A comprehensive model for the diffusion and hybridization processes of nucleic acid probes in fluorescence in situ hybridization.


Journal

Biotechnology and bioengineering
ISSN: 1097-0290
Titre abrégé: Biotechnol Bioeng
Pays: United States
ID NLM: 7502021

Informations de publication

Date de publication:
10 2020
Historique:
received: 04 03 2020
revised: 02 06 2020
accepted: 05 06 2020
entrez: 18 9 2020
pubmed: 19 9 2020
medline: 10 8 2021
Statut: ppublish

Résumé

Fluorescence in situ hybridization (FISH) has been extensively used in the past decades for the detection and localization of microorganisms. However, a mechanistic approach of the whole FISH process is still missing, and the main limiting steps for the hybridization to occur remain unclear. In here, FISH is approached as a particular case of a diffusion-reaction kinetics, where molecular probes (MPs) move from the hybridization solution to the target RNA site within the cells. Based on literature models, the characteristic times taken by different MPs to diffuse across multiple cellular barriers, as well as the reaction time associated with the formation of the duplex molecular probe-RNA, were estimated. Structural and size differences at the membrane level of bacterial and animal cells were considered. For bacterial cells, the limiting step for diffusion is likely to be the peptidoglycan layer (characteristic time of 7.94 × 10

Identifiants

pubmed: 32946120
doi: 10.1002/bit.27462
doi:

Substances chimiques

Fluorescent Dyes 0
Nucleic Acid Probes 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

3212-3223

Subventions

Organisme : Fundação para a Ciência e a Tecnologia
ID : POCI-01-0145-FEDER-029961
Pays : International
Organisme : Fundação para a Ciência e a Tecnologia
ID : POCI-01-0145-FEDER-031011
Pays : International
Organisme : Fundação para a Ciência e a Tecnologia
ID : SFRH/BD/143491/2019
Pays : International
Organisme : Fundação para a Ciência e a Tecnologia
ID : SFRH/BDE/51909/2012
Pays : International
Organisme : Fundação para a Ciência e a Tecnologia
ID : UIDB/00511/2020
Pays : International

Informations de copyright

© 2020 Wiley Periodicals LLC.

