Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-09T06:56:22.816Z Has data issue: false hasContentIssue false

Application of pulsed electric fields for the elimination of highly drug-resistant Candida grown under modelled microgravity conditions

Published online by Cambridge University Press:  04 September 2018

Eglė Lastauskienė*
Affiliation:
Institute of Biosciences, Center of Life Sciences, Vilnius University, Sauletekio ave 7, 10257, Vilnius, Lithuania
Vitalij Novickij
Affiliation:
Institute of High Magnetic Fields, Vilnius Gediminas Technical University, Naugarduko st. 41, 03227, Vilnius, Lithuania
Auksė Zinkevičienė
Affiliation:
Department of Immunology, State Research Institute Centre for Innovative Medicine, Santariškių st. 5, 08406, Vilnius, Lithuania
Irutė Girkontaitė
Affiliation:
Department of Immunology, State Research Institute Centre for Innovative Medicine, Santariškių st. 5, 08406, Vilnius, Lithuania
Algimantas Paškevičius
Affiliation:
Laboratory of Biodeterioration Research, Nature Research Centre, Akademijos st. 2, 08412, Vilnius, Lithuania Laboratory of Microbiology of the Centre of Laboratory Medicine, Vilnius University Hospital Santaros Clinics, Santariškių st. 2, 08661, Vilnius, Lithuania
Jurgita Švedienė
Affiliation:
Laboratory of Biodeterioration Research, Nature Research Centre, Akademijos st. 2, 08412, Vilnius, Lithuania
Svetlana Markovskaja
Affiliation:
Laboratory of Mycology, Nature Research Centre, Zaliuju ezeru st. 49, 08406, Vilnius, Lithuania
Jurij Novickij
Affiliation:
Institute of High Magnetic Fields, Vilnius Gediminas Technical University, Naugarduko st. 41, 03227, Vilnius, Lithuania
*
Author for correspondence: Eglė Lastauskienė, E-mail: [email protected]

Abstract

Candida lusitaniae and C. guilliermondii are perfect model organisms for the study of Candida genera behaviour in various conditions. Both of them are rare pathogens capable to cause candidiasis in the patients with weakened immune system and can undergo morphology switches related to the increased antifungal drug resistance. Candida genera yeasts are able to inhabit diverse range of ecological niches including space ships and space stations. During the long-term expeditions, astronauts are affected by various factors that can change the state immune system. In such conditions, the commensal usually non-pathogenic microorganisms can spread through the body of the host and cause infections. Weakened immune system and limited use of drugs in spaceships promote the search of the alternative methods for the biocontrol of microorganisms. Several studies demonstrate that microorganisms are altering their gene expression, physiology, morphology, pathogenicity and evolving resistance to the antifungals under microgravity conditions. Our research indicated that switch to the pseudohyphae morphology leads up 30-fold increased resistance to amphotericin B in C. lusitaniae and C. guilliermondii. Cultivation of yeasts in rotary cell culture system (RCCS) is related to the altered cell growth and resistance to the antifungal treatment. Our results showed that growth in the RCCS led to the extreme increase in cell resistance to amphotericin B as compared with the standard growth conditions. In our research, we applied electroporation for the biocontrol of two Candida species. C. lusitaniae and C. guilliermondii cells grown in RCCS exhibited significantly increased survivability after pulsed electric field (PEF) treatment in comparison with cells grown under routine conditions. We have shown that PEF bursts of 2.5–25 kV cm−1 of 100 µs × 8 duration display a dose-dependent permeabilization of both studied Candida species. Our research indicated that budding cells and pseudohyphae morphology cells, with increased resistance to amphotericin B, can be effectively inactivated after applying PEF higher than 15 kV cm−1.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andre, FM and Mir, LM (2010) Nucleic acids electrotransfer in vivo: mechanisms and practical aspects. Current Gene Therapy 10, 267280.10.2174/156652310791823380Google Scholar
