Advertisement

Polyhydroxyalkanoates Applications in Antimicrobial Agents Delivery and Wound Healing

  • Veronica S. Giourieva
  • Rigini M. Papi
  • Anastasia A. PantazakiEmail author
Chapter

Abstract

Bacterial infections constitute a significant and increasing problem in healthcare originated from both bacterial colonization and biofilm development in biomaterials, a prelude to the onset of systemic infection and consequently the dysfunction of implanted devices. In addition, a serious issue is the growing incidence of multi-drug resistant bacteria, which cannot be killed using multiple antibiotics, coined by the term “superbugs”. Enormous efforts have focused on developing drugs which, at one hand, exhibit as characteristics great effectiveness and at the other hand, make the evolutionary resistant bacteria susceptible to them. The development of novel, more potent antibiotics able to overcome this acquired resistance remains until now, a provocation for the scientific world because novel modes of antibacterial activity are necessary. Biopolymeric antimicrobials have appeared as a hopeful nominee for investigation and evolution in the field of antibacterial therapy. Poly([R]-3-hydroxyalkanoates) (PHAs), the wide family of the naturally-synthesizing bacterial bio-polyesters, constitute one of the principal nominees, which dominates in prospective for utilization in the field of biomedical applications. They constitute a large class of biodegradable biopolymers that exhibit biocompatibility obtaining minimal tissue toxicity. Exploiting these properties, PHAs has been used as a matrix to construct slow-release formulations of antibiotic delivery, providing them antimicrobial, antifungal, anti-biofilm, anti-inflammatory and virucidal properties dependent on the conjugated/enclosed therapeutic agent. Moreover, the antimicrobial activity that PHAs themselves, or their derivatives have been reported to exhibit should not be ignored. Wound healing is a novel medical area where PHAs are also extended based on the same principle of the drug delivery for rapid tissue regeneration. This review covers all this collective information.

Keywords

Polyhydroxyalkanoates Antibacterial agent Biofilm PHA derivatives Wound healing Drug delivery 

References

  1. Aggarwal V, Bakhshi H, Ecker N, Parvizi J, Gehrke T, Kendoff D (2014) Organism profile in periprosthetic joint infection: pathogens differ at two arthroplasty infection referral centers in Europe and in the United States. J Knee Surg 27:399–406.  https://doi.org/10.1055/s-0033-1364102 CrossRefPubMedGoogle Scholar
  2. Allen AD, Daley P, Ayorinde FO, Gugssa A, Anderson WA, Eribo BE (2012) Characterization of medium chain length (R)-3-hydroxycarboxylic acids produced by Streptomyces sp. JM3 and the evaluation of their antimicrobial properties. World J Microbiol Biotechnol 28:2791–2800.  https://doi.org/10.1007/s11274-012-1089-z CrossRefPubMedGoogle Scholar
  3. Arias CA, Murray BE (2009) Antibiotic-resistant bugs in the 21st century – a clinical super-challenge. N Engl J Med 360:439–443.  https://doi.org/10.1056/NEJMp0804651 CrossRefPubMedGoogle Scholar
  4. Basnett P, Ching KY, Stolz M, Knowles JC, Boccaccini AR, Smith C, Locke IC, Keshavarz T, Roy I (2013) Novel poly(3-hydroxyoctanoate)/poly(3-hydroxybutyrate) blends for medical applications. React Funct Polym 73:1340–1348.  https://doi.org/10.1016/j.reactfunctpolym.2013.03.019 CrossRefGoogle Scholar
  5. Brophy MR, Deasy PB (1986) In vitro and in vivo studies on biodegradable polyester microparticles containing sulphamethizole. Int J Pharm 29:223–231.  https://doi.org/10.1016/0378-5173(86)90119-5 CrossRefGoogle Scholar
  6. Burgos N, Armentano I, Fortunati E, Dominici F, Luzi F, Fiori S, Cristofaro F, Visai L, Jiménez A, Kenny JM (2017) Functional properties of plasticized bio-based poly(lactic acid)-poly(hydroxybutyrate) (PLA-PHB) films for active food packaging. Food Bioprocess Technol 10:770–780.  https://doi.org/10.1007/s11947-016-1846-3 CrossRefGoogle Scholar
  7. Burke TR, Knight M, Chandrasekhar B (1989) Solid-phase synthesis of viscosin, a cyclic depsipeptide with antibacterial and antiviral properties. Tetrahedron Lett 30:519–522CrossRefGoogle Scholar