Références

Algotsson, M., Burrows, M. W., Hedin, D. J., Laurin, Y., Palmgren, R., & Zou, J. (2017). Sample preservation method and sample preservation substrate, Patent WO2013066249A1.
Angelova, M. I., & Tsoneva, I. (1999). Interactions of DNA with giant liposomes. Chemistry and Physics of Lipids, 101(1), 123-137. https://doi.org/10.1016/S0009-3084(99)00060-2
Azevedo, A. S., Sousa, I. M., Fernandes, R. M., Azevedo, N. F., & Almeida, C. (2019). Optimizing locked nucleic acid/2′-O-methyl-RNA fluorescence in situ hybridization (LNA/2′OMe-FISH) procedure for bacterial detection. PLoS One, 14(5), e0217689. https://doi.org/10.1371/journal.pone.0217689
Bakshi, S., Siryaporn, A., Goulian, M., & Weisshaar, J. C. (2012). Superresolution imaging of ribosomes and RNA polymerase in live Escherichia coli cells. Molecular Microbiology, 85(1), 21-38. https://doi.org/10.1111/j.1365-2958.2012.08081.x
Batani, G., Bayer, K., Böge, J., Hentschel, U., & Thomas, T. (2019). Fluorescence in situ hybridization (FISH) and cell sorting of living bacteria. Scientific Reports, 9, 18618. https://doi.org/10.1038/s41598-019-55049-2
Bayer, M. E. (1991). Zones of membrane adhesion in the cryofixed envelope of Escherichia coli. Journal of Structural Biology, 107(3), 268-280. https://doi.org/10.1016/1047-8477(91)90052-X
Beeby, M., Gumbart, J. C., Roux, B., & Jensen, G. J. (2013). Architecture and assembly of the Gram-positive cell wall. Molecular Microbiology, 88(4), 664-672. https://doi.org/10.1111/mmi.12203
Behrens, S., Fuchs, B. M., Mueller, F., & Amann, R. (2003). Is the in situ accessibility of the 16S rRNA of Escherichia coli for Cy3-labeled oligonucleotide probes predicted by a three-dimensional structure model of the 30S ribosomal subunit? Applied and Environmental Microbiology, 69(8), 4935-4941. https://doi.org/10.1128/AEM.69.8.4935-4941.2003
van den Berg, J., Boersma, A. J., & Poolman, B. (2017). Microorganisms maintain crowding homeostasis. Nature Reviews Microbiology, 15(5), 309-318. https://doi.org/10.1038/nrmicro.2017.17
Bidnenko, E., Mercier, C., Tremblay, J., Tailliez, P., & Kulakauskas, S. (1998). Estimation of the state of the bacterial cell wall by fluorescent In situ hybridization. Applied and Environmental Microbiology, 64(8), 3059-3062.
Carisey, A., Stroud, M., Tsang, R., & Ballestrem, C. (2011). Fluorescence recovery after photobleaching. In C. M.Wells & M.Parsons (Eds.), Cell migration: Developmental methods and protocols (pp. 387-402). New York, NY: Humana Press. https://doi.org/10.1007/978-1-61779-207-6_26
Chai, Q., Singh, B., Peisker, K., Metzendorf, N., Ge, X., Dasgupta, S., & Sanyal, S. (2014). Organization of ribosomes and nucleoids in Escherichia coli cells during growth and in quiescence. Journal of Biological Chemistry, 289(16), 11342-11352. https://doi.org/10.1074/jbc.M114.557348
Chien, A.-C., Hill, N. S., & Levin, P. A. (2012). Cell size control in bacteria. Current Biology, 22(9), R340-R349. https://doi.org/10.1016/j.cub.2012.02.032
Clark, D. S., & Blanch, H. W. (1997). Biochemical engineering. New York, NY: Marcel Dekker.
Cooper, G. M., Hausman, R. E., & Hausman, R. E. (2000). The cell: A molecular approach (10). Washington, DC: ASM Press.
Corriou, J.-P., & Azzaro-Pantel, C. (2015). Process optimization strategies, Green process engineering (pp. 27-48). Boca Raton, FL: CRC Press. https://doi.org/10.1201/b18533-4
Cowan, S. W., Schirmer, T., Rummel, G., Steiert, M., Ghosh, R., Pauptit, R. A., … Rosenbusch, J. P. (1992). Crystal structures explain functional properties of two E. coli porins. Nature, 358(6389), 727-733. https://doi.org/10.1038/358727a0
Cussler, E. L. (1997). Diffusion: Mass transfer in fluid systems (p. 580). Cambridge, UK: Cambridge University Press. https://doi.org/10.1017/CBO9780511805134.010
DeLong, E., Wickham, G., & Pace, N. (1989). Phylogenetic stains: Ribosomal RNA-based probes for the identification of single cells. Science, 243(4896), 1360-1363. https://doi.org/10.1126/science.2466341
