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  • 1.
    Boge, Lukas
    RISE, Sweden; Chalmers University of Technology, Sweden.
    Lipid-based liquid crystals as drug delivery vehicles for antimicrobial peptides2018Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    The development of antimicrobial resistance is a great challenge within health sectors worldwide. Thus, demand for new, efficient treatments is urgent in order to treat various bacterial infections. Antimicrobial peptides (AMPs) are a group of antibiotics that have gained more and more attraction in the past decade. AMPs suffer from relatively low stability due to proteolytic and chemical degradation. As a consequence, carrier systems to protect the AMPs are highly needed to achieve efficient treatments in the clinic. In this thesis, lipid-based liquid crystalline (LC) structures have been examined as carriers for AMPs. LC structures of polar lipids have potential to be used as carriers and delivery systems in various pharmaceutical applications. This is due to their ability to solubilize and encapsulate hydrophilic, hydrophobic and amphiphilic substances. An important feature of these LC systems is that they can coexist with an excess of water, which enables fragmentation of the highly viscous gels into LC nanoparticles (LCNPs), i.e. cubosomes and hexosomes, in the presence of a suitable stabilizer. Peptides and proteins can be incorporated into the lipid self-assembled structures, thereby protecting them from chemical and proteolytic degradation. Cubosomes and hexosomes were investigated as drug delivery vehicles for the three AMPs: i) AP114, an improved plectasin derivative originating from the fungus Pseudoplectania nigrella, ii) DPK-060, derived from the endogenous human protein kininogen and iii) LL-37, a human AMP found in the cathelicidin family. Phase behavior, different preparation methodologies of the LCNPs, antimicrobial effect and proteolytic protection of the AMPs were studied. Moreover, the interaction between AMP-loaded particles with bacteria and bacterial mimicking membranes was investigated. Formulations aimed for pulmonary and topical administration were also evaluated. Results showed that cubic LC phases were most sensitive to the incorporation of AMPs. Depending on the nature of the AMP, different changes in the curvature of the systems were observed. Cubosomes loaded with AMPs exhibited good antimicrobial activity and were found to protect the proteolytic sensitive LL-37 from enzymatic degradation. Data strongly suggested that the release of AMP from the particles cannot solely be explained by the antimicrobial effect. Cubosomes loaded with LL-37 are thought to adsorb onto bacterial membranes, resulting in cell death.

  • 2.
    Boge, Lukas
    et al.
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation. Chalmers University of Technology, Sweden.
    Browning, Kathryn
    University of Copenhagen, Denmark.
    Nordström, Randi
    Uppsala University, Sweden.
    Campana, Mario
    Rutherford Appleton Laboratory, UK.
    Damgaard, Liv
    University of Copenhagen, Denmark.
    Seth Caous, Josefin
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Hellsing, Maja
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation.
    Ringstad, Lovisa
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Andersson, Martin
    Chalmers University of Technology, Sweden.
    Peptide-Loaded Cubosomes Functioning as an Antimicrobial Unit against Escherichia coli2019In: ACS Applied Materials and Interfaces, ISSN 1944-8244, E-ISSN 1944-8252, Vol. 11, no 24, p. 21314-21322Article in journal (Refereed)
    Abstract [en]

    Dispersions of cubic liquid crystalline phases, also known as cubosomes, have shown great promise as delivery vehicles for a wide range of medicines. Due to their ordered structure, comprising alternating hydrophilic and hydrophobic domains, cubosomes possess unique delivery properties and compatibility with both water-soluble and -insoluble drugs. However, the drug delivery mechanism and cubosome interaction with human cells and bacteria are still poorly understood. Herein, we reveal how cubosomes loaded with the human cathelicidin antimicrobial peptide LL-37, a system with high bacteria-killing effect, interact with the bacterial membrane and provide new insights into the eradication mechanism. Combining the advanced experimental techniques neutron reflectivity and quartz crystal microbalance with dissipation monitoring, a mechanistic drug delivery model for LL-37-loaded cubosomes on bacterial mimicking bilayers was constructed. Moreover, the cubosome interaction with Escherichia coli was directly visualized using super-resolution laser scanning microscopy and cryogenic electron tomography. We could conclude that cubosomes loaded with LL-37 adsorbed and distorted bacterial membranes, providing evidence that the peptide-loaded cubosomes function as an antimicrobial unit.

  • 3.
    Boge, Lukas
    et al.
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor, Life Science. Chalmers University of Technology, Sweden.
    Bysell, Helena
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor, Life Science.
    Ringstad, Lovisa
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor, Life Science.
    Wennman, David
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Process Development, Analys och fastfas.
    Umerska, Anita
    University of Angers, France.
    Cassisa, Viviane
    CHU Angers, France.
    Eriksson, Jonny
    Uppsala University, Sweden.
    Joly-Guillou, Marie-Laure
    CHU Angers, France.
    Edwards, Katarina
    Uppsala University, Sweden.
    Andersson, Martin
    Chalmers University of Technology, Sweden.
    Lipid-based liquid crystals as carriers for antimicrobial peptides: Phase behavior and antimicrobial effect2016In: Langmuir, ISSN 0743-7463, E-ISSN 1520-5827, Vol. 32, no 17, p. 4217-4228Article in journal (Refereed)
    Abstract [en]

    The number of antibiotic-resistant bacteria is increasing worldwide, and the demand for novel antimicrobials is constantly growing. Antimicrobial peptides (AMPs) could be an important part of future treatment strategies of various bacterial infection diseases. However, AMPs have relatively low stability, because of proteolytic and chemical degradation. As a consequence, carrier systems protecting the AMPs are greatly needed, to achieve efficient treatments. In addition, the carrier system also must administrate the peptide in a controlled manner to match the therapeutic dose window. In this work, lyotropic liquid crystalline (LC) structures consisting of cubic glycerol monooleate/water and hexagonal glycerol monooleate/oleic acid/water have been examined as carriers for AMPs. These LC structures have the capability of solubilizing both hydrophilic and hydrophobic substances, as well as being biocompatible and biodegradable. Both bulk gels and discrete dispersed structures (i.e., cubosomes and hexosomes) have been studied. Three AMPs have been investigated with respect to phase stability of the LC structures and antimicrobial effect: AP114, DPK-060, and LL-37. Characterization of the LC structures was performed using small-angle X-ray scattering (SAXS), dynamic light scattering, ζ-potential, and cryogenic transmission electron microscopy (Cryo-TEM) and peptide loading efficacy by ultra performance liquid chromatography. The antimicrobial effect of the LCNPs was investigated in vitro using minimum inhibitory concentration (MIC) and time-kill assay. The most hydrophobic peptide (AP114) was shown to induce an increase in negative curvature of the cubic LC system. The most polar peptide (DPK-060) induced a decrease in negative curvature while LL-37 did not change the LC phase at all. The hexagonal LC phase was not affected by any of the AMPs. Moreover, cubosomes loaded with peptides AP114 and DPK-060 showed preserved antimicrobial activity, whereas particles loaded with peptide LL-37 displayed a loss in its broad-spectrum bactericidal properties. AMP-loaded hexosomes showed a reduction in antimicrobial activity.

  • 4.
    Boge, Lukas
    et al.
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation. Chalmers University of Technology, Sweden.
    Hallstensson, Karin
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation.
    Ringstad, Lovisa
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation.
    Johansson, Jenny
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Andersson, Therese
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Davoudi, Mina
    Lund University, Sweden.
    Larsson, Tomas
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Mahlapuu, Margit
    Promore Pharma AB, Sweden; University of Gothenburg, Sweden.
    Håkansson, Joakim
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Andersson, Martin
    Chalmers University of Technology, Sweden.
    Cubosomes for topical delivery of the antimicrobial peptide LL-372019In: European journal of pharmaceutics and biopharmaceutics, ISSN 0939-6411, E-ISSN 1873-3441, Vol. 134, p. 60-67Article in journal (Refereed)
    Abstract [en]

    In this study, the use of cubosomes for topical delivery of the antimicrobial peptide (AMP) LL-37 was investigated. Topical delivery of AMPs is of great interest for treatment of skin infections caused by bacteria, such as Staphylococcus aureus. AMP containing cubosomes were produced by three different preparation protocols and compared: (i) pre-loading, where LL-37 was incorporated into a liquid crystalline gel, which thereafter was dispersed into nanoparticles, (ii) post-loading, where LL-37 was let to adsorb onto pre-formed cubosomes, and (iii) hydrotrope-loading, where LL-37 was incorporated during the spontaneously formed cubosomes in an ethanol/glycerol monooleate mixture. Particle size and size distribution were analyzed using dynamic light scattering (DLS), liquid crystalline structure by small angle x-ray scattering (SAXS) and release of LL-37 by a fluorescamine assay. Proteolytic protection of LL-37 as well as bactericidal effect after enzyme exposure was investigated. The skin irritation potential of cubosomes was examined by an in vitro epidermis model. Finally, the bacterial killing property of the cubosomes was examined by an ex vivo pig skin wound infection model with Staphylococcus aureus. Data showed that a high loading of LL-37 induced formation of vesicles in case of cubosomes prepared by sonication (pre-loading). No release of LL-37 was observed from the cubosomes, indicating strong association of the peptide to the particles. Proteolysis studies showed that LL-37 was fully protected against enzymatic attacks while associated with the cubosomes, also denoting strong association of the peptide to the particles. As a consequence, bactericidal effect after enzyme exposure remained, compared to pure LL-37 which was subjected to proteolysis. No skin irritation potential of the cubosomes was found, thus enabling for topical administration. The ex vivo wound infection model showed that LL-37 in pre-loaded cubosomes killed bacteria most efficient.

  • 5.
    Boge, Lukas
    et al.
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation. Chalmers University of Technology, Sweden.
    Västberg, Amanda
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation.
    Umerska, Anita
    Université Bretagne Loire, France.
    Bysell, Helena
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation.
    Eriksson, Jonny
    Uppsala University, Sweden.
    Edwards, Katarina
    Uppsala University, Sweden.
    Millqvist-Fureby, Anna
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation.
    Andersson, Martin
    Chalmers University of Technology, Sweden.
    Freeze-dried and re-hydrated liquid crystalline nanoparticles stabilized with disaccharides for drug-delivery of the plectasin derivative AP114 antimicrobial peptide2018In: Journal of Colloid and Interface Science, ISSN 0021-9797, E-ISSN 1095-7103, Vol. 522, p. 126-135Article in journal (Refereed)
    Abstract [en]

    Liquid crystalline nanoparticles (LCNPs), e.g. cubosomes and hexosomes, are receiving more and more attraction as drug delivery vehicles. Dry powder formulation that forms LCNPs upon hydration can be advantageous to make new routes of administration accessible. In this work, we investigate use of three disaccharides (lactose, trehalose and sucrose) as protective matrices for glycerol monooleate based LCNP forming powders produced by freeze-drying. Phase behavior, particle size and size distributions at the different preparation steps were monitored by small angle x-ray scattering (SAXS) and dynamic light scattering (DLS). Particle appearance was imaged by cryogenic transmission electron microscopy (cryo-TEM). Moreover, the therapeutic relevant antimicrobial peptide AP114 (plectasin derivative) was incorporated in the formulations. Peptide encapsulation and release as well as in vitro antibacterial effect were investigated. Results showed that all freeze-dried powders did form particles with liquid crystalline structure upon hydration. However, a phase transition from the bicontinuous cubic Pn3m to the reversed hexagonal was observed, as a consequence of sugar addition and the freeze-drying procedure. Data indicates that trehalose is the preferred choice of lyo-protectant in order to maintain a mono-modal particle size distribution. In addition, antimicrobial activity of AP114-containing formulations was found to be highest for the formulation containing trehalose. The release kinetics of AP114 from the nanoparticles was strongly affected by the dimensions of the hexagonal phase. Larger dimension of the hexagonal phase, significantly improved the release of AP114 and antimicrobial activity of the formulation.

  • 6.
    Håkansson, Joakim
    et al.
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Ringstad, Lovisa
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Umerska, Anita
    Université de Lorraine, France; Université Bretagne Loire, France.
    Johansson, Jenny
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Andersson, Therese
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Boge, Lukas
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Rozenbaum, René T
    University of Groningen, Netherlands.
    Sharma, Prashant K
    University of Groningen, Netherlands.
    Tollbäck, Petter
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Björn, Camilla
    RISE - Research Institutes of Sweden, Bioscience and Materials, Chemistry and Materials.
    Saulnier, Patrick
    Université Bretagne Loire, France.
    Mahlapuu, Margit
    Promore Pharma AB, Sweden.
    Characterization of the in vitro, ex vivo, and in vivo Efficacy of the Antimicrobial Peptide DPK-060 Used for Topical Treatment.2019In: Frontiers in Cellular and Infection Microbiology, E-ISSN 2235-2988, Vol. 9, article id 174Article in journal (Refereed)
    Abstract [en]

    Antimicrobial peptides, also known as host defense peptides, have recently emerged as a promising new category of therapeutic agents for the treatment of infectious diseases. This study evaluated the preclinical in vitro, ex vivo, and in vivo antimicrobial activity, as well as the potential to cause skin irritation, of human kininogen-derived antimicrobial peptide DPK-060 in different formulations designed for topical delivery. We found that DPK-060 formulated in acetate buffer or poloxamer gel caused a marked reduction of bacterial counts of Staphylococcus aureus in vitro (minimum microbicidal concentration <5 μg/ml). We also found that DPK-060 in poloxamer gel significantly suppressed microbial survival in an ex vivo wound infection model using pig skin and in an in vivo mouse model of surgical site infection (≥99 or ≥94% reduction in bacterial counts was achieved with 1% DPK-060 at 4 h post-treatment, respectively). Encapsulation of DPK-060 in different types of lipid nanocapsules or cubosomes did not improve the bactericidal potential of the peptide under the applied test conditions. No reduction in cell viability was observed in response to administration of DPK-060 in any of the formulations tested. In conclusion, the present study confirms that DPK-060 has the potential to be an effective and safe drug candidate for the topical treatment of microbial infections; however, adsorption of the peptide to nanocarriers failed to show any additional benefits.

  • 7.
    Matougui, Nada
    et al.
    Inserm, France.
    Boge, Lukas
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor, Life Science.
    Groo, Anne-Claire
    Inserm, France.
    Umerska, Anita
    Inserm, France.
    Ringstad, Lovisa
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor, Life Science.
    Bysell, Helena
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor, Life Science.
    Saulnier, Patrick
    Inserm, France; CHU Angers, France.
    Lipid-based nanoformulations for peptide delivery2016In: International Journal of Pharmaceutics, ISSN 0378-5173, E-ISSN 1873-3476, Vol. 502, no 1-2, p. 80-97Article, review/survey (Refereed)
    Abstract [en]

    Nanoformulations have attracted a lot of attention because of their size-dependent properties. Among the array of nanoformulations, lipid nanoformulations (LNFs) have evoked increasing interest because of the advantages of their high degree of biocompatibility and versatility. The performance of lipid nanoformulations is greatly influenced by their composition and structure. Therapeutic peptides represent a growing share of the pharmaceutical market. However, the main challenge for their development into commercial products is their inherent physicochemical and biological instability. Important peptides such as insulin, calcitonin and cyclosporin A have been incorporated into LNFs. The association or encapsulation of peptides within lipid-based carriers has shown to protect the labile molecules against enzymatic degradation. This review describes strategies used for the formulation of peptides and some methods used for the assessment of association efficiency. The advantages and drawbacks of such carriers are also described.

  • 8.
    Mira, Isabel
    et al.
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor, Life Science.
    Andersson, Martin
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor, Life Science.
    Boge, Lukas
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor, Life Science.
    Blute, Irena
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor, Life Science.
    Carlsson, Gilbert
    RISE, SP – Sveriges Tekniska Forskningsinstitut, SP Kemi Material och Ytor.
    Foam forming revisited Part I. Foaming behaviour of fibre-surfactant systems2014In: Nordic Pulp & Paper Research Journal, ISSN 0283-2631, E-ISSN 2000-0669, Vol. 29, no 4, p. 679-688Article in journal (Refereed)
    Abstract [en]

    The foaming properties of typical chemithermo-mechanical (CTMP) and kraft pulp paper making formulations in the presence of a series of surfactants were investigated using a lab-scale foaming set up. Foamability, foam stability, and bubble size distribution of the generated foam-fibre systems were measured. The foaming behaviour of the fibre/surfactant systems was found to be dependent on the surfactant concentration. Foams fulfilling the target requirements of air content (ca. 65% v/v air) and average bubble size (25 to 75 μm in radius) were obtained with all the seven surfactants tested. Three of the surfactants were found to allow for a rapid foaming in the system, namely sodium dodecyl sulphate (SDS), a commercial mixture of alkyl and ethoxylated alkyl sulphates, (MixSAES) and a commercial mixture of short chain alkyl glucosides (C8/C10Gluc). The rapid foaming is believed to be an intrinsic property of mixtures of surfactants with the right molecular structures and in the right proportion with respect to each other. On the other hand, the minimum surfactant concentrations required to reach the target foam volumes were lowest for surfactants with an anionic character. Further, the type of pulp fibre and the presence of GCC in the surfactant/pulp formulation were found to have very little effect on the foaming performance of the suspensions.

  • 9.
    Valente, Filippo
    et al.
    University of Padua, Italy.
    Bysell, Helena
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation.
    Simoni, Edi
    University of Padua, Italy.
    Boge, Lukas
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation.
    Eriksson, Mimmi
    RISE - Research Institutes of Sweden, Bioscience and Materials, Surface, Process and Formulation.
    Martini, Alessandro
    University of Padua, Italy.
    Astolfi, Laura
    University of Padua, Italy.
    Evaluation of toxicity of glycerol monooleate nanoparticles on PC12 cell line.2018In: International Journal of Pharmaceutics, ISSN 0378-5173, E-ISSN 1873-3476, Vol. 539, no 1-2, p. 23-30, article id S0378-5173(18)30054-1Article in journal (Refereed)
    Abstract [en]

    An innovative approach to improve drug delivery is the use of glycerol monooleate nanoparticles. Numerous studies describe their high versatility, low toxicity and ability to carry relatively high loads of conjugated compounds including scarcely soluble ones, providing sustained drug release and increasing drug diffusion and half-life. Despite a growing interest in their potential use for therapeutic applications, there are surprisingly few literature data concerning the toxic effects of these nanoparticles at high concentrations in vitro and in vivo, and their effects on cell metabolism. We produced and characterized from a physical-chemical point of view glycerol monooleate nanoparticles and tested them on the PC12 cell line, a rat model of neuronal differentiation. The toxicity of these nanoparticles was evaluated by molecular methods on cell viability, cell cycle, nanoparticle uptake and induction of apoptosis. The results showed that glycerol monooleate nanoparticles up to 100 μg/mL had no toxic effects on PC12 cells, did not induce significant changes in the cell cycle nor cause apoptosis. The nanoparticles entered PC12 cells 8 h after treatment, successfully delivering the conjugate compound inside cells. Overall, glycerol monooleate nanoparticles did not exhibit significant toxicity on PC12 cell line in concentrations up to 100 µg/mL, supporting their therapeutic use as drug delivery systems.

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