  8. Busscher HJ, van der Mei HC (2012) How do bacteria know they are on a surface and regulate their response to an adhering state? PLoS Pathog 8:e1002440.  https://doi.org/10.1371/journal.ppat.1002440 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Castro-Mayorga JL, Martínez-Abad A, Fabra MJ, Olivera C, Reis M, Lagarón JM (2014) Stabilization of antimicrobial silver nanoparticles by a polyhydroxyalkanoate obtained from mixed bacterial culture. Int J Biol Macromol 71:103–110.  https://doi.org/10.1016/j.ijbiomac.2014.06.059 CrossRefPubMedGoogle Scholar
  10. Castro-Mayorga J, Fabra M, Cabedo L, Lagaron JM (2016a) On the use of the electrospinning coating technique to produce antimicrobial polyhydroxyalkanoate materials containing in situ-stabilized silver nanoparticles. Nanomaterials 7:4.  https://doi.org/10.3390/nano7010004 CrossRefPubMedCentralGoogle Scholar
  11. Castro-Mayorga JL, Fabra MJ, Lagaron JM (2016b) Stabilized nanosilver based antimicrobial poly(3-hydroxybutyrate-co-3-hydroxyvalerate) nanocomposites of interest in active food packaging. Innov Food Sci Emerg Technol 33:524–533.  https://doi.org/10.1016/j.ifset.2015.10.019 CrossRefGoogle Scholar
  12. Castro-Mayorga JL, Randazzo W, Fabra MJ, Lagaron JM, Aznar R (2017) Antiviral properties of silver nanoparticles against norovirus surrogates and their efficacy in coated polyhydroxyalkanoates systems. LWT-Food Sci Technol 79:503–510.  https://doi.org/10.1016/j.lwt.2017.01.065 CrossRefGoogle Scholar
  13. Castro-Mayorga JL, Freitas F, Reis M, Prieto A, Lagaron JM (2018) Biosynthesis of silver nanoparticles and polyhydroxybutyrate nanocomposites of interest in antimicrobial applications. Int J Biol Macromol 108:426–435.  https://doi.org/10.1016/j.ijbiomac.2017.12.007 CrossRefPubMedGoogle Scholar
  14. Chen G-Q (2009) A microbial polyhydroxyalkanoates (PHA) based bio- and materials industry. Chem Soc Rev 38:2434–2446.  https://doi.org/10.1039/b812677c CrossRefPubMedGoogle Scholar
  15. Chen LJ, Wang M (2002) Production and evaluation of biodegradable composites based on PHB–PHV copolymer. Biomaterials 23:2631–2639.  https://doi.org/10.1016/S0142-9612(01)00394-5 CrossRefPubMedGoogle Scholar
  16. Chen G-Q, Wu Q (2005a) The application of polyhydroxyalkanoates as tissue engineering materials. Biomaterials 26:6565–6578.  https://doi.org/10.1016/j.biomaterials.2005.04.036 CrossRefPubMedGoogle Scholar
  17. Chen G-Q, Wu Q (2005b) Microbial production and applications of chiral hydroxyalkanoates. Appl Microbiol Biotechnol 67:592–599.  https://doi.org/10.1007/s00253-005-1917-2 CrossRefPubMedGoogle Scholar
  18. Chen L, Bromberg L, Hatton TA, Rutledge GC (2008) Electrospun cellulose acetate fibers containing chlorhexidine as a bactericide. Polymer (Guildf) 49:1266–1275.  https://doi.org/10.1016/j.polymer.2008.01.003 CrossRefGoogle Scholar
  19. Chiba T, Nakai T (1985) A synthetic approach to (+)-thienamycin from methyl (R)-3-hydroxybutanoate. A new entry to (3 R, 4 R)-3-[(R)-1-hydroxyethyl]-4-acetoxy-2-azetidinone. Chem Lett 14:651–654.  https://doi.org/10.1246/cl.1985.651 CrossRefGoogle Scholar
  20. Chung GM, Kim WH, Kim RB, Kim BY, Rhee HY (2012) Biocompatibility and antimicrobial activity of poly (3-hydroxyoctanoate) grafted with vinylimidazole. Int J Biol Macromol 50:310–316.  https://doi.org/10.1016/j.ijbiomac.2011.12.007 CrossRefPubMedGoogle Scholar
  21. Clokie MR, Millard AD, Letarov AV, Heaphy S (2011) Phages in nature. Bacteriophage 1:31–45.  https://doi.org/10.4161/bact.1.1.14942 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Cornell RJ, Donaruma LG (1965) 2-Methacryloxytropones. Intermediates for the synthesis of biologically active polymers. J Med Chem 8:388–390CrossRefGoogle Scholar
  23. Costerton JW, Geesey GG, Cheng K-J (1978) How bacteria stick. Sci Am 238:86–95.  https://doi.org/10.1038/scientificamerican0178-86 CrossRefPubMedGoogle Scholar
  24. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464.  https://doi.org/10.1146/annurev.mi.41.100187.002251 CrossRefPubMedGoogle Scholar
  25. Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1322CrossRefGoogle Scholar
  26. Costerton W, Veeh R, Shirtliff M, Pasmore M, Post C, Ehrlich G (2003) The application of biofilm science to the study and control of chronic bacterial infections. J Clin Invest 112:1466–1477.  https://doi.org/10.1172/JCI200320365 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Darouiche RO (2004) Treatment of infections associated with surgical implants. N Engl J Med 350:1422–1429.  https://doi.org/10.1056/NEJMra035415 CrossRefPubMedGoogle Scholar
