Bioinformatic Analysis of the Genetic Mechanism of Biomineralization of Biogenic Magnetic Nanoparticles in Bacteria Capable of Tumor-Specific Accumulation
Keywords:cancer therapy, biogenic magnetic nanoparticles, biomineralization, Mam-proteins, bacterial colonization, cancerous tumors, genetic vector, targeted drug delivery system
Background. Current methods of targeted cancer therapy are not always effective enough and can lead to side effects, such as an increased risk of autoimmune diseases. It is known that some bacteria are capable of specific accumulation in malignant tumors, and therefore can be used as an alternative means of targeted drug delivery. However, the genetic mechanism of tumor-specific accumulation of bacteria is not fully understood and needs to be studied in more detail.
Objective. This work aims to identify, by methods of comparative genomics methods, magnetically controlled bacteria among those for which tumor-specific accumulation has already been experimentally shown.
Methods. To identify magnetically controlled bacterial strains, i.e., bacteria that biomineralize biogenic magnetic nanoparticles (BMN), the method of comparative genomics was used, namely: pairwise alignment of proteomes with amino acid sequences of Mam-proteins of required for biomineralization of BMN in magnetotactic bacteria Magnetospirillum gryphiswaldense MSR-1. Sequence alignments were performed in the BLAST program of the US National Center for Biotechnology Information (NCBI).
Results. The conducted bioinformatic analysis showed that strains of bacteria in which the ability to accumulate specifically in tumors has been experimentally proven are potential producers of BMN of different types. Among them there are potential producers of intracellular crystalline BMN, potential producers of intracellular amorphous BMN, and extracellular crystalline BMN
Conclusions. It is expedient to use bacteria-producing BMN as gene vectors and systems of targeted drug delivery to tumors that biomineralize BMN.
Piataev NA, Mielcaiev GG, Kopin PI. Target transport of antitumor chemopreparations: Modern technologies and development prospects. Povolzhskiy Onkologicheskiy Vesnik. 2012;2:60-71.
Cheng Y, Zak O, Aisen P, Harrison SC, Walz T. Structure of the human transferrin receptor-transferrin complex. Cell. 2004;116(4):565-76. DOI: 10.1016/S0092-8674(04)00130-8
Scott AM, Allison JP, Wolchok JD. Monoclonal antibodies in cancer therapy. Cancer Immun. 2012;12:14.
Thomas A, Teicher BA, Hassan R. Antibody–drug conjugates for cancer therapy. Lancet Oncol. 2016;17(6):e254-62. DOI: 10.1016/S1470-2045(16)30030-4
Beenish NA, Nosheen F, Sundus R, Sadia M, Wajiha A. Bacterial and liposomal vector guided drug delivery system via tumor markers carrier gene to treat neoplasm. J Appl Pharm. 2016;08(01). DOI: 10.4172/1920-4159.1000206
Baban CK, Cronin M, O'Hanlon D, O'Sullivan GC, Tangney M. Bacteria as vectors for gene therapy of cancer. Bioeng Bugs. 2010;1(6):385-94. DOI: 10.4161/bbug.1.6.13146
van Dessel N, Swofford CA, Forbes NS. Potent and tumor specific: arming bacteria with therapeutic proteins. Ther Deliv. 2015 Mar;6(3):385-99. DOI: 10.4155/tde.14.113
Minton NP. Clostridia in cancer therapy. Nat Rev Microbiol. 2003 Dec;1(3):237-42. DOI: 10.1038/nrmicro777
Wei MQ, Mengesha A, Good D, Anné J. Bacterial targeted tumour therapy-dawn of a new era. Cancer Lett. 2008 Jan 18;259(1):16-27. DOI: 10.1016/j.canlet.2007.10.034
Al-Mariri A, Tibor A, Lestrate P, Mertens P, de Bolle X, Letesson JJ. Yersinia enterocolitica as a vehicle for a naked DNA vaccine encoding Brucella abortus bacterioferritin or P39 antigen. Infect Immun. 2002 Apr;70(4):1915-23. DOI: 10.1128/IAI.70.4.1915-1923.2002
Yu YA, Shabahang S, Timiryasova TM, Zhang Q, Beltz R, Gentschev I, et al. Visualization of tumors and metastases in live animals with bacteria and vaccinia virus encoding light-emitting proteins. Nat Biotechnol. 2004 Mar;22(3):313-20. DOI: 10.1038/nbt937
Song S, Vuai MS, Zhong M. The role of bacteria in cancer therapy – enemies in the past, but allies at present. Infect Agent Cancer. 2018 Mar 15;13(1):9. DOI: 10.1186/s13027-018-0180-y
Tangney M, van Pijkeren JP, Gahan CGM. The use of Listeria monocytogenes as a DNA delivery vector for cancer gene therapy. Bioeng Bugs. 2010 Jul-Aug;1(4):284-7. DOI: 10.4161/bbug.1.4.11725
Cronin M, Morrissey D, Rajendran S, el Mashad SM, van Sinderen D, O'Sullivan GC, et al. Orally administered bifido-bacteria as vehicles for delivery of agents to systemic tumors. Mol Ther. 2010 Jul;18(7):1397-407. DOI: 10.1038/mt.2010.59
Virginia Tech. Bacteria-based drug delivery system that outperforms conventional methods. ScienceDaily. 2018 Dec 20.
Juutilainen J, Herrala M, Luukkonen J, Naarala J, Hore PJ. Magnetocarcinogenesis: is there a mechanism for carcinogenic effects of weak magnetic fields? Proc Biol Sci. 2018 May 30;285(1879):20180590. DOI: 10.1098/rspb.2018.0590
Chehun VF, Gorobets SV, Gorobets OY, Demianenko IV. Magnetic nanostructures in tumor cells application of scanning probemicroscopy to study the structural organization magnetosensitive phase in tumor cells. Visnyk NAN Ukrayiny. 2011;11:13-20.
Brem F, Hirt AM, Winklhofer M, Frei K, Yonekawa Y, Wieser H-G, et al. Magnetic iron compounds in the human brain: a comparison of tumour and hippocampal tissue. J R Soc Interface. 2006 Dec 22;3(11):833-41. DOI: 10.1098/rsif.2006.0133
Gorobets SV, Gorobets OY. Function of biogenic magnetic nanoparticles in organisms. Adv Funct Mater. 2012;19:18-26.
Gorobets OY, Gorobets SV, Gorobets YI. Biogenic magnetic nanoparticles: Biomineralization in prokaryotes and eukaryotes. In: Dekker encyclopedia of nanoscience and nanotechnology. 3rd ed. 2013. p. 9.
National Center for Biotechnology Information [Internet]. Ncbi.nlm.nih.gov. 2022 [cited 2022 Jun 26]. Available from: https://www.ncbi.nlm.nih.gov/
Felfoul O, Mohammadi M, Taherkhani S, de Lanauze D, Zhong Xu Y, Loghin D, et al. Magneto-aerotactic bacteria deliver drug-containing nanoliposomes to tumour hypoxic regions. Nat Nanotechnol. 2016 Nov;11(11):941-947. DOI: 10.1038/nnano.2016.137
Kuzajewska D, Wszołek A, Żwierełło W, Kirczuk L, Maruszewska A. Magnetotactic bacteria and magnetosomes as smart drug delivery systems: A new weapon on the battlefield with cancer? Biology (Basel). 2020 May 19;9(5):102. DOI: 10.3390/biology9050102
Gorobets O, Gorobets S, Koralewski M. Physiological origin of biogenic magnetic nanoparticles in health and disease: from bacteria to humans. Int J Nanomedicine. 2017 Jun 12;12:4371-95. DOI: 10.2147/IJN.S130565
Heppner F, Muse JR. The liquefaction (oncolysis) of malignant gliomas by a non pathogenic Clostridium. Acta Neurochir (Wien). 1978;42(1-2):123-5. DOI: 10.1007/BF01406639
Friedlos F, Lehouritis P, Ogilvie L, Hedley D, Davies L, Bermudes D, et al. Attenuated salmonella targets prodrug activating enzyme carboxypeptidase G2 to mouse melanoma and human breast and colon carcinomas for effective suicide gene therapy. Clin Cancer Res. 2008 Jul 1;14(13):4259-66. DOI: 10.1158/1078-0432.CCR-07-4800
Weibel S, Stritzker J, Eck M, Goebel W, Szalay AA. Colonization of experimental murine breast tumours by Escherichia coli K-12 significantly alters the tumour microenvironment. Cell Microbiol. 2008 Jun;10(6):1235-48. DOI: 10.1111/j.1462-5822.2008.01122.x
Chiang CJ, Huang PH. Metabolic engineering of probiotic Escherichia coli for cytolytic therapy of tumors. Sci Rep. 2021 Mar 12;11(1):5853. DOI: 10.1038/s41598-021-85372-6
Flickinger J, Rodeck U, Snook A. Listeria monocytogenes as a vector for cancer immunotherapy: Current understanding and progress. Vaccines (Basel). 2018 Jul 25;6(3):48. DOI: 10.3390/vaccines6030048
Galmbacher K, Heisig M, Hotz C, Wischhusen J, Galmiche A, Bergmann B, et al. Shigella mediated depletion of macrophages in a murine breast cancer model is associated with tumor regression. PLoS One. 2010 Mar 8;5(3):e9572. DOI: 10.1371/journal.pone.0009572
Goldufsky J, Wood S, Hajihossainlou B, Rehman T, Majdobeh O, Kaufman HL, et al. Pseudomonas aeruginosa exotoxin T induces potent cytotoxicity against a variety of murine and human cancer cell lines. J Med Microbiol. 2015 Feb;64(Pt 2):164-73. DOI: 10.1099/jmm.0.000003-0