De Los Santos, C., Chang, C.-W., Mycek, M.-A., & Cardullo, R. A. (2015). FRAP, FLIM, and FRET: Detection and analysis of cellular dynamics on a molecular scale using fluorescence microscopy. Molecular Reproduction and Development, 82(7-8), 587-604. https://doi.org/10.1002/mrd.22501
Fontenete, S., Guimarães, N., Wengel, J., & Azevedo, N. F. (2015). Prediction of melting temperatures in fluorescence in situ hybridization (FISH) procedures using thermodynamic models. Critical Reviews in Biotechnology, 8551, 1-12. https://doi.org/10.3109/07388551.2014.993589
Fontenete, S., Leite, M., Guimarães, N., Madureira, P., Ferreira, R. M., Figueiredo, C., … Azevedo, N. F. (2015). Towards fluorescence in vivo hybridization (FIVH) detection of H. pylori in gastric mucosa using advanced LNA probes. PLoS One, 10(4), 0125494. https://doi.org/10.1371/journal.pone.0125494.
Fulton, A. B. (1982). How crowded is the cytoplasm? Cell, 30(2), 345-347. https://doi.org/10.1016/0092-8674(82)90231-8
Gameiro, D., Pérez-Pérez, M., Pérez-Rodríguez, G., Monteiro, G., Azevedo, N. F., & Lourenço, A. (2015). Computational resources and strategies to construct single-molecule metabolic models of microbial cells. Briefings in Bioinformatics, bbv0, 17, 96.
Garcia-Ochoa, F., Gomez, E., Santos, V. E., & Merchuk, J. C. (2010). Oxygen uptake rate in microbial processes: An overview. In. Biochemical Engineering Journal, 49(3), 289-307. https://doi.org/10.1016/j.bej.2010.01.011
Golding, I., & Cox, E. C. (2006). Physical nature of bacterial cytoplasm. Physical Review Letters, 96(9), 098102. https://doi.org/10.1103/PhysRevLett.96.098102.
Graham, L. L., Beveridge, T. J., & Nanninga, N. (2017). Periplasmic space and the concept of the periplasm. Trends in Biochemical Sciences, 16, 328-329. https://doi.org/10.1016/0968-0004(91)90135-I
Grossman, N., Ron, E. A., & Woldringh, C. L. (1982). Changes in cell dimensions during amino acid starvation of Escherichia coli. Journal of Bacteriology, 152(1), 35-41.
Holst, O., Moran, A. P., & Brennan, P. J. (2010). Chapter 1-Overview of the glycosylated components of the bacterial cell envelope, Microbial glycobiology (pp. 1-13). Cambridge, MA: Academic Press. https://doi.org/10.1016/B978-0-12-374546-0.00001-8
Hrabovszky, E., & Petersen, S. L. (2002). Increased concentrations of radioisotopically-labeled complementary ribonucleic acid probe, dextran sulfate, and dithiothreitol in the hybridization buffer can improve results of in situ hybridization histochemistry. The Journal of Histochemistry and Cytochemistry: Official Journal of the Histochemistry Society, 50(10), 1389-1400. https://doi.org/10.1177/002215540205001012
Huber, D., Voith von Voithenberg, L., & Kaigala, G. V. (2018). Fluorescence in situ hybridization (FISH): History, limitations and what to expect from micro-scale FISH? Micro and Nano Engineering, 1, 15-24. https://doi.org/10.1016/j.mne.2018.10.006
Kalwarczyk, T., Tabaka, M., & Holyst, R. (2012). Biologistics-diffusion coefficients for complete proteome of Escherichia coli. Bioinformatics, 28(22), 2971-2978. https://doi.org/10.1093/bioinformatics/bts537
Kalwarczyk, T., Ziȩbacz, N., Bielejewska, A., Zaboklicka, E., Koynov, K., Szymański, J., … Hołyst, R. (2011). Comparative analysis of viscosity of complex liquids and cytoplasm of mammalian cells at the nanoscale. Nano Letters, 11(5), 2157-2163. https://doi.org/10.1021/nl2008218
Katz, A., Alimova, A., Xu, M., Rudolph, E., Shah, M. K., Savage, H. E., … Alfano, R. R. (2003). Bacteria size determination by elastic light scattering. IEEE Journal of Selected Topics in Quantum Electronics, 9(2), 277-287.
Kilså, J. K., Ørum, H., Nielsen, P. E., & Nordén, B. (1997). Kinetics for hybridization of peptide nucleic acids (PNA) with DNA and RNA studied with the BIAcore technique. Biochemistry, 36(16), 5072-5077. https://doi.org/10.1021/bi9627525
Koller, E., Vincent, T. M., Chappell, A., De, S., Manoharan, M., & Bennett, C. F. (2011). Mechanisms of single-stranded phosphorothioate modified antisense oligonucleotide accumulation in hepatocytes. Nucleic Acids Research, 39(11), 4795-4807.
Lambert, P. A. (2002). Cellular impermeability and uptake of biocides and antibiotics in gram-positive bacteria and mycobacteria. Journal of Applied Microbiology, 92, 46S-54S. https://www.ncbi.nlm.nih.gov/pubmed/12000612