  28. Davey ME, O’toole GA (2000) Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 64:847–867.  https://doi.org/10.1128/MMBR.64.4.847-867.2000 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Defoirdt T, Halet D, Sorgeloos P, Bossier P, Verstraete W (2006) Short-chain fatty acids protect gnotobiotic Artemia franciscana from pathogenic Vibrio campbellii. Aquaculture 261:804–808.  https://doi.org/10.1016/j.aquaculture.2006.06.038 CrossRefGoogle Scholar
  30. Defoirdt T, Boon N, Sorgeloos P, Verstraete W, Bossier P (2009) Short-chain fatty acids and poly-β-hydroxyalkanoates: (New) biocontrol agents for a sustainable animal production. Biotechnol Adv 27:680–685.  https://doi.org/10.1016/j.biotechadv.2009.04.026 CrossRefPubMedGoogle Scholar
  31. DeLeo FR, Chambers HF (2009) Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era. J Clin Invest 119:2464–2474.  https://doi.org/10.1172/JCI38226 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Delie F, Blanco-Príeto MJ (2005) Polymeric particulates to improve oral bioavailability of peptide drugs. Molecules 10:65–80.  https://doi.org/10.3390/10010065 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Desbois A, Lawlor K (2013) Antibacterial activity of long-chain polyunsaturated fatty acids against Propionibacterium acnes and Staphylococcus aureus. Mar Drugs 11:4544–4557.  https://doi.org/10.3390/md11114544 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Desbois AP, Smith VJ (2010) Antibacterial free fatty acids: activities, mechanisms of action and biotechnological potential. Appl Microbiol Biotechnol 85:1629–1642.  https://doi.org/10.1007/s00253-009-2355-3 CrossRefPubMedGoogle Scholar
  35. Dhand C, Venkatesh M, Barathi VA, Harini S, Bairagi S, Goh Tze Leng E, Muruganandham N, Low KZW, Fazil MHUT, Loh XJ, Shirivasa DK, Liu SP, Beuerman RW, Verma NK, Ramakrishna S, Lakshminarayanan R (2017) Bio-inspired crosslinking and matrix-drug interactions for advanced wound dressings with long-term antimicrobial activity. Biomaterials 138:153–168.  https://doi.org/10.1016/j.biomaterials.2017.05.043 CrossRefPubMedGoogle Scholar
  36. Díez-Pascual A, Díez-Vicente A (2014) Poly(3-hydroxybutyrate)/ZnO bionanocomposites with improved mechanical, barrier and antibacterial properties. Int J Mol Sci 15:10950–10973.  https://doi.org/10.3390/ijms150610950 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Dinjaski N, Fernández-Gutiérrez M, Selvam S, Parra-Ruiz FJ, Lehman SM, San Román J, García E, García JL, García AJ, Prieto MA (2014) PHACOS, a functionalized bacterial polyester with bactericidal activity against methicillin-resistant Staphylococcus aureus. Biomaterials 35:14–24.  https://doi.org/10.1016/j.biomaterials.2013.09.059 CrossRefPubMedGoogle Scholar
  38. Donadio S, Maffioli S, Monciardini P, Sosio M, Jabes D (2010) Antibiotic discovery in the twenty-first century: current trends and future perspectives. J Antibiot (Tokyo) 63:423–430.  https://doi.org/10.1038/ja.2010.62 CrossRefGoogle Scholar
  39. Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8:881–890.  https://doi.org/10.3201/eid0809.020063 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Escapa IF, Morales V, Martino VP, Pollet E, Avérous L, García JL, Prieto MA (2011) Disruption of β-oxidation pathway in Pseudomonas putida KT2442 to produce new functionalized PHAs with thioester groups. Appl Microbiol Biotechnol 89:1583–1598.  https://doi.org/10.1007/s00253-011-3099-4 CrossRefPubMedGoogle Scholar
  41. Fan X, Jiang Q, Sun Z, Li G, Ren X, Liang J, Huang TS (2015) Preparation and characterization of electrospun antimicrobial fibrous membranes based on polyhydroxybutyrate (PHB). Fibers Polym 16:1751–1758.  https://doi.org/10.1007/s12221-015-5108-1 CrossRefGoogle Scholar
  42. Fernandes JG, Correia DM, Botelho G, Padrão J, Dourado F, Ribeiro C, Lanceros-Méndez S, Sencadas V (2014) PHB-PEO electrospun fiber membranes containing chlorhexidine for drug delivery applications. Polym Test 34:64–71.  https://doi.org/10.1016/j.polymertesting.2013.12.007 CrossRefGoogle Scholar
  43. Fischbach MA, Walsh CT (2009) Antibiotics for emerging pathogens. Science 325:1089–1093.  https://doi.org/10.1126/science.1176667 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Fischer CL, Drake DR, Dawson DV, Blanchette DR, Brogden KA, Wertz PW (2012) Antibacterial activity of sphingoid bases and fatty acids against gram-positive and gram-negative bacteria. Antimicrob Agents Chemother 56:1157–1161.  https://doi.org/10.1128/AAC.05151-11 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Fux CA, Costerton JW, Stewart PS, Stoodley P (2005) Survival strategies of infectious biofilms. Trends Microbiol 13:34–40.  https://doi.org/10.1016/j.tim.2004.11.010 CrossRefPubMedGoogle Scholar
  46. Gallo J, Holinka M, Moucha CS (2014) Antibacterial surface treatment for orthopaedic implants. Int J Mol Sci 15:13849–13880.  https://doi.org/10.3390/ijms150813849 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Gantois I, Ducatelle R, Pasmans F, Haesebrouck F, Hautefort I, Thompson A, Hinton JC, Van Immerseel F (2006) Butyrate specifically down-regulates Salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol 72:946–949.  https://doi.org/10.1128/AEM.72.1.946-949.2006 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Gomes ME, Reis RL (2004) Biodegradable polymers and composites in biomedical applications: from catgut to tissue engineering. Part 1 available systems and their properties. Int Mater Rev 49:261–273.  https://doi.org/10.1179/095066004225021918 CrossRefGoogle Scholar
  49. Gumel AM, Razaif-Mazinah MRM, Anis SNS, Annuar MSM (2015) Poly (3-hydroxyalkanoates)-co-(6-hydroxyhexanoate) hydrogel promotes angiogenesis and collagen deposition during cutaneous wound healing in rats. Biomed Mater 10:045001.  https://doi.org/10.1088/1748-6041/10/4/045001 CrossRefPubMedGoogle Scholar
  50. Gwynn MN, Portnoy A, Rittenhouse SF, Payne DJ (2010) Challenges of antibacterial discovery revisited. Ann N Y Acad Sci 1213:5–19.  https://doi.org/10.1111/j.1749-6632.2010.05828.x CrossRefPubMedGoogle Scholar
  51. Hetrick EM, Schoenfisch MH (2006) Reducing implant-related infections: active release strategies. Chem Soc Rev 35:780–789.  https://doi.org/10.1039/b515219b CrossRefPubMedGoogle Scholar
  52. Hu S-G, Jou C-H, Yang M-C (2003) Antibacterial and biodegradable properties of polyhydroxyalkanoates grafted with chitosan and chitooligosaccharides via ozone treatment. J Appl Polym Sci 88:2797–2803.  https://doi.org/10.1002/app.12055 CrossRefGoogle Scholar
  53. Huang CB, Altimova Y, Myers TM, Ebersole JL (2011) Short- and medium-chain fatty acids exhibit antimicrobial activity for oral microorganisms. Arch Oral Biol 56:650–654.  https://doi.org/10.1016/j.archoralbio.2011.01.011 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Ignatova M, Manolova N, Rashkov I, Markova N (2016) Quaternized chitosan/κ-carrageenan/caffeic acid-coated poly(3-hydroxybutyrate) fibrous materials: preparation, antibacterial and antioxidant activity. Int J Pharm 513:528–537.  https://doi.org/10.1016/j.ijpharm.2016.09.062 CrossRefPubMedGoogle Scholar
  55. Iida J, Une T, Ishihara C, Nishimura K, Tokura S, Mizukoshi N, Azuma I (1987) Stimulation of non-specific host resistance against Sendai virus and Escherichia coli infections by chitin derivatives in mice. Vaccine 5:270–274CrossRefGoogle Scholar
  56. Ismail I, Gurusamy TP, Ramachandran H, Al-Ashraf Amirul A (2017) Enhanced production of poly(3-hydroxybutyrate-co-4-hydroxybutyrate) copolymer and antimicrobial yellow pigmentation from Cupriavidus sp. USMAHM13 with antibiofilm capability. Prep Biochem Biotechnol 47:388–396.  https://doi.org/10.1080/10826068.2016.1252925 CrossRefPubMedGoogle Scholar
  57. Jendrossek D, Handrick R (2002) Microbial degradation of polyhydroxyalkanoates. Annu Rev Microbiol 56:403–432CrossRefGoogle Scholar
  58. Jeon JM, Brigham CJ, Kim YH, Kim H-J, Yi D-H, Kim H, Rha C, Sinskey A, Yang Y-H (2014) Biosynthesis of poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) (P(HB-co-HXX)) from butyrate using engineered Ralstonia eutropha. Appl Microbiol Biotechnol 98:5461.  https://doi.org/10.1007/s00253-014-5617-7 CrossRefPubMedGoogle Scholar
  59. Johnson K, Jiang Y, Kleerebezem R, Muyzer G, van Loosdrecht M (2009) Enrichment of a mixed bacterial culture with a high polyhydroxyalkanoate storage capacity. Biomacromolecules 10:670.  https://doi.org/10.1021/bm8013796 CrossRefPubMedGoogle Scholar
  60. Kai D, Low ZW, Liow SS, Abdul Karim A, Ye H, Jin G, Li K, Loh XJ (2015) Development of lignin supramolecular hydrogels with mechanically responsive and self-healing properties. ACS Sustain Chem Eng 3:2160–2169.  https://doi.org/10.1021/acssuschemeng.5b00405 CrossRefGoogle Scholar
  61. Kandhasamy S, Perumal S, Madhan B, Umamaheswari N, Banday JA, Perumal PT, Santhanakrishnan VP (2017) Synthesis and fabrication of collagen-coated ostholamide electrospun nanofiber scaffold for wound healing. ACS Appl Mater Interfaces 9:8556–8568.  https://doi.org/10.1021/acsami.6b16488 CrossRefPubMedGoogle Scholar
  62. Kaplan JB, Ragunath C, Velliyagounder K, Fine DH, Ramasubbu N (2004) Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 48:2633–2636.  https://doi.org/10.1128/AAC.48.7.2633-2636.2004 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Karahaliloglu Z, Ercan B, Taylor EN, Chung S, Denkbaş EB, Webster TJ (2015) Antibacterial nanostructured polyhydroxybutyrate membranes for guided bone regeneration. J Biomed Nanotechnol 11:2253–2263.  https://doi.org/10.1166/jbn.2015.2106 CrossRefPubMedGoogle Scholar
  64. Ke Y, Zhang XY, Ramakrishna S, He LM, Wu G (2016) Synthetic routes to degradable copolymers deriving from the biosynthesized polyhydroxyalkanoates: a mini review. Express Polym Lett 10:36–53.  https://doi.org/10.3144/expresspolymlett.2016.5 CrossRefGoogle Scholar
  65. Ke Y, Liu C, Zhang X, Xiao M, Wu G (2017) Surface modification of polyhydroxyalkanoates toward enhancing cell compatibility and antibacterial activity. Macromol Mater Eng 302:1700258.  https://doi.org/10.1002/mame.201700258 CrossRefGoogle Scholar
  66. Kehail AA, Brigham CJ (2017) Anti-biofilm activity of solvent-cast and electrospun polyhydroxyalkanoate membranes treated with lysozyme. J Polym Environ.  https://doi.org/10.1007/s10924-016-0921-1 CrossRefGoogle Scholar
  67. Kiedrowski MR, Horswill AR (2011) New approaches for treating staphylococcal biofilm infections. Ann N Y Acad Sci 1241:104–121.  https://doi.org/10.1111/j.1749-6632.2011.06281.x CrossRefPubMedGoogle Scholar
  68. Kim DY, Kim HW, Chung MG, Rhee YH (2007) Biosynthesis, modification, and biodegradation of bacterial medium-chain-length polyhydroxyalkanoates. J Microbiol 45:87–97PubMedGoogle Scholar
  69. Kim HW, Chung MG, Kim YB, Rhee YH (2008) Graft copolymerization of glycerol 1,3-diglycerolate diacrylate onto poly(3-hydroxyoctanoate) to improve physical properties and biocompatibility. Int J Biol Macromol 43:307–313.  https://doi.org/10.1016/j.ijbiomac.2008.07.002 CrossRefPubMedGoogle Scholar
  70. Koneman EW, Allen SD, Janda WM, Sohreckenberger PC, Winn WC (1997) Color atlas and textbook of diagnostic microbiology. Lippincott, New York, 1736 pGoogle Scholar
  71. Korsatko W, Wabnegg B, Braunegg G, Lafferty MR, Strempfl F (1983) Poly-D-(-)-3-hydroxybutyric acid (PHBA) a biodegradable carrier for long term medication dosage 1. Pharm Ind 45:525–527Google Scholar
  72. Laverty G, Gorman SP, Gilmore BF (2013) Biomolecular mechanisms of staphylococcal biofilm formation. Future Microbiol 8:509–524.  https://doi.org/10.2217/fmb.13.7 CrossRefPubMedGoogle Scholar
  73. Lee SY, Park SH, Lee Y, Lee S (2002) Production of chiral and other valuable compounds from microbial polyester. In: Doi Y, Steinbüchel A (eds) Biopolymers. Wiley-VCH, Germany, pp 375–387.  https://doi.org/10.1002/3527600035.bpol4014 CrossRefGoogle Scholar
  74. Li Z, Loh XJ (2015) Water soluble polyhydroxyalkanoates: future materials for therapeutic applications. Chem Soc Rev 44:2865–2879.  https://doi.org/10.1039/c5cs00089k CrossRefPubMedGoogle Scholar
  75. Li Z, Yang J, Loh XJ (2016) Polyhydroxyalkanoates: opening doors for a sustainable future. NPG Asia Mater 8:e265.  https://doi.org/10.1038/am.2016.48 CrossRefGoogle Scholar
  76. Li Y, Na R, Wang X, Liu H, Zhao L, Sun X, Ma G, Cui F (2017) Fabrication of antimicrobial peptide-loaded PLGA/Chitosan composite microspheres for long-acting bacterial resistance. Molecules 22:E1637.  https://doi.org/10.3390/molecules22101637 CrossRefPubMedGoogle Scholar
  77. Lipovsky A, Thallinger B, Perelshtein I, Ludwig R, Sygmund C, Nyanhongo GS, Guebitz GM, Gedanken A (2015) Ultrasound coating of polydimethylsiloxanes with antimicrobial enzymes. J Mater Chem B 3:7014–7019.  https://doi.org/10.1039/C5TB00671F CrossRefGoogle Scholar
  78. Loh XJ (2017) Latest advances in antibacterial materials. J Mol Eng Mater 5:1740001.  https://doi.org/10.1142/S2251237317400019 CrossRefGoogle Scholar
  79. Lou Q, Ma Y, Che X, Zhong J, Sun X, Zhang H (2016) Preparation and characterization of polyhydroxyalkanoate bioplastics with antibacterial activity. Sheng Wu Gong Cheng Xue Bao 32:1052–1059.  https://doi.org/10.13345/j.cjb.150488 CrossRefPubMedGoogle Scholar
  80. Luef KP, Stelzer F, Wiesbrock F (2015) Poly (hydroxy alkanoate)s in medical applications. Chem Biochem Eng Q 29:287–297.  https://doi.org/10.15255/CABEQ.2014.2261 CrossRefPubMedPubMedCentralGoogle Scholar
  81. Mah T-FC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9:34–39.  https://doi.org/10.1016/S0966-842X(00)01913-2 CrossRefPubMedGoogle Scholar
  82. Marcano A, Ba O, Thebault P, Crétois R, Marais S, Duncan AC (2015) Elucidation of innovative antibiofilm materials. Colloids Surf B Biointerfaces 136:56–63.  https://doi.org/10.1016/j.colsurfb.2015.08.007 CrossRefPubMedGoogle Scholar
  83. Mifune J, Nakamura S, Fukui T (2010) Engineering of pha operon on Cupriavidus necator chromosome for efficient biosynthesis of poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) from vegetable oil. Polym Degrad Stab 95:1305–1312.  https://doi.org/10.1016/j.polymdegradstab.2010.02.026 CrossRefGoogle Scholar
  84. Moritz M, Geszke-Moritz M (2013) The newest achievements in synthesis, immobilization and practical applications of antibacterial nanoparticles. Chem Eng J 228:596–613.  https://doi.org/10.1016/j.cej.2013.05.046 CrossRefGoogle Scholar
  85. Mozejko J, Ciesielski S (2013) Saponified waste palm oil as an attractive renewable resource for mcl-polyhydroxyalkanoate synthesis. J Biosci Bioeng 116:485–492.  https://doi.org/10.1016/j.jbiosc.2013.04.014 CrossRefPubMedGoogle Scholar
  86. Narayanan A, Ramana KV (2013) Synergized antimicrobial activity of eugenol incorporated polyhydroxybutyrate films against food spoilage microorganisms in conjunction with pediocin. Appl Biochem Biotechnol 170:1379–1388.  https://doi.org/10.1007/s12010-013-0267-2 CrossRefPubMedGoogle Scholar
  87. Naveen N, Kumar R, Balaji S, Uma TS, Natrajan TS, Sehgal PK (2010) Synthesis of nonwoven nanofibers by electrospinning – a promising biomaterial for tissue engineering and drug delivery. Adv Eng Mater 12:380–387.  https://doi.org/10.1002/adem.200980067 CrossRefGoogle Scholar
  88. Ohashi T, Hasegawa J (1992a) D-(−)-β-hydroxycarboxylic acids as raw materials for captopril and beta lactams. In: Collins A, Sheldrake G, Crosby J (eds) Chirality in industry. Wiley, New York, pp 269–278Google Scholar
  89. Ohashi T, Hasegawa J (1992b) New preparative methods for optically active β- hydroxycarboxylic acids. In: Collins AN, Sheldrake GN, Crosby J (eds) Chirality in industry. Wiley, New York, pp 249–268Google Scholar
  90. Onaizi SA, Leong SSJ (2011) Tethering antimicrobial peptides: current status and potential challenges. Biotechnol Adv 29:67–74.  https://doi.org/10.1016/j.biotechadv.2010.08.012 CrossRefPubMedGoogle Scholar
  91. Pamp SJ, Gjermansen M, Tolker-Nielsen T (2007) The biofilm matrix: a sticky framework. In: Kjelleberg S, Givskov M (eds) The biofilm mode of life: mechanisms and adaptations. HorizonBioscience, Norfolk, pp 37–69Google Scholar
  92. Panith N, Assavanig A, Lertsiri S, Bergkvist M, Surarit R, Niamsiri N (2016) Development of tunable biodegradable polyhydroxyalkanoates microspheres for controlled delivery of tetracycline for treating periodontal disease. J Appl Polym Sci 133:44128–44141.  https://doi.org/10.1002/app.44128 CrossRefGoogle Scholar
  93. Paraje MG (2011) Antimicrobial resistance in biofilms. In: Mendez-Vilas A (ed) Science against microbial pathogens: communicating current research and technological advances. Formatex Research Center, Badajoz, pp 736–744 ISBN 978-84-939843-1-1Google Scholar
  94. Peng L-H, Huang Y-F, Zhang C-Z, Niu J, Chen Y, Chu Y, Jiang Z-H, Gao J-Q, Mao Z-W (2016) Integration of antimicrobial peptides with gold nanoparticles as unique non-viral vectors for gene delivery to mesenchymal stem cells with antibacterial activity. Biomaterials 103:137–149.  https://doi.org/10.1016/j.biomaterials.2016.06.057 CrossRefPubMedGoogle Scholar
  95. Pihlstrom BL, Michalowicz BS, Johnson NW (2005) Periodontal diseases. Lancet 366:1809–1820.  https://doi.org/10.1016/S0140-6736(05)67728-8 CrossRefPubMedGoogle Scholar
  96. Prabaharan M (2011) Prospective of guar gum and its derivatives as controlled drug delivery systems. Int J Biol Macromol 49:117–124.  https://doi.org/10.1016/j.ijbiomac.2011.04.022 CrossRefPubMedGoogle Scholar
  97. Pramanik N, Mitra T, Khamrai M, Bhattacharyya A, Mukhopadhyay P, Gnanamani A, Basu RK, Kundu PP (2015) Characterization and evaluation of curcumin loaded guar gum/polyhydroxyalkanoates blend films for wound healing applications. RSC Adv 5:63489–63501.  https://doi.org/10.1039/C5RA10114J CrossRefGoogle Scholar
  98. Radivojevic J, Skaro S, Senerovic L, Vasiljevic B, Guzik M, Kenny ST, Maslak V, Nikodinovic-Runic J, O’Connor KE (2016) Polyhydroxyalkanoate-based 3-hydroxyoctanoic acid and its derivatives as a platform of bioactive compounds. Appl Microbiol Biotechnol 100:161–172.  https://doi.org/10.1007/s00253-015-6984-4 CrossRefPubMedGoogle Scholar
  99. Rai D, Singh JK, Roy N, Panda D (2008) Curcumin inhibits FtsZ assembly: an attractive mechanism for its antibacterial activity. Biochem J 410:147–155.  https://doi.org/10.1042/BJ20070891 CrossRefPubMedGoogle Scholar
  100. Rai M, Yadav A, Gade A (2009) Silver nanoparticles as a new generation of antimicrobials. Biotechnol Adv 27:76–83.  https://doi.org/10.1016/j.biotechadv.2008.09.002 CrossRefPubMedGoogle Scholar
  101. Ren Q, Ruth K, Thöny-Meyer L, Zinn M (2010) Enatiomerically pure hydroxycarboxylic acids: current approaches and future perspectives. Appl Microbiol Biotechnol 87:41–52.  https://doi.org/10.1007/s00253-010-2530-6 CrossRefPubMedPubMedCentralGoogle Scholar
  102. Rodríguez-Contreras A, García Y, Manero JM, Rupérez E (2017) Antibacterial PHAs coating for titanium implants. Eur Polym J 90:66–78.  https://doi.org/10.1016/j.eurpolymj.2017.03.004 CrossRefGoogle Scholar
  103. Rossi S, Azghani AO, Omri A (2004) Antimicrobial efficacy of a new antibiotic-loaded poly(hydroxybutyric-co-hydroxyvaleric acid) controlled release system. J Antimicrob Chemother 54:1013–1018.  https://doi.org/10.1093/jac/dkh477 CrossRefPubMedGoogle Scholar
  104. Ruth K, Grubelnik A, Hartmann R, Egli T, Zinn M, Ren Q (2007) Efficient production of (R)-3-hydroxycarboxylic acids by biotechnological conversion of polyhydroxyalkanoates and their purification. Biomacromolecules 8:279–286.  https://doi.org/10.1021/bm060585a CrossRefPubMedGoogle Scholar
  105. Sandoval A, Arias-Barrau E, Bermejo F, Caedo L, Naharro G, Olivera ER, Luengo JM (2005) Production of 3-hydroxy-n-phenylalkanoic acids by a genetically engineered strain of Pseudomonas putida. Appl Microbiol Biotechnol 67:97–105.  https://doi.org/10.1007/s00253-004-1752-x CrossRefPubMedGoogle Scholar
  106. Schacht VJ, Neumann LV, Sandhi SK, Chen L, Henning T, Klar PJ, Theophel K, Schnell S, Bunge M (2013) Effects of silver nanoparticles on microbial growth dynamics. J Appl Microbiol 114:25–35CrossRefGoogle Scholar
  107. Seebach D, Albert M, Arvidsson P, Rueping M, Schreiber J (2001) From the biopolymer PHB to biological investigations of unnatural β- and γ-peptides. Chimia (Aarau) 55:345–353Google Scholar
  108. Seidel W, Seebach D (1982) Grahamimycin A1 synthesis and determination of configuration and chirality. Tetrahedron Lett 23:159–162CrossRefGoogle Scholar
  109. Seuring B, Seebach D (1978) Syntheses and determinations of the absolute-configurations of norpyrenophorin, pyrenophorin, and vermiculine. Liebigs Ann Chem 12:2044–2073CrossRefGoogle Scholar
  110. Seymour RA, Heasman PA (2005) Tetracyclines in the management of periodontal diseases. J Clin Periodontol 22:22–35.  https://doi.org/10.1111/j.1600-051X.1995.tb01767.x CrossRefGoogle Scholar
  111. Shah SR, Tatara AM, D’Souza RN, Mikos AG, Kasper FK (2013) Evolving strategies for preventing biofilm on implantable materials. Mater Today 16:177–182.  https://doi.org/10.1016/j.mattod.2013.05.003 CrossRefGoogle Scholar
  112. Shiraki M, Endo T, Saito T (2006) Fermentative production of (R)-(−)-3-hydroxybutyrate using 3-hydroxybutyrate dehydrogenase null mutant of Ralstonia eutropha and recombinant Escherichia coli. J Biosci Bioeng 102:529–534.  https://doi.org/10.1263/jbb.102.529 CrossRefPubMedGoogle Scholar
  113. Shishatskaya EI, Nikolaeva ED, Vinogradova ON, Volova TG (2016) Experimental wound dressings of degradable PHA for skin defect repair. J Mater Sci Mater Med 27:165.  https://doi.org/10.1007/s10856-016-5776-4 CrossRefPubMedGoogle Scholar
  114. Siedenbiedel F, Tiller JC (2012) Antimicrobial polymers in solution and on surfaces: overview and functional principles. Polymers (Basel) 4:46–71.  https://doi.org/10.3390/polym4010046 CrossRefGoogle Scholar
  115. Solaiman DKY, Ashby RD, Zerkowski JA, Krishnama A, Vasanthan N (2015) Control-release of antimicrobial sophorolipid employing different biopolymer matrices. Biocatal Agric Biotechnol 4:342–348.  https://doi.org/10.1016/j.bcab.2015.06.006 CrossRefGoogle Scholar
  116. Souli M, Galani I, Giamarellou H (2008) Emergence of extensively drug-resistant and pandrug-resistant gram-negative bacilli in Europe. Euro Surveill 13:19045.  https://doi.org/10.2807/ese.13.47.19045-en CrossRefPubMedGoogle Scholar
  117. Stejskalová A, Almquist BD (2017) Using biomaterials to rewire the process of wound repair. Biomater Sci 5:1421–1434.  https://doi.org/10.1039/C7BM00295E CrossRefPubMedPubMedCentralGoogle Scholar
  118. Stoodley P, Hall-Stoodley L, Costerton B, DeMeo P, Shirtliff M, Gawalt E, Kathju S (2013) Biofilms, biomaterials, and device-related infections. In: Ratner B, Hoffman AS, Schoen FJ, Lemons JE (eds) Biomaterials science: an introduction to materials in medicine. Academic, Waltham, pp 565–583 ISBN 0-12-582460-2CrossRefGoogle Scholar
  119. Sutter MA, Seebach D (1983) Synthesis of (2E, 4E, 6S, 7R,10E, 12E, 14S, 15R)-6,7,14,15-tetramethyl-8,16-dioxa-2,4,10,12-cyclohexadecatet- raene-1,9-diones-A model system for elaiophylin. Liebigs Ann Chem 14:939–949.  https://doi.org/10.1002/chin.198339350 CrossRefGoogle Scholar
  120. Tappel R, Pan W, Bergey N, Wang Q, Patterson I, Ozumba O, Matsumoto K, Taguchi S, Nomura C (2014) Engineering Escherichia coli for improved production of short-chain-length-co-medium-chain-length poly[(R)-3-hydroxyalkanoate] (scl- R co -mcl PHA) Copolymers from renewable nonfatty acid feedstocks. Sustain Chem Eng 2:1879.  https://doi.org/10.1021/sc500217p CrossRefGoogle Scholar
  121. Tenover FC (2006) Mechanisms of antimicrobial resistance in bacteria. Am J Med 119:S3–S10.  https://doi.org/10.1016/j.amjmed.2006.03.011 CrossRefPubMedGoogle Scholar
  122. Teow S-Y, Liew K, Ali SA, Khoo AS-B, Peh S-C (2016) Antibacterial action of curcumin against Staphylococcus aureus: a brief review. J Trop Med 2016:1–10.  https://doi.org/10.1155/2016/2853045 CrossRefGoogle Scholar
  123. Thallinger B, Prasetyo EN, Nyanhongo GS, Guebitz GM (2013) Antimicrobial enzymes: an emerging strategy to fight microbes and microbial biofilms. Biotechnol J 8:97–109.  https://doi.org/10.1002/biot.201200313 CrossRefPubMedGoogle Scholar
  124. Veleirinho B, Coelho DS, Dias PF, Maraschin M, Ribeiro-do-Valle RM, Lopes-da-Silva JA (2012) Nanofibrous poly(3-hydroxybutyrate-co-3-hydroxyvalerate)/chitosan scaffolds for skin regeneration. Int J Biol Macromol 51:343–350.  https://doi.org/10.1016/j.ijbiomac.2012.05.023 CrossRefPubMedGoogle Scholar
  125. Verraedt E, Pendela M, Adams E, Hoogmartens J, Martens JA (2010) Controlled release of chlorhexidine from amorphous microporous silica. J Control Release 142:47–52.  https://doi.org/10.1016/j.jconrel.2009.09.022 CrossRefPubMedGoogle Scholar
  126. Wang C, Sauvageau D, Elias A (2016) Immobilization of active bacteriophages on polyhydroxyalkanoate surfaces. ACS Appl Mater Interfaces 8:1128–1138.  https://doi.org/10.1021/acsami.5b08664 CrossRefPubMedGoogle Scholar
  127. Webb JS, Thompson LS, James S, Charlton T, Tolker-nielsen T, Koch B, Givskov M, Kjelleberg S, Al WET, Acteriol JB (2003) Cell death in Pseudomonas aeruginosa biofilm development. J Bacteriol 185:4585–4592.  https://doi.org/10.1128/JB.185.15.4585 CrossRefPubMedPubMedCentralGoogle Scholar
  128. Williams SF, Martin DP (2005) Applications of Polyhydroxyalkanoates (PHA) in medicine and pharmacy. In: Doi Y, Steinbüchel A (eds) Biopolymers online. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim.  https://doi.org/10.1002/3527600035.bpol4004 CrossRefGoogle Scholar
  129. Williamson DH, Mellanby J, Krebs HA (1961) Enzymic determination of D(-)-β-hydroxybutyric acid acetoacetic acid in blood. Biochem J 82:90–96CrossRefGoogle Scholar
  130. Wu Q, Wang Y, Chen G-Q (2009) Medical application of microbial biopolyesters polyhydroxyalkanoates. Artif Cells Blood Substit Biotechnol 37:1–12.  https://doi.org/10.1080/10731190802664429 CrossRefGoogle Scholar
  131. Zaborowska M, Welch K, Brånemark R, Khalilpour P, Engqvist H, Thomsen P, Trobos M (2014) Bacteria-material surface interactions: methodological development for the assessment of implant surface induced antibacterial effects. J Biomed Mater Res Part B Appl Biomater 103:179–187.  https://doi.org/10.1002/jbm.b.33179 CrossRefPubMedGoogle Scholar
  132. Zhu X, Jun Loh X (2015) Layer-by-layer assemblies for antibacterial applications. Biomater Sci 3:1505–1518.  https://doi.org/10.1039/C5BM00307E CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Veronica S. Giourieva
    • 1
  • Rigini M. Papi
    • 1
  • Anastasia A. Pantazaki
    • 1
    Email author
  1. 1.Laboratory of Biochemistry, Department of ChemistryAristotle University of ThessalonikiThessalonikiGreece

Personalised recommendations