Genistein in 1:1 inclusion complexes with ramified cyclodextrins: Theoretical, physicochemical and biological evaluation

International Journal of Molecular Sciences

Volumn 15, Issue 2, 2014, Pages 1962-1982

  Danciu, Corina ^a   Soica, Codruta ^a   Oltean, Mircea ^b   Avram, Stefana ^a   Borcan, Florin ^a   Csanyi, Erzsebet ^c   Ambrus, Rita ^c   Zupko, Istvan ^c   Muntean, Delia ^a   Dehelean, Cristina A ^a   Craina, Marius ^a   Popovici, Ramona A ^a  

^a VICTOR BABES UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

^b BABE BOLYAI UNIVERSITY   (Romania)

^c UNIVERSITY OF SZEGED   (Hungary)

Author keywords

Antiangiogenic; Antibacterial; Antiproliferative; Cyclodextrin; Genistein; SEM; Thermal analysis; X ray diffraction

Indexed keywords

CYCLODEXTRIN; GENISTEIN; ANTIINFECTIVE AGENT; ANTINEOPLASTIC AGENT;

ANGIOGENESIS; ANTIMICROBIAL ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BACTERIAL STRAIN; BIOAVAILABILITY; CHORIOALLANTOIS; COMPLEX FORMATION; CONTROLLED STUDY; DIFFERENTIAL SCANNING CALORIMETRY; DISK DIFFUSION; HUMAN; HUMAN CELL; MINIMUM INHIBITORY CONCENTRATION; MORPHOMETRICS; NONHUMAN; SCANNING ELECTRON MICROSCOPY; SCREENING; SOLUBILITY; STEREOMICROSCOPY; SURVIVAL; X RAY DIFFRACTION; CALORIMETRY; CELL PROLIFERATION; CHEMICAL STRUCTURE; CHEMISTRY; CONFORMATION; DOSE RESPONSE; DRUG EFFECTS; DRUG STABILITY; IC50; MICROBIAL SENSITIVITY TEST; TUMOR CELL LINE;

ANTI-BACTERIAL AGENTS; ANTINEOPLASTIC AGENTS; CALORIMETRY; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLODEXTRINS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG STABILITY; GENISTEIN; HUMANS; INHIBITORY CONCENTRATION 50; MICROBIAL SENSITIVITY TESTS; MODELS, MOLECULAR; MOLECULAR CONFORMATION; X-RAY DIFFRACTION;

EID: 84893067157     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15021962     Document Type: Article

References (64)

1. Rahman, S.; Islam, R.; Swaraz, A.; Ansari, A.; Parvez, A.K.; Paul, D.K. An insight on genistein as potential pharmacological and therapeutic agent. Asian Pac. J. Trop. Biomed. 2012, 2, S1924-S1937.
2. Taylor, C.K.; Levy, R.M.; Elliott, J.C.; Burnett, B.P. The effect of genistein aglycone on cancer and cancer risk: A review of in vitro, preclinical, and clinical studies. Nutr. Rev. 2009, 67, 398-415.
3. Polkowski, K.; Mazurek, P.A. Biological properties of genistein. A review of in vitro and in vivo data. Acta Pol. Pharm. 2000, 57, 135-155.
4. Pavese, J.M.; Farmer, R.L.; Bergan, R.C. Inhibition of cancer cell invasion and metastasis by genistein. Cancer Metastasis Rev. 2010, 29, 465-482.
5. Danciu, C.; Soica, C.; Csanyi, E.; Ambrus, R.; Feflea, S.; Peev, C.; Dehelean, C. Changes in the anti-inflammatory activity of soy isoflavonoid genistein versus genistein incorporated in two types of cyclodextrin derivatives. Chem. Cent. J. 2012, 6, 58.
6. Hoffmann, D. Medical herbalism: The Science and Practice of Herbal Medicine; Inner Traditions, Bear & Co.: Rochester, VT, USA, 2003.
7. Barrett, J.R. The science of soy: What do we really know? Environ. Health Perspect. 2006, 114, A352-A358.
8. Qin, W.; Zhu, W.; Shi, H.; Hewett, J.E.; Ruhlen, R.L.; MacDonald, R.S.; Rottinghaus, G.E.; Chen, Y.C.; Sauter, E.R. Soy isoflavones have an antiestrogenic effect and alter mammary promoter hypermethylation in healthy premenopausal women. Nutr. Cancer 2009, 61, 238-244.
9. Gercel-Taylor, C.; Feitelson, A.K.; Taylor, D.D. Inhibitory effect of genistein and daidzein on ovarian cancer cell growth. Anticancer Res. 2004, 24, 795-800.
10. Kronenberg, F. Menopausal hot flashes: A review of physiology and biosociocultural perspective on methods of assessment. J. Nutr. 2010, 140, 1380S-1385S.
11. Evans, M.; Elliott, J.G.; Sharma, P.; Berman, R.; Guthrie, N. The effect of synthetic genistein on menopause symptom management in healthy postmenopausal women: A multi-center, randomized, placebo-controlled study. Maturitas 2011, 68, 189-196.
12. Altavilla, D.; Crisafulli, A.; Marini, H.; Esposito, M.; D'Anna, R.; Corrado, F.; Bitto, A.; Squadrito, F. Cardiovascular effects of the phytoestrogen genistein. Curr. Med. Chem. Cardiovasc. Hematol. Agents 2004, 2, 179-186.
13. Wei, H.; Saladi, R.; Lu, Y.; Wang, Y.; Palep, S.R.; Moore, J.; Phelps, R.; Shyong, E.; Lebwohl, M.G. Isoflavone genistein: Photoprotection and clinical implications in dermatology. J. Nutr. 2003, 133, 3811S-3819S.
14. Foti, P.; Erba, D.; Riso, P.; Spadafranca, A.; Criscuoli, F.; Testolin, G. Comparison between daidzein and genistein antioxidant activity in primary and cancer lymphocytes. Arch. Biochem. Biophys. 2005, 433, 421-427.
15. Gao, F.; Wei, D.; Bian, T.; Xie, P.; Zou, J.; Mu, H.; Zhang, B.; Zhou, X. Genistein attenuated allergic airway inflammation by modulating the transcription factors T-bet, GATA-3 and STAT-6 in a murine model of asthma. Pharmacology 2012, 89, 229-236.
16. Ruijter, J.; Valstar, M.J.; Narajczyk, M.; Wegrzyn, G.; Kulik, W.; Ijist, L.; Wagemans, T.; van der Wal, W.M.; Wijburg, F.A. Genistein in Sanfilippo disease: A randomized controlled crossover trial. Ann. Neurol. 2012, 71, 110-120.
17. Uckun, F.M.; Evans, W.E.; Forsyth, C.J.; Waddick, K.G.; Ahlgren, L.T.; Chelstrom, L.M.; Burkhardt, A.; Bolen, J.; Myers, D.E. Biotherapy of B-cell precursor leukemia by targeting genistein to CD19-associated tyrosine kinases. Science 1995, 267, 886-891.
18. Rusin, A.; Krawczyk, Z.; Grynkiewicz, G.; Gogler, A.; Zawisza-Puchałka, J.; Szeja, W. Synthetic derivatives of genistein, their properties and possible applications. Acta Biochim. Pol. 2010, 57, 23-34.
19. Del Valle, E.M.M. Cyclodextrins and their uses: A review. Process Biochem. 2004, 39, 1033-1046.
20. Faustino, C.M.C.; Calado, A.R.T.; Garcia-Rio, L. Interactions between β-cyclodextrin and an amino acid-based anionic gemini surfactant derived from cysteine. J. Colloid Interface Sci. 2012, 367, 286-292.
21. Loftsson, T.; Duchêne, D. Cyclodextrins and their pharmaceutical applications. Int. J. Pharm. 2007, 329, 1-11.
22. Szejtli, J. Medicinal applications of cyclodextrins. Med. Res. Rev. 1994, 14, 353-386.
23. Daruházi, A.E.; Szente, L.; Balogh, B.; Mátyus, P.; Béni, S.; Takács, M.; Gergely, A.; Horváth, P.; Szoke, E.; Lemberkovics, E. Utility of cyclodextrins in the formulation of genistein part 1. Preparation and physicochemical properties of genistein complexes with native cyclodextrins. J. Pharm. Biomed. Anal. 2008, 48, 636-640.
24. Lee, S.-H.; Kim, Y.H.; Yu, H.-J.; Cho, N.-S.; Kim, T.-H.; Kim, D.C.; Chung, C.B.; Hwang, Y.I.; Kim, K.H. Enhanced bioavailability of soy isoflavones by complexation with beta-cyclodextrin in rats. Biosci. Biotechnol. Biochem. 2007, 71, 2927-2933.
25. Boys, S.F.; Bernardi, F. Calculation of small molecular interactions by differences of separate total energies-Some procedures with reduced errors. Mol. Phys. 1970, 19, 553-566.
26. Dua, K.; Pabreja, K.; Ramana, M.V.; Lather, V. Dissolution behavior of β-cyclodextrin molecular inclusion complexes of aceclofenac. J. Pharm. Bioallied Sci. 2011, 3, 417-425.
27. Ficarra, R.; Ficarra, P.; di Bella, M.R.; Raneri, D.; Tommasini, S.; Calabrò, M.L.; Gamberini, M.C.; Rustichelli, C. Study of beta-blockers/beta-cyclodextrins inclusion complex by NMR, DSC, X-ray and SEM investigation. J. Pharm. Biomed. Anal. 2000, 23, 33-40.
28. Pralhad, T.; Rajendrakumar, K. Study of freeze-dried quercetin-cyclodextrin binary systems by DSC, FT-IR, X-ray diffraction and SEM analysis. J. Pharm. Biomed. Anal. 2004, 34, 333-339.
29. Liu, Y.; Chen, G.-S.; Li, L.; Zhang, H.-Y.; Cao, D.-X.; Yuan, Y.-J. Inclusion complexation and solubilization of paclitaxel by bridged bis(β-cyclodextrin)s containing a tetraethylenepentaamino spacer. J. Med. Chem. 2003, 46, 4634-4637.
30. Shim, H.-Y.; Park, J.-H.; Paik, H.-D.; Nah, S.-Y.; Kim, D.S.; Han, Y.S. Genistein-induced apoptosis of human breast cancer MCF-7 cells involves calpain-caspase and apoptosis signaling kinase 1-p38 mitogen-activated protein kinase activation cascades. Anticancer Drugs 2007, 18, 649-657.
31. Singletary, K.W.; Frey, R.S.; Li, J.Y. Differential effects of genistein on cell proliferation, cyclin B1, and p34cdc2 in transformed and nontransformed human breast cells. Pharm. Biol. 2002, 40, 35-42.
32. Solomon, L.A.; Ali, S.; Banerjee, S.; Munkarah, A.R.; Morris, R.T.; Sarkar, F.H. Sensitization of ovarian cancer cells to cisplatin by genistein: The role of NF-kappaB. J. Ovarian Res. 2008, 1, 9.
33. Gossner, G.; Choi, M.; Tan, L.; Fogoros, S.; Griffith, K.A.; Kuenker, M.; Liu, J.R. Genistein-induced apoptosis and autophagocytosis in ovarian cancer cells. Gynecol. Oncol. 2007, 105, 23-30.
34. Zhang, B.; Liu, J.Y.; Pan, J.S.; Han, S.P.; Yin, X.X.; Wang, B.; Hu, G. Combined treatment of ionizing radiation with genistein on cervical cancer HeLa cells. J. Pharmacol. Sci. 2006, 102, 129-135.
35. Sahin, K.; Tuzcu, M.; Basak, N.; Caglayan, B.; Kilic, U.; Sahin, F.; Kucuk, O. Sensitization of cervical cancer cells to cisplatin by genistein: The role of nfb and akt/mtor signaling pathways. J. Oncol. 2012, 2012, doi:10.1155/2012/461562.
36. Hipler, U.C.; Schönfelder, U.; Hipler, C.; Elsner, P. Influence of cyclodextrins on the proliferation of HaCaT keratinocytes in vitro. J. Biomed. Mat. Res. Part A 2007, 83, 70-79.
37. Yadav, V.R.; Prasad, S.; Kannappan, R.; Ravindran, J.; Chaturvedi, M.M.; Vaahtera, L.; Parkkinen, J.; Aggarwal, B.B. Cyclodextrin-complexed curcumin exhibits anti-inflammatory and antiproliferative activities superior to those of curcumin through higher cellular uptake. Biochem. Pharmacol. 2010, 80, 1021-1032.
38. Mendonça, E.A.M.; Lira, M.C.B.; Rabello, M.M.; Cavalcanti, I.M.F.; Galdino, S.L.; Pitta, I.R.; Lima Mdo, C.; Pitta, M.G.; Hernandes, M.Z.; Santos-Magalhães, N.S. Enhanced antiproliferative activity of the new anticancer candidate LPSF/AC04 in cyclodextrin inclusion complexes encapsulated into liposomes. AAPS 2012, 13, 1355-1366.
39. Pourgholami, M.H.; Wangoo, K.T.; Morris, D.L. Albendazole-cyclodextrin complex: Enhanced cytotoxicity in ovarian cancer cells. Anticancer Res. 2008, 28, 2775-2779.
40. Li, W.; Chen, L.; Huang, Z.; Wu, X.; Zhang, Y.; Hu, Q.; Wang, Y. The influence of cyclodextrin modification on cellular uptake and transfection efficiency of polyplexes. Org. Biomol. Chem. 2011, 9, 7799-7806.
41. Dhule, S.S.; Penfornis, P.; Frazier, T.; Walker, R.; Feldman, J.; Tan, G.; He, J.; Alb, A.; John, V.; Pochampally, R. Curcumin-loaded γ-cyclodextrin liposomal nanoparticles as delivery vehicles for osteosarcoma. Nanomedicine 2012, 8, 440-451.
42. Arun, R.; Ashok Kumar, C.K.; Sravanthi, V.V.N.S.S. Cyclodextrins as drug carrier molecule: A review. Sci. Pharm. 2008, 76, 567-598.
43. Weber, P.; Wagner, M.; Schneckenburger, H. Cholesterol dependent uptake and interaction of doxorubicin in MCF-7 breast cancer cells. Int. J. Mol. Sci. 2013, 14, 8358-8366.
44. Ulanowska, K.; Majchrzyk, A.; Moskot, M.; Jakóbkiewicz-Banecka, J.; We{ogonek}grzyn, G. Assessment of antibacterial effects of flavonoids by estimation of generation times in liquid bacterial cultures. Biologia 2007, 62, 132-135.
45. Hong, H.; Landauer, M.R.; Foriska, M.A.; Ledney, G.D. Antibacterial activity of the soy isoflavone genistein. J. Basic Microbiol. 2006, 46, 329-335.
46. Zaki, M.; Zaid, A.; Magd, M.; AbouZid, S. Antibacterial effects of isoflavones isolated from Cicer arietinum. Int. J. Nat. Prod. Res. 2013, 2, 1-5.
47. Verdrengh, M.; Collins, L.V.; Bergin, P.; Tarkowski, A. Phytoestrogen genistein as an anti-staphylococcal agent. Microbes Infect. 2004, 6, 86-92.
48. Sun, H-K.; Seshadri, M.; Lingard, S.; Monaghan, W.; Faoagali, J.; Chan, E.; McDonald, H.; Houston, T.; King, M.; Peak, I.; et al. Antibacterial activity of beta-cyclodextrin and 2-hydroxypropyl-beta-cyclodextrin trimethoprim complexes. Am. J. Microbiol. 2011, 2, 1-8.
49. Denadai, A.M.; Teixeira, K.I.; Santoro, M.M.; Pimenta, A.M.; Cortés, M.E.; Sinisterra, R.D. Supramolecular self-assembly of β-cyclodextrin: An effective carrier of the antimicrobial agent chlorhexidine. Carbohydr. Res. 2007, 342, 2286-2296.
50. Wang, J.; Cai, Z. Incorporation of the antibacterial agent, miconazole nitrate into a cellulosic fabric grafted with β-cyclodextrin. Carbohydr. Polym. 2008, 72, 695-700.
51. Farina, H.G.; Pomies, M.; Alonso, D.F.; Gomez, D.E. Antitumor and antiangiogenic activity of soy isoflavone genistein in mouse models of melanoma and breast cancer. Oncol. Rep. 2006, 16, 885-891.
52. Kiriakidis, S.; Högemeier, O.; Starcke, S.; Dombrowski, F.; Hahne, J.C.; Pepper, M.; Jha, H.C.; Wernert, N. Novel tempeh (fermented soyabean) isoflavones inhibit in vivo angiogenesis in the chicken chorioallantoic membrane assay. Br. J. Nutr. 2005, 93, 317-323.
53. Banerjee, S.; Li, Y.; Wang, Z.; Sarkar, F.H. Multi-targeted therapy of cancer by genistein. Cancer Lett. 2008, 269, 226-242.
54. Dehelean, C.A.; Soica, C.; Peev, C.; Ciurlea, S.; Feflea, S.; Kasa, P., Jr. A pharmaco-toxicological evaluation of betulinic acid mixed with hydroxipropilgamma cyclodextrin on in vitro and in vivo Models. Farmacia 2011, 59, 51-59.
55. Gaussian 09, Revision A.02; Frisch, M.J., Trucks, G.W., Schlegel, H.B., Scuseria, G.E., Robb, M.A., Cheeseman, J.R., Scalmani, G., Barone, V., Mennucci, B., Petersson, G.A., et al. Eds.; Gaussian Inc.: Wallingford, CT, USA, 2009.
56. Grimme, S. Semiempirical GGA-type density functional constructed with a long-range dispersion correction. J. Comput. Chem. 2006, 27, 1787-1799.
57. Cances, E.; Mennucci, B.; Tomasi, J. A new integral equation formalism for the polarizable continuum model: Theoretical background and applications to isotropic and anisotropic dielectrics. J. Chem. Phys. 1997, 107, 3032-3043.
58. Cossi, M.; Barone, V.; Mennucci, B.; Tomasi, J. Ab initio study of ionic solutions by a polarizable continuum dielectric model. Chem. Phys. Lett. 1998, 286, 253-260.
59. Cossi, M.; Scalmani, G.; Rega, N.; Barone, V. New developments in the polarizable continuum model for quantum mechanical and classical calculations on molecules in solution. J. Chem. Phys. 2002, 117, 43-54.
60. Phase-Solubility Techniques; Higuchi, T., Connors, A., Eds.; Wiley Interscience: New York, NY, USA, 1965; Volume 4, pp. 117-211.
61. Mosmann, T. Rapid colorimetric assay for cellular growth and survival: Application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65, 55-63.
62. Ribatti, D.; Vacca, A.; Roncali, L.; Dammacco, F. The chick embryo chorioallantoic membrane as a model for in vivo research on angiogenesis. Int. J. Dev. Biol. 1996, 40, 1189-1197.
63. Dehelean, C.A.; Feflea, S.; Gheorgheosu, D.; Ganta, S.; Cimpean, A.M.; Muntean, D.; Amiji, M.M. Anti-angiogenic and anti-cancer evaluation of betulin nanoemulsion in chicken chorioallantoic membrane and skin carcinoma in Balb/c mice. J. Biomed. Nanotechnol. 2013, 9, 577-589.
64. Ribatti, D. The Chick Embryo Chorioallantoic Membrane in the Study of Angiogenesis and Metastasis; Springer Science + Business Media B.V.: Dordrecht, The Netherlands, 2010.