Asner, SA, Giulieri, S, Diezi, M, Marchetti, O and Sanglard, D (2015) Acquired multidrug antifungal resistance in Candida lusitaniae during therapy. Antimicrobial Agents and Chemotherapy 59, 77157722.Google Scholar
Aviles, H, Belay, T, Vance, M and Sonnenfeld, G (2005) Effects of space flight conditions on the function of the immune system and catecholamine production simulated in a rodent model of hindlimb unloading. Neuroimmunomodulation 12, 173181.Google Scholar
Castro, VA, Thrasher, AN, Healy, M, Ott, CM and Pierson, DL (2004) Microbial characterization during the early habitation of the international space station. Microbial Ecology 47, 119126.10.1007/s00248-003-1030-yGoogle Scholar
Cohrs, RJ, Mehta, SK, Schmid, DS, Gilden, DH and Pierson, DL (2008) Asymptomatic reactivation and shed of infectious varicella zoster virus in astronauts. Journal of Medical Virology 80, 11161122.10.1002/jmv.21173Google Scholar
Crabbé, A, Pycke, B, Van Houdt, R, Monsieurs, P, Nickerson, C, Leys, N and Cornelis, P (2010) Response of pseudomonas aeruginosa PAO1 to low shear modelled microgravity involves AlgU regulation. Environmental Microbiology 12, 15451564.Google Scholar
Crucian, B, Zwart, S, Mehta, S, Stowe, R, Uchakin, P, Quiriarte, H, Pierson, D, Smith, SM, Sams, C (2013) Immune system dysregulation persists during long-duration spaceflight. Journal of Allergy and Clinical Immunology 131, AB210.Google Scholar
Crucian, BE, Stowe, RP, Pierson, DL and Sams, CF (2008) Immune system dysregulation following short- vs long-duration spaceflight. Aviation, Space, and Environmental Medicine 79, 835843.Google Scholar
Favel, A, Michel-Nguyen, A, Peyron, F, Martin, C, Thomachot, L, Datry, A, Bouchara, JP, Challier, S, Noël, T, Chastin, C and Regli, P (2003) Colony morphology switching of Candida lusitaniae and acquisition of multidrug resistance during treatment of a renal infection in a newborn: case report and review of the literature. Diagnostic Microbiology and Infectious Disease 47, 331339Google Scholar
Ferguson, M, Byrnes, C, Sun, L, Marti, G, Bonde, P, Duncan, M and Harmon, JW (2005) Wound healing enhancement: electroporation to address a classic problem of military medicine. World Journal of Surgery 29(Suppl. 1), S55S59.Google Scholar
Hawkins, JL and Baddour, LM (2003) Candida lusitaniae infections in the era of fluconazole availability. Journal of Biochemistry and Molecular Biology 36, e14e18.Google Scholar
Horneck, G, Klaus, DM and Mancinelli, RL (2010) Space microbiology. Microbiology and Molecular Biology Reviews 74, 121156.Google Scholar
Kacena, M and Todd, P (1997) Growth characteristics of E. coli and B. subtilis cultured on an agar substrate in microgravity. Microgravity Science and Technology 10, 5862.Google Scholar
Kambouris, ME, Zagoriti, Z, Lagoumintzis, G and Poulas, K (2014) From therapeutic electrotherapy to electroceuticals: formats, applications and prospects of electrostimulation. Annual Research & Review in Biology 4, 30543070.10.9734/ARRB/2014/10563Google Scholar
Khan, MSA, Malik, A and Ahmad, I (2012) Anti-candidal activity of essential oils alone and in combination with amphotericin B or fluconazole against multi-drug resistant isolates of Candida albicans. Medical Mycology 50, 3342.Google Scholar
Klaus, DM (2003) Space microbiology: microgravity and microorganisms. Encyclopedia of Environmental Microbiology 1–6, 29963003.Google Scholar
Kotnik, T, Pucihar, G and Miklavčič, D (2010) Induced transmembrane voltage and its correlation with electroporation-mediated molecular transport. Journal of Membrane Biology 236, 313.10.1007/s00232-010-9279-9Google Scholar
Krassowska, W and Filev, PD (2007) Modeling electroporation in a single cell. Biophysical Journal 92, 404417.Google Scholar
Lastauskiene, E, Zinkevičiene, A, Girkontaite, I, Kaunietis, A and Kvedariene, V (2014) Formic acid and acetic acid induce a programmed cell death in pathogenic Candida species. Current Microbiology 69, 303310.Google Scholar
Li, SL (2004) Electroporation gene therapy: new developments in vivo and in vitro. Current Gene Therapy 4, 309316.Google Scholar
Messer, SA, Jones, RN and Fritsche, TR (2006) International surveillance of Candida spp. and Aspergillus spp.: report from the SENTRY Antimicrobial Surveillance Program (2003). Journal of Clinical Microbiology 44, 17821787.Google Scholar
Messer, SA, Moet, GJ, Kirby, JT and Jones, RN (2009) Activity of contemporary antifungal agents, including the novel echinocandin anidulafungin, tested against Candida spp., Cryptococcus spp., and Aspergillus spp.: report from the SENTRY antimicrobial surveillance program (2006 to 2007). Journal of Clinical Microbiology 47, 19421946.Google Scholar
Miklavčič, D, Mali, B, Kos, B, Heller, R and Serša, G (2014) Electrochemotherapy: from the drawing board into medical practice. Biomedical Engineering Online 13, 29.Google Scholar
Miller, NS, Dick, JD and Merz, WG (2006) Phenotypic switching in Candida lusitaniae on copper sulfate indicator agar: association with amphotericin B resistance and filamentation. Journal of Clinical Microbiology 44, 15361539.Google Scholar
Mir, LM (2001) Therapeutic perspectives of in vivo cell electropermeabilization. Bioelectrochemistry 53, 110.Google Scholar
Montoro, J, Mullol, J, Jáuregui, I, Dávila, I, Ferrer, M, Bartra, J, Del Cuvillo, A, Sastre, J and Valero, A (2009) Stress and allergy. Journal of Investigational Allergology & Clinical Immunology 19, 4047.Google Scholar
Nickerson, CA, Ott, CM, Wilson, JW, Ramamurthy, R and Pierson, DL (2004) Microbial responses to microgravity and other low-shear environments. Microbiology and Molecular Biology Reviews 68, 345361.Google Scholar
Nislow, C, Lee, AY, Allen, PL, Giaever, G, Smith, A, Gebbia, M, Stodieck, LS, Hammond, JS, Birdsall, HH and Hammond, TG (2015) Genes required for survival in microgravity revealed by genome-wide yeast deletion collections cultured during spaceflight. Biomed Research International 2015, 976458.Google Scholar
Novickij, V, Grainys, A, Lastauskienė, E, Kananavičiūtė, R, Pamedytytė, D, Zinkevičienė, A, Kalėdienė, L, Novickij, J, Paškevičius, A and Švedienė, J (2015) Growth inhibition and membrane permeabilization of Candida lusitaniae using varied pulse shape electroporation. Biomed Research International 2015, 457896.Google Scholar
Novickij, V, Grainys, A, Lastauskienė, E, Kananavičiūtė, R, Pamedytytė, D, Kalėdienė, L, Novickij, J and Miklavčič, D (2016) Pulsed electromagnetic field assisted in vitro electroporation: a pilot study. Scientific Reports 6, 33537.Google Scholar
Ott, CM, Bruce, RJ and Pierson, DL (2004) Microbial characterization of free floating condensate aboard the mir space station. Microbial Ecology 47, 133136.10.1007/s00248-003-1038-3Google Scholar
Pfaller, MA, Castanheira, M, Messer, SA, Moet, GJ and Jones, RN (2010) Variation in Candida spp. distribution and antifungal resistance rates among bloodstream infection isolates by patient age: report from the SENTRY Antimicrobial Surveillance Program (2008–2009). Diagnostic Microbiology and Infectious Disease 68, 278283.Google Scholar
Pucihar, G, Kotnik, T, Valič, B and Miklavčič, D (2006) Numerical determination of transmembrane voltage induced on irregularly shaped cells. Annals of Biomedical Engineering 34, 642652.Google Scholar
Pucihar, G, Miklavčič, D and Kotnik, T (2009) A time-dependent numerical model of transmembrane voltage inducement and electroporation of irregularly shaped cells. IEEE Transactions on Biomedical Engineering 56, 14911501.Google Scholar
Rems, L and Miklavčič, D (2016) Tutorial: electroporation of cells in complex materials and tissue. Journal of Applied Physics 119, 201101.Google Scholar
Sack, M, Sigler, J, Frenzel, S, Eing, C, Arnold, J, Michelberger, T, Frey, W, Attmann, F, Stukenbrock, L and Müller, G (2010) Research on industrial-scale electroporation devices fostering the extraction of substances from biological tissue. Food Engineering Reviews 2, 147156.Google Scholar
Saulis, G (2010) Electroporation of cell membranes: the fundamental effects of pulsed electric fields in food processing. Food Engineering Reviews 2, 5273.Google Scholar
Sersa, G, Miklavcic, D, Cemazar, M, Rudolf, Z, Pucihar, G and Snoj, M (2008) Electrochemotherapy in treatment of tumours. European Journal of Surgical Oncology 34, 232240.Google Scholar
Sersa, G, Cemazar, M and Snoj, M (2009) Electrochemotherapy of tumours. Current Oncology 16, 3435.Google Scholar
Sonnenfeld, G (2005) The immune system in space, including Earth-based benefits of space-based research. Current Pharmaceutical Biotechnology 6, 343349.Google Scholar
Teissie, J (2014) Electropermeabilization of the cell membrane. Methods in Molecular Biology 1121, 2546.Google Scholar
Teissie, J, Golzio, M and Rols, MP (2005) Mechanisms of cell membrane electropermeabilization: a minireview of our present (lack of?) knowledge. Biochimica et Biophysica Acta 1724, 270280.Google Scholar
Thompson, DS, Carlisle, PL and Kadosh, D (2011) Coevolution of morphology and virulence in Candida species. Eukaryotic Cell 10, 11731182.Google Scholar
Tixador, R, Richoilley, G, Gasset, G, Templier, J, Bes, JC, Moatti, N and Lapchine, L (1985) Study of minimal inhibitory concentration of antibiotics on bacteria cultivated in vitro in space (Cytos 2 experiment). Aviation, Space, and Environmental Medicine 56, 748751.Google Scholar
Valič, B, Pavlin, M and Miklavčič, D (2004) The effect of resting transmembrane voltage on cell electropermeabilization: a numerical analysis. Bioelectrochemistry 63, 311315.Google Scholar
Wilson, JW, Ott, CM, Höner zu Bentrup, K, Ramamurthy, R, Quick, L, Porwollik, S, Cheng, P, McClelland, M, Tsaprailis, G, Radabaugh, T, Hunt, A, Fernandez, D, Richter, E, Shah, M, Kilcoyne, M, Joshi, L, Nelman-Gonzalez, M, Hing, S, Parra, M, Dumars, P, Norwood, K, Bober, R, Devich, J, Ruggles, A, Goulart, C, Rupert, M, Stodieck, L, Stafford, P, Catella, L, Schurr, MJ, Buchanan, K, Morici, L, McCracken, J, Allen, P, Baker-Coleman, C, Hammond, T, Vogel, J, Nelson, R, Pierson, DL, Stefanyshyn-Piper, HM and Nickerson, CA (2007) Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq. Proceedings of the National Academy of Sciences of the USA 104, 1629916304.Google Scholar
Zinkeviciene, A, Vaiciulioniene, N, Baranauskiene, I, Kvedariene, V, Emuzyte, R and Citavicius, D (2011) Cutaneous yeast microflora in patients with atopic dermatitis. Open Medicine 6, 713719.Google Scholar