Ultrasound-targeted microbubble destruction enhances human β-defensin 3 activity against antibiotic-resistant staphylococcus biofilms

Inflammation

Volumn 36, Issue 5, 2013, Pages 983-996

  Zhu, Chen ^a   He, Nianan ^b   Cheng, Tao ^a   Tan, Honglue ^a   Guo, Yongyuan ^a   Chen, Desheng ^a   Cheng, Mengqi ^a   Yang, Zhi ^a   Zhang, Xianlong ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b ANHUI MEDICAL UNIVERSITY   (China)

Author keywords

defensin; biofilm; microbubbles; Staphylococcus; ultrasound

Indexed keywords

BETA DEFENSIN 3; SONOVUE;

ANTIBIOTIC RESISTANCE; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL COUNT; BACTERIAL GENE; BIOFILM; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENE EXPRESSION; ICAAD GENE; ICAR GENE; MECA GENE; MICROBUBBLE; NONHUMAN; STAPHYLOCOCCUS; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS EPIDERMIDIS; ULTRASOUND; ULTRASOUND TARGETED MICROBUBBLE DESTRUCTION; ULTRASOUND TRANSDUCER;

STAPHYLOCOCCUS;

ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; BETA-DEFENSINS; BIOFILMS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; GENE EXPRESSION; HUMANS; METHICILLIN-RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL SENSITIVITY TESTS; MICROBUBBLES; SOUND; STAPHYLOCOCCUS EPIDERMIDIS;

EID: 84885177334     PISSN: 03603997     EISSN: 15732576     Source Type: Journal    
DOI: 10.1007/s10753-013-9630-2     Document Type: Article

References (43)

1. Darouiche, R.O. 2004. Treatment of infections associated with surgical implants. The New England Journal of Medicine 350: 1422-1429.
2. Montanaro, L., P. Speziale, D. Campoccia, S. Ravaioli, I. Cangini, G. Pietrocola, S. Giannini, and C.R. Arciola. 2011. Scenery of Staphylococcus implant infections in orthopedics. Future Microbiology 6: 1329-1349.
3. Campoccia, D., L. Montanaro, P. Speziale, and C.R. Arciola. 2010. Antibiotic-loaded biomaterials and the risks for the spread of antibiotic resistance following their prophylactic and therapeutic clinical use. Biomaterials 31: 6363-6377.
4. Shi, Z., K.G. Neoh, E.T. Kang, C. Poh, and W. Wang. 2009. Titanium with surface-grafted dextran and immobilized bone morphogenetic protein-2 for inhibition of bacterial adhesion and enhancement of osteoblast functions. Tissue Engineering. Part A 15: 417-426.
5. Blum-Menezes, D., O.J. Bratfich, M.C. Padoveze, and M.L. Moretti. 2009. Hospital strain colonization by Staphylococcus epidermidis. Brazilian Journal of Medical and Biological Research 42: 294-298.
6. Patel, Z.M., P.H. Hwang, A. Chernomorsky, D.T. Bravo, B.L. Nguyen, K. Nesterova, and J.V. Nayak. 2012. Low-frequency pulsed ultrasound in the nasal cavity and paranasal sinuses: A feasibility and distribution study. International Forum of Allergy Rhinology 2: 303-308.
7. Dijkmans, P.A., L.J. Juffermans, R.J. Musters, A. van Wamel, F.J. ten Cate, W. van Gilst, C.A. Visser, N. de Jong, and O. Kamp. 2004. Microbubbles and ultrasound: From diagnosis to therapy. European Journal of Echocardiography 5: 245-256.
8. He, N., J. Hu, H. Liu, T. Zhu, B. Huang, X. Wang, Y. Wu, W. Wang, and D. Qu. 2011. Enhancement of vancomycin activity against biofilms by using ultrasound-targeted microbubble destruction. Antimicrobial Agents and Chemotherapy 55: 5331-5337.
9. Qin, Z., X. Yang, L. Yang, J. Jiang, Y. Ou, S. Molin, and D. Qu. 2007. Formation and properties of in vitro biofilms of ica-negative Staphylococcus epidermidis clinical isolates. Journal of Medical Microbiology 56: 83-93.
10. Hancock, R.E. 2005. Mechanism of action of newer antibiotics for Gram-positive pathogens. The Lancet Infectious Diseases 5: 209-218.
11. Harder, J., J. Bartels, E. Christophers, and J.M. Schroder. 2001. Isolation and characterization of human beta-defensin-3, a novel human inducible peptide antibiotic. Journal of Biological Chemistry 276: 5707-5713.
12. Maisetta, G., G. Batoni, S. Esin, W. Florio, D. Bottai, F. Favilli, and M. Campa. 2006. In vitro bactericidal activity of human beta-defensin 3 against multidrug-resistant nosocomial strains. Antimicrobial Agents and Chemotherapy 50: 806-809.
13. Warnke, P.H., I.N. Springer, P.A. Russo, J. Wiltfang, H. Essig, M. Kosmahl, E. Sherry, and Y. Acil. 2006. Innate immunity in human bone. Bone 38: 400-408.
14. Huang, Q., H.J. Yu, G.D. Liu, X.K. Huang, L.Y. Zhang, Y.G. Zhou, J.Y. Chen, F. Lin, Y. Wang, and J. Fei. 2012. Comparison of the effects of human β-defensin 3, Vancomycin, and Clindamycin on Staphylococcus aureus biofilm formation. Orthopedics 35: e53-e60.
15. Zhu, C., H. Tan, T. Cheng, H. Shen, J. Shao, Y. Guo, S. Shi, and X. Zhang. 2012. Human β-defensin 3 inhibits antibiotic-resistant Staphylococcus biofilm formation. Journal of Surgical Research. doi: 10.1016/j.jss.2012.11.048.
16. Nihonyanagi, S., Y. Kanoh, K. Okada, T. Uozumi, Y. Kazuyama, T. Yamaguchi, N. Nakazaki, K. Sakurai, Y. Hirata, S. Munekata, S. Ohtani, T. Takemoto, Y. Bandoh, and T. Akahoshi. 2012. Clinical usefulness of multiplex PCR lateral flow in MRSA detection: a novel, rapid genetic testing method. Inflammation 35: 927-934.
17. Arciola, C.R., D. Campoccia, L. Baldassarri, M.E. Donati, V. Pirini, S. Gamberini, and L. Montanaro. 2006. Detection of biofilm formation in Staphylococcus epidermidis from implant infections: Comparison of a PCR method that recognizes the presence of ica genes with two classic phenotypic methods. Journal of Biomedical Materials Research. Part A 76: 425-430.
18. Quaia, E., F. Calliada, M. Bertolotto, S. Rossi, L. Garioni, L. Rosa, and R. Pozzi-Mucelli. 2004. Characterization of focal liver lesions with contrast-specific US modes and a sulfur hexafluoride-filled microbubble contrast agent: Diagnostic performance and confidence. Radiology 232: 420-430.
19. van der Plas, M.J., G.N. Jukema, S.W. Wai, H.C. Dogterom-Ballering, E.L. Lagendijk, C. van Gulpen, J.T. van Dissel, G.V. Bloemberg, and P.H. Nibbering. 2008. Maggot excretions/secretions are differentially effective against biofilms of Staphylococcus aureus and Pseudomonas aeruginosa. Journal of Antimicrobial Chemotherapy 61: 117-122.
20. Kim, H.J., J.F. Greenleaf, R.R. Kinnick, J.T. Bronk, and M.E. Bolander. 1996. Ultrasound-mediated transfection of mammalian cells. Hum. Gene Therapy 7: 1339-1346.
21. Li, M., D.J. Cha, Y. Lai, A.E. Villaruz, D.E. Sturdevant, and M. Otto. 2007. The antimicrobial peptide-sensing system aps of Staphylococcus aureus. Molecular Microbiology 66: 1136-1147.
22. Bjerkan, G., E. Witsø, and K. Bergh. 2009. Sonication is superior to scraping for retrieval of bacteria in biofilm on titanium and steel surfaces in vitro. Acta Orthopaedica 80: 245-250.
23. Peng, Z.X., B. Tu, Y. Shen, L. Du, L. Wang, S.R. Guo, and T.T. Tang. 2011. Quaternized chitosan inhibits icaA transcription and biofilm formation by staphylococcus on a titanium surface. Antimicrobial Agents and Chemotherapy 55: 860-866.
24. Tan, H., Z. Peng, Q. Li, X. Xu, S. Guo, and T. Tang. 2012. The use of quaternised chitosan-loaded PMMA to inhibit biofilm formation and downregulate the virulence-associated gene expression of antibiotic-resistant staphylococcus. Biomaterials 33: 365-377.
25. Rohde, H., S. Frankenberger, U. Zähringer, and D. Mack. 2011. Structure, function and contribution of polysaccharide intercellular adhesin (PIA) to Staphylococcus epidermidis biofilm formation and pathogenesis of biomaterial-associated infections. European Journal of Cell Biology 89: 103-111.
26. Jeng, W.Y., T.P. Ko, C.I. Liu, R.T. Guo, C.L. Liu, H.L. Shr, and A.H. Wang. 2008. Crystal structureof IcaR, a repressor of the TetR family implicated in biofilm formation in Staphylococcus epidermidis. Nucleic Acids Research 36: 1567-1577.
27. Katayama, Y., T. Ito, and K. Hiramatsu. 2000. A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrobial Agents and Chemotherapy 44: 1549-1555.
28. Runyan, C.M., J.C. Carmen, B.L. Beckstead, J.L. Nelson, R.A. Robison, and W.G. Pitt. 2006. Low-frequency ultrasound increases outer membrane permeability of Pseudomonas aeruginosa. Journal of General and Applied Microbiology 52: 295-301.
29. Carmen, J.C., J.L. Nelson, B.L. Beckstead, C.M. Runyan, R.A. Robison, G.B. Schaalje, and W.G. Pitt. 2004. Ultrasonic-enhanced gentamicin transport through colony biofilms of Pseudomonas aeruginosa and Escherichia coli. Journal of Infection and Chemotherapy 10: 193-199.
30. Juffermans, L.J., P.A. Dijkmans, R.J. Musters, C.A. Visser, and O. Kamp. 2006. Transient permeabilization of cell membranes by ultrasound-exposed microbubbles is related to formation of hydrogen peroxide. American Journal of Physiology - Heart and Circulatory Physiology 291: H1595-H1601.
31. Li, P., Y. Zheng, H. Ran, J. Tan, Y. Lin, Q. Zhang, J. Ren, and Z. Wang. 2012. Ultrasound triggered drug release from 10-hydroxycamptothecin-loaded phospholipid microbubbles for targeted tumor therapy in mice. Journal of Controlled Release 162: 349-354.
32. Moosavi Nejad, S., S.H. Hosseini, H. Akiyama, and K. Tachibana. 2011. Optical observation of cell sonoporation with low intensity ultrasound. Biochemical and Biophysical Research Communications 413: 218-223.
33. Han, Y.W., A. Ikegami, P. Chung, L. Zhang, and C.X. Deng. 2007. Sonoporation is an efficient tool for intracellular fluorescent dextran delivery and one-step double-crossover mutant construction in Fusobacterium nucleatum. Applied and Environmental Microbiology 73: 3677-3683.
34. Nishikawa, T., A. Yoshida, A. Khanal, M. Habu, I. Yoshioka, K. Toyoshima, T. Takehara, T. Nishihara, K. Tachibana, and K. Tominaga. 2010. A study of the efficacy of ultrasonic waves in removing biofilms. Gerodontology 27: 199-206.
35. Xu, J., T.A. Bigelow, L.J. Halverson, J.M. Middendorf, and B. Rusk. 2012. Minimization of treatment time for in vitro 1.1 MHz destruction of Pseudomonas aeruginosa biofilms by high-intensity focused ultrasound. Ultrasonics 52: 668-675.
36. Santamato, A., V. Solfrizzi, F. Panza, G. Tondi, V. Frisardi, B.G. Leggin, M. Ranieri, and P. Fiore. 2009. Short-term effects of high-intensity laser therapy versus ultrasound therapy in the treatment of people with subacromial impingement syndrome: A randomized clinical trial. Physical Therapy 89: 643-652.
37. Yu, H., S. Chen, and P. Cao. 2012. Synergistic bactericidal effects and mechanisms of low intensity ultrasound and antibiotics against bacteria: A review. Ultrasonics Sonochemistry 19: 377-382.
38. Maisetta, G., F.L. Brancatisano, S. Esin, M. Campa, and G. Batoni. 2011. Gingipains produced by Porphyromonas gingivalis ATCC49417 degrade human-β-defensin 3 and affect peptide's antibacterial activity in vitro. Peptides 32: 1073-1077.
39. Maisetta, G., M. Di Luca, S. Esin, W. Florio, F.L. Brancatisano, D. Bottai, M. Campa, and G. Batoni. 2008. Evaluation of the inhibitory effects of human serum components on bactericidal activity of human beta defensin 3. Peptides 29: 1-6.
40. Hengge, U.R. 2006. Gene therapy progress and prospects: The skin - easily accessible, but still far away. Gene Therapy 13: 1555-1563.
41. Yu, Q., R.I. Lehrer, and J.P. Tam. 2000. Engineered salt-insensitive alpha defensins with end-to -end circularizeed structures. Journal of Biological Chemistry 275: 3943-3949.
42. Hirsch, T., M. Spielmann, B. Zuhaili, M. Fossum, M. Metzig, T. Koehler, H.U. Steinau, F. Yao, A.B. Onderdonk, L. Steinstraesser, and E. Eriksson. 2009. Human beta-defensin-3 promotes wound healing in infected diabetic wounds. The Journal of Gene Medicine 11: 220-228.
43. Gibson, A.L., C.L. Thomas-Virnig, J.M. Centanni, S.J. Schlosser, C.E. Johnston, K.F. Van Winkle, A. Szilagyi, L.K. He, R. Shankar, and B.L. Allen-Hoffmann. 2012. Nonviral human beta defensin-3 expression in a bioengineered human skin tissue: A therapeutic alternative for infected wounds. Wound Repair and Regeneration 20: 414-424.