Antiproliferative Activity of Buddleja saligna (Willd.) against Melanoma and In Vivo Modulation of Angiogenesis
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
NA
University of Pretoria
SFD13080220333
National Research Foundation-DAAD
DST/CON 0059/2019
The Department of Science and Innovation, South Africa
NA
The Innovation Hub, South Africa
NA
L'Oreal-UNESCO
UIDP/04378/2020 and UIDB/04378/2020
FCT-MCTES
PubMed
36558948
PubMed Central
PMC9782150
DOI
10.3390/ph15121497
PII: ph15121497
Knihovny.cz E-zdroje
- Klíčová slova
- Buddleja saligna, angiogenesis, antiproliferative activity, ex ovo YSM, melanoma,
- Publikační typ
- časopisecké články MeSH
Melanoma cells secrete pro-angiogenic factors, which stimulates growth, proliferation and metastasis, and therefore are key therapeutic targets. Buddleja saligna (BS), and an isolated triterpenoid mixture (DT-BS-01) showed a fifty percent inhibitory concentration (IC50) of 33.80 ± 1.02 and 5.45 ± 0.19 µg/mL, respectively, against melanoma cells (UCT-MEL-1) with selectivity index (SI) values of 1.64 and 5.06 compared to keratinocytes (HaCat). Cyclooxygenase-2 (COX-2) inhibition was observed with IC50 values of 35.06 ± 2.96 (BS) and 26.40 ± 4.19 µg/mL (DT-BS-01). BS (30 µg/mL) significantly inhibited interleukin (IL)-6 (83.26 ± 17.60%) and IL-8 (100 ± 0.2%) production, whereas DT-BS-01 (5 µg/mL) showed 51.07 ± 2.83 (IL-6) and 0 ± 6.7% (IL-8) inhibition. Significant vascular endothelial growth factor (VEGF) inhibition, by 15.84 ± 4.54 and 12.21 ± 3.48%, respectively, was observed. In the ex ovo chick embryo yolk sac membrane assay (YSM), BS (15 µg/egg) significantly reduced new blood vessel formation, with 53.34 ± 11.64% newly formed vessels. Silver and palladium BS nanoparticles displayed noteworthy SI values. This is the first report on the significant anti-angiogenic activity of BS and DT-BS-01 and should be considered for preclinical trials as there are currently no US Food and Drug Administration (FDA) approved drugs to inhibit angiogenesis in melanoma.
College of Pharmacy JSS Academy of Higher Education and Research Mysuru 570015 India
Department of Physics and Astronomy University of Missouri Columbia MO 65211 USA
School of Natural Resources University of Missouri Columbia MO 65211 USA
Sinclair Research Centre Auxvasse MO 65231 USA
University of Missouri Research Reactor University of Missouri Columbia MO 65212 USA
Zobrazit více v PubMed
The Skin Cancer Foundation Skin Cancer Facts & Statistics. [(accessed on 7 January 2021)]. Available online: https://www.skincancer.org/skin-cancer-information/skin-cancer-facts/
Khazaei Z., Ghorat F., Jarrahi A.M., Adineh H.A., Sohrabivafa M., Goodarzi E. Global Incidence and Mortality of Skin Cancer by Histological Subtype and Its Relationship with the Human Development Index (HDI); an Ecology Study in 2018. World Cancer Res. J. 2019;6:e1265.
