythritol lipid-induced differentiation of melanoma B16 cells. Journal of Biological Chemistry, 276, 39903–39910. https://doi.org/10.1074/jbc.M010281200.
Acknowledgements
The authors are grateful to CAPES-PRINT, Projects numbers 88887.310560/2018-00 and 88887.310373/2018-00, and also PNPD-CAPES (Process number 88882.316483/2019-01) and PROEX-CAPES (Process number 88882.345312/2019-01) for the scholarships. We also thank TOYOBO Co., Ltd for kindly providing MEL-B.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics Approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Competing Interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Feuser, P.E., Coelho, A.L.S., de Melo, M.E. et al. Apoptosis Induction in Murine Melanoma (B16F10) Cells by Mannosylerythritol Lipids-B; a Glycolipid Biosurfactant with Antitumoral Activities. Appl Biochem Biotechnol 193, 3855–3866 (2021). https://doi.org/10.1007/s12010-021-03620-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12010-021-03620-x