Langer-Safer, P. R., Levine, M., & Ward, D. C. (1982). Immunological method for mapping genes on Drosophila polytene chromosomes. Proceedings of the National Academy of Sciences of the United States of America, 79(14), 4381-4385.
Lukacs, G. L., Haggie, P., Seksek, O., Lechardeur, D., Freedman, N., & Verkman, A. S. (2000). Size-dependent DNA mobility in cytoplasm and nucleus. Journal of Biological Chemistry, 275(3), 1625-1629. https://doi.org/10.1074/jbc.275.3.1625
Mastro, A. M., Babich, M. A., Taylor, W. D., & Keith, A. D. (1984). Diffusion of a small molecule in the cytoplasm of mammalian cells. Proceedings of the National Academy of Sciences of the United States of America, 81, 3414-3418. https://doi.org/10.1073/pnas.81.11.3414
van Meer, G., Voelker, D. R., & Feigenson, G. W. (2008). Membrane lipids: Where they are and how they behave. Nature Reviews Molecular Cell Biology, 9(2), 112-124. https://doi.org/10.1038/nrm2330
Mitra, K., Ubarretxena-Belandia, I., Taguchi, T., Warren, G., & Engelman, D. M. (2004). Modulation of the bilayer thickness of exocytic pathway membranes by membrane proteins rather than cholesterol. Proceedings of the National Academy of Sciences of the United States of America, 101(12), 4083-4088. https://doi.org/10.1073/pnas.0307332101
Mogensen, J. E., & Otzen, D. E. (2005). Interactions between folding factors and bacterial outer membrane proteins. Molecular Microbiology, 57(2), 326-346.
Moter, A., & Göbel, U. B. (2000). Fluorescence in situ hybridization (FISH) for direct visualization of microorganisms. Journal of Microbiological Methods, 41(2), 85-112. https://doi.org/10.1016/S0167-7012(00)00152-4
Mullineaux, C. W., & Kirchhoff, H. (2007). Using fluorescence recovery after photobleaching to measure lipid diffusion in membranes. In A. M.Dopico (Ed.), Methods in membrane lipids (pp. 267-275). New York, NY: Humana Press. https://doi.org/10.1007/978-1-59745-519-0_18
Nikaido, H. (2003). Molecular basis of bacterial outer membrane permeability revisited. Microbiology and Molecular Biology Reviews, 67(4), 593-656. https://doi.org/10.1128/MMBR.67.4.593
Panja, S., Jana, B., Aich, P., & Basu, T. (2008). In vitro interaction between calt thymus DNA and Escherichia coli LPS in the presence of divalent cation Ca2+. Biopolymers, 89(7), 606-613. https://doi.org/10.1002/bip.20964
Robertson, R. M., Laib, S., & Smith, D. E. (2006). Diffusion of isolated DNA molecules: Dependence on length and topology. Proceedings of the National Academy of Sciences of the United States of America, 103(19), 7310-7314. https://doi.org/10.1073/pnas.0601903103
Rocha, R., Santos, R. S., Madureira, P., Almeida, C., & Azevedo, N. F. (2016). Optimization of peptide nucleic acid fluorescence in situ hybridization (PNA-FISH) for the detection of bacteria: The effect of pH, dextran sulfate and probe concentration. Journal of Biotechnology, 226, 1-7. https://doi.org/10.1016/j.jbiotec.2016.03.047
Santos, R. S., Figueiredo, C., Azevedo, N. F., Braeckmans, K., & De Smedt, S. C. (2017). Nanomaterials and molecular transporters to overcome the bacterial envelope barrier: Towards advanced delivery of antibiotics. Advanced Drug Delivery Reviews, 136-137, 28-48. https://doi.org/10.1016/j.addr.2017.12.010
Schlessinger, J., Axelrod, D., Koppel, D. E., Webb, W. W., & Elson, E. L. (1977). Lateral transport of a lipid probe and labeled proteins on a cell membrane. Science, 195(4275), 307-309.
Schoen, I., Krammer, H., & Braun, D. (2009). Hybridization kinetics is different inside cells. Proceedings of the National Academy of Sciences of the United States of America, 106(51), 21649-21654. https://doi.org/10.1073/pnas.0901313106
Thermo Fisher Scientific (n.d.). Macromolecular components of E. coli and HeLa cells. Retrieved from https://www.thermofisher.com/pt/en/home/references/ambion-tech-support/rna-tools-and-calculators/macromolecular-components-of-e.html
