Generic placeholder image

Infectious Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5265
ISSN (Online): 2212-3989

Research Article

Evaluation of Antimicrobial Effects of Photo-sonodynamic Antimicrobial Chemotherapy Based on Nano-micelle Curcumin on Virulence Gene Expression Patterns in Acinetobacter baumannii

Author(s): Maryam Pourhajibagher , Narjes Talaei and Abbas Bahador *

Volume 22, Issue 3, 2022

Published on: 11 January, 2022

Article ID: e201221199163 Pages: 8

DOI: 10.2174/1871526522666211220121725

Price: $65

Abstract

Background: Abaumannii baumannii rapidly resistant to a wide range of antimicrobial agents. The combination of Antimicrobial Photodynamic Therapy (aPDT) and Sonodynamic Antimicrobial Chemotherapy (SACT), known as Photo-Sonodynamic Antimicrobial Chemotherapy (PSACT), has received considerable attention as one of the emerging and promising strategies against microbial infections.

Objective: This study aimed to investigate the antimicrobial effects of PSACT based on nano-micelle curcumin (N-MCur) on the virulence gene expression patterns in A. baumannii.

Materials and Methods: N-MCur as a photo-sonosensitizer was synthesized and confirmed. To determine sub-significant reduction dose of PSACT, sub-significant reduction dose of N-MCur and blue laser light during aPDT, and ultrasound power output during SACT was assessed. Finally, changes in the expression of genes involved in treated A. baumannii by minimum sub-significant reduction dose of PSACT were determined using quantitative real-time-PCR (qRT-PCR).

Results: PSACT using 12.5 mM N-MCur at the ultrasound power outputs of 28.7, 36.9, and 45.2 mW/cm2 with 4 min irradiation time of the blue laser, as well as 6.2 mM N-MCur at an ultrasound power output of 45.2 mW/cm2 plus 3 min blue laser irradiation time exhibited the significant dosedependent reduction against A. baumannii cell viability compared to the control group (P<0.05). After treatment of A. baumannii using 3.1 mM N-MCur + 2 min blue laser irradiation time + 28.7 mW/cm2 ultrasound as the minimum sub-significant reduction doses of PSACT, mRNA expression was significantly upregulated to 6.0-, 11.2-, and 13.7-folds in recA, blsA, and dnaK and downregulated to 8.6-, 10.1-, and 14.5-folds in csuE, espA, and abaI, respectively.

Conclusion: N-MCur-mediated PSACT could regulate the expression of genes involved in A. baumannii pathogenesis. Therefore, PSACT can be proposed as a promising application to treat infections caused by A. baumannii.

Keywords: Acinetobacter baumannii, antimicrobial photodynamic therapy, sonodynamic therapy, biofilms, curcumin, chemotherapy.

