Cytotoxicity and Antibacterial Effect of Trp-Substituted CM11 Cationic Peptide Against Drug-Resistant Isolates of Brucella melitensis Alone and in Combination with Recommended Antibiotics

Abdel-Maksoud M, House B, Wasfy M, Abdel-Rahman B, Pimentel G, Roushdy G, Dueger E (2012) In vitro antibiotic susceptibility testing of Brucella isolates from Egypt between 1999 and 2007 and evidence of probable rifampin resistance. Ann Clin Microbiol Antimicrob 11:24 Akhvlediani T et al (2017) Epidemiological and clinical features of brucellosis in the country of Georgia. PLoS ONE 12:e0170376 Amani J, A Barjini K, Moghaddam M, Asadi M A (2015) In vitro synergistic effect of the CM11 antimicrobial peptide in combination with common antibiotics against clinical isolates of six species of multidrug-resistant pathogenic bacteria. Protein Pept Lett 22:940–951 Andreu D, Ubach J, Boman A, Wåhlin B, Wade D, Merrifield R, Boman HG (1992) Shortened cecropin A-melittin hybrids significant size reduction retains potent antibiotic activity. FEBS Lett 296:190–194 Asadi FT, Hashemi SH, Alikhani MY, Moghimbeigi A, Naseri Z (2017) Clinical and diagnostic aspects of brucellosis and antimicrobial susceptibility of Brucella isolates in Hamedan. Iran Jpn J Infect Dis 70:235–238 Bacalum M, Radu M (2015) Cationic antimicrobial peptides cytotoxicity on mammalian cells: an analysis using therapeutic index integrative concept. Int J Pept Res Ther 21:47–55 Barbosa Pauletti R et al. (2015) Reduced susceptibility to rifampicin and resistance to multiple antimicrobial agents among Brucella abortus isolates from cattle in Brazil. PLoS ONE 10:e0132532 Bayram Y, Korkoca H, Aypak C, Parlak M, Cikman A, Kilic S, Berktas M (2011) Antimicrobial susceptibilities of Brucella isolates from various clinical speciemens. Int J Med Sci 8:198 Bi X, Wang C, Ma L, Sun Y, Shang D (2013) Investigation of the role of tryptophan residues in cationic antimicrobial peptides to determine the mechanism of antimicrobial action. J Appl Microbiol 115:663–672 Bi X, Wang C, Dong W, Zhu W, Shang D (2014) Antimicrobial properties and interaction of two Trp-substituted cationic antimicrobial peptides with a lipid bilayer. J Antibiot 67:361 Biemer JJ (1973) Antimicrobial susceptibility testing by the Kirby-Bauer disc diffusion method Ann Clin Lab Sci 3:135–140 Cardoso PG, Macedo GC, Azevedo V, Oliveira SC (2006) Brucella spp noncanonical LPS: structure, biosynthesis, and interaction with host immune system. Microb Cell Fact 5:13 Chan DI, Prenner EJ, Vogel HJ (2006) Tryptophan- and arginine-rich antimicrobial peptides: structures and mechanisms of action. Biochim et Biophys Acta 1758:1184–1202. https://doi.org/10.1016/j.bbamem.2006.04.006 Chattopadhyay A, Rawat SS, Greathouse DV, Kelkar DA, Koeppe RE (2008) Role of tryptophan residues in gramicidin channel organization and function. Biophys J 95:166–175 del Pozo JSG, Solera J (2012) Systematic review and meta-analysis of randomized clinical trials in the treatment of human brucellosis. PLoS ONE 7:e32090 Deshmukh A et al (2015) In vitro antimicrobial susceptibility testing of human Brucella melitensis isolates from Qatar between 2014–2015. BMC Microbiol 15:121 Dougherty DA (1996) Cation-pi interactions in chemistry and biology: a new view of benzene, Phe, Tyr, and Trp. Science 271:163–168 Eze MO et al (2000) Effects of opsonization and gamma interferon on growth of Brucella melitensis 16M in mouse peritoneal macrophages in vitro. Infect Immun 68:257–263 Guerra H (2007) The brucellae and their success as pathogens. Crit Rev Microbiol 33:325–331 Hasani SM, Mirnejad R, Amani J, javad Vafadar M (2016) Comparing rapid and specific detection of Brucella in clinical samples by PCR-ELISA and multiplex-PCR method. Iran J Pathol 11:144 Hashim R et al. (2014) Identification and in vitro antimicrobial susceptibility of Brucella species isolated from human brucellosis. Int J Microbiol 2014:5 Heiat M, Aghamollaei H, Moghaddam MM, Kooshki H (2014) Using CM11 peptide as a cell permeable agent for the improvement of conventional plasmid transformation methods in Escherichia coli and Bacillus subtilis. Minerva Biotechnol 26:149–157 Jin L et al (2016) A designed tryptophan- and lysine/arginine-rich antimicrobial peptide with therapeutic potential for clinical antibiotic-resistant candida albicans vaginitis. J Med Chem 59:1791–1799. https://doi.org/10.1021/acs.jmedchem.5b01264 Juffer AH, Shepherd CM, Vogel HJ (2001) Protein–membrane electrostatic interactions: application of the Lekner summation technique. J Chem Phys 114:1892–1905 Kaminski HM, Feix JB (2011) Effects of d-lysine substitutions on the activity and selectivity of antimicrobial peptide CM. Polymers 3(4):2088–2106 Khandelia H, Kaznessis YN (2007) Cation–π interactions stabilize the structure of the antimicrobial peptide indolicidin near membranes: molecular dynamics simulations. J Phys Chem B 111:242–250 Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132 Lorian V (2005) Antibiotics in laboratory medicine. Lippincott Williams & Wilkins, Philadelphia Matsueda GR, Stewart JM (1981) A p-methylbenzhydrylamine resin for improved solid-phase synthesis of peptide amides. Peptides 2:45–50 Maves RC et al (2011) Antimicrobial susceptibility of Brucella melitensis isolates in Peru. Antimicrob Agents Chemother 55:1279–1281 Moghaddam MM, Abolhassani F, Babavalian H, Mirnejad R, Barjini KA, Amani J (2012) Comparison of in vitro antibacterial activities of two cationic peptides CM15 and CM11 against five pathogenic bacteria: Pseudomonas aeruginosa, Staphylococcus aureus, Vibrio cholerae, Acinetobacter baumannii, and Escherichia coli. Probiotics Antimicrob Proteins 4:133–139 Moghaddam MM, Barjini KA, Ramandi MF, Amani J (2014) Investigation of the antibacterial activity of a short cationic peptide against multidrug-resistant Klebsiella pneumoniae and Salmonella typhimurium strains and its cytotoxicity on eukaryotic cells. World J Microbiol Biotechnol 30:1533–1540. https://doi.org/10.1007/s11274-013-1575-y Moghaddam MM, Aghamollaei H, Kooshki H, Barjini KA, Mirnejad R, Choopani A (2015) The development of antimicrobial peptides as an approach to prevention of antibiotic resistance. Rev Med Microbiol 26:98–110 Mohammadi Azad Z, Moravej H, Fasihi-Ramandi M, Masjedian F, Nazari R, Mirnejad R, Moosazadeh Moghaddam M (2017) In vitro synergistic effects of a short cationic peptide and clinically used antibiotics against drug-resistant isolates of Brucella melitensis. J Med Microbiol. https://doi.org/10.1099/jmm.0.000524 Musallam I, Abo-Shehada M, Hegazy Y, Holt H, Guitian F (2016) Systematic review of brucellosis in the Middle East: disease frequency in ruminants and humans and risk factors for human infection. Epidemiol Infect 144:671–685 Olsen S, Palmer M (2014) Advancement of knowledge of Brucella over the past 50 years. Vet Pathol 51:1076–1089 Pappas G, Papadimitriou P, Akritidis N, Christou L, Tsianos EV (2006) The new global map of human brucellosis. Lancet Infect Dis 6:91–99 Persson S, Killian JA, Lindblom G (1998) Molecular ordering of interfacially localized tryptophan analogs in ester- and ether-lipid bilayers studied by 2H-NMR. Biophys J 75:1365–1371 Petersen FN, Jensen MO, Nielsen CH (2005) Interfacial tryptophan residues: a role for the cation-pi effect? Biophys J 89:3985–3996. https://doi.org/10.1529/biophysj.105.061804 Piranfar V, Sharif M, Hashemi M, Vahdati AR, Mirnejad R (2015) Detection and discrimination of two Brucella species by multiplex real-time PCR and high-resolution melt analysis curve from human blood and comparison of results using RFLP. Iran J Basic Med Sci 18:909 Ramandi F, Piranfar M, J Nadoushan V, R Sarshoori M, Misialek JJ, Heiat M, Moosazadeh Moghaddam M M (2017) Dose-response effects of the CM11 as a short cationic antimicrobial peptide on histopathological and biochemical changes mice. Curr Chem Biol 11:150–157 Rashidi K, Motaharinia Y, Rezaee MA, Asadzade N, Hazhir MS, Mohsenpour B, Hossaini W, Zandi F, Rahmani MR (2011) Determination of antibiotic resistance of Brucella spp. isolated from brucellosis patients in Kurdistan. J Large Anim Clin Sci Res 4:41–48 (in Persian) Razzaghi R, Rastegar R, Momen-Heravi M, Erami M, Nazeri M (2016) Antimicrobial susceptibility testing of Brucella melitensis isolated from patients with acute brucellosis in a centre of Iran. Indian J Med Microbiol 34:342 Saberi F, Kamali M, Taheri RA, Ramandi MF, Bagdeli S, Mirnejad R (2016) Development of surface plasmon resonance-based immunosensor for detection of Brucella melitensis. J Braz Chem Soc 27:1960–1965 Shepherd CM, Schaus KA, Vogel HJ, Juffer AH (2001) Molecular dynamics study of peptide-bilayer adsorption. Biophys J 80:579–596 Silva MT (2012) Classical labeling of bacterial pathogens according to their lifestyle in the host: inconsistencies and alternatives. Front Microbiol 3:71 Wayne P (2011) Clinical and Laboratory Standards Institute; 2011 CLSI Performance standards for antimicrobial susceptibility testing 20th Informational Supplement CLSI document M100-S21 Yau W-M, Wimley WC, Gawrisch K, White SH (1998a) The preference of tryptophan for membrane interfaces. Biochemistry 37:14713–14718 Yau WM, Wimley WC, Gawrisch K, White SH (1998b) The preference of tryptophan for membrane interfaces. Biochemistry 37:14713–14718. https://doi.org/10.1021/bi980809c Zhu X, Ma Z, Wang J, Chou S, Shan A (2014) Importance of tryptophan in transforming an amphipathic peptide into a Pseudomonas aeruginosa-targeted antimicrobial peptide. PLoS ONE 9:e114605