Seltmann, G., & Holst, O. (2002). In G.Seltmann & O.Holst (Eds.), Periplasmic space and rigid layer BT-The bacterial cell wall (pp. 103-132). Berlin, Germany: Springer. https://doi.org/10.1007/978-3-662-04878-8_3
Silhavy, T., Kahne, D., & Walker, S. (2010). The bacterial cell envelope. Cold Spring Harbor Perspectives in Biology, 2(5), 1-16. https://doi.org/10.1101/cshperspect.a000414
Simard, C., Lemieux, R., & Côté, S. (2001). Urea substitutes toxic formamide as destabilizing agent in nucleic acid hybridizations with RNA probes. Electrophoresis, 22(13), 2679-2683. https://doi.org/10.1002/1522-2683(200108)22:13<2679::AID-ELPS2679>3.0.CO;2-L
Tischer, K., Zeder, M., Klug, R., Pernthaler, J., Schattenhofer, M., Harms, H., & Wendeberg, A. (2012). Fluorescence in situ hybridization (CARD-FISH) of microorganisms in hydrocarbon contaminated aquifer sediment samples. Systematic and Applied Microbiology, 35(8), 526-532. https://doi.org/10.1016/j.syapm.2012.01.004
Vollmer, W., & Seligman, S. J. (2010). Architecture of peptidoglycan: More data and more models. Trends in Microbiology, 18(2), 59-66. https://doi.org/10.1016/j.tim.2009.12.004
Wahl, G. M., Stern, M., & Stark, G. R. (1979). Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proceedings of the National Academy of Sciences of the United States of America, 76(8), 3683-3687. https://doi.org/10.1073/pnas.76.8.3683
Walton, S. P., Stephanopoulos, G. N., Yarmush, M. L., & Roth, C. M. (2002). Thermodynamic and kinetic characterization of antisense oligodeoxynucleotide binding to a structured mRNA. Biophysical Journal, 82(1), 366-377. https://doi.org/10.1016/S0006-3495(02)75401-5
Xu, X.-H., & Yeung, E. S. (1997). Direct measurement of single-molecule diffusion and photodecomposition in free solution. Science, 275(5303), 1106-1109. https://doi.org/10.1126/science.275.5303.1106
Yilmaz, L. S., & Noguera, D. R. (2004a). Mechanistic approach to the problem of hybridization efficiency in fluorescent in situ hybridization. Applied and Environmental Microbiology, 70(12), 7126-7139. https://doi.org/10.1128/AEM.70.12.7126-7139.2004
Yilmaz, L. S., & Noguera, D. R. (2004b). Mechanistic approach to the problem of hybridization efficiency in fluorescent in situ hybridization. Applied and Environmental Microbiology, 70(12), 7126-7139. https://doi.org/10.1128/AEM.70.12.7126-7139.2004
Young, A. P., Jackson, D. J., & Wyeth, R. C. (2020). A technical review and guide to RNA fluorescence in situ hybridization. PeerJ, 8, e8806. https://doi.org/10.7717/peerj.8806
Zhao, L., Kroenke, C. D., Song, J., Piwnica-Worms, D., Ackerman, J. J. H., & Neil, J. J. (2008). Intracellular water-specific MR of microbead-adherent cells: The HeLa cell intracellular water exchange lifetime. NMR in Biomedicine, 21(2), 159-164. https://doi.org/10.1002/nbm.1173
Zimmerman, S. B., & Trach, S. O. (1991). Estimation of macromolecule concentrations and excluded volume effects for the cytoplasm of Escherichia coli. Journal of Molecular Biology, 222(3), 599-620. https://doi.org/10.1016/0022-2836(91)90499-V

Auteurs

Joana F Lima (JF)

LEPABE - Laboratory for Process Engineering, Environment, Biotechnology and Energy, Faculty of Engineering, University of Porto, Porto, Portugal.
Biomode, S.A., Braga, Portugal.
i3S, Instituto de Investigação e Inovação em Saúde, Universidade do Porto, Porto, Portugal.
Institute of Molecular Pathology and Immunology of the University of Porto, Porto, Portugal.

Paulo Maia (P)

LEPABE - Laboratory for Process Engineering, Environment, Biotechnology and Energy, Faculty of Engineering, University of Porto, Porto, Portugal.

Beatriz T Magalhães (B)

LEPABE - Laboratory for Process Engineering, Environment, Biotechnology and Energy, Faculty of Engineering, University of Porto, Porto, Portugal.

Laura Cerqueira (L)

LEPABE - Laboratory for Process Engineering, Environment, Biotechnology and Energy, Faculty of Engineering, University of Porto, Porto, Portugal.
Biomode, S.A., Braga, Portugal.

Nuno F Azevedo (NF)

LEPABE - Laboratory for Process Engineering, Environment, Biotechnology and Energy, Faculty of Engineering, University of Porto, Porto, Portugal.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH