We use cookies to improve your experience. By continuing to browse this site, you accept our cookie policy.×
Skip main navigation
Aging Health
Bioelectronics in Medicine
Biomarkers in Medicine
Breast Cancer Management
CNS Oncology
Colorectal Cancer
Concussion
Epigenomics
Future Cardiology
Future Medicine AI
Future Microbiology
Future Neurology
Future Oncology
Future Rare Diseases
Future Virology
Hepatic Oncology
HIV Therapy
Immunotherapy
International Journal of Endocrine Oncology
International Journal of Hematologic Oncology
Journal of 3D Printing in Medicine
Lung Cancer Management
Melanoma Management
Nanomedicine
Neurodegenerative Disease Management
Pain Management
Pediatric Health
Personalized Medicine
Pharmacogenomics
Regenerative Medicine

Identification and characterization of Staphylococcus spp. and their susceptibility to insect apolipophorin III

    Marta Palusińska-Szysz

    *Author for correspondence:

    E-mail Address: marta.szysz@poczta.umcs.lublin.pl

    Department of Genetics and Microbiology, Institute of Biological Sciences, Faculty of Biology & Biotechnology, Maria Curie-Sklodowska University, Akademicka 19 St., 20-033 Lublin, Poland

    ,
    Agnieszka Zdybicka-Barabas

    Department of Immunobiology, Institute of Biological Sciences, Faculty of Biology & Biotechnology, Maria Curie-Sklodowska University, Akademicka 19 St., 20-033 Lublin, Poland

    ,
    Magdalena Frąc

    Institute of Agrophysics, Polish Academy of Sciences, Doświadczalna 4 St., 20-290 Lublin, Poland

    ,
    Wiesław I Gruszecki

    Department of Biophysics, Institute of Physics, Maria Curie-Skłodowska University, Maria Curie-Skłodowska Square 1, 20-031 Lublin, Poland

    ,
    Sylwia Wdowiak-Wróbel

    Department of Genetics and Microbiology, Institute of Biological Sciences, Faculty of Biology & Biotechnology, Maria Curie-Sklodowska University, Akademicka 19 St., 20-033 Lublin, Poland

    ,
    Emilia Reszczyńska

    Department of Plant Physiology & Biophysics, Institute of Biological Sciences, Faculty of Biology & Biotechnology, Maria Curie-Skłodowska University, Akademicka 19 St., 20-033 Lublin, Poland

    ,
    Dorota Skorupska

    Dermatological Clinic, Jana Sawy 1B St., 20-632 Lublin, Poland

    ,
    Paweł Mak

    Department of Analytical Biochemistry, Faculty of Biochemistry, Biophysics & Biotechnology, Jagiellonian University, Gronostajowa 7 St., 30-387 Krakow

    &
    Małgorzata Cytryńska

    Department of Immunobiology, Institute of Biological Sciences, Faculty of Biology & Biotechnology, Maria Curie-Sklodowska University, Akademicka 19 St., 20-033 Lublin, Poland

    Published Online:https://doi.org/10.2217/fmb-2019-0328

    Aim: This study investigated the effect of an insect antimicrobial protein, apolipophorin III (apoLp-III), against two newly isolated, identified and characterized clinical strains of Staphylococcus spp. Materials & methods: Both strains were identified by 16S rRNA sequencing and metabolic and phenotypic profiling. The antibacterial activity of apoLp-III was tested using a colony counting assay. ApoLp-III interaction with bacterial cell surface was analyzed by Fourier transform IR spectroscopy. Results:Staphylococcus epidermidis and Staphylococcus capitis were identified. ApoLp-III exerted a dose-dependent bactericidal effect on the tested strains. The differences in the Staphylococcus spp. surface components may contribute to the various sensitivities of these strains to apoLp-III. Conclusion: ApoLp-III may provide a baseline for development of antibacterial preparations against Staphylococcus spp. involved in dermatological problems.

    Papers of special note have been highlighted as: • of interest; •• of considerable interest

    References

    • 1. Dwivedi P, Tomar RS. Growing of Staphylococcus aureus cells with soil components enhances virulence in mice caused by soft tissue infections. Int. J. Pharma Bio Sci. Spl. Ed. (Int-BIONANO 2016) Conference Proceedings (ISSN: 0975-6299) 230–236 (2016).
    • 2. Binomar M, Al Qumaizi K, Al Shaqha WM, Khan FI, Bobbitt K, Anwer R. Screening of different soil sources of New York City for antimicrobial activity against methicillin-resistant Staphylococcus aureus (MRSA). J. Pure Appl. Microbiol. 9(2), 77–86 (2015).
    • 3. Chambers HF, Deleo FR. Waves of resistance: staphylococcus aureus in the antibiotic era. Nat. Rev. Microbiol. 7(9), 629–641 (2009).
    • 4. Domingo P, Fontanet A. Management of complications associated with totally implantable ports in patients with AIDS. AIDS Patient Care STDS 15(1), 7–13 (2001).
    • 5. Ghassemi A, Farhangi H, Badiee Z, Banihashem A, Mosaddegh MR. Evaluation of nosocomial infection in patients at hematology-oncology ward of Dr. Sheikh Children's Hospital. Iran. J. Ped. Hematol. Oncol. 5(4), 179–185 (2015).
    • 6. Wu H, Moser C, Wang HZ, Høiby N, Song ZJ. Strategies for combating bacterial biofilm infections. Int. J. Oral Sci. 7(1), 1–7 (2014).
    • 7. Sabaté Brescó M, Harris LG, Thompson K et al. Pathogenic mechanisms and host interactions in Staphylococcus epidermidis device-related infection. Front. Microbiol. 8(1401), 1–24 (2017).
    • 8. Becker K, Heilmann C, Peters G. Coagulase-negative staphylococci. Clin. Microbiol. Rev. 27(4), 870–926 (2014).
    • 9. Chong J, Quach C, Blanchard AC et al. Molecular epidemiology of a vancomycin-intermediate heteroresistant Staphylococcus epidermidis outbreak in a neonatal intensive care unit. Antimicrob. Agents Chemother. 60(10), 5673–5681 (2016).
    • 10. Mendes RE, Deshpande LM, Costello AJ, Farrell DJ. Molecular epidemiology of Staphylococcus epidermidis clinical isolates from U.S. hospitals. Antimicrob. Agents Chemother. 56(9), 4656–4661 (2012).
    • 11. Najar-Peerayeh S, Moghadas AJ, Behmanesh M. Antibiotic susceptibility and mecA frequency in Staphylococcus epidermidis, isolated from Intensive Care Unit patients. Jundishapur J. Microbiol. 7(8), e11188 (2014).
    • 12. Barbier F, Ruimy R, Barbier F et al. Methicillin-resistant coagulase-negative staphylococci in the community: high homology of SCCmec IVa between Staphylococcus epidermidis and major clones of methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 202(2), 270–281 (2010).
    • 13. Widerström M, McCullough CA, Coombs GW, Monsen T, Christiansen KJ. A multidrug-resistant Staphylococcus epidermidis clone (ST2) is an ongoing cause of hospital-acquired infection in a Western Australian Hospital. J. Clin. Microbiol. 50(6), 2147–2151 (2012).
    • 14. Wojda I. Immunity of the greater wax moth Galleria mellonella. Insect Sci. 24(3), 342–357 (2017).
    • 15. Cutuli MA, Petronio Petronio G, Vergalito F et al. Galleria mellonella as a consolidated in vivo model hosts: new developments in antibacterial strategies and novel drug testing. Virulence 10(1), 527–541 (2019). •• Summarizes the existing knowledge about use of Galleria mellonella larvae as alternative model host.
    • 16. Rossoni RD, Ribeiro FC, Dos Santos HFS et al. Galleria mellonella as an experimental model to study human oral pathogens. Arch. Oral Biol. 101, 13–22 (2019).
    • 17. Hernandez RJ, Hesse E, Dowling AJ et al. Using the wax moth larva Galleria mellonella infection model to detect emerging bacterial pathogens. PeerJ 6, e6150 (2019).
    • 18. Sheehan G, Dixon A, Kavanagh K. Utilization of Galleria mellonella larvae to characterize the development of Staphylococcus aureus infection. Microbiology 165(8), 863–875 (2019).
    • 19. Niere M, Dettloff M, Maier T, Ziegler M, Wiesner A. Insect immune activation by apolipophorin III is correlated with the lipid-binding properties of this protein. Biochemistry 40(38), 11502–11508 (2001).
    • 20. Chiu MH, Wan Ch-P, Weers PMM, Prenner EJ. Apolipophorin III interaction with model membranes composed of phosphatidylcholine and sphingomyelin using differential scanning calorimetry. Biochim. Biophys. Acta 1788(10), 2160–2168 (2009).
    • 21. Garda HA, Arrese EL, Soulages JL. Structure of apolipophorin III in discoidal lipoproteins. Interhelical distances in the lipid-bound state and conformational change upon binding to lipid. J. Biol. Chem. 277(22), 19773–19782 (2002).
    • 22. Sahoo D, Weers PMM, Ryan RO, Narayanaswami V. Lipid triggered molecular switch of apoLp-III helix bundle to an extended helix conformation. J. Mol. Biol. 321(2), 201–214 (2002).
    • 23. Van der Horst DJ, Van Hoof D, Van Marrewijk WJA, Rodenburg KW. Alternative lipid mobilization: the insect shuttle system. Mol. Cell. Biochem. 239(1–2), 113–119 (2002).
    • 24. Weers PM, Ryan RO. Apolipophorin III: role model apolipoprotein. Insect. Biochem. Mol. Biol. 36(4), 231–240 (2006).
    • 25. Zdybicka-Barabas A, Cytryńska M. Apolipophorins and insects immune response. Invert. Surviv. J. 10(1), 58–68 (2013). •• Describes the role of apolipophorins, with a special emphasis on apolipophorin III, in insect immune response.
    • 26. Whitten MM, Tew IF, Lee BL, Ratcliffe NA. A novel role for an insect apolipoprotein (apolipophorin III) in beta-1,3-glucan pattern recognition and cellular encapsulation reactions. J. Immunol. 172(4), 2177–2185 (2004).
    • 27. Zdybicka-Barabas A, Januszanis B, Mak P, Cytryńska M. An atomic force microscopy study of Galleria mellonella apolipophorin III effect on bacteria. Biochim. Biophys. Acta 1808(7), 1896–1906 (2011).
    • 28. Oztug M, Martinon D, Weers PM. Characterization of the apoLp-III/LPS complex: insight into the mode of binding interaction. Biochemistry 51(31), 6220–6227 (2012).
    • 29. Halwani AE, Niven DF, Dunphy GB. Apolipophorin-III and the interactions of lipoteichoic acids with the immediate immune responses of Galleria mellonella. J. Invertebr. Pathol. 76, 233–241 (2000).
    • 30. Leon LJ, Idangodage H, Wan CL, Weers PMM. Apolipophorin III: lipopolysaccharide binding requires helix bundle opening. Biochem. Biophys. Res. Commun. 348(4), 1328–1333 (2006).
    • 31. Pratt CC, Weers PMM. Lipopolysaccharide binding of an exchangeable apolipoprotein, apolipophorin III, from Galleria mellonella. Biol. Chem. 385(11), 1113–1119 (2004).
    • 32. Zakarian RJ, Dunphy GB, Albert PJ, Rau ME. Apolipophorin-III affects the activity of the haemocytes of Galleria mellonella larvae. J. Insect Physiol. 48(7), 715–723 (2002).
    • 33. Götz P, Weise C, Kopacek P, Losen S, Wiesner A. Isolated apolipophorin III from Galleria mellonella stimulates the immune reactions of this insect. J. Insect Physiol. 43(4), 383–391 (1997).
    • 34. Halwani AE, Dunphy GB. Apolipophorin III in Galleria mellonella potentiates hemolymph lytic activity. Dev. Comp. Immunol. 23(7–8), 563–570 (1999).
    • 35. Niere M, Meisslitzer C, Dettloff M, Weise C, Ziegler M, Wiesner A. Insect immune activation by recombinant Galleria mellonella apolipophorin III. Biochim. Biophys. Acta 1433(1–2), 16–26 (1999).
    • 36. Kim HJ, Je HJ, Park SY et al. Immune activation of apolipophorin-III and its distribution in hemocyte from Hyphantria cunea. Insect Biochem. Mol. Biol. 34(10), 1011–1023 (2004).
    • 37. Zdybicka-Barabas A, Stączek S, Mak P, Skrzypiec K, Mendyk E, Cytryńska M. Synergistic action of Galleria mellonella apolipophorin III and lysozyme against Gram-negative bacteria. Biochim. Biophys. Acta 1828(6), 1449–1456 (2013).
    • 38. Zdybicka-Barabas A, Cytryńska M. Involvement of apolipophorin III in antibacterial defense of Galleria mellonella larvae. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 158(1), 90–98 (2011).
    • 39. Zdybicka-Barabas A, Stączek S, Mak P, Piersiak T, Skrzypiec K, Cytryńska M. The effect of Galleria mellonella apolipophorin III on yeasts and filamentous fungi. J. Insect Physiol. 58(1), 164–177 (2012).
    • 40. Zdybicka-Barabas A, Palusińska-Szysz M, Gruszecki WI, Mak P, Cytryńska M. Galleria mellonella apolipophorin III – an apolipoprotein with anti-Legionella pneumophila activity. Biochim. Biophys. Acta 1838(10), 2689–2697 (2014). • Reports on anti-Legionella pneumophila activity of insect apolipophorin III and possible mechanism responsible for this activity.
    • 41. Palusińska-Szysz M, Zdybicka-Barabas A, Pawlikowska-Pawlęga B, Mak P, Cytryńska M. Anti-Legionella dumoffii activity of Galleria mellonella defensin and apolipophorin III. Int. J. Mol. Sci. 13(12), 17048–17064 (2012).
    • 42. Palusińska-Szysz M, Zdybicka-Barabas A, Reszczyńska E et al. The lipid composition of Legionella dumoffii membrane modulates the interaction with Galleria mellonella apolipophorin III. Biochim. Biophys. Acta 1861(7), 617–629 (2016).
    • 43. Pitcher DG, Saunders NA, Owen RJ. Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett. Appl. Microbiol. 8(4), 151–156 (1989).
    • 44. Weisburg WG, Barns SM, Pelletier DA et al. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol. 173(2), 697–703 (1991).
    • 45. Liu D. Molecular Detection of Human Bacterial Pathogens. CRC Press, Boca Raton, FL, USA (2011).
    • 46. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680 (1994).
    • 47. Nicholas KB, Nicholas HBJ. GeneDoc. Pittsburgh Supercomputing Center, Pittsburgh, PA, USA (1997).
    • 48. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30(12), 2725–2729 (2013).
    • 49. Felsenstein J. PHYLIP. Phylogeny Inference Package, version 3.5c., University of Washington, Seattle, WA, USA (1993).
    • 50. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16(2), 111–120 (1980).
    • 51. Page RD. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12(4), 357–358 (1996).
    • 52. Schägger H, von Jagow G. Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166, 368–379 (1987).
    • 53. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254 (1976).
    • 54. Tamm LK, Tatulian S. Infrared spectroscopy of proteins and peptides in lipid bilayers. Quart. Rev. Biophys. 30, 365–429 (1997).
    • 55. Al Hennawi HET, Mahdi EM, Memish ZA. Native valve Staphylococcus capitis infective endocarditis: a mini review. Infection 48(1), 3–5 (2020).
    • 56. Argemi X, Hansmann Y, Prola K, Prévost G. Coagulase-negative staphylococci pathogenomics. Int. J. Mol. Sci. 20(5), 1215 (2019).
    • 57. Natsis NE, Cohen PR. Coagulase-negative Staphylococcus skin and soft tissue infections. Am. J. Clin. Dermatol. 19(5), 671–677 (2018). • Coagulase-negative staphylococcal organisms should not always be considered as contaminants or normal flora, but rather as causative pathogens of human skin and soft tissue.
    • 58. Gonzalez T, Biagini Myers JM, Herr AB, Khurana Hershey GK. Staphylococcal biofilms in atopic dermatitis. Curr. Allergy Asthma Rep. 17(12), 81 (2017). • Staphylococcal colonization of the skin impacts skin barrier function and plays multiple important roles in atopic dermatitis pathogenesis.
    • 59. Morgenstern M, Erichsen C, Hackl S et al. Antibiotic resistance of commensal Staphylococcus aureus and coagulase-negative Staphylococci in an international cohort of surgeons: a prospective point-prevalence study. PLoS ONE 11(2), e0148437 (2016).
    • 60. Solis N, Cain JA, Cordwell SJ. Comparative analysis of Staphylococcus epidermidis strains utilizing quantitative and cell surface shaving proteomics. J. Proteomics 130, 190–199 (2016).
    • 61. Saporito P, Mouritzen MV, Løbner-Olesen A, Jenssen H. LL-37 fragments have antimicrobial activity against Staphylococcus epidermidis biofilms and wound healing potential in HaCaT cell line. J. Pep. Sci. 24(7), e3080 (2018).
    • 62. Joo HS, Otto M. Mechanisms of resistance to antimicrobial peptides in staphylococci. Biochim. Biophys. Acta 1848(11), 3055–3061 (2015).
    • 63. Lai Y, Villaruz AE, Li M, Cha DJ, Sturdevant DE, Otto M. The human anionic antimicrobial peptide dermcidin induces proteolytic defence mechanisms in staphylococci. Mol. Microbiol. 63(2), 497–506 (2007).
    • 64. Otto M. Staphylococcus epidermidis – the ‘accidental’ pathogen. Nat. Rev. Microbiol. 7(8), 555–567 (2009). • Describes the molecular basis of the commensal and infectious lifestyles of Staphylococcus epidermidis.