Self-assembled squalenoylated penicillin bioconjugates: An original approach for the treatment of intracellular infections

ACS Nano

Volumn 6, Issue 5, 2012, Pages 3820-3831

  Miramoth, Nicolas Sé ^a   Di Meo, Chiara ^a   Zouhiri, Fatima ^a   Saïd Hassane, Fatouma ^a   Valetti, Sabrina ^a   Gorges, Roseline ^c   Nicolas, Valérie ^c   Poupaert, Jacques H ^d   Chollet Martin, Sylvie ^c   Desmaële, Didier ^b   Gref, Ruxandra ^a   Couvreur, Patrick ^a  

^a UNIV PARIS SUD   (France)

^b UNIVERSITÉ PARIS SUD   (France)

^c UNIVERSITÉ PARIS SACLAY   (France)

^d UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

Author keywords

Antibiotic; Intracellular infections; Nanoparticle; Penicillin G; Squalene

Indexed keywords

ANTI-BACTERIAL ACTIVITY; ANTIBIOTIC RESISTANCE; BACTERIAL INFECTIONS; BIO-CONJUGATION; BIOCONJUGATES; CELLULAR UPTAKE; COLOCALIZATION; CULTURE MEDIUM; ENDOCYTIC PATHWAYS; INTRACELLULAR INFECTIONS; INTRACELLULAR PATHOGENS; MACROPHAGE CELL LINE; NEGATIVE CHARGE; PENICILLIN G; PH SENSITIVE; POLYDISPERSITY INDICES; S. AUREUS; SELF-ASSEMBLED; SQUALENE; STABILITY STUDY; SUPRAMOLECULAR ORGANIZATIONS;

ANTIBIOTICS; BACTERIA; CELL CULTURE; CONFOCAL MICROSCOPY; FLOW CYTOMETRY; NANOPARTICLES;

SYNTHESIS (CHEMICAL);

PENICILLIN DERIVATIVE; SQUALENE;

ARTICLE; BACTERIAL INFECTION; CHEMISTRY; HUMAN; MICROBIOLOGICAL EXAMINATION; TRANSMISSION ELECTRON MICROSCOPY;

BACTERIAL INFECTIONS; HUMANS; MICROBIAL SENSITIVITY TESTS; MICROSCOPY, ELECTRON, TRANSMISSION; PENICILLINS; SQUALENE;

EID: 84864674602     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn204928v     Document Type: Article

References (51)

1. Laskay, T.; van Zandbergen, G.; Solbach, W. Neutrophil Granulocytes-Trojan Horses for Leishmania Major and Other Intracellular Microbes? Trends Microbiol. 2003, 11, 210-214.
2. Abeylath, S. C.; Turos, E. Drug Delivery Approaches to Overcome Bacterial Resistance to Beta-Lactam Antibiotics. Expert Opin. Drug Delivery 2008, 5, 931-949.
3. Pinto-Alphandary, H.; Andremont, A.; Couvreur, P. Targeted Delivery of Antibiotics Using Liposomes and Nanoparticles: Research and Applications. Int. J. Antimicrob. Agents 2000, 13, 155-168.
4. Drulis-Kawa, Z.; Dorotkiewicz-Jach, A. Liposomes as Delivery Systems for Antibiotics. Int. J. Pharm. 2010, 387, 187-198.
5. Pinto-Alphandary, H.; Balland, O.; Laurent, M.; Andremont, A.; Puisieux, F.; Couvreur, P. Intracellular Visualization of Ampicillin-Loaded Nanoparticles in Peritoneal Macrophages Infected in Vitro with Salmonella Typhimurium. Pharm. Res. 1994, 11, 38-46.
6. Forestier, F.; Gerrier, P.; Chaumard, C.; Quero, A. M.; Couvreur, P.; Labarre, C. Effect of Nanoparticle-Bound Ampicillin on the Survival of Listeria Monocytogenes in Mouse Peritoneal Macrophages. J. Antimicrob. Chemother. 1992, 30, 173-179.
7. Couvreur, P.; Stella, B.; Reddy, L. H.; Hillaireau, H.; Dubernet, C.; Desmaele, D.; Lepetre-Mouelhi, S.; Rocco, F.; Dereuddre-Bosquet, N.; Clayette, P.; et al. Squalenoyl Nanomedicines as Potential Therapeutics. Nano Lett. 2006, 6, 2544-2548.
8. Sen, S. E.; Prestwich, G. D. Squalene Analogues Containing Isopropylidene Mimics as Potential Inhibitors of Pig Liver Squalene Epoxidase and Oxidosqualene Cyclase. J. Med. Chem. 1989, 32, 2152-2158.
9. Daehne, W.; Frederiksen, E.; Gundersen, E.; Lund, F.; Morch, P.; Petersen, H. J.; Roholt, K.; Tybring, L.; Godtfredsen, W. O. Acyloxymethyl Esters of Ampicillin. J. Med. Chem. 1970, 13, 607-612.
10. Jansen, A. B.; Russell, T. J. Some Novel Penicillin Derivatives. J. Chem. Soc. 1965, 65, 2127-2132.
11. Baltzer, B.; Binderup, E.; von Daehne, W.; Godtfredsen, W. O.; Hansen, K.; Nielsen, B.; Sorensen, H.; Vangedal, S. Mutual Pro-Drugs of Beta-Lactam Antibiotics and Beta-Lactamase Inhibitors. J. Antibiot. (Tokyo) 1980, 33, 1183-1192.
12. Klein, L. L.; Yeung, C. M.; Kurath, P.; Mao, J. C.; Fernandes, P. B.; Lartey, P. A.; Pernet, A. G. Synthesis and Activity of Nonhydrolyzable Pseudomonic Acid Analogues. J. Med. Chem. 1989, 32, 151-160.
13. Couvreur, P.; Reddy, L. H.; Mangenot, S.; Poupaert, J. H.; Desmaele, D.; Lepetre-Mouelhi, S.; Pili, B.; Bourgaux, C.; Amenitsch, H.; Ollivon, M. Discovery of New Hexagonal Supramolecular Nanostructures Formed by Squalenoylation of an Anticancer Nucleoside Analogue. Small 2008, 4, 247-253.
14. Dewar, M. J.; Storch, D. M. Alternative View of Enzyme Reactions. Proc. Natl. Acad. Sci. U. S. A. 1985, 82, 2225-2229.
15. Jorgensen, J. H.; Swenson, J. M.; Tenover, F. C.; Barry, A.; Ferraro, M. J.; Murray, P. R.; Reller, L. B. Development of Interpretive Criteria and Quality Control Limits for Macrolide and Clindamycin Susceptibility Testing of Streptococcus Pneumoniae. J. Clin. Microbiol. 1996, 34, 2679-2684.
16. Holten, K. B.; Onusko, E. M. Appropriate Prescribing of Oral Beta-Lactam Antibiotics. Am. Fam. Physician 2000, 62, 611-620.
17. Briones, E.; Colino, C. I.; Lanao, J. M. Delivery Systems to Increase the Selectivity of Antibiotics in Phagocytic Cells. J. Controlled Release 2008, 125, 210-227.
18. Hamilton-Miller, J. M. Antibiotic Resistance from Two Perspectives: Man and Microbe. Int. J. Antimicrob. Agents 2004, 23, 209-212.
19. Martinez, J. L.; Fajardo, A.; Garmendia, L.; Hernandez, A.; Linares, J. F.; Martinez-Solano, L.; Sanchez, M. B. A Global View of Antibiotic Resistance. FEMS Microbiol. Rev. 2009, 33, 44-65.
20. Balland, O.; Pinto-Alphandary, H.; Pecquet, S.; Andremont, A.; Couvreur, P. The Uptake of Ampicillin-Loaded Nanoparticles by Murine Macrophages Infected with Salmonella Typhimurium. J. Antimicrob. Chemother. 1994, 33, 509-522.
21. Balland, O.; Pinto-Alphandary, H.; Viron, A.; Puvion, E.; Andremont, A.; Couvreur, P. Intracellular Distribution of Ampicillin in Murine Macrophages Infected with Salmonella Typhimurium and Treated with (3h) Ampicillin-Loaded Nanoparticles. J. Antimicrob. Chemother. 1996, 37, 105-115.
22. Lemarchand, C.; Gref, R.; Passirani, C.; Garcion, E.; Petri, B.; Muller, R.; Costantini, D.; Couvreur, P. Influence of Polysaccharide Coating on the Interactions of Nanoparticles with Biological Systems. Biomaterials 2006, 27, 108-118.
23. Semiramoth, N.; Gleizes, A.; Turbica, I.; Sandre, C.; Marin-Esteban, V.; Gorges, R.; Servin, A.; Chollet-Martin, S. Afa/Dr-Expressing, Diffusely Adhering Escherichia Coli Strain C1845 Triggers F1845 Fimbria-Dependent Phosphatidylserine Externalization on Neutrophil-Like Differentiated Plb-985 Cells through an Apoptosis-Independent Mechanism. Infect. Immun. 2010, 78, 2974-2983.
24. Owens, D. E., 3rd; Peppas, N. A. Opsonization, Biodistribution, and Pharmacokinetics of Polymeric Nanoparticles. Int. J. Pharm. 2006, 307, 93-102.
25. Garzoni, C.; Kelley, W. L. Staphylococcus Aureus: New Evidence for Intracellular Persistence. Trends Microbiol. 2009, 17, 59-65.
26. Barcia-Macay, M.; Seral, C.; Mingeot-Leclercq, M. P.; Tulkens, P. M.; Van Bambeke, F. Pharmacodynamic Evaluation of the Intracellular Activities of Antibiotics against Staphylococcus Aureus in a Model of Thp-1 Macrophages. Antimicrob. Agents Chemother. 2006, 50, 841-851.
27. Kubica, M.; Guzik, K.; Koziel, J.; Zarebski, M.; Richter, W.; Gajkowska, B.; Golda, A.; Maciag-Gudowska, A.; Brix, K.; Shaw, L.; et al. A Potential New Pathway for Staphylococcus Aureus Dissemination: The Silent Survival of S. Aureus Phagocytosed by Human Monocyte-Derived Macrophages. PLoS One 2008, 3, e1409.
28. Melter, O.; Radojevic, B. Small Colony Variants of Staphylococcus Aureus-Review. Folia Microbiol. (Praha) 2010, 55, 548-558.
29. Kiss, A. L.; Geuze, H. J. Caveolae Can Be Alternative Endocytotic Structures in Elicited Macrophages. Eur. J. Cell Biol. 1997, 73, 19-27.
30. Perry, D. G.; Daugherty, G. L.; Martin, W. J., 2nd Clathrin-Coated Pit-Associated Proteins Are Required for Alveolar Macrophage Phagocytosis. J. Immunol. 1999, 162, 380-386.
31. Rajendran, L.; Knolker, H. J.; Simons, K. Subcellular Targeting Strategies for Drug Design and Delivery. Nat. Rev. Drug Discovery 2010, 9, 29-42.
32. Ivanov, A. I. Pharmacological Inhibition of Endocytic Pathways: Is It Specific Enough to Be Useful? Methods Mol. Biol. 2008, 440, 15-33.
33. Aggarwal, P.; Hall, J. B.; McLeland, C. B.; Dobrovolskaia, M. A.; McNeil, S. E. Nanoparticle Interaction with Plasma Proteins as It Relates to Particle Biodistribution, Biocompatibility and Therapeutic Efficacy. Adv. Drug Delivery Rev. 2009, 61, 428-437.
34. Dobrovolskaia, M. A.; Patri, A. K.; Zheng, J.; Clogston, J. D.; Ayub, N.; Aggarwal, P.; Neun, B. W.; Hall, J. B.; McNeil, S. E. Interaction of Colloidal Gold Nanoparticles with Human Blood: Effects on Particle Size and Analysis of Plasma Protein Binding Profiles. Nanomedicine 2009, 5, 106-117.
35. Goppert, T. M.; Muller, R. H. Protein Adsorption Patterns on Poloxamer-and Poloxamine-Stabilized Solid Lipid Nanoparticles (Sln). Eur. J. Pharm. Biopharm. 2005, 60, 361-372.
36. Kim, H. R.; Andrieux, K.; Delomenie, C.; Chacun, H.; Appel, M.; Desmaele, D.; Taran, F.; Georgin, D.; Couvreur, P.; Taverna, M. Analysis of Plasma Protein Adsorption onto Pegylated Nanoparticles by Complementary Methods: 2-De, Ce and Protein Lab-on-Chip System. Electrophoresis 2007, 28, 2252-2261.
37. Thode, K.; Luck, M.; Semmler, W.; Muller, R. H.; Kresse, M. Determination of Plasma Protein Adsorption on Magnetic Iron Oxides: Sample Preparation. Pharm. Res. 1997, 14, 905-910.
38. Goppert, T. M.; Muller, R. H. Adsorption Kinetics of Plasma Proteins on Solid Lipid Nanoparticles for Drug Targeting. Int. J. Pharm. 2005, 302, 172-186.
39. Moghimi, S. M.; Muir, I. S.; Illum, L.; Davis, S. S.; Kolb-Bachofen, V. Coating Particles with a Block Co-Polymer (Poloxamine-908) Suppresses Opsonization but Permits the Activity of Dysopsonins in the Serum. Biochim. Biophys. Acta 1993, 1179, 157-165.
40. Ogawara, K.; Furumoto, K.; Nagayama, S.; Minato, K.; Higaki, K.; Kai, T.; Kimura, T. Pre-Coating with Serum Albumin Reduces Receptor-Mediated Hepatic Disposition of Polystyrene Nanosphere: Implications for Rational Design of Nanoparticles. J. Controlled Release 2004, 100, 451-455.
41. Cedervall, T.; Lynch, I.; Lindman, S.; Berggard, T.; Thulin, E.; Nilsson, H.; Dawson, K. A.; Linse, S. Understanding the Nanoparticle-Protein Corona Using Methods to Quantify Exchange Rates and Affinities of Proteins for Nanoparticles. Proc. Natl. Acad. Sci. U. S. A. 2007, 104, 2050-2055.
42. Carrstensen, H.; Muller, R. H.; Muller, B. W. Particle Size, Surface Hydrophobicity and Interaction with Serum of Parenteral Fat Emulsions and Model Drug Carriers as Parameters Related to Res Uptake. Clin. Nutr. 1992, 11, 289-297.
43. Muller, R. H.; Ruhl, D.; Luck, M.; Paulke, B. R. Influence of Fluorescent Labelling of Polystyrene Particles on Phagocytic Uptake, Surface Hydrophobicity, and Plasma Protein Adsorption. Pharm. Res. 1997, 14, 18-24.
44. Norman, M. E.; Williams, P.; Illum, L. Human Serum Albumin as a Probe for Surface Conditioning (Opsonization) of Block Copolymer-Coated Microspheres. Biomaterials 1992, 13, 841-849.
45. Sahay, G.; Alakhova, D. Y.; Kabanov, A. V. Endocytosis of Nanomedicines. J. Controlled Release 2010, 145, 182-195.
46. Renard, C.; Vanderhaeghe, H. J.; Claes, P. J.; Zenebergh, A.; Tulkens, P. M. Influence of Conversion of Penicillin G into a Basic Derivative on Its Accumulation and Subcellular Localization in Cultured Macrophages. Antimicrob. Agents Chemother. 1987, 31, 410-416.
47. Tulkens, P. M. Intracellular Distribution and Activity of Antibiotics. Eur. J. Clin. Microbiol. Infect. Dis. 1991, 10, 100-106.
48. Andersen, O. S. Elementary Aspects of Acid-Base Permeation and pH Regulation. Ann. N. Y. Acad. Sci. 1989, 574, 333-353.
49. Vaudaux, P.; Waldvogel, F. A. Gentamicin Antibacterial Activity in the Presence of Human Polymorphonuclear Leukocytes. Antimicrob. Agents Chemother. 1979, 16, 743-749.
50. Trouillet, S.; Rasigade, J. P.; Lhoste, Y.; Ferry, T.; Vandenesch, F.; Etienne, J.; Laurent, F. A Novel Flow Cytometry-Based Assay for the Quantification of Staphylococcus Aureus Adhesion to and Invasion of Eukaryotic Cells. J. Microbiol. Methods 2011, 86, 145-149.
51. Toyooka, K.; Takai, S.; Kirikae, T. Rhodococcus Equi Can Survive a Phagolysosomal Environment in Macrophages by Suppressing Acidification of the Phagolysosome. J. Med. Microbiol. 2005, 54, 1007-1015.