Structural and thermodynamic characterization of doxycycline/β-cyclodextrin supramolecular complex and its bacterial membrane interactions

Colloids and Surfaces B: Biointerfaces

Volumn 118, Issue , 2014, Pages 194-201

  Suárez, Diego F ^a   Consuegra, Jessika ^a   Trajano, Vivianne C ^a   Gontijo, Sávio M L ^a   Guimarães, Pedro P G ^a   Cortés, Maria E ^a   Denadai, Ângelo L ^b   Sinisterra, Rubén D ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b FEDERAL UNIVERSITY OF JUIZ DE FORA   (Brazil)

Author keywords

Antimicrobial; Cytotoxicity; Doxycycline; Membrane interactions; Susceptibility; Cyclodextrin

Indexed keywords

BACTERIA; CELL MEMBRANES; CELL PROLIFERATION; CYTOLOGY; CYTOTOXICITY; ENZYME INHIBITION; EQUILIBRIUM CONSTANTS; HYDROGEN BONDS; MAGNETIC SUSCEPTIBILITY;

ANTIMICROBIAL; DOXYCYCLINE; HYDROGEN BONDING INTERACTIONS; MATRIX METALLOPROTEINASES; MEMBRANE INTERACTIONS; OSTEOBLAST PROLIFERATION; SUPRAMOLECULAR COMPLEXES; THERMODYNAMIC CHARACTERIZATION;

CYCLODEXTRINS;

BETA CYCLODEXTRIN; DOXYCYCLINE; BETA CYCLODEXTRIN DERIVATIVE;

ANIMAL CELL; ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL CELL; BACTERIAL MEMBRANE; BACTERIUM ADHERENCE; CELL PROLIFERATION; CELL SIZE; COMPLEX FORMATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; DRUG CYTOTOXICITY; DRUG EFFECT; DRUG POTENTIATION; DRUG STRUCTURE; ENTHALPY; ENTROPY; EQUILIBRIUM CONSTANT; HYDROGEN BOND; INFRARED SPECTROSCOPY; ION PAIR EXTRACTION; MINIMAL BACTERIAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; NEWBORN; NONHUMAN; OSTEOBLAST; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; SERODIAGNOSIS; SOLID STATE; STAPHYLOCOCCUS AUREUS; THERMODYNAMICS; THERMOGRAVIMETRY; ZETA POTENTIAL; ANIMAL; CALORIMETRY; CELL DEATH; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; HYDRODYNAMICS; LIGHT; METABOLISM; MICROBIAL SENSITIVITY TEST; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; RADIATION SCATTERING; STATIC ELECTRICITY; WISTAR RAT;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

ANIMALS; BETA-CYCLODEXTRINS; CALORIMETRY; CELL DEATH; CELL MEMBRANE; CELL PROLIFERATION; DIFFERENTIAL THERMAL ANALYSIS; DOXYCYCLINE; HYDRODYNAMICS; LIGHT; MAGNETIC RESONANCE SPECTROSCOPY; MICROBIAL SENSITIVITY TESTS; OSTEOBLASTS; PROTON MAGNETIC RESONANCE SPECTROSCOPY; RATS, WISTAR; SCATTERING, RADIATION; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; STAPHYLOCOCCUS AUREUS; STATIC ELECTRICITY; THERMODYNAMICS; THERMOGRAVIMETRY;

EID: 84900835901     PISSN: 09277765     EISSN: 18734367     Source Type: Journal    
DOI: 10.1016/j.colsurfb.2014.01.028     Document Type: Article

References (51)

1. Josefsson E., Tarkowski A. Staphylococcus aureus-muoed inflammation and bone destruction in experimental models of septic arthritis. J. Periodontal. Res. 1999, 34:387-392.
2. Xu Y., Rivas J.M., Brown E.L., Hang X., Hook M. Virulence potential of the Staphylococcal adhesin CNA in experimental arthritis is determined by its affinity for collagen. J. Infect. Dis. 2004, 189:2323-2333.
3. Elkington P.T., O'Kane C.M., Friedland J.S. The paradox of matrix metalloproteinases in infectious disease. Clin. Exp. Immunol. 2005, 142:12-20.
4. Burrage P.S., Mix K.S., Brinckerhoff C.E. Matrix metalloproteinases: role in arthritis. Front. Biosci. 2006, 11:529-543.
5. Seymour R.A., Heasman P.A. Tetracyclines in the management of periodontal-diseases. A review. J. Clin. Periodontol. 1995, 22:22-35.
6. Gueders M.M., Bertholet P., Perin F., Rocks N., Maree R., Botta V., Louis R., Foidart J.M., Noel A., Evrard B., Cataldo D.D. A novel formulation of inhaled doxycycline reduces allergen-induced inflammation, hyperresponsiveness and remodeling by matrix metalloproteinases and cytokines modulation in a mouse model of asthma. Biochem. Pharmacol. 2008, 75:514-526.
7. Griffin M.O., Fricovsky E., Ceballos G., Villarreal F. Tetracyclines: a pleitropic family of compounds with promising therapeutic properties. Review of the literature. Am. J. Physiol.-Cell Physiol. 2010, 299:C539-C548.
8. Gomes P.S., Fernandes M.H. Effect of therapeutic levels of doxycycline and minocycline in the proliferation and differentiation of human bone marrow osteoblastic cells. Arch. Oral Biol. 2007, 52:251-259.
9. Chopra I., Roberts M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol. Biol. Rev. 2001, 65:232-260. second page, table of contents.
10. Ito T., Okuma K., Ma X.X., Yuzawa H., Hiramatsu K. Insights on antibiotic resistance of Staphylococcus aureus from its whole genome: genomic island SCC. Drug Resist. Updat. 2003, 6:41-52.
11. Brandenburg K., Arraiza M.D., Lehwark-Ivetot G., Moriyon I., Zahringer U. The interaction of rough and smooth form lipopolysaccharides with polymyxins as studied by titration calorimetry. Thermochim. Acta 2002, 394:53-61.
12. Jelesarov I., Bosshard H.R. Isothermal titration calorimetry and differential scanning calorimetry as complementary tools to investigate the energetics of biomolecular recognition. J. Mol. Recognit. 1999, 12:3-18.
13. Bouchemal K., Mazzaferro S. How to conduct and interpret ITC experiments accurately for cyclodextrin-guest interactions. Drug Discov. Today 2012, 17:623-629.
14. Loftsson T., Masson M., Brewster M.E. Self-association of cyclodextrins and cyclodextrin complexes. J. Pharm. Sci. 2004, 93:1091-1099.
15. Davis M.E., Brewster M.E. Cyclodextrin-based pharmaceutics: past, present and future. Nat. Rev. Drug Discov. 2004, 3:1023-1035.
16. Vyas A., Saraf S., Saraf S. Cyclodextrin based novel drug delivery systems. J. Incl. Phenom. Macro. Chemistry 2008, 62:23-42.
17. Vargas-Estrada D., Gracia-Mora J., Sumano H. Pharmacokinetic study of an injectable long-acting parenteral formulation of doxycycline hyclate in calves. Res. Vet. Sci. 2008, 84:477-482.
18. He Z.-x., Wang Z.-h., Zhang H.-h., Pan X., Su W.-r., Liang D., Wu C.-b. Doxycycline and hydroxypropyl-β-cyclodextrin complex in poloxamer thermal sensitive hydrogel for ophthalmic delivery. Acta Pharma. Sin. B 2011, 1:254-260.
19. Werner M.H. Advance User's Guide, Brucker. <940712> 1994, Spectrospin AG, Fallanden.
20. Rahman A. One and Two Dimensional NMR Spectroscopy 1989, Elsevier, New York.
21. Guerra W., Silva I.R., Azevedo E.A., Monteiro A., Bucciarelli-Rodriguez M., Chartone-Souza E., Silveira J.N., Fontes A.P.S., Pereira-Maia E.C. Three new complexes of platinum(II) with doxycycline, oxytetracycline and chlortetracycline and their antimicrobial activity. J. Braz. Chem. Soc. 2006, 17:1627-1633.
22. Schneider H.J., Hacket F., Rudiger V., Ikeda H. NMR studies of cyclodextrins and cyclodextrin complexes. Chem. Rev. 1998, 98:1755-1785.
23. Monteiro A.S., Miranda T.T., Lula I., Denadai A.M.L., Sinisterra R.D., Santoro M.M., Santos V.L. Inhibition of Candida albicans CC biofilms formation in polystyrene plate surfaces by biosurfactant produced by Trichosporon montevideense CLOA72. Colloids Surf. B- Biointerfaces 2011, 84:467-476.
24. CLSI Performance Standards for Antimicrobial Susceptibility Testing; Twenty-First Informational Supplement. CLSI document M100-S21. 2011, Clinical and Laboratory Standards Institute, Wayne, PA.
25. Z.N.S.U. Manual 2004, Malvern Instruments, Worcestershire, United Kingdom.
26. Jensen C.E., dos Santos R.A., Denadai A.M., Santos C.F., Braga A.N., Sinisterra R.D. Pharmaceutical composition of valsartan: beta-cyclodextrin: physico-chemical characterization and anti-hypertensive evaluation. Molecules 2010, 15:4067-4084.
27. de Alvarenga E.S., Lima C.F., Denadai A.M.L. Study of aqueous solution of sodiumdodecylsulfate and polyethyleneoxide 10000 by NMR NOESY. Z. Naturforsch A 2004, 59:291-294.
28. Denadai A.M.L., Santoro M.M., Texeira A.V., Sinisterra R.D. New insights regarding the cyclodextrin/AAS self-assembly: a molar ratio dependent system. Mater. Sci. Eng. C: Mater. Biol. Appl. 2010, 30:417-422.
29. Lula I., De Sousa F.B., Denadai A.M.L., de Lima G.F., Duarte H.A., dos Mares Guia T.R., Faljoni-Alario A., Santoro M.M., de Camargo A.C.M., dos Santos R.A.S., Sinisterra R.D. Interaction between bradykinin potentiating nonapeptide (BPP9a) and beta-cyclodextrin: a structural and thermodynamic study. Mater. Sci. Eng. C: Mater. Biol. Appl. 2012, 32:244-253.
30. Bakkour Y., Vermeersch G., Morcellet M., Boschin F., Martel B., Azaroual N. Formation of cyclodextrin inclusion complexes with doxycyclin-hyclate: NMR investigation of their characterisation and stability. J. Incl. Phenom. Macro Chemistry 2006, 54:109-114.
31. Denadai A.M., Ianzer D., Alcantara A.F., Santoro M.M., Santos C.F., Lula I.S., de Camargo A.C., Faljoni-Alario A., dos Santos R.A., Sinisterra R.D. Novel pharmaceutical composition of bradykinin potentiating penta peptide with beta-cyclodextrin: physical-chemical characterization and anti-hypertensive evaluation. Int. J. Pharm. 2007, 336:90-98.
32. de Paula W.X., Denadai A.M., Santoro M.M., Braga A.N., Santos R.A., Sinisterra R.D. Supramolecular interactions between losartan and hydroxypropyl-beta-CD: ESI mass-spectrometry, NMR techniques, phase solubility, isothermal titration calorimetry and anti-hypertensive studies. Int. J. Pharm. 2011, 404:116-123.
33. deSousa F.B., Denadai Â.M.L., Lula I.S.e., Nascimento C.S., Neto N.S.G.F., Lima A.C., Almeida W.B.d., Sinisterra R.D. Supramolecular self-assembly of cyclodextrin and higher water soluble guest: thermodynamics and topological studies. J. Am. Chem. Soc. 2008, 130:8426-8436.
34. Turnbull W.B., Daranas A.H. On the value of c: can low affinity systems be studied by isothermal titration calorimetry?. J. Am. Chem. Soc. 2003, 125:14859-14866.
35. Denadai A.M., Santoro M.M., Lopes M.T., Chenna A., de Sousa F.B., Avelar G.M., Gomes M.R., Guzman F., Salas C.E., Sinisterra R.D. A supramolecular complex between proteinases and beta-cyclodextrin that preserves enzymatic activity: physicochemical characterization. BioDrugs 2006, 20:283-291.
36. Rekharsky M.V., Inoue Y. Complexation thermodynamics of cyclodextrins. Chem. Rev. 1998, 98:1875-1917.
37. Rybak M.J., Leonard S.N., Rossi K.L., Cheung C.M., Sader H.S., Jones R.N. Characterization of vancomycin-heteroresistant Staphylococcus aureus from the metropolitan area of Detroit, Michigan, over a 22-year period (1986 to 2007) (vol. 46, p. 2950, 2008). J. Clin. Microbiol. 2008, 46:4119.
38. Davies J., Davies D. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev. 2010, 74:417-433.
39. Colaizzi J.L., Klink P.R. pH-partition behavior of tetracyclines. J. Pharm. Sci. 1969, 58:1184-1189.
40. Blackwood R.K., English A.R., Perlman D. Structure-activity relationships in the tetracycline series. Advances in Applied Microbiology 1970, vol. 13:237-266. Academic Press.
41. Coleman A.W., Nicolis I., Keller N., Dalbiez J.P. Aggregation of cyclodextrins-an explanation of the abnormal solubility of beta-cyclodextrin. J. Inclus. Phenom. Mol. 1992, 13:139-143.
42. Messner M., Kurkov S.V., Flavia-Piera R., Brewster M.E., Loftsson T. Self-assembly of cyclodextrins: the effect of the guest molecule. Int. J. Pharm. 2011, 408:235-247.
43. Denadai A.M., Teixeira K.I., Santoro M.M., Pimenta A.M., Cortes M.E., Sinisterra R.D. Supramolecular self-assembly of beta-cyclodextrin: an effective carrier of the antimicrobial agent chlorhexidine. Carbohydr. Res. 2007, 342:2286-2296.
44. Elimelech M., Chen W.H., Waypa J.J. Measuring the zeta (electrokinetic) potential of reverse-osmosis membranes by a streaming potential analyzer. Desalination 1994, 95:269-286.
45. Ouhara K., Komatsuzawa H., Kawai T., Nishi H., Fujiwara T., Fujiue Y., Kuwabara M., Sayama K., Hashimoto K., Sugai M. Increased resistance to cationic antimicrobial peptide LL-37 in methicillin-resistant strains of Staphylococcus aureus. J. Antimicrob. Chemother. 2008, 61:1266-1269.
46. Strominger J.L., Park J.T., Thompson R.E. Composition of the cell wall of Staphylococcus aureus-its relation to the mechanism of action of penicillin. J. Biol. Chem. 1959, 234:3263-3268.
47. Cummins C.S., Harris H. The chemical composition of the cell wall in some gram-positive bacteria and its possible value as a taxonomic character. J. Gen. Microbiol. 1956, 14:583-600.
48. Navarre W.W., Schneewind O. Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol. Mol. Biol. Rev. 1999, 63:174-229.
49. Wilson W.W., Wade M.M., Holman S.C., Champlin F.R. Status of methods for assessing bacterial cell surface charge properties based on zeta potential measurements. J. Microbiol. Methods 2001, 43:153-164.
50. Teixeira K.I., Araujo P.V., Almeida B.R.N., Bohorquez G.A.M., Sinisterra R.D., Cortes M.E. Ultrastructural changes in bacterial membranes induced by nano-assemblies beta-cyclodextrin chlorhexidine: SEM, AFM, and TEM evaluation. Pharm. Dev. Technol. 2012, 20:20.
51. Sorsa T., Golub L.M. Is the excessive inhibition of matrix metalloproteinases (MMPs) by potent synthetic MMP inhibitors (MMPIs) desirable in periodontitis and other inflammatory diseases? That is: 'Leaky' MMPIs vs excessively efficient drugs. Oral Dis. 2005, 11:408-409.