Different Cutibacterium acnes Phylotypes Release Distinct Extracellular Vesicles
Abstract
:1. Introduction
2. Results
2.1. Morphological Characteristics of Cutibacterial EVs
2.2. Protein Profile of C. acnes Cell Fractions and Isolated EVs
2.3. Lipid Profiles of EVs and Whole-Cell Extracts
2.4. MALDI-TOF MS Lipid Profiling
3. Discussion
4. Materials and Methods
4.1. Bacterial Culture and Isolation of Extracellular Vesicles
4.2. TEM and DLS
4.3. SDS-PAGE Analysis of EV and Cutibacterium Protein Fractions
4.4. Lipid Extraction
4.5. TLC Analysis
4.6. MALDI-TOF MS Analysis
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Bose, S.; Aggarwal, S.; Singh, D.V.; Acharya, N. Extracellular vesicles: An emerging platform in gram-positive bacteria. Microb. Cell 2020, 7, 312–322. [Google Scholar] [CrossRef] [PubMed]
- Chudzik, A.; Paściak, M. Bakteryjne pęcherzyki zewnątrzkomórkowe jako mediatory komunikacji międzykomórkowej. Postepy Hig. Med. Dosw. 2020, 74, 572–588. [Google Scholar] [CrossRef]
- Tsai, Y.L.; Tsai, W.C.; Qing, Z.; Chang, C.J. Dichotomous effects of microbial membrane vesicles on the regulation of immunity. Med. Microecol. 2020, 3, 100009. [Google Scholar] [CrossRef]
- Nagakubo, T.; Nomura, N.; Toyofuku, M. Cracking Open Bacterial Membrane Vesicles. Front. Microbiol. 2020, 10, 3026. [Google Scholar] [CrossRef] [Green Version]
- Dagnelie, M.A.; Corvec, S.; Khmarri, A.; Dreno, B. Bacterial extracellular vesicles: A new way to decipher host-microbiota communications in inflammatory dermatoses. Exp. Dermatol. 2020, 29, 22–28. [Google Scholar] [CrossRef] [Green Version]
- Haas-Neill, S.; Forsythe, P. A Budding Relationship: Bacterial Extracellular Vesicles in the Microbiota-Gut-Brain Axis. Int. J. Mol. Sci. 2020, 21, 8899. [Google Scholar] [CrossRef]
- Ñahui Palomino, R.A.; Vanpouille, C.; Costantini, P.E.; Margolis, L. Microbiota–host communications: Bacterial extracellular vesicles as a common language. PLoS Pathog. 2021, 17, e1009508. [Google Scholar] [CrossRef]
- Herrmann, I.K.; Wood, M.J.A.; Fuhrmann, G. Extracellular vesicles as a next-generation drug delivery platform. Nat. Nanotechnol. 2021, 16, 748–759. [Google Scholar] [CrossRef]
- Sabanovic, B.; Piva, F.; Cecati, M.; Giulietti, M. Promising Extracellular Vesicle-Based Vaccines against Viruses, Including SARS-CoV-2. Biology 2021, 10, 94. [Google Scholar] [CrossRef]
- Bek-Thomsen, M.; Lomholt, H.B.; Kilian, M. Acne is Not Associated with Yet-Uncultured Bacteria. J. Clin. Microbiol. 2008, 46, 3355–3360. [Google Scholar] [CrossRef] [Green Version]
- Jeon, J.; Mok, H.J.; Choi, Y.; Park, S.C.; Jo, H.; Her, J.; Han, J.K.; Kim, Y.K.; Kim, K.P.; Ban, C. Proteomic analysis of extracellular vesicles derived from Propionibacterium acnes. Prot. Clin. Appl. 2017, 11, 1600040. [Google Scholar] [CrossRef] [PubMed]
- Dessinioti, C.; Katsambas, A.D. The role of Propionibacterium acnes in acne pathogenesis: Facts and controversies. Clin. Dermatol. 2010, 28, 2–7. [Google Scholar] [CrossRef] [PubMed]