Graphical Abstract

[1]
Ayoub Moubareck C, Hammoudi Halat D. Insights into Acinetobacter baumannii: a review of microbiological, virulence, and resistance traits in a threatening nosocomial pathogen. Antibiotics (Basel) 2020; 9(3): 119-23.
[http://dx.doi.org/10.3390/antibiotics9030119] [PMID: 32178356]
[2]
Tan YT, Tillett DJ, McKay IA. Molecular strategies for overcoming antibiotic resistance in bacteria. Mol Med Today 2000; 6(8): 309-14.
[http://dx.doi.org/10.1016/S1357-4310(00)01739-1] [PMID: 10904248]
[3]
Vrancianu CO, Gheorghe I, Czobor IB, Chifiriuc MC. Antibiotic resistance profiles, molecular mechanisms and innovative treatment strategies of Acinetobacter baumannii. Microorganisms 2020; 8(6): 935-75.
[http://dx.doi.org/10.3390/microorganisms8060935] [PMID: 32575913]
[4]
Gallagher P, Baker S. Developing new therapeutic approaches for treating infections caused by multi-drug resistant Acinetobacter baumannii: Acinetobacter baumannii therapeutics. J Infect 2020; 81(6): 857-61.
[http://dx.doi.org/10.1016/j.jinf.2020.10.016] [PMID: 33115656]
[5]
Russo A, Gavaruzzi F, Ceccarelli G, et al. Multidrug-resistant Acinetobacter baumannii infections in COVID-19 patients hospitalized in intensive care unit. Infection 2021; 1: 1-10.
[http://dx.doi.org/10.1007/s15010-021-01643-4] [PMID: 34176088]
[6]
Wang H, Wang J, Yu P, et al. Identification of antibiotic resistance genes in the multidrug-resistant Acinetobacter baumannii strain, MDR-SHH02, using whole-genome sequencing. Int J Mol Med 2017; 39(2): 364-72.
[http://dx.doi.org/10.3892/ijmm.2016.2844] [PMID: 28035408]
[7]
Ben Othman A, Zribi M, Masmoudi A, Abdellatif S, Ben Lakhal S, Fendri C. Multiresistance and endemic status of Acinetobacter baumannii associated with nosocomial infections in a tunisian hospital: a critical situation in the intensive care units. Braz J Microbiol 2011; 42(2): 415-22.
[http://dx.doi.org/10.1590/S1517-83822011000200001] [PMID: 24031648]
[8]
Pourhajibagher M, Mokhtaran M, Esmaeili D, Bahador A. Assessment of biofilm formation among Acinetobacter baumannii strains isolated from burned patients. Pharm Lett 2016; 8: 225-9.
[9]
Eze EC, Chenia HY, El Zowalaty ME. Acinetobacter baumannii biofilms: effects of physicochemical factors, virulence, antibiotic resistance determinants, gene regulation, and future antimicrobial treatments. Infect Drug Resist 2018; 11: 2277-99.
[http://dx.doi.org/10.2147/IDR.S169894] [PMID: 30532562]
[10]
Cha K, Oh HK, Jang JY, et al. Characterization of two novel bacteriophages infecting Multidrug-Resistant (MDR) Acinetobacter baumannii and evaluation of their therapeutic efficacy in vivo. Front Microbiol 2018; 9: 696.
[http://dx.doi.org/10.3389/fmicb.2018.00696] [PMID: 29755420]
[11]
Wang Y, Li J, Geng S, et al. Aloe-emodin-mediated antimicrobial photodynamic therapy against multidrug-resistant Acinetobacter baumannii: an in vivo study. Photodiagn Photodyn Ther 2021; 34: 102311.
[http://dx.doi.org/10.1016/j.pdpdt.2021.102311] [PMID: 33930578]
[12]
Pourhajibagher M, Partoazar A, Alaeddini M, Etemad-Moghadam S, Bahador A. Photodisinfection effects of silver sulfadiazine nanoliposomes doped-curcumin on Acinetobacter baumannii: a mouse model. Nanomedicine (Lond) 2020; 15(5): 437-52.
[http://dx.doi.org/10.2217/nnm-2019-0315] [PMID: 32028870]
[13]
Pourhajibagher M, Bahador A. In vitro application of sonodynamic antimicrobial chemotherapy as a sonobactericidal therapeutic approach for bacterial infections: a systematic review and meta-analysis. J Lasers Med Sci 2020; 11(4)(Suppl. 1): S1-7.