Hanahan D., Weinberg R.A. The Hallmarks of Cancer. Cell. 2000;100:57–70. doi: 10.1016/S0092-8674(00)81683-9. PubMed DOI
Emmett M.S., Dewing D., Pritchard-Jones R.O. Angiogenesis and Melanoma-From Basic Science to Clinical Trials. Am. J. Cancer Res. 2011;1:868. PubMed PMC
Hubler W.R., Wolf J.E. Melanoma.Tumor Angiogenesis and Human Neoplasia. Cancer. 1976;38:187–192. doi: 10.1002/1097-0142(197607)38:1<187::AID-CNCR2820380129>3.0.CO;2-D. PubMed DOI
Warren B., Shubik P. The Growth of the Blood Supply to Melanoma Transplants in the Hamster Cheek Pouch-PubMed. Lab. Investig. 1966;15:464–478. PubMed
Mahabeleshwar G.H., Byzova T.V. Angiogenesis in Melanoma. Semin. Oncol. 2007;34:555–565. doi: 10.1053/j.seminoncol.2007.09.009. PubMed DOI PMC
Bar-Eli M. Role of Interleukin-8 in Tumor Growth and Metastasis of Human Melanoma. Pathobiology. 1999;67:12–18. doi: 10.1159/000028045. PubMed DOI
Nürnberg W., Tobias D., Otto F., Henz B.M., Schadendorf D. Expression of Interleukin-8 Detected by in Situ Hybridization Correlates with Worse Prognosis in Primary Cutaneous Melanoma. J. Pathol. 1999;189:546–551. doi: 10.1002/(SICI)1096-9896(199912)189:4<546::AID-PATH487>3.0.CO;2-L. PubMed DOI
Ugurel S., Rappl G., Tilgen W., Reinhold U. Increased Serum Concentration of Angiogenic Factors in Malignant Melanoma Patients Correlates with Tumor Progression and Survival. J. Clin. Oncol. 2001;19:577–583. doi: 10.1200/JCO.2001.19.2.577. PubMed DOI
Mahler D.A., Huang S., Tabrizi M., Bell G.M. Efficacy and Safety of a Monoclonal Antibody Recognizing Lnterleukin-8 in COPD: A Pilot Study. Chest. 2004;126:926–934. doi: 10.1378/chest.126.3.926. PubMed DOI
Naugler W.E., Karin M. The Wolf in Sheep’s Clothing: The Role of Interleukin-6 in Immunity, Inflammation and Cancer. Trends Mol. Med. 2008;14:109–119. doi: 10.1016/j.molmed.2007.12.007. PubMed DOI
Hoejberg L., Bastholt L., Schmidt H. Interleukin-6 and Melanoma. Melanoma Res. 2012;22:327–333. doi: 10.1097/CMR.0b013e3283543d72. PubMed DOI
Moretti S., Pinzi C., Spallanzani A., Berti E., Chiarugi A., Mazzoli S., Fabiani M., Vallecchi C., Herlyn M. Immunohistochemical Evidence of Cytokine Networks during Progression of Human Melanocytic Lesions. Int. J. Cancer. 1999;84:160–168. doi: 10.1002/(SICI)1097-0215(19990420)84:2<160::AID-IJC12>3.0.CO;2-R. PubMed DOI
Goulet A., Einsphar J., Alberts D., Beas A., Burk C., Bhattacharyya A., Bangert J., Harmon J., Fujiwara H., Koki A., et al. Analysis of Cyclooxygenase 2 (COX-2) Expression during Malignant Melanoma Progression-PubMed. Cancer Biol. Ther. 2003;2:713–718. doi: 10.4161/cbt.2.6.627. PubMed DOI
Wu W.K.K., Yiu Sung J.J., Lee C.W., Yu J., Cho C.H. Cyclooxygenase-2 in Tumorigenesis of Gastrointestinal Cancers: An Update on the Molecular Mechanisms. Cancer Lett. 2010;295:7–16. doi: 10.1016/j.canlet.2010.03.015. PubMed DOI
National Cancer Institute Bevacizumab. [(accessed on 7 January 2021)]; Available online: https://www.cancer.gov/about-cancer/treatment/drugs/bevacizumab.
Chanda N., Kattumuri V., Shukla R., Zambre A., Katti K., Upendran A., Kulkarni R.R. Bombesin Functionalized Gold Nanoparticles Show in Vitro and in Vivo Cancer Receptor Specificity. Proc. Natl. Acad. Sci. USA. 2010;107:8760–8765. doi: 10.1073/pnas.1002143107. PubMed DOI PMC
Thipe V.C., Amiri K.P., Bloebaum P., Raphael A.K., Khoobchandani M., Katti K.K., Jurisson S.S., Katti K.V. Development of Resveratrol-Conjugated Gold Nanoparticles: Interrelationship of Increased Resveratrol Corona on Anti-Tumor Efficacy against Breast, Pancreatic and Prostate Cancers. Int. J. Nanomed. 2019;14:4413–4428. doi: 10.2147/IJN.S204443. PubMed DOI PMC
Tangthong T., Piroonpan T., Thipe V.C., Khoobchandani M., Katti K., Katti K.V., Pasanphan W. Water-Soluble Chitosan Conjugated DOTA-Bombesin Peptide Capped Gold Nanoparticles as a Targeted Therapeutic Agent for Prostate Cancer. Nanotechnol. Sci. Appl. 2021;14:69–89. doi: 10.2147/NSA.S301942. PubMed DOI PMC
Khoobchandani M., Katti K.K., Karikachery A.R., Thipe V.C., Bloebaum P.L.R., Katti K.V. Biotechnology Products in Everyday Life. Springer International Publishing; Cham, Switzerland: 2019. Targeted Phytochemical-Conjugated Gold Nanoparticles in Cancer Treatment.
Khoobchandani M., Katti K.K., Karikachery A.R., Thipe V.C., Srisrimal D., Dhurvas Mohandoss D.K., Darshakumar R.D., Joshi C.M., Katti V.K. New Approaches in Breast Cancer Therapy Through Green Nanotechnology and Nano-Ayurvedic Medicine-Pre-Clinical and Pilot Human Clinical Investigations. Int. J. Nanomed. 2020;15:181–197. doi: 10.2147/IJN.S219042. PubMed DOI PMC
Roma-Rodrigues C., Fernandes A.R., Baptista P. V Counteracting the Effect of Leukemia Exosomes by Antiangiogenic Gold Nanoparticles. Int. J. Nanomed. 2019;14:6843–6854. doi: 10.2147/IJN.S215711. PubMed DOI PMC
Baharara J., Namvar F., Mousavi M., Ramezani T., Mohamad R. Anti-Angiogenesis Effect of Biogenic Silver Nanoparticles Synthesized Using Saliva Officinalis on Chick Chorioalantoic Membrane (CAM) Molecules. 2014;19:13498–13508. doi: 10.3390/molecules190913498. PubMed DOI PMC
Li L., Zhang W., Desikan Seshadri V.D., Cao G. Synthesis and Characterization of Gold Nanoparticles from Marsdenia Tenacissima and Its Anticancer Activity of Liver Cancer HepG2 Cells. Artif. Cells Nanomed. Biotechnol. 2019;47:3029–3036. doi: 10.1080/21691401.2019.1642902. PubMed DOI
Anselmo A.C., Mitragotri S. Nanoparticles in the Clinic: An Update. Bioeng. Transl. Med. 2019;4:e10143. doi: 10.1002/btm2.10143. PubMed DOI PMC
Bonvalot S., Rutkowski P.L., Thariat J., Carrère S., Ducassou A., Sunyach M.-P., Agoston P., Hong A., Mervoyer A., Rastrelli M., et al. NBTXR3, a First-in-Class Radioenhancer Hafnium Oxide Nanoparticle, plus Radiotherapy versus Radiotherapy Alone in Patients with Locally Advanced Soft-Tissue Sarcoma (Act.In.Sarc): A Multicentre, Phase 2–3, Randomised, Controlled Trial. Lancet Oncol. 2019;20:1148–1159. doi: 10.1016/S1470-2045(19)30326-2. PubMed DOI
Đorđević S., Gonzalez M.M., Conejos-Sánchez I., Carreira B., Pozzi S., Acúrcio R.C., Satchi-Fainaro R., Florindo H.F., Vicent M.J. Current Hurdles to the Translation of Nanomedicines from Bench to the Clinic. Drug Deliv. Transl. Res. 2021;12:500–525. doi: 10.1007/s13346-021-01024-2. PubMed DOI PMC
Cragg G.M., Pezzuto J.M. Natural Products as a Vital Source for the Discovery of Cancer Chemotherapeutic and Chemopreventive Agents. Med. Princ. Pract. 2016;25:41–59. doi: 10.1159/000443404. PubMed DOI PMC
Newman D., Cragg G. Natural Products as Sources of New Drugs over the 30 Years from 1981 to 2010. J. Nat. Prod. 2012;75:311–335. doi: 10.1021/np200906s. PubMed DOI PMC
Howes M.-J.R., Quave C.L., Collemare J., Tatsis E.C., Twilley D., Lulekal E., Farlow A., Li L., Cazar M.-E., Leaman D.J., et al. Molecules from Nature: Reconciling Biodiversity Conservation and Global Healthcare Imperatives for Sustainable Use of Medicinal Plants and Fungi. Plants People Planet. 2020;2:463–481. doi: 10.1002/ppp3.10138. DOI
Koh H.K., Geller A.C., Miller D.R., Grossbart T.A., Lew R.A. Prevention and Early Detection Strategies for Melanoma and Skin Cancer. Current Status. Arch. Dermatol. 1996;132:436–443. doi: 10.1001/archderm.1996.03890280098014. PubMed DOI
Aubrey A. Buddleja Saligna|PlantZAfrica. [(accessed on 30 October 2021)]. Available online: http://pza.sanbi.org/buddleja-saligna.
Su M., Huang J., Liu S., Xiao Y., Qin X., Liu J., Pi C., Luo T., Li J., Chen X., et al. The Anti-Angiogenic Effect and Novel Mechanisms of Action of Combretastatin A-4. Sci. Rep. 2016;6:1–11. doi: 10.1038/srep28139. PubMed DOI PMC
Bamuamba K., Gammon D., Meyers P., Dijoux-Franca M., Scott G. Anti-Mycobacterial Activity of Five Plant Species Used as Traditional Medicines in the Western Cape Province (South Africa) J. Ethnopharmacol. 2008;117:385–390. doi: 10.1016/j.jep.2008.02.007. PubMed DOI
Chukwujekwu J., Amoo S., de Kock C., Smith P., Van Staden J. Antiplasmodial, Acetylcholinesterase and Alpha-Glucosidase Inhibitory and Cytotoxicity Properties of Buddleja Saligna. S. Afr. J. Bot. 2014;94:6–8. doi: 10.1016/j.sajb.2014.05.003. DOI
Singh A., Venugopala K., Khedr M., Pillay M., Nwaeze K., Coovadia Y., Shode F., Odhav B. Antimycobacterial, Docking and Molecular Dynamic Studies of Pentacyclic Triterpenes from Buddleja Saligna Leaves. J. Biomol. Struct. Dyn. 2017;35:2654–2664. doi: 10.1080/07391102.2016.1227725. PubMed DOI
Caunii A., Oprean C., Cristea M., Ivan A., Danciu C., Tatu C., Paunescu V., Marti D., Tzanakakis G., Spandidos D.A., et al. Effects of Ursolic and Oleanolic on SK-MEL-2 Melanoma Cells: In Vitro and in Vivo Assays. Int. J. Oncol. 2017;51:1651–1660. doi: 10.3892/ijo.2017.4160. PubMed DOI PMC
Mahmoudi M., Rabe S., Balali-Mood M., Karimi G., Tabasi N., Riahi-Zanjani B. Ursolic Acid Induced Apoptotic Cell Death Following Activation of Caspases in Isolated Human Melanoma Cells. Cell Biol. Int. 2015;39:230–236. doi: 10.1002/cbin.10376. PubMed DOI
Oprean C., Ivan A., Bojin F., Cristea M., Soica C., Drăghia L., Caunii A., Paunescu V., Tatu C. Selective in Vitro Anti-Melanoma Activity of Ursolic and Oleanolic Acids. Toxicol. Mech. Methods. 2018;28:148–156. doi: 10.1080/15376516.2017.1373881. PubMed DOI
Ghosh S., Bishayee K., Khuda-Bukhsh A. Oleanolic Acid Isolated from Ethanolic Extract of Phytolacca Decandra Induces Apoptosis in A375 Skin Melanoma Cells: Drug-DNA Interaction and Signaling Cascade. J. Integr. Med. 2014;12:102–114. doi: 10.1016/S2095-4964(14)60015-7. PubMed DOI
Chukwujekwu J.C., Rengasamy K.R.R., Kock C.A.d., Smith P.J., Slavětínská L.P., van Staden J. Alpha-Glucosidase Inhibitory and Antiplasmodial Properties of Terpenoids from the Leaves of Buddleja saligna Willd. J. Enzym. Inhib. Med. Chem. 2015;31:63–66. doi: 10.3109/14756366.2014.1003927. PubMed DOI
Pratheeshkumar P., Kuttan G. Oleanolic Acid Induces Apoptosis by Modulating P53, Bax, Bcl-2 and Caspase-3 Gene Expression and Regulates the Activation of Transcription Factors and Cytokine Profile in B16F. J. Environ. Pathol. Toxicol. Oncol. 2011;30:21–31. doi: 10.1615/JEnvironPatholToxicolOncol.v30.i1.30. PubMed DOI
Fuliaş A., Ledeţi I., Vlase G., Vlase T., Şoica C., Dehelean C., Oprean C., Bojin F., Şuta L.-M., Bercean V., et al. Thermal Degradation, Kinetic Analysis, and Apoptosis Induction in Human Melanoma for Oleanolic and Ursolic Acids. J. Therm. Anal. Calorim. 2015;125:759–768. doi: 10.1007/s10973-015-5052-8. DOI
Harmand P., Duval R., Delage C., Simon A. Ursolic Acid Induces Apoptosis through Mitochondrial Intrinsic Pathway and Caspase-3 Activation in M4Beu Melanoma Cells. Int. J. Cancer. 2005;114:1–11. doi: 10.1002/ijc.20588. PubMed DOI
Manu K., Kuttan G. Ursolic Acid Induces Apoptosis by Activating P53 and Caspase-3 Gene Expressions and Suppressing NF-KappaB Mediated Activation of Bcl-2 in B16F-10 Melanoma Cells. Int. Immunopharmacol. 2008;8:974–981. doi: 10.1016/j.intimp.2008.02.013. PubMed DOI
Ringbom T., Segura L., Noreen Y., Perera P., Bohlin L. Ursolic Acid from Plantago Major, a Selective Inhibitor of Cyclooxygenase-2 Catalyzed Prostaglandin Biosynthesis. J. Nat. Prod. 1998;61:1212–1215. doi: 10.1021/np980088i. PubMed DOI
Subbaramaiah K., Dannenberg A.J. Cyclooxygenase 2: A Molecular Target for Cancer Prevention and Treatment. Trends Pharmacol. Sci. 2003;24:96–102. doi: 10.1016/S0165-6147(02)00043-3. PubMed DOI
Kim M., Kim J., Han S., Kim H. Ursolic Acid Isolated from Guava Leaves Inhibits Inflammatory Mediators and Reactive Oxygen Species in LPS-Stimulated Macrophages. Immunopharmacol. Immunotoxicol. 2015;37:228–235. doi: 10.3109/08923973.2015.1021355. PubMed DOI
Li M., Han Z., Bei W., Rong X., Guo J., Hu X. Oleanolic Acid Attenuates Insulin Resistance via NF-ΚB to Regulate the IRS1-GLUT4 Pathway in HepG2 Cells. Evid. Based. Complement. Alternat. Med. 2015;2015:643102. doi: 10.1155/2015/643102. PubMed DOI PMC
Kim H., Han S., Sung H., Park S., Kang M., Han S., Kang Y. Blockade of Visfatin Induction by Oleanolic Acid via Disturbing IL-6-TRAF6-NF-ΚB Signaling of Adipocytes. Exp. Biol. Med. 2014;239:284–292. doi: 10.1177/1535370213514511. PubMed DOI
Lee C., Wu S., Chen J., Li C., Lo H., Cheng W., Lin J., Chang Y., Hsiang C., Ho T. Eriobotrya Japonica Leaf and Its Triterpenes Inhibited Lipopolysaccharide-Induced Cytokines and Inducible Enzyme Production via the Nuclear Factor-KappaB Signaling Pathway in Lung Epithelial Cells. Am. J. Chin. Med. 2008;36:1185–1198. doi: 10.1142/S0192415X0800651X. PubMed DOI
Yang G., Zhang R., Lou B., Cheng K., Xiong J., Hu J. Chemical Constituents from Melastoma Dodecandrum and Their Inhibitory Activity on Interleukin-8 Production in HT-29 Cells. Nat. Prod. Res. 2014;28:1383–1387. doi: 10.1080/14786419.2014.903480. PubMed DOI
Kanjoormana M., Kuttan G. Antiangiogenic Activity of Ursolic Acid. Integr. Cancer Ther. 2010;9:224–235. doi: 10.1177/1534735410367647. PubMed DOI
Lee D.-H., Lee J., Jeon J., Kim K.-J., Yun J.-H., Jeong H.-S., Lee E.H., Koh Y.J., Cho C.-H. Oleanolic Acids Inhibit Vascular Endothelial Growth Factor Receptor 2 Signaling in Endothelial Cells: Implication for Anti-Angiogenic Therapy. Mol. Cells. 2018;41:780. doi: 10.14348/MOLCELLS.2018.0207. PubMed DOI PMC
Cárdenas C., Quesada A.R., Medina M.Á. Effects of Ursolic Acid on Different Steps of the Angiogenic Process. Biochem. Biophys. Res. Commun. 2004;320:402–408. doi: 10.1016/j.bbrc.2004.05.183. PubMed DOI
Sohn K., Lee H., Chung H., Young H., Yi S., Kim K. Anti-Angiogenic Activity of Triterpene Acids. Cancer Lett. 1995;94:213–218. doi: 10.1016/0304-3835(95)03856-R. PubMed DOI
Padalia H., Moteriya P., Chanda S. Green Synthesis of Silver Nanoparticles from Marigold Flower and Its Synergistic Antimicrobial Potential. Arab. J. Chem. 2015;8:732–741. doi: 10.1016/j.arabjc.2014.11.015. DOI
Elia P., Zach R., Hazan S., Kolusheva S., Porat Z., Zeiri Y. Green Synthesis of Gold Nanoparticles Using Plant Extracts as Reducing Agents. Int. J. Nanomed. 2014;9:4021. doi: 10.2147/IJN.S57343. PubMed DOI PMC
Lebaschi S., Hekmati M., Veisi H. Green Synthesis of Palladium Nanoparticles Mediated by Black Tea Leaves (Camellia sinensis) Extract: Catalytic Activity in the Reduction of 4-Nitrophenol and Suzuki-Miyaura Coupling Reaction under Ligand-Free Conditions. J. Colloid Interface Sci. 2017;485:223–231. doi: 10.1016/j.jcis.2016.09.027. PubMed DOI
Twilley D., Moodley D., Rolfes H., Moodley I., McGaw L.J., Madikizela B., Summers B., Raaff L.A., Lategan M., Kgatuke L., et al. Ethanolic Extracts of South African Plants, Buddleja saligna Willd. and Helichrysum odoratissimum (L.) Sweet, as Multifunctional Ingredients in Sunscreen Formulations. S. Afr. J. Bot. 2021;137:171–182. doi: 10.1016/j.sajb.2020.10.010. DOI
Lall N., Henley-Smith C.J., Canha M.N.D., Oosthuizen C.B., Berrington D. Viability Reagent, PrestoBlue, in Comparison with Other Available Reagents, Utilized in Cytotoxicity and Antimicrobial Assays. Int. J. Microbiol. 2013;2013:420601. doi: 10.1155/2013/420601. PubMed DOI PMC
Reininger E.A., Bauer R. Prostaglandin-H-Synthase (PGHS)-1 and -2 Microtiter Assays for the Testing of Herbal Drugs and in Vitro Inhibition of PGHS-Isoenzyms by Polyunsaturated Fatty Acids from Platycodi Radix. Phytomedicine. 2006;13:164–169. doi: 10.1016/j.phymed.2005.03.006. PubMed DOI
Twilley D., Langhansová L., Palaniswamy D., Lall N. Evaluation of Traditionally Used Medicinal Plants for Anticancer, Antioxidant, Anti-Inflammatory and Anti-Viral (HPV-1) Activity. S. Afr. J. Bot. 2017;112:494–500. doi: 10.1016/j.sajb.2017.05.021. DOI
Arablou T., Aryaeian N., Khodaverdi S., Kolahdouz-Mohammadi R., Moradi Z., Rashidi N., Delbandi A.-A. The Effects of Resveratrol on the Expression of VEGF, TGF-β, and MMP-9 in Endometrial Stromal Cells of Women with Endometriosis. Sci. Rep. 2021;11:1–12. doi: 10.1038/s41598-021-85512-y. PubMed DOI PMC
Muhammad Nihad A.S., Deshpande R., Kale V.P., Bhonde R.R., Datar S.P. Establishment of an in Ovo Chick Embryo Yolk Sac Membrane (YSM) Assay for Pilot Screening of Potential Angiogenic and Anti-Angiogenic Agents. Cell Biol. Int. 2018;42:1474–1483. doi: 10.1002/CBIN.11051. PubMed DOI
Datar S., Shah R., Talele G., Bhonde R. In Vivo Screening of Potential Anti-Angiogenic Homeopathic Medicines Using Chick Embryo YSM Model. Cell Cell. Life Sci. J. 2020;5:1–6. doi: 10.23880/cclsj-16000158. DOI
Kuhnen S., Lemos P.M.M., Campestrini L.H., Ogliari J.B., Dias P.F., Maraschin M. Antiangiogenic Properties of Carotenoids: A Potential Role of Maize as Functional Food. J. Funct. Foods. 2009;1:284–290. doi: 10.1016/j.jff.2009.04.001. DOI
Wang H., Cheng-yu L., Wang X., Bao Y., Meng X., Yin W., Yu-xin L. Chick Yolk Sac Membrane Assay: A Novel Angiogenesis Model. J. Biol. Res. 2007;7:93–97.
Zhou Q., Qi C.L., Li Y., He X.D., Li J.C., Zhang Q.Q., Tian L., Zhang M., Han Z., Wang H., et al. A Novel Four-Step System for Screening Angiogenesis Inhibitors. Mol. Med. Rep. 2013;8:1734–1740. doi: 10.3892/mmr.2013.1704. PubMed DOI
Belleri M., Ribatti D., Nicoli S., Cotelli F., Forti L., Vannini V., Stivala L.A., Presta M. Antiangiogenic and Vascular-Targeting Activity of the Microtubule-Destabilizing Trans-Resveratrol Derivative 3,5,4′-Trimethoxystilbene. Mol. Pharmacol. 2005;67:1451–1459. doi: 10.1124/mol.104.009043. PubMed DOI
Belleri M., Ribatti D., Savio M., Stivala L.A., Forti L., Tanghetti E., Alessi P., Coltrini D., Bugatti A., Mitola S., et al. Alphavbeta3 Integrin-Dependent Antiangiogenic Activity of Resveratrol Stereoisomers. Mol. Cancer Ther. 2008;7:3761–3770. doi: 10.1158/1535-7163.MCT-07-2351. PubMed DOI