- Mollerup, S.; Friis-Nielsen, J.; Vinner, L.; Hansen, T.A.; Richter, S.R.; Fridholm, H.; Herrera, J.A.R.; Lund, O.; Brunak, S.; Izarzugaza, J.M.G.; et al. Propionibacterium acnes: Disease-Causing Agent or Common Contaminant? Detection in Diverse Patient Samples by Next-Generation Sequencing. J. Clin. Microbiol. 2016, 54, 980–987. [Google Scholar] [CrossRef] [Green Version]
- Platsidaki, E.; Dessinioti, C. Recent advances in understanding Propionibacterium acnes (Cutibacterium acnes) in acne. F1000Research 2018, 7, 1953. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nouioui, I.; Carro, L.; García-López, M.; Meier-Kolthoff, J.P.; Woyke, T.; Kyrpides, N.C.; Pukall, R.; Klenk, H.P.; Goodfellow, M.; Göker, M. Genome-Based Taxonomic Classification of the Phylum Actinobacteria. Front. Microbiol. 2018, 9, 2007. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dekio, I.; McDowell, A.; Sakamoto, M.; Tomida, S.; Ohkuma, M. Proposal of the new combination, Cutibacterium acnes subsp. elongatum comb. nov., and emended descriptions of the genus Cutibacterium, Cutibacterium acnes subsp. acnes and Cutibacterium acnes subsp. defendens. Int. J. Syst. Evol. Microbiol. 2019, 69, 1087–1092. [Google Scholar] [CrossRef]
- Kilian, M.; Scholz, C.F.P.; Lomholt, H.B. Multilocus Sequence Typing and Phylogenetic Analysis of Propionibacterium acnes. J. Clin. Microbiol. 2012, 50, 1158–1165. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Scholz, C.F.P.; Jensen, A.; Lomholt, H.B.; Brüggemann, H.; Kilian, M. A Novel High-Resolution Single Locus Sequence Typing Scheme for Mixed Populations of Propionibacterium acnes In Vivo. PLoS ONE 2014, 9, e104199. [Google Scholar] [CrossRef] [Green Version]
- McDowell, A.; Nagy, I.; Magyari, M.; Barnard, E.; Patrick, S. The Opportunistic Pathogen Propionibacterium acnes: Insights into Typing, Human Disease, Clonal Diversification and CAMP Factor Evolution. PLoS ONE 2013, 8, e70897. [Google Scholar] [CrossRef] [Green Version]
- Cohen, R.J.; Shannon, B.A.; McNEAL, J.E.; Shannon, T.O.M.; Garrett, K.L. Propionibacterium acnes associated with inflammation in radical prostatectomy specimens: A possible link to cancer evolution. J. Urol. 2005, 173, 1969–1974. [Google Scholar] [CrossRef] [Green Version]
- Yu, Y.; Champer, J.; Agak, G.W.; Kao, S.; Modlin, R.L.; Kim, J. Different Propionibacterium acnes Phylotypes Induce Distinct Immune Responses and Express Unique Surface and Secreted Proteomes. J. Investig. Dermatol. 2016, 136, 2221–2228. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Choi, E.J.; Lee, H.G.; Bae, I.H.; Kim, W.; Park, J.; Lee, T.R.; Cho, E.G. Propionibacterium acnes-Derived Extracellular Vesicles Promote Acne-Like Phenotypes in Human Epidermis. J. Investig. Dermatol. 2018, 138, 1371–1379. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Prados-Rosales, R.; Brown, L.; Casadevall, A.; Montalvo-Quirós, S.; Luque-Garcia, J.L. Isolation and identification of membrane vesicle-associated proteins in Gram-positive bacteria and mycobacteria. MethodsX 2014, 1, 124–129. [Google Scholar] [CrossRef] [PubMed]
- Mergenhagen, S.E.; Bladen, H.A.; Hsu, K.C. Electron microscopic localization of endotoxic lipopolysaccharide in Gram-negative organisms. Ann. N. Y. Acad. Sci. 1966, 133, 279–291. [Google Scholar] [CrossRef]
- Lee, E.Y.; Choi, D.Y.; Kim, D.K.; Kim, J.W.; Park, J.O.; Kim, S.; Kim, S.H.; Desiderio, D.M.; Kim, Y.K.; Kim, K.P.; et al. Gram-positive bacteria produce membrane vesicles: Proteomics-based characterization of Staphylococcus aureus-derived membrane vesicles. Proteomics 2009, 9, 5425–5436. [Google Scholar] [CrossRef]
- Jiang, Y.; Kong, Q.; Roland, K.L.; Curtiss, R. Membrane vesicles of Clostridium perfringens type A strains induce innate and adaptive immunity. Int. J. Med. Microbiol. 2014, 304, 431–443. [Google Scholar] [CrossRef] [Green Version]
- Resch, U.; Tsatsaronis, J.A.; Le Rhun, A.; Stübiger, G.; Rohde, M.; Kasvandik, S.; Holzmeister, S.; Tinnefeld, P.; Wai, S.N.; Charpentier, E. A Two-Component Regulatory System Impacts Extracellular Membrane-Derived Vesicle Production in Group A Streptococcus. mBio 2016, 7, e00207–e00216. [Google Scholar] [CrossRef] [Green Version]
- Spittaels, K.J.; Ongena, R.; Zouboulis, C.C.; Crabbé, A.; Coenye, T. Cutibacterium acnes Phylotype I and II Strains Interact Differently With Human Skin Cells. Front. Cell. Infect. Microbiol. 2020, 10, 575164. [Google Scholar]
- Jeon, J.; Park, S.C.; Her, J.; Lee, J.W.; Han, J.K.; Kim, Y.K.; Kim, K.P.; Ban, C. Comparative lipidomic profiling of the human commensal bacterium Propionibacterium acnes and its extracellular vesicles. RSC Adv. 2018, 8, 15241–15247. [Google Scholar] [CrossRef] [Green Version]
- Araiza-Villanueva, M.; Avila-Calderón, E.D.; Flores-Romo, L.; Calderón-Amador, J.; Sriranganathan, N.; Qublan, H.A.; Witonsky, S.; Aguilera-Arreola, M.; Ruiz-Palma, M.D.S.; Ruiz, E.A.; et al. Proteomic analysis of membrane blebs of Brucella abortus 2308 and RB51 and their evaluation as an acellular vaccine. Front. Microbiol. 2019, 10, 2714. [Google Scholar] [CrossRef]
- Breil, C.; Abert Vian, M.; Zemb, T.; Kunz, W.; Chemat, F. “Bligh and Dyer” and Folch Methods for Solid–Liquid–Liquid Extraction of Lipids from Microorganisms. Comprehension of Solvatation Mechanisms and towards Substitution with Alternative Solvents. Int. J. Mol. Sci. 2017, 18, 708. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Knoke, L.R.; Abad Herrera, S.; Götz, K.; Justesen, B.H.; Günther Pomorski, T.; Fritz, C.; Schäkermann, S.; Bandow, J.E.; Aktas, M. Agrobacterium tumefaciens Small Lipoprotein Atu8019 Is Involved in Selective Outer Membrane Vesicle (OMV) Docking to Bacterial Cells. Front. Microbiol. 2020, 11, 1228. [Google Scholar] [CrossRef] [PubMed]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Chudzik, A.; Migdał, P.; Paściak, M. Different Cutibacterium acnes Phylotypes Release Distinct Extracellular Vesicles. Int. J. Mol. Sci. 2022, 23, 5797. https://doi.org/10.3390/ijms23105797
Chudzik A, Migdał P, Paściak M. Different Cutibacterium acnes Phylotypes Release Distinct Extracellular Vesicles. International Journal of Molecular Sciences. 2022; 23(10):5797. https://doi.org/10.3390/ijms23105797
Chicago/Turabian StyleChudzik, Anna, Paweł Migdał, and Mariola Paściak. 2022. "Different Cutibacterium acnes Phylotypes Release Distinct Extracellular Vesicles" International Journal of Molecular Sciences 23, no. 10: 5797. https://doi.org/10.3390/ijms23105797