Anti-angiogenic and anti-cancer evaluation of betulin nanoemulsion in chicken chorioallantoic membrane and skin carcinoma in Balb/c mice

Journal of Biomedical Nanotechnology

Volumn 9, Issue 4, 2013, Pages 577-589

  Dehelean, Cristina A ^a   Feflea, Stefana ^a   Gheorgheosu, Dorina ^a   Ganta, Srinivas ^b   Cimpean, Anca M ^a   Muntean, Danina ^a   Amiji, Mansoor M ^b  

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

^b NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Anti Angiogenic Effect; Betulin; Chorioallantoic Membrane; Mitochondrial Respiration; Nanoemulsion; Skin Cancer; VEGF Expression

Indexed keywords

ANTI-ANGIOGENIC EFFECT; BETULIN; CHORIO-ALLANTOIC MEMBRANES; MITOCHONDRIAL RESPIRATION; NANOEMULSION; SKIN CANCERS; VEGF EXPRESSION;

CAMS; CELL CULTURE; MAMMALS; MITOCHONDRIA; TUMORS;

SKIN;

7,12 DIMETHYLBENZ[A]ANTHRACENE; BETULIN; PHORBOL 13 ACETATE 12 MYRISTATE; VASCULOTROPIN;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTIANGIOGENIC ACTIVITY; ANTIINFLAMMATORY ACTIVITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CAPILLARY DENSITY; CHICKEN; CHORIOALLANTOIS; CONTROL; DRUG PENETRATION; EMBRYO; HISTOLOGY; IN VIVO STUDY; ISOLATED LIVER; MITOCHONDRION; MOUSE; NANOEMULSION; NONHUMAN; PROTEIN EXPRESSION; RESPIRATORY FUNCTION; SKIN CARCINOMA; STEREOMICROSCOPY; TREATMENT DURATION; YOLK SAC;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTICARCINOGENIC AGENTS; CELL RESPIRATION; CHICK EMBRYO; CHORIOALLANTOIC MEMBRANE; EMULSIONS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED BALB C; NANOPARTICLES; NEOVASCULARIZATION, PHYSIOLOGIC; OXYGEN CONSUMPTION; SKIN NEOPLASMS; TRITERPENES; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84876543679     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2013.1563     Document Type: Article

References (46)

1. S. Alakurtti, T. Makela, S. Koskimies, and J. Yli-Kauhaluoma, Pharmacological properties of the ubiquitous natural product betulin. Eur. J. Pharm. Sci. 29, 1 (2006).
2. C. A. Dehelean, C. M. Soica, C. C. Toma, S. Feflea, A. T. Gruia, and P. Kasa, Antitumoral activity of betulin, a compound present in birch tree, in formulations with cyclodextrin. Studia Univ. VG, SSV 20, 55 (2010).
3. C. A. Dehelean, S. Feflea, G. Srinivas, and A. Mansoor, Antiangiogenic effects of betulinic acid administered in nanoemulsion formulation using chorioallantoic membrane assay. J. Biomed. Nanotechnol. 7, 317 (2011).
4. M. N. Laszczyk, Pentacyclic triterpenes of the lupane, oleanane and ursane group as tools in cancer therapy. Planta Med. 75, 1549 (2009).
5. R. Muceniece, K. Saleniece, U. Riekstina, L. Krigere, Z. Dzirkale, R. Mezhapuke, O. Zharkova, and V. Klusa, Betulin binds to melanocortin receptors and antagonizes alpha-melanocyte stimulating hormone induced cAMP generation in mouse melanoma cells. Cell Biochem. Funct. 25, 591 (2007).
6. S. Fulda, Betulinic acid: A natural product with anticancer activity. Mol. Nutr. Food Res. 53, 140 (2009).
7. C. Dehelean, C. Soica, C. Peev, and E. Seclaman, Physico-chemical and molecular analysis of antitumoral pentacyclic triterpenes in complexation with gammacyclodextrin. Rev. Chim. 59, 887 (2008).
8. A. S. Saraf, Applications of novel drug delivery system for herbal formulations. Fitoterapia 81, 680 (2010).
9. S. Ganta, H. Devalapally, B. C. Baguley, S. Garg, and M. M. Amiji, Microfluidic preparation of chlorambucil nanoemulsion formulations and evaluation of cytotoxicity and pro-apoptotic activity in tumor cells. J. Biomed. Nanotechnol. 4, 165 (2008).
10. K. Y. Ham, M. Choe, and S. W. Kim, Effects of Vitamin A and E on the Protein Kinase C activity and antioxidative parameters during carcinogenesis induced by DMBA and TPA. Korean Biochem J. 23, 486 (1990).
11. H. C. Lee and Y. H. Wei, Mitochondrial DNA instability and metabolic shift in human cancers. Int. J. Mol. Sci. 10, 674 (2009).
12. A. M. Al-Attar, The influence of dietary grape seed oil on DMBAinduced liver enzymes disturbance in the frog Rana ridibunda. Pakistan Journal of Nutrition 3, 304 (2004).
13. C. Dehelean, A. Muresan, S. Ciurlea, D. Ionescu, C. Peev, C. Soica, and L. Redes, Toxicological evaluations for 7,12- dimethylbenzanthracen as tumor promoter in experimental model. Rev. Med. Chir. Soc. Med. Iasi. 113,99 (2009).
14. C. Dwivedi, E. R. Maydew, J. J. Hora, D. M. Ramaeker, and X. Guan, Chemopreventive effects of various concentrations of -santololon skin cancer development in CD1-mice. Eur. J. Cancer Prev. 14, 473 (2005).
15. D. Ribatti, B. Nico, A. Vacca, L. Roncali, P. H. Burri, and V. Djonov, Chorioallantoic membrane capillary bed: A useful target for studying angiogenesis and anti-angiogenesis in vivo. The Anat. Rec. 264, 317 (2001).
16. Y. Li, K. He, Y. Huang, D. Zheng, C. Gao, L. Cui, and Y. H. Jin, Betulin induces mitochondrial cytochrome c release associated apoptosis in human cancer cells. Culture 49, 630 (2010).
17. H. Kommera, G. N. Kaluderovíc, J. Kalbitz, and R. Paschke, Lupane Triterpenoids-Betulin and Betulinic acid derivatives induce apoptosis in tumor cells. Invest. New Drugs 29, 266 (2009).
18. M. Ristow and J. M. Cuezva, Oxidative phosphorylation and cancer: The ongoing Warburg hypothesis. Cellular Respiration and Carcinogenesis, edited by S. P. Apte, Humana Press, New York (2009), pp. 1-18.
19. K. M. Owens, J. S. Modica-Napolitano, and K. K. Singh, Mitochondria and Cancer edited by K. K. Singh and L. C. Costello, Springer, New York (2009), pp. 1-21.
20. O. Warburg, On the origin of cancer cells. Science 123, 309 (1956).
21. M. Ristow, T. J. Schultz, Warbug and his Legacy, in Mitochondria and Cancer, edited by K. K. Singh and L. C. Costello, Springer, New York (2009), pp. 23-38.
22. B. E. Baysal, Mitochondrial Tumor Suppressors, in Mithochondria and Cancer, edited by K. K. Singh and L. C. Costello, Springer, New York (2009), pp. 151-162.
23. A. Tangeras and A. N. Malviya, Oxygen uptake, ATPase activity, and superoxide dismutase activity in isolated rat liver mitochondria are not influenced by the tumor promoter 12-O-tetradecanoylphorbol- 13-acetate. Carcinogenesis 4, 509 (1983).
24. L. Formentini, I. Martinez-Reyes, and J. M. Cuezva, The mitochondrial bioenergetic capacity of carcinomas. IUBMB Life 62, 554 (2010).
25. J. A. Wittwer, D. Robbins, F. Wang, S. Codarin, X. Shen, C. G. Kevil, T. T. Huang, H. Van Remmen, A. Richardson, and Y. Zhao, Enhancing mitochondrial respiration suppresses tumor promoter TPA-induced PKM2 expression and cell transformation in skin epidermal JB6 cells. Cancer Prev. Res. (Phila) 4, 1476 (2011).
26. Y. Li, D. L. Wheeler, H. N. Ananthaswamy, A. K. Verma, and T. D. Oberley, Differential tumor biology effects of double-initiation in a mouse skin chemical carcinogenesis model comparing wild type versus protein kinase cepsilon overexpression mice. Toxicol. Pathol. 35, 942 (2007).
27. C. D. Woodworth, E. Michael, L. Smith, K. Vijayachandra, A. Glick, H. Hennings, and S. H. Yuspa, Strain-dependent differences in malignant conversion of mouse skin tumors is an inherent property of the epidermal keratinocyte. Carcinogenesis 25, 1771 (2004).
28. J. Monga, C. S. Chauhan, and M. Sharma, Human epithelial carcinoma cytotoxicity and inhibition of DMBA/TPA induced squamous cell carcinoma in Balb/c mice by Acacia catechu heartwood. J. Pharm. Pharmacol. 63, 1470 (2011).
29. R. Feng, W. He, Q. Liu, and H. Ochi, Age-related susceptibility of chemical carcinogenesis in Balb/c mice. J. Anti. Aging. Med. 5, 283 (2002).
30. A. M. Al-Attar, The influence of dietary grapeseed oil on DMBAinduced liver enzymes disturbance in the frog. Rana Ridibunda. Pakistan J. Nutr. 3, 304 (2004).
31. C. Rosado, P. Pinto, and L. M. Rodrigues, Comparative assesment of the performance of two generations of Tewameter: TM210 and TM300. Int. J. Cosmet. Sci. 27, 237 (2005).
32. C. Huyke, J. Reuter, M. Rodig, A. Kersten, M. Laszczyk, A. Scheffler, D. Nashan, and C. Schempp, Treatment of actinic keratoses with anovel betulin-based oleogel, a prospective, randomized, comparative pilot study. J. Dtsch. Dermatol. Ges. 7, 128 (2009).
33. T. Yamashita, T. Kuwahara, S. Gonzalez, and M. Takahashi, Noninvasive visualization of melanin and melanocytes by reflectancemode confocal microscopy. J. Invest. Dermatol. 124, 235 (2005).
34. K. S. Chun, J. K. Kundu, K. K. Park, W. Y. Chung, and Y. J. Surh, Inhibition of phorbol ester-induced mouse skin tumor promotion and COX-2 expression by celecoxib: C/EBP as a potential molecular target. Cancer Res. Treat. 38, 152 (2006).
35. C. J. Conti, Vascular endothelial growth factor: regulation in the mouse skin carcinogenesis model and use in antiangiogenesis cancer therapy. Oncologist 7, 4 (2002).
36. G. Zhao, W. Yan, and D. Cao, Simultaneous determination of betulin and betulinic acid in white birch bark using RP-HPLC. J. Pharm. Biomed. Anal. 43, 959 (2007).
37. D. Ribatti, The chick embryo chorioallantoic membrane in the study of tumor angiogenesis, A review. Rom. J. Morphol. Embryol. 49, 131 (2008).
38. D. Ribatti, Chapter 6. Different Morphological Techniques and Methods of Quantifying the Angiogenic Response Used in the Study of Vascularization in the Chorioallantoic Membrane in The Chick Embryo Chorioallantoic Membrane in the Study of Angiogenesis and Metastasis, edited by D. Ribatti, Springer, Dordrecht (2010), pp. 72-76.
39. S. A. Mousa, L. O'Connor, T. G. Rossman, and E. Block, Pro-angiogenesis action of arsenic and its reversal by seleniumderived compounds. Carcinogenesis 28, 962 (2007).
40. N. Weidner, J. Folkman, F. Pozza, P. Bevilacqua, E. N. Allred, D. H. Moore, S. Meli, and G. Gasparini, Tumor angiogenesis: A new significant and independent prognostic indicator in early-stage breast carcinoma. J. Natl. Cancer. Inst. 84, 1875 (1992).
41. S. Quagliata, S. Pacini, T. Punzi, C. Malentacchi, M. Ruggiero, and G. Delfino, Bombesin promotes vasculogenesis and angiogenesis in chick chorio-allantoic membrane: A morphometric, structural, and ultrastructural study. J. Morphol. 83, 72 (2008).
42. S.-T. Huang, J.-H. S. Pang, and R.-C. Yang, Anti-cancer effects of Phyllanthus urinaria and relevant mechanisms. Chang Gung Med. J. 33, 477 (2010).
43. R. Demir, G. Peros, and W. Hohenberger, Definition of the "Drug-Angiogenic-Activity-Index" that allows the quantification of the positive and negative angiogenic active drugs: A study based on the chorioallantoic membrane model. Pathol. Oncol. Res. 17, 309 (2011).
44. D. Dhawan, S. Balasubramanian, A. J. Amonkar, and N. Singh, Chemopreventive effect of 4-demethyl epipodophyllotoxin on DMBA/TPA-induced mouse skin carcinogenesis. Carcinogenesis 20, 997 (1999).
45. K. Yoshimura, K Harii, Y. Masuda, M. Takahashi, T. Aoyama, and T. Iga, Usefulness of a narrow band reflectance spectrophotometer in evaluating effects of depigmenting treatment. Aesthetic. Plast. Surg. 25, 129 (2001).
46. A. G. Gornall, C. J. Bardawill, and M. M. David, Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 177, 751 (1949).