Cronin M, Stanton RM, Francis KP, Tangney M. Bacterial vectors for imaging and cancer gene therapy: a review. Cancer Gene Ther. 2012 Nov;19(11):731-40. DOI: 10.1038/cgt.2012.59
Lee CH, Wu CL, Tai YS, Shiau AL. Systemic administration of attenuated Salmonella choleraesuis in combination with cisplatin for cancer therapy. Mol Ther. 2005 May;11(5):707-16. DOI: 10.1016/j.ymthe.2005.01.008
Castellarin M, Warren RL, Freeman JD, Dreolini L, Krzywinski M, Strauss J, et al. Fusobacterium nucleatum infection is prevalent in human colorectal carcinoma. Genome Res. 2012 Feb;22(2):299-306. DOI: 10.1101/gr.126516.111
Sawant SS, Patil SM, Gupta V, Kunda NK. Microbes as medicines: Harnessing the power of bacteria in advancing cancer treatment. Int J Mol Sci. 2020 Oct 14;21(20):7575. DOI: 10.3390/ijms21207575
Park SY, Kim JH, Lee YJ, Lee SJ, Kim Y. Surfactin suppresses TPA-induced breast cancer cell invasion through the inhibition of MMP-9 expression. Int J Oncol. 2013 Jan;42(1):287-96. DOI: 10.3892/ijo.2012.1695
Gorobets O, Gorobets S, Sorokina L. Biomineralization and synthesis of biogenic magnetic nanoparticles and magneto-sensitive inclusions in microorganisms and fungi. Funct Mater. 2014;21(4):427-36. DOI: 10.15407/fm21.04.427
Gorobets S, Gorobets O, Sharau I, Milenko Y. Magnetically controlled vector based on E coli Nissle 1917. arXiv [Preprint] 2020. DOI: 10.48550/arXiv.2002.01958
Asgari G, Khoshniyat R, Moradi Golrokhi M. Survey of magneto-tactic properties of Escherichia coli under static magnetic fields. Avicenna J Environ Health Eng. 2020;7(1):14-9. DOI: 10.34172/ajehe.2020.03
Vainshtein M, Suzina N, Kudryashova E, Ariskina E. New magnet-sensitive structures in bacterial and archaeal cells. Biol Cell. 2002;94(1):29-35. DOI: 10.1016/S0248-4900(02)01179-6
Gorobets S, Gorobets O, Butenko K. Potential producers of biogenic magnetic nanoparticles among pathogenic and opportunistic microorganisms. Innov Biosyst Bioeng. 2018;2(1):33-41. DOI: 10.20535/ibb.2018.2.1.127260
Kotakadi SM, Borelli DPR, Nannepaga JS. Therapeutic applications of magnetotactic bacteria and magnetosomes: A review emphasizing on the cancer treatment. Front Bioeng Biotechnol. 2022 Apr 25;10:789016. DOI: 10.3389/fbioe.2022.789016
Gorobets S, Gorobets O, Gorobets Y, Bulaievska M. Chain-like structures of biogenic and nonbiogenic magnetic nanoparticles in vascular tissues. Bioelectromagnetics. 2022 Feb;43(2):119-43. DOI: 10.1002/bem.22390
How to Cite
Copyright (c) 2022 The Author(s)
This work is licensed under a Creative Commons Attribution 4.0 International License.
The ownership of copyright remains with the Authors.
Authors may use their own material in other publications provided that the Journal is acknowledged as the original place of publication and National Technical University of Ukraine “Igor Sikorsky Kyiv Polytechnic Institute” as the Publisher.
Authors are reminded that it is their responsibility to comply with copyright laws. It is essential to ensure that no part of the text or illustrations have appeared or are due to appear in other publications, without prior permission from the copyright holder.IBB articles are published under Creative Commons licence:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under CC BY 4.0 that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.