Computational simulations of microalgae-derived bioactive compounds as a novel inhibitor against B-Raf V600E-driven melanoma

Fiddy Semba Prasetiya Wanda Destiarani Irene Retno Cahya Prihastaningtyas Mochamad Untung Kurnia Agung Muhammad Yusuf   

Open Access   

Published:  Jan 10, 2023

DOI: 10.7324/JAPS.2023.10012
Abstract

Melanoma is one of the most aggressive types of cancer, which has shown a tremendous surge in the last 50 years. Therapy for advanced-type melanoma is still a challenge because of the low response rate and 10-year survival. Therefore, drug discovery efforts need to be made to fight this cancer. To date, the development of big data and 3D has made it easier for researchers to understand the structure of proteins or enzymes that play an important role as receptors in melanoma cancer to be used as specific targets for diagnosis and therapy, for instance, the B-Raf V600E. This study examined the potential of active compounds from microalgae for developing melanoma anticancer drugs. The database was constructed using data mining from MarinLit and the related publications from 1970 to 2020. In silico methods such as molecular docking, virtual screening, and molecular dynamic simulations were used to find the most potential candidates. A total of 25 compounds passed the virtual screening stage. The top three compounds based on the binding free energy compared to a natural ligand and commercial drug are cholesta-5,7-dien-3beta-ol, 24-oxocholesterol acetate, lathosterol, and two additional compounds, phycocyanin and phycocyanobilin, were also selected due to their massive production from the most commonly cultured microalgae worldwide, Arthrospira sp. (previously known as Spirulina sp.). Furthermore, ADME analysis and toxicity tests were also carried out. Molecular dynamics simulation showed that phycocyanin was the best potential candidate for melanoma anticancer drugs, with free binding energies ranging from −65 to −80 kcal/mol. This result was also supported by root mean square deviation, root mean square fluctuation, and distance parameter data. This study may accelerate molecular research in producing therapeutic compounds for melanoma cancer, thus allowing it to continue developing pharmaceutical products that benefit human health.


Keyword:     B-Raf V600E melanoma molecular dynamics phycocyanin virtual screening


Citation:

Prasetiya FS, Destiarani W, Prihastaningtyas IRC, Agung MUK, Yusuf M. Computational simulations of microalgae-derived bioactive compounds as a novel inhibitor against B-Raf V600E driven melanoma. J Appl Pharm Sci, 2023. https://doi.org/10.7324/JAPS.2023.10012

Copyright: © The Author(s). This is an open-access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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Reference

Afriza D, Suriyah WH, Ichwan SJA. In silico analysis of molecular interactions between the anti-apoptotic protein survivin and dentatin, nordentatin, and quercetin. J Phys Conf Ser, 2018; 1073(3):032001. https://doi.org/10.1088/1742-6596/1073/3/032001

Ahinko M, Niinivehmas S, Jokinen E, Pentikäinen OT. Suitability of MMGBSA for the selection of correct ligand binding modes from docking results. Chem Biol Drug Des, 2019; 93(4):522-38. https://doi.org/10.1111/cbdd.13446

Belter B, Haase-Kohn C, Pietzsch J. Biomarkers in malignant melanoma: recent trends and critical perspective. In: Ward WH, Farma JM (Eds.). Cutaneous melanoma: etiology and therapy, Codon Publications, Brisbane, AU, 2017. https://doi.org/10.15586/codon.cutaneousmelanoma.2017.ch3

Billard G, Dauguet JC, Maume D, Bert M. Sterols and chemotaxonomy of marine chrysophyceae. Bot Mar, 1990; 33(3):225-8. https://doi.org/10.1515/botm.1990.33.3.225

Bokesch HR, O'Keefe BR, McKee TC, Pannell LK, Patterson GM, Gardella RS, Sowder RC 2nd, Turpin J, Watson K, Buckheit RW Jr, Boyd MR. A potent novel anti-HIV protein from the cultured cyanobacterium Scytonema varium. Biochemistry, 2003; 42(9):2578-84. https://doi.org/10.1021/bi0205698

Boobis A, Gundert-Remy U, Kremers P, Macheras P, Pelkonen O. In silico prediction of ADME and pharmacokinetics. Eur J Pharm Sci, 2002; 17(4-5):183-93. https://doi.org/10.1016/S0928-0987(02)00185-9

Case DA, Betz RM, Cerutti DS, Cheatham TE III, Darden TA, Duke RE, Giese TJ, Gohlke H, Goetz AW, Homeyer N, Izadi S, Janowski P, Kaus J, Kovalenko A, Lee TS, LeGrand S, Li P, Lin C, Luchko T, Luo R, Madej B, Mermelstein D, Xiao L, Kollman PA. Amber 2016 Reference Manual. University of California, San Francisco, CA, 2016.

Cerny MA. Prevalence of non-cytochrome P450-mediated metabolism in food and drug administration-approved oral and intravenous drugs: 2006-2015. Drug Metab Dispos, 2016; 44:1246-52. https://doi.org/10.1124/dmd.116.070763

Chapman PB, Hauschild A, Robert C, Haanen JB, Ascierto P, Larkin J, Dummer R, Garbe C, Testori A, Maio M, Hogg D, Lorigan P, Lebbe C, Jouary T, Schadendorf D, Ribas A, O'Day SJ, Sosman JA, Kirkwood JM, Eggermont AM, Dreno B, Nolop K, Li J, Nelson B, Hou J, Lee RJ, Flaherty KT, McArthur GA, BRIM-3 Study Group. Improved survival with vemurafenib in melanoma with BRAF V600E mutation. New Engl J Med, 2011; 364(26):2507-16. https://doi.org/10.1056/NEJMoa1103782

Chen J, Jiao R, Jiang Y, Bi Y, Chen ZY. Algal sterols are as effective as β-sitosterol in reducing plasma cholesterol concentration. J Agric Food Chem, 2014; 62(3):675-81. https://doi.org/10.1021/jf404955n

Cherng SC, Cheng SN, Tarn A, Chou TC. Anti-inflammatory activity of c-phycocyanin in lipopolysaccharide-stimulated RAW 264.7 macrophages. Life Sci, 2007; 81(19-20):1431-5. https://doi.org/10.1016/j.lfs.2007.09.009

Cope N, Novak B, Candelora C, Wong K, Cavallo M, Gunderwala A, Liu Z, Li Y, Wang Z. Biochemical characterization of full-length oncogenic BRAFV600E together with molecular dynamics simulations provide insight into the activation and inhibition mechanisms of RAF kinases. Chem Bio Chem, 2019; 20(22):2850-61. https://doi.org/10.1002/cbic.201900266

Daina A, Michielin O, Zoete V. ILOGP: a simple, robust, and efficient description of n-octanol/water partition coefficient for drug design using the GB/SA approach. J Chem Inf Model, 2014; 54(12):3284-301. https://doi.org/10.1021/ci500467k

Daina A, Michielin O, Zoete V. SwissADME: a free web tool to evaluate pharmacokinetics, drug-likeness and medicinal chemistry friendliness of small molecules. Sci Rep, 2017; 7(1):1-13. https://doi.org/10.1038/srep42717

Davies H, Bignell GR, Cox C, Stephens P, Edkins S, Clegg S, Teague J, Woffendin H, Garnett MJ, Bottomley W, Davis N, Dicks E, Ewing R, Floyd Y, Gray K, Hall S, Hawes R, Hughes J, Kosmidou V, Menzies A, Mould C, Parker A, Stevens C, Watt S, Hooper S, Wilson R, Jayatilake H, Gusterson BA, Cooper C, Shipley J, Hargrave D, Pritchard-Jones K, Maitland N, Chenevix-Trench G, Riggins GJ, Bigner DD, Palmieri G, Cossu A, Flanagan A, Nicholson A, Ho JW, Leung SY, Yuen ST, Weber BL, Seigler HF, Darrow TL, Paterson H, Marais R, Marshall CJ, Wooster R, Stratton MR, Futreal PA. Mutations of the BRAF gene in human cancer. Nature, 2002; 417(6892):949-54. https://doi.org/10.1038/nature00766

Davis AP, Grondin CJ, Johnson RJ, Sciaky D, Wiegers J, Wiegers TC, Mattingly CJ. Comparative toxicogenomics database (CTD): update 2021. Nucleic Acids Res, 2021; 49:D1138-43. https://doi.org/10.1093/nar/gkaa891

De Morais MG, Vaz BDS, De Morais EG, Costa JAV. Biologically active metabolites synthesized by microalgae. BioMed Res Int, 2015; 2015:835761. https://doi.org/10.1155/2015/835761

Destiarani W, Mulyani R, Yusuf M, Maksum IP. Molecular dynamics simulation of T10609C and C10676G mutations of mitochondrial ND4L gene associated with proton translocation in type 2 diabetes mellitus and cataract patients. Bioinform Biol Insights, 2020; 14:1177932220978672. https://doi.org/10.1177/1177932220978672

Dixit VA, Lal LA, Agrawal SR. Recent advances in the prediction of non-CYP450-mediated drug metabolism. Wiley Interdiscip Rev Comput Mol Sci, 2017; 7(6):e1323. https://doi.org/10.1002/wcms.1323

Doak BC, Kihlberg J. Drug discovery beyond the rule of 5- opportunities and challenges. Exp Opin Drug Discov, 2017; 12(2):115-9. https://doi.org/10.1080/17460441.2017.1264385

Domingues B, Lopes J, Soares P, Populo H. Melanoma treatment in review. Immunotargets Ther, 2018; 7:35-49. https://doi.org/10.2147/ITT.S134842

Dong JJ, Li QS, Wang SF, Li CY, Zhao X, Qiu HY, Zhao MY, Zhu HL. Synthesis, biological evaluation and molecular docking of novel 5-phenyl-1H-pyrazol derivatives as potential BRAFV600E inhibitors. Org Biomol Chem, 2013; 11(37):6328-37. https://doi.org/10.1039/c3ob40776d

Duc Nguyen H, Hee Jo W, Hong Minh Hoang N, Kim MS. Anti-inflammatory effects of B vitamins protect against tau hyperphosphorylation and cognitive impairment induced by 1,2 diacetyl benzene: an in vitro and in silico study. Int Immunopharmacol, 2022; 108:108736. https://doi.org/10.1016/j.intimp.2022.108736

Carranza EA, Newman M. Clinical periodontology. 9th edition, W. B. Saunders, Philadelphia, PA, 2012.

Ekins S, Mestres J, Testa B. In silico pharmacology for drug discovery: applications to targets and beyond. Br J Pharmacol, 2007; 152(1):21-37. https://doi.org/10.1038/sj.bjp.0707306

Feinstein WP, Brylinski M. Calculating an optimal box size for ligand docking and virtual screening against experimental and predicted binding pockets. J Cheminform, 2015; 7(1):18. https://doi.org/10.1186/s13321-015-0067-5

Fernández-Rojas B, Hernández-Juárez J, Pedraza-Chaverri J. Nutraceutical properties of phycocyanin. J Funct Foods, 2014; 11:375-92. https://doi.org/10.1016/j.jff.2014.10.011

Francavilla M, Trotta P, Luque R. Phytosterols from Dunaliella tertiolecta and Dunaliella salina: a potentially novel industrial application. Bioresour Technol, 2010; 101(11):4144-50. https://doi.org/10.1016/j.biortech.2009.12.139

Friedrich A, Olejniczak K. Evaluation of carcinogenicity studies of medicinal products for human use authorised via the European centralised procedure (1995-2009). Regul Toxicol Pharmacol, 2011; 60(2):225-48. https://doi.org/10.1016/j.yrtph.2011.04.001

Fu W, Nelson DR, Yi Z, Xu M, Khraiwesh B, Jijakli K, Chaiboonchoe A, Alzahmi A, Al-Khair D, Brynjolfsson S, Salehi-Ashtiani K. Bioactive compounds from microalgae: current development and prospects. Studies in natural products chemistry. Elsevier, pp 199-225, 2017. https://doi.org/10.1016/B978-0-444-63929-5.00006-1

Gan J, Ma S, Zhang D. Non-cytochrome P450-mediated bioactivation and its toxicological relevance. Drug Metab Rev, 2016; 48(4):473-501. https://doi.org/10.1080/03602532.2016.1225756

Ganesan A. The impact of natural products upon modern drug discovery. Curr Opin Chem Biol, 2008; 12(3):306-17. https://doi.org/10.1016/j.cbpa.2008.03.016

Gastineau R, Turcotte F, Pouvreau JB, Morançais M, Fleurence J, Windarto E, Prasetiya FS, Arsad S, Jaouen P, Babin M, Coiffard L, Couteau C, Bardeau JF, Jacquette B, Leignel V, Hardivillier Y, Marcotte I, Bourgougnon N, Tremblay R, Deschênes JS, Badawy H, Pasetto P, Davidovich N, Hansen G, Dittmer J, Mouget JL. Marennine, promising blue pigments from a widespread Haslea diatom species complex. Mar Drugs, 2014; 12(6):3161-89. https://doi.org/10.3390/md12063161

Ghosal A. Evaluation of the clearance mechanism of non-CYP-mediated drug metabolism and DDI as a victim drug. In: Ma S, Chowdhury S (Eds.). Identification and quantification of drugs, metabolites, drug metabolizing enzymes, and transporters. Elsevier Science, pp 237-71, 2020. https://doi.org/10.1016/B978-0-12-820018-6.00008-9

Grover P, Bhatnagar A, Kumari N, Narayan Bhatt A, Kumar Nishad D, Purkayastha J. C-Phycocyanin-a novel protein from Spirulina platensis-in vivo toxicity, antioxidant and immunomodulatory studies. Saudi J Biol Sci, 2021; 28(3):1853-9. https://doi.org/10.1016/j.sjbs.2020.12.037

Haling JR, Sudhamsu J, Yen I, Sideris S, Sandoval W, Phung Wç, Bravo BJ, Giannetti AM, Peck A, Masselot A, Morales T, Smith D, Brandhuber BJ, Hymowitz SG, Malek S. Structure of the BRAF-MEK complex reveals a kinase activity independent role for BRAF in MAPK signaling. Cancer Cell, 2014; 26(3):402-13. https://doi.org/10.1016/j.ccr.2014.07.007

Hamouda RA, El-Naggar NEA. Cyanobacteria-based microbial cell factories for production of industrial products. In: Singh V (Ed.). Microbial cell factories engineering for production of biomolecules, Elsevier, pp 277-302, 2021. https://doi.org/10.1016/B978-0-12-821477-0.00007-6

Hodgson J. ADMET-turning chemicals into drugs. Nature Biotechnol, 2001; 19(8):722-6. https://doi.org/10.1038/90761

Hoseini SM, Khosravi-Darani K, Mozafari MR. Nutritional and medical applications of Spirulina microalgae. Mini Rev Med Chem, 2013; 13(8):1231-7. https://doi.org/10.2174/1389557511313080009

Hughes JP, Rees SS, Kalindjian SB, Philpott KL. Principles of early drug discovery. Br J Pharmacol, 2011; 162(6):1239-49. https://doi.org/10.1111/j.1476-5381.2010.01127.x

Hutomo M, Moosa MK. Indonesian marine and coastal biodiversity: present status. Indian J Mar Sci, 2005; 34(1):88-97.

Jakob JA, Bassett RL Jr, Ng CS, Curry JL, Joseph RW, Alvarado GC, Rohlfs ML, Richard J, Gershenwald JE, Kim KB, Lazar AJ, Hwu P, Davies MA. NRAS mutation status is an independent prognostic factor in metastatic melanoma. Cancer, 2012; 118(16):4014-23. https://doi.org/10.1002/cncr.26724

Jiang L, Wang Y, Yin Q, Liu G, Liu H, Huang Y, Li B. Phycocyanin: a potential drug for cancer treatment. J Cancer, 2017; 8(17):3416-29. https://doi.org/10.7150/jca.21058

Jin W, Liu G, Zhong W, Sun C, Zhang Q. Polysaccharides from Sargassum thunbergii : monthly variations and anti-complement and anti-tumour. Int J Biol Macromol, 2017; 105:1526-31 https://doi.org/10.1016/j.ijbiomac.2017.05.104

Kaboli PJ, Ismail P, Ling KH. Molecular modeling, dynamics simulations, and binding efficiency of berberine derivatives: a new group of RAF inhibitors for cancer treatment. PLoS One, 2018; 13(3):1-19. https://doi.org/10.1371/journal.pone.0193941

Khan T, Khan AR, Raza S, Azad I, Lawrence AJ. Medicinal and environmental chemistry: experimental advances and simulations. Bentham Science Publisher, 2021. https://doi.org/10.2174/97898149982771210101

Laskowski RA, MacArthur MW, Moss DS, Thornton JM. PROCHECK: a program to check the stereochemical quality of protein structures. J Appl Crystallogr, 1993; 26(2):283-91. https://doi.org/10.1107/S0021889892009944

Laskowski RA, Swindells MB. LigPlot+: multiple ligand-protein interaction diagrams for drug discovery. J Chem Inf Model, 2011; 51:2778-86. https://doi.org/10.1021/ci200227u

Leblond JD, Dahmen JL, Seipelt RL, Elrod-Erickson MJ, Kincaid R, Howard JC, Evens TJ, Chapman PJ. Lipid composition of chlorarachniophytes (Chlorarachniophyceae) from the genera Bigelowiella, Gymnochlora, and Lotharella. J Phycol, 2005; 41(2):311-21. https://doi.org/10.1111/j.1529-8817.2005.04082.x

Leblond JD, Timofte HI, Roche SA, Porter NM. Sterols of glaucocystophytes. Phycol Res, 2011; 59(2):129-34. https://doi.org/10.1111/j.1440-1835.2011.00610.x

Lee S, Chang GS, Lee IH, Chung JE, Sung KY, No K. The PreADME: PC-based program for batch prediction of ADME properties. EuroQSAR 2004, 2004; 9:5-10.

Lee SK, Lee IH, Kim HJ, Chang GS, Chung JE, No KT. The PreADME approach: web-based program for rapid prediction of physico-chemical, drug absorption and drug-like properties. EuroQSAR 2002 designing drugs and crop protectants: processes, problems and solutions. Blackwell Publishing, Malden, MA, pp 418-420, 2003.

Liao G, Gao B, Gao Y, Yang X, Cheng X, Ou Y. Phycocyanin inhibits tumorigenic potential of pancreatic cancer cells: role of apoptosis and autophagy. Sci Rep, 2016; 6:1-12. https://doi.org/10.1038/srep34564

Liu Q, Huang Y, Zhang R, Cai T, Cai Y. Medical application of Spirulina platensis derived C-phycocyanin. Evid Based Complement Alternat Med, 2016; 2016:7803846. https://doi.org/10.1155/2016/7803846

Lobell M, Molnár L, Keserü GM. Recent advances in the prediction of blood-brain partitioning from molecular structure. J Pharm Sci, 2003; 92(2):360-70. https://doi.org/10.1002/jps.10282

Long GV, Menzies AM, Nagrial AM, Haydu LE, Hamilton AL, Mann GJ, Hughes TM, Thompson JF, Scolyer RA, Kefford RF. Prognostic and clinicopathologic associations of oncogenic BRAF in metastatic melanoma. J Clin Oncol, 2011; 29(10):1239-46. https://doi.org/10.1200/JCO.2010.32.4327

Luebker SA, Koepsell SA. Diverse mechanisms of BRAF inhibitor resistance in melanoma identified in clinical and preclinical studies. Front Oncol, 2019; 9:1-8. https://doi.org/10.3389/fonc.2019.00268

Luo C, Xie P, Marmorstein R. Identification of BRAF inhibitors through in silico screening. J Med Chem, 2008; 51:6121-7. https://doi.org/10.1021/jm800539g

Lv J, Yang X, Ma H, Hu X, Wei Y, Zhou W, Li L. The oxidative stability of microalgae oil (Schizochytrium aggregatum) and its antioxidant activity after simulated gastrointestinal digestion: relationship with constituents. Eur J Lipid Sci Technol, 2015; 117(12):1928-39. https://doi.org/10.1002/ejlt.201400588

Lynch T, Neff AP. The effect of cytochrome P450 metabolism on drug response, interactions, and adverse effects. Am Fam Phys, 2007; 76(3):391-6.

Ma XL, Chen C, Yang J. Predictive model of blood-brain barrier penetration of organic compounds. Acta Pharmacol Sin, 2005; 26(4):500-12. https://doi.org/10.1111/j.1745-7254.2005.00068.x

Maloney RC, Zhang M, Jang H, Nussinov R. The mechanism of activation of monomeric B-Raf V600E. Comput Struct Biotechnol J, 2021; 19:3349-63. https://doi.org/10.1016/j.csbj.2021.06.007

Marshall JA, Nichols PD, Hallegraeff GM. Chemotaxonomic survey of sterols and fatty acids in six marine raphidophyte algae. J Appl Phycol, 2002; 14(4):255-65. https://doi.org/10.1023/A:1021101203543

Martínez Andrade KA, Lauritano C, Romano G, Ianora A. Marine microalgae with anti-cancer properties. Mar Drugs, 2018; 16(5):165. https://doi.org/10.3390/md16050165

Matthews NH, Li WQ, Qureshi AA, Weinstock MA, Cho E. Epidemiology of melanoma. Progress in clinical cancer. vol. 6, pp 139-49, 2017.

McDonnell AM, Dang CH. Basic review of the cytochrome P450 system. J Adv Pract Oncol, 2013; 4(4):263. https://doi.org/10.6004/jadpro.2013.4.4.7

Mendes A, Reis A, Vasconcelos R, Guerra P, Lopes Da Silva T. Crypthecodinium cohnii with emphasis on DHA production: a review. J Appl Phycol, 2009; 21(2):199-214. https://doi.org/10.1007/s10811-008-9351-3

Meng XY, Zhang HX, Mezei M, Cui M. Molecular docking: a powerful approach for structure-based drug discovery. Curr Comput Aided Drug Des, 2012; 7(2):146-57. https://doi.org/10.2174/157340911795677602

Mercer KE, Pritchard CA. Raf proteins and cancer: B-Raf is identified as a mutational target. Biochim Biophys Acta Rev Cancer, 2003; 1653(1):25-40. https://doi.org/10.1016/S0304-419X(03)00016-7

Mishra SK, Shrivastav A, Maurya RR, Patidar SK, Haldar S, Mishra S. Effect of light quality on the C-phycoerythrin production in marine cyanobacteria Pseudanabaena sp. isolated from Gujarat coast, India. Protein Expr Purif, 2012; 81:5-10. https://doi.org/10.1016/j.pep.2011.08.011

Moretti S, Macchiarulo A, De Falco V, Avenia N, Barbi F, Carta C, Cavaliere A, Melillo RM, Passeri L, Santeusanio F, Tartaglia M, Santoro M, Puxeddu E. Biochemical and molecular characterization of the novel BRAF V599Ins mutation detected in a classic papillary thyroid carcinoma. Oncogene, 2006; 25(30):4235-40. https://doi.org/10.1038/sj.onc.1209448

Newman DJ, Cragg GM. Natural products as sources of new drugs over the nearly four decades from 01/1981 to 09/2019. J Nat Prod, 2020; 83(3):770-803. https://doi.org/10.1021/acs.jnatprod.9b01285

Nguyen HD, Kim MS. The protective effects of curcumin on metabolic syndrome and its components: in-silico analysis for genes, transcription factors, and microRNAs involved. Arch Biochem Biophys, 2022; 727:109326. https://doi.org/10.1016/j.abb.2022.109326

Norn C, Wicky BIM, Juergens D, Liu S, Kim D, Tischer D, Koepnick B, Anishchenko I; Foldit Players, Baker D, Ovchinnikov S. Protein sequence design by conformational landscape optimization. Proc Natl Acad Sci U S A, 2021; 118(11):1-7. https://doi.org/10.1101/2020.07.23.218917

Padyana AK, Bhat VB, Madyastha KM, Rajashankar KR, Ramakumar S. Crystal structure of a light-harvesting protein C-phycocyanin from Spirulina platensis. Biochem Biophys Res Commun, 2001; 282(4):893-8. https://doi.org/10.1006/bbrc.2001.4663

Park E, Rawson S, Li K, Kim BW, Ficarro SB, Pino GG, Sharif H, Marto JA, Jeon H, Eck MJ. Architecture of autoinhibited and active BRAF-MEK1-14-3-3 complexes. Nature, 2019; 575(7783):545-50. https://doi.org/10.1038/s41586-019-1660-y

Ponomarenko LP, Stonik IV, Aizdaicher NA, Orlova TY, Popovskaya GI, Pomazkina GV, Stonik VA. Sterols of marine microalgae Pyramimonas cf. cordata (Prasinophyta), Attheya ussurensis sp. nov. (Bacillariophyta) and a spring diatom bloom from Lake Baikal. Comp Biochem Physiol B Biochem Mol Biol, 2004; 138(1):65-70. https://doi.org/10.1016/j.cbpc.2004.02.007

Prakash S, Sasikala SL, Aldous VHJ. Isolation and identification of MDR-Mycobacterium tuberculosis and screening of partially characterised antimycobacterial compounds from chosen marine micro algae. Asian Pac J Trop Med, 2010; 3(8):655-61. https://doi.org/10.1016/S1995-7645(10)60158-7

Prasetiya FS, Ramdhani DS, Mulyani Y, Mochamad U, Agung K, Arsad S, Mouget J. Antioxidant activities of culture supernatant Haslea ostrearia adapted in Indonesia. AACL Bioflux, 2021; 14(1):111-9.

Prasetiya FS, Sunarto S, Bachtiar E, Agung MUK, Nathanael B, Pambudi AC, Lestari AD, Astuty S, Mouget J. Effect of the blue pigment produced by the tropical diatom Haslea nusantara on marine organisms from different trophic levels and its bioactivity. Aquac Rep, 2020; 17:100389. https://doi.org/10.1016/j.aqrep.2020.100389

Queiroz MI, Vieira JG, Maroneze MM. Morphophysiological, structural, and metabolic aspects of microalgae. Elsevier Inc., 2020. https://doi.org/10.1016/B978-0-12-818536-0.00002-6

Rasmussen HE, Blobaum KR, Park YK, Ehlers SJ, Lu F, Lee JY. Lipid extract of Nostoc commune var. sphaeroides Kützing, a blue-green alga, inhibits the activation of sterol regulatory element binding proteins in HepG2 cells. J Nutr, 2008; 138(3):476-81. https://doi.org/10.1093/jn/138.3.476

Ravi M, Tentu S, Baskar G, Rohan Prasad S, Raghavan S, Jayaprakash P, Jeyakanthan J, Rayala SK, Venkatraman G. Molecular mechanism of anti-cancer activity of phycocyanin in triple-negative breast cancer cells. BMC Cancer, 2015; 15(1):1-13. https://doi.org/10.1186/s12885-015-1784-x

Rizo J, Sari L, Qi Y, Im W, Lin MM. All-atom molecular dynamics simulations of Synaptotagmin-SNARE-complexin complexes bridging a vesicle and a flat lipid bilayer. eLife, 2022; 11:1-28. https://doi.org/10.7554/eLife.76356

Sosman JA, Kim KB, Schuchter L, Gonzalez R, Pavlick AC, Weber JS, McArthur GA, Hutson TE, Moschos SJ, Flaherty KT, Hersey P, Kefford R, Lawrence D, Puzanov I, Lewis KD, Amaravadi RK, Chmielowski B, Lawrence HJ, Shyr Y, Ye F, Li J, Nolop KB, Lee RJ, Joe AK, Ribas A. survival in BRAF V600-mutant advanced melanoma treated with vemurafenib. N Engl J Med, 2012; 366(8):707-14. https://doi.org/10.1056/NEJMoa1112302

Tang HSC, Chen YC. Insight into molecular dynamics simulation of BRAF(V600E) and potent novel inhibitors for malignant melanoma. Int J Nanomed, 2015; 10:3131-46. https://doi.org/10.2147/IJN.S80150

Tao X, Huang Y, Wang C, Chen F, Yang L, Ling L, Che Z, Chen X. Recent developments in molecular docking technology applied in food science: a review. Int J Food Sci Technol, 2020; 55(1):33-45. https://doi.org/10.1111/ijfs.14325

Tripathi R, Shalini R, Singh RK. Prophyletic origin of algae as potential repository of anticancer compounds. Evolutionary diversity as a source for anticancer molecules. Academic Press, pp 155-89, 2021. https://doi.org/10.1016/B978-0-12-821710-8.00007-2

Tuveson DA, Weber BL, Herlyn M. BRAF as a potential therapeutic target in melanoma and other malignancies. Cancer Cell, 2003; 4(2):95-8. https://doi.org/10.1016/S1535-6108(03)00189-2

Umar AB, Uzairu A, Shallangwa GA, Uba S. Molecular docking strategy to design novel V600E-BRAF kinase inhibitors with prediction of their drug-likeness and pharmacokinetics ADMET properties. Chem Afr, 2021; 4(1):189-205. https://doi.org/10.1007/s42250-020-00200-0

Volkman JK, Barrett SM, Dunstan GA, Jeffrey SW. Sterol biomarkers for microalgae from the green algal class Prasinophyceae. Org Geochem, 1994; 21(12):1211-8. https://doi.org/10.1016/0146-6380(94)90164-3

Walmsley RM, Billinton N. How accurate is in vitro prediction of carcinogenicity? Br J Pharmacol, 2011; 162(6):1250-8. https://doi.org/10.1111/j.1476-5381.2010.01131.x

Wan PT, Garnett MJ, Roe SM, Lee S, Niculescu-Duvaz D, Good VM, Jones CM, Marshall CJ, Springer CJ, Barford D, Marais R, Cancer Genome Project. Mechanism of activation of the RAF-ERK signaling pathway by oncogenic mutations of B-RAF. Cell, 2004; 116(6):855-67. https://doi.org/10.1016/S0092-8674(04)00215-6

Wang GM, Wang X, Zhu JM, Guo BB, Yang Z, Xu ZJ, Li B, Wang HY, Meng LH, Zhu WL, Ding J. Docking-based structural splicing and reassembly strategy to develop novel deazapurine derivatives as potent B-Raf V600E inhibitors. Acta Pharmacol Sin, 2017; 38:1059-68. https://doi.org/10.1038/aps.2016.173

Webb B, Sali A. Comparative protein structure modeling using MODELLER. Curr Protoc Bioinformatics, 2016; 2016:5.6.1-37. https://doi.org/10.1002/cpbi.3

Wu B, Zhang Z, Dou G, Lv X, Ge J, Wang H, Xie H, Zhu D. Novel natural inhibitors targeting B-RAF(V600E) by computational study. Bioengineered, 2021; 12(1):2970-83. https://doi.org/10.1080/21655979.2021.1943113

Wu CH, Arighi C, Ross K. Protein bioinformatics: from protein modifications and networks to proteomics. Methods in molecular biology. Humana Press, New York, NY, vol. 1558, p 472, 2017. https://doi.org/10.1007/978-1-4939-6783-4

Wu Y, Wang G. Machine learning based toxicity prediction: from chemical structural description to transcriptome analysis. Int J Mol Sci, 2018; 19(8):2358. https://doi.org/10.3390/ijms19082358

Yang F, Li B, Chu XM, Lv CY, Xu YJ, Yang P. Molecular mechanism of inhibitory effects of C-phycocyanin combined with all-trans-retinoic acid on the growth of HeLa cells in vitro. Tumor Biol, 2014; 35(6):5619-28. https://doi.org/10.1007/s13277-014-1744-0

Yang Y, Shi CY, Xie J, Dai JH, He SL, Tian Y. Identification of potential dipeptidyl peptidase (DPP)-IV inhibitors among moringa oleifera phytochemicals by virtual screening, molecular docking analysis, ADME/ T-based prediction, and in vitro analyses. Molecules, 2020; 25(1):189. https://doi.org/10.3390/molecules25010189

Yasukawa K, Akihisa T, Kanno H, Kaminaga T, Izumida M, Sakoh T, Tamura T, Takido M. Inhibitory effects of sterols isolated from Chlorella vulgaris on 12-0-tetradecanoylphorbol-13-acetate-induced inflammation and tumor promotion in mouse skin. Biol Pharm Bull, 1996; 19(4):573-6. https://doi.org/10.1248/bpb.19.573

Yu M, Tan P, Ye Y, Voneshen DJ, Xing X, Hong L. One-dimensional nature of protein low-energy vibrations. Phys Rev Res, 2020; 2(3):1-6. https://doi.org/10.1103/PhysRevResearch.2.032050

Zhang W, Qiu KX, Yu F, Xie XG, Zhang SQ, Chen YJ, Xie HD. Virