Development of a dry, stable and inhalable acyl-homoserine-lactone-acylase powder formulation for the treatment of pulmonary Pseudomonas aeruginosa infections

European Journal of Pharmaceutical Sciences

Volumn 48, Issue 4-5, 2013, Pages 637-643

  Wahjudi, Mariana ^a,b   Murugappan, Senthil ^a   Van Merkerk, Ronald ^a   Eissens, Anko C ^a   Visser, Marinella R ^a   Hinrichs, Wouter L J ^a   Quax, Wim J ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF SURABAYA   (Indonesia)

Author keywords

Acyl homoserine lactone acylase; Inulin; Mannitol; Spray freeze dried PvdQ; Trehalose

Indexed keywords

AMIDASE; ANTIBIOTIC AGENT; INULIN; MANNITOL; PVDQ PROTEIN; TREHALOSE; UNCLASSIFIED DRUG;

ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG FORMULATION; DRUG STABILITY; DRUG STORAGE; DRY POWDER; ENZYME ACTIVITY; ENZYME STABILITY; ENZYMIC BIOSENSOR; FREEZE DRYING; HOST CELL; IN VITRO STUDY; IN VIVO STUDY; INHALATIONAL DRUG ADMINISTRATION; LUNG INFECTION; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; QUORUM SENSING; SPRAY DRYING; STORAGE TEMPERATURE;

ACYL-BUTYROLACTONES; ADMINISTRATION, INHALATION; AMIDOHYDROLASES; ANTI-BACTERIAL AGENTS; BACTERIAL PROTEINS; DRUG STABILITY; ESCHERICHIA COLI; EXCIPIENTS; INULIN; MANNITOL; MICROSCOPY, ELECTRON, SCANNING; POWDER DIFFRACTION; POWDERS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; TREHALOSE; X-RAY DIFFRACTION;

EID: 84873449341     PISSN: 09280987     EISSN: 18790720     Source Type: Journal    
DOI: 10.1016/j.ejps.2012.12.015     Document Type: Article

References (50)

1. J.P. Amorij, V. Saluja, A.H. Petersen, W.L. Hinrichs, A. Huckriede, and H.W. Frijlink Pulmonary delivery of an inulin-stabilized influenza subunit vaccine prepared by spray-freeze drying induces systemic, mucosal humoral as well as cell-mediated immune responses in BALB/c mice Vaccine 25 2007 8707 8717
2. J.D. Andya, Y.F. Maa, H.R. Costantino, P.A. Nguyen, N. Dasovich, T.D. Sweeney, C.C. Hsu, and S.J. Shire The effect of formulation excipients on protein stability and aerosol performance of spray-dried powders of a recombinant humanized anti-IgE monoclonal antibody Pharm. Res. 16 1999 350 358
3. S.A. Audouy, G. van der Schaaf, W.L. Hinrichs, H.W. Frijlink, J. Wilschut, and A. Huckriede Development of a dried influenza whole inactivated virus vaccine for pulmonary immunization Vaccine 29 2011 4345 4352
4. T. Bjarnsholt, P.O. Jensen, T.H. Jakobsen, R. Phipps, A.K. Nielsen, M.T. Rybtke, T. Tolker-Nielsen, M. Givskov, N. Hoiby, O. Ciofu, and Scandinavian Cystic Fibrosis Study Consortium Quorum sensing and virulence of Pseudomonas aeruginosa during lung infection of cystic fibrosis patients PLoS ONE 5 2010 e10115
5. M. Bokhove, P. Nadal Jimenez, W.J. Quax, and B.W. Dijkstra The quorum-quenching N-acyl homoserine lactone acylase PvdQ is an Ntn-hydrolase with an unusual substrate-binding pocket Proc. Natl. Acad. Sci. USA 107 2010 686 691
6. H.R. Costantino, J.D. Andya, P.A. Nguyen, N. Dasovich, T.D. Sweeney, S.J. Shire, C.C. Hsu, and Y.F. Maa Effect of mannitol crystallization on the stability and aerosol performance of a spray-dried pharmaceutical protein, recombinant humanized anti-IgE monoclonal antibody J. Pharm. Sci. 87 1998 1406 1411
7. R. Czajkowski, and S. Jafra Quenching of acyl-homoserine lactone-dependent quorum sensing by enzymatic disruption of signal molecules Acta Biochim. Pol. 56 2009 1 16
8. D. Davies Understanding biofilm resistance to antibacterial agents Nat. Rev. Drug Discov. 2 2003 114 122
9. T.R. De Kievit, and B.H. Iglewski Quorum sensing, gene expression, and Pseudomonas biofilms Methods Enzymol. 310 1999 117 128
10. T. Defoirdt, N. Boon, and P. Bossier Can bacteria evolve resistance to quorum sensing disruption? PLoS Pathog. 6 2010 e1000989
11. H. Donabedian Quorum sensing and its relevance to infectious diseases J. Infect. 46 2003 207 214
12. D.L. Erickson, R. Endersby, A. Kirkham, K. Stuber, D.D. Vollman, H.R. Rabin, I. Mitchell, and D.G. Storey Pseudomonas aeruginosa quorum-sensing systems may control virulence factor expression in the lungs of patients with cystic fibrosis Infect. Immun. 70 2002 1783 1790
13. S. Favre-Bonte, J.C. Pache, J. Robert, D. Blanc, J.C. Pechere, and C. van Delden Detection of Pseudomonas aeruginosa cell-to-cell signals in lung tissue of cystic fibrosis patients Microb. Pathog. 32 2002 143 147
14. S. Favre-Bonte, T. Kohler, and C. Van Delden Biofilm formation by Pseudomonas aeruginosa: role of the C4-HSL cell-to-cell signal and inhibition by azithromycin J. Antimicrob. Chemother. 52 2003 598 604
15. L.T.R. Furlán, A.P. Padilla, and M. Campderros Development of a functional beverage formulation with high protein content, inulin and Stevia Int. J. Food Eng. 7 2011 1 16
16. H. Heijerman, E. Westerman, S. Conway, D. Touw, G. Doring, and consensus working group Inhaled medication and inhalation devices for lung disease in patients with cystic fibrosis: a European consensus J. Cyst Fibros 8 2009 295 315
17. M. Hentzer, K. Riedel, T.B. Rasmussen, A. Heydorn, J.B. Andersen, M.R. Parsek, S.A. Rice, L. Eberl, S. Molin, N. Hoiby, S. Kjelleberg, and M. Givskov Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound Microbiology 148 2002 87 102
18. M. Hentzer, L. Eberl, J. Nielsen, and M. Givskov Quorum sensing: a novel target for the treatment of biofilm infections BioDrugs 17 2003 241 250
19. W.L. Hinrichs, M.G. Prinsen, and H.W. Frijlink Inulin glasses for the stabilization of therapeutic proteins Int. J. Pharm. 215 2001 163 174
20. K. Izutsu, and S. Kojima Excipient crystallinity and its protein-structure-stabilizing effect during freeze-drying J. Pharm. Pharmacol. 54 2002 1033 1039
21. K. Izutsu, S. Yoshioka, and S. Kojima Physical stability and protein stability of freeze-dried cakes during storage at elevated temperatures Pharm. Res. 11 1994 995 999
22. K. Izutsu, C. Yomota, and N. Aoyagi Inhibition of mannitol crystallization in frozen solutions by sodium phosphates and citrates Chem. Pharm. Bull. (Tokyo) 55 2007 565 570
23. P.O. Jensen, T. Bjarnsholt, R. Phipps, T.B. Rasmussen, H. Calum, L. Christoffersen, C. Moser, P. Williams, T. Pressler, M. Givskov, and N. Hoiby Rapid necrotic killing of polymorphonuclear leukocytes is caused by quorum-sensing-controlled production of rhamnolipid by Pseudomonas aeruginosa Microbiology 153 2007 1329 1338
24. C. Johansen, P. Falholt, and L. Gram Enzymatic removal and disinfection of bacterial biofilms Appl. Environ. Microbiol. 63 1997 3724 3728
25. A.M. Jones, M.E. Dodd, J. Morris, C. Doherty, J.R. Govan, and A.K. Webb Clinical outcome for cystic fibrosis patients infected with transmissible pseudomonas aeruginosa: an 8 years prospective study Chest 137 2010 1405 1409
26. T.J. Kamerzell, and C.R. Middaugh The complex inter-relationships between protein flexibility and stability J. Pharm. Sci. 97 2008 3494 3517
27. S. Kiran, P. Sharma, K. Harjai, and N. Capalash Enzymatic quorum quenching increases antibiotic susceptibility of multidrug resistant Pseudomonas aeruginosa Iran. J. Microbiol. 3 2011 1 12
28. H.P. Lai, P.R. Hsueh, Y.C. Chen, P.I. Lee, C.Y. Lu, M.Y. Lu, W.C. Lin, Y.C. Hsieh, C.Y. Lee, K.H. Lin, and L.M. Huang Bacteremia in hematological and oncological children with febrile neutropenia: experience in a tertiary medical center in Taiwan J. Microbiol. Immunol. Infect. 36 2003 197 202
29. Y.H. Liao, M.B. Brown, T. Nazir, A. Quader, and G.P. Martin Effects of sucrose and trehalose on the preservation of the native structure of spray-dried lysozyme Pharm. Res. 19 2002 1847 1853
30. M. Loiselle, and K.W. Anderson The use of cellulase in inhibiting biofilm formation from organisms commonly found on medical implants Biofouling 19 2003 77 85
31. M.L. Mayer, J.A. Sheridan, C.J. Blohmke, S.E. Turvey, and R.E. Hancock The Pseudomonas aeruginosa autoinducer 3O-C12 homoserine lactone provokes hyperinflammatory responses from cystic fibrosis airway epithelial cells PLoS ONE 6 2011 e16246
32. P. Nadal Jimenez, G. Koch, E. Papaioannou, M. Wahjudi, J. Krzeslak, T. Coenye, R.H. Cool, and W.J. Quax Role of PvdQ in Pseudomonas aeruginosa virulence under iron-limiting conditions Microbiology 156 2010 49 59
33. P. Nadal Jimenez, G. Koch, J.A. Thompson, K.B. Xavier, R.H. Cool, and W.J. Quax The multiple signaling systems regulating virulence in Pseudomonas aeruginosa Microbiol. Mol. Biol. Rev. 76 1 2012 46 65
34. E. Papaioannou, M. Wahjudi, P. Nadal-Jimenez, G. Koch, R. Setroikromo, and W.J. Quax Quorum-quenching acylase reduces the virulence of Pseudomonas aeruginosa in a caenorhabditis elegans infection model Antimicrob. Agents Chemother. 53 2009 4891 4897
35. T.W. Randolph Phase separation of excipients during lyophilization: effects on protein stability J. Pharm. Sci. 86 1997 1198 1203
36. T.B. Rasmussen, M.E. Skindersoe, T. Bjarnsholt, R.K. Phipps, K.B. Christensen, P.O. Jensen, J.B. Andersen, B. Koch, T.O. Larsen, M. Hentzer, L. Eberl, N. Hoiby, and M. Givskov Identity and effects of quorum-sensing inhibitors produced by Penicillium species Microbiology 151 2005 1325 1340
37. J.D. Shrout, D.L. Chopp, C.L. Just, M. Hentzer, M. Givskov, and M.R. Parsek The impact of quorum sensing and swarming motility on Pseudomonas aeruginosa biofilm formation is nutritionally conditional Mol. Microbiol. 62 2006 1264 1277
38. P.K. Singh, A.L. Schaefer, M.R. Parsek, T.O. Moninger, M.J. Welsh, and E.P. Greenberg Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms Nature 407 2000 762 764
39. C.F. Sio, and W.J. Quax Improved b-lactam acylases and their use as industrial biocatalysts Curr. Opin. Biotechnol. 15 2004 349 355
40. C.F. Sio, A.M. Riemens, J.M. van der Laan, R. Verhaert, and W.J. Quax Directed evolution of a glutaryl acylase into an adipyl acylase Eur. J. Biochem. 269 2002 4495
41. C.F. Sio, L.G. Otten, R.H. Cool, S.P. Diggle, P.G. Braun, R. Bos, M. Daykin, M. Camara, P. Williams, and W.J. Quax Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1 Infect. Immun. 74 2006 1673 1682
42. P.S. Stewart, and J.W. Costerton Antibiotic resistance of bacteria in biofilms Lancet 358 2001 135 138
43. C. Van Delden, and B.H. Iglewski Cell-to-cell signaling and Pseudomonas aeruginosa infections Emerg. Infect. Dis. 4 1998 551 560
44. M. Wahjudi, E. Papaioannou, O. Hendrawati, A.H. van Assen, R. van Merkerk, R.H. Cool, G.J. Poelarends, and W.J. Quax PA0305 of Pseudomonas aeruginosa is a quorum quenching acylhomoserine lactone acylase belonging to the Ntn hydrolase superfamily Microbiology 157 2011 2042 2055
45. K.R. Ward, G.D. Adams, H.O. Alpar, and W.J. Irwin Protection of the enzyme l-asparaginase during lyophilisation-a molecular modelling approach to predict required level of lyoprotectant Int. J. Pharm. 187 1999 153 162
46. E.M. Westerman, H.G. Heijerman, and H.W. Frijlink Dry powder inhalation versus wet nebulisation delivery of antibiotics in cystic fibrosis patients Expert Opin. Drug Deliv. 4 2007 91 94
47. P. Williams, and M. Camara Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules Curr. Opin. Microbiol. 12 2009 182 191
48. M.K. Winson, S. Swift, L. Fish, J.P. Throup, F. Jorgensen, S.R. Chhabra, B.W. Bycroft, P. Williams, and G.S. Stewart Construction and analysis of luxCDABE-based plasmid sensors for investigating N-acyl homoserine lactone-mediated quorum sensing FEMS Microbiol. Lett. 163 1998 185 192
49. H. Zhu, T.C. Conibear, S.J. Thuruthyil, and M.D. Willcox Pseudomonas aeruginosa quorum-sensing signal molecules induce IL-8 production by human corneal epithelial cells Eye Contact Lens 34 2008 179 181
50. G.S. Zijlstra, M. Rijkeboer, D. Jan van Drooge, M. Sutter, W. Jiskoot, M. van de Weert, W.L. Hinrichs, and H.W. Frijlink Characterization of a cyclosporine solid dispersion for inhalation AAPS J. 9 2007 E190 9