[http://dx.doi.org/10.34172/jlms.2020.S1] [PMID: 33995962]
[14]
Serpe L, Giuntini F. Sonodynamic antimicrobial chemotherapy: First steps towards a sound approach for microbe inactivation. J Photochem Photobiol B 2015; 150: 44-9.
[http://dx.doi.org/10.1016/j.jphotobiol.2015.05.012] [PMID: 26037696]
[15]
Jurenka JS. Anti-inflammatory properties of curcumin, a major constituent of Curcuma longa: a review of preclinical and clinical research. Altern Med Rev 2009; 14(2): 141-53.
[PMID: 19594223]
[16]
Trigo Gutierrez JK, Zanatta GC, Ortega ALM, et al. Encapsulation of curcumin in polymeric nanoparticles for antimicrobial Photodynamic Therapy. PLoS One 2017; 12(11): e0187418.
[http://dx.doi.org/10.1371/journal.pone.0187418] [PMID: 29107978]
[17]
Pourhajibagher M, Rahimi Esboei B, Hodjat M, Bahador A. Sonodynamic excitation of nanomicelle curcumin for eradication of Streptococcus mutans under sonodynamic antimicrobial chemotherapy: enhanced anti-caries activity of nanomicelle curcumin. Photodiagn Photodyn Ther 2020; 30: 101780.
[http://dx.doi.org/10.1016/j.pdpdt.2020.101780] [PMID: 32315777]
[18]
Wang Z, Liu C, Zhao Y, Hu M, Ma D, Zhang P. Photomagnetic nanoparticles in dual-modality imaging and photo-sonodynamic activity against bacteria. Chem Eng J 2019; 356: 811-8.
[http://dx.doi.org/10.1016/j.cej.2018.09.077]
[19]
Pang X, Li D, Zhu J, Cheng J, Liu G. Beyond antibiotics: photo/sonodynamic approaches for bacterial theranostics. Nano-Micro Lett 2020; 12(1): 144.
[http://dx.doi.org/10.1007/s40820-020-00485-3] [PMID: 34138184]
[20]
Liu Y, Chen S, Sun J, et al. Folate-targeted and oxygen/indocyanine green-loaded lipid nanoparticles for dual-mode imaging and photo-sonodynamic/photothermal therapy of ovarian cancer in vitro and in vivo. Mol Pharm 2019; 16(10): 4104-20.
[http://dx.doi.org/10.1021/acs.molpharmaceut.9b00339] [PMID: 31517495]
[21]
Pourhajibagher M, Boluki E, Chiniforush N, et al. Modulation of virulence in Acinetobacter baumannii cells surviving photodynamic treatment with toluidine blue. Photodiagn Photodyn Ther 2016; 15: 202-12.
[http://dx.doi.org/10.1016/j.pdpdt.2016.07.007] [PMID: 27444886]
[22]
Miles AA, Misra SS, Irwin JO. The estimation of the bactericidal power of the blood. J Hyg (Lond) 1938; 38(6): 732-49.
[PMID: 20475467]
[23]
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001; 25(4): 402-8.
[http://dx.doi.org/10.1006/meth.2001.1262] [PMID: 11846609]
[24]
Rosenthal I, Sostaric JZ, Riesz P. Sonodynamic therapy-a review of the synergistic effects of drugs and ultrasound. Ultrason Sonochem 2004; 11(6): 349-63.
[http://dx.doi.org/10.1016/j.ultsonch.2004.03.004] [PMID: 15302020]
[25]
Pan X, Wang H, Wang S, et al. Sonodynamic therapy (SDT): a novel strategy for cancer nanotheranostics. Sci China Life Sci 2018; 61(4): 415-26.
[http://dx.doi.org/10.1007/s11427-017-9262-x] [PMID: 29666990]
[26]
Wan GY, Liu Y, Chen BW, Liu YY, Wang YS, Zhang N. Recent advances of sonodynamic therapy in cancer treatment. Cancer Biol Med 2016; 13(3): 325-38.
[http://dx.doi.org/10.20892/j.issn.2095-3941.2016.0068] [PMID: 27807500]
[27]
Wang X, Zhong X, Gong F, Chao Y, Cheng L. Newly developed strategies for improving sonodynamic therapy. Mater Horiz 2020; 7(8): 2028-46.
[http://dx.doi.org/10.1039/D0MH00613K]
[28]
Trendowski M. The promise of sonodynamic therapy. Cancer Metastasis Rev 2014; 33(1): 143-60.
[http://dx.doi.org/10.1007/s10555-013-9461-5] [PMID: 24346159]
[29]
Kolarova H, Tomankova K, Bajgar R, Kolar P, Kubinek R. Photodynamic and sonodynamic treatment by phthalocyanine on cancer cell lines. Ultrasound Med Biol 2009; 35(8): 1397-404.
[http://dx.doi.org/10.1016/j.ultrasmedbio.2009.03.004] [PMID: 19515482]
[30]
Costley D, Mc Ewan C, Fowley C, et al. Treating cancer with sonodynamic therapy: a review. Int J Hyperthermia 2015; 31(2): 107-17.
[http://dx.doi.org/10.3109/02656736.2014.992484] [PMID: 25582025]
[31]
Alves F, Pavarina AC, Mima EGO, McHale AP, Callan JF. Antimicrobial sonodynamic and photodynamic therapies against Candida albicans. Biofouling 2018; 34(4): 357-67.
[http://dx.doi.org/10.1080/08927014.2018.1439935] [PMID: 29671631]
[32]
Shen Y, Ou J, Chen X, et al. An in vitro study on sonodynamic treatment of human colon cancer cells using sinoporphyrin sodium as sonosensitizer. Biomed Eng Online 2020; 19(1): 52.
[http://dx.doi.org/10.1186/s12938-020-00797-w] [PMID: 32552718]
[33]
Xu F, Hu M, Liu C, Choi SK. Yolk-structured multifunctional up-conversion nanoparticles for synergistic photodynamic-sonodynamic antibacterial resistance therapy. Biomater Sci 2017; 5(4): 678-85.
[http://dx.doi.org/10.1039/C7BM00030H] [PMID: 28280817]
[34]
Golic A, Vaneechoutte M, Nemec A, Viale AM, Actis LA, Mussi MA. Staring at the cold sun: blue light regulation is distributed within the genus Acinetobacter. PLoS One 2013; 8(1): e55059.
[http://dx.doi.org/10.1371/journal.pone.0055059] [PMID: 23358859]
[35]
Mussi MA, Gaddy JA, Cabruja M, et al. The opportunistic human pathogen Acinetobacter baumannii senses and responds to light. J Bacteriol 2010; 192(24): 6336-45.
[http://dx.doi.org/10.1128/JB.00917-10] [PMID: 20889755]
[36]
Brust R, Haigney A, Lukacs A, et al. Ultrafast structural dynamics of BlsA, a photoreceptor from the pathogenic bacterium Acinetobacter baumannii. J Phys Chem Lett 2014; 5(1): 220-4.
[http://dx.doi.org/10.1021/jz4023738] [PMID: 24723998]
[37]
Gayoso CM, Mateos J, Méndez JA, et al. Molecular mechanisms involved in the response to desiccation stress and persistence in Acinetobacter baumannii. J Proteome Res 2014; 13(2): 460-76.
[http://dx.doi.org/10.1021/pr400603f] [PMID: 24299215]
[38]
Cardoso K, Gandra RF, Wisniewski ES, et al. DnaK and GroEL are induced in response to antibiotic and heat shock in Acinetobacter baumannii. J Med Microbiol 2010; 59(Pt 9): 1061-8.
[http://dx.doi.org/10.1099/jmm.0.020339-0] [PMID: 20576751]
[39]
Aranda J, Bardina C, Beceiro A, et al. Acinetobacter baumannii RecA protein in repair of DNA damage, antimicrobial resistance, general stress response, and virulence. J Bacteriol 2011; 193(15): 3740-7.
[http://dx.doi.org/10.1128/JB.00389-11] [PMID: 21642465]
[40]
Bales PM, Renke EM, May SL, Shen Y, Nelson DC. Purification and characterization of biofilm-associated EPS exopolysaccharides from ESKAPE organisms and other pathogens. PLoS One 2013; 8(6): e67950.
[http://dx.doi.org/10.1371/journal.pone.0067950] [PMID: 23805330]
[41]
McConnell MJ, Actis L, Pachón J. Acinetobacter baumannii: human infections, factors contributing to pathogenesis and animal models. FEMS Microbiol Rev 2013; 37(2): 130-55.
[http://dx.doi.org/10.1111/j.1574-6976.2012.00344.x] [PMID: 22568581]
[42]
Tang J, Chen Y, Wang X, Ding Y, Sun X, Ni Z. Contribution of the AbaI/AbaR quorum sensing system to resistance and virulence of Acinetobacter baumannii clinical strains. Infect Drug Resist 2020; 13: 4273-81.
[http://dx.doi.org/10.2147/IDR.S276970] [PMID: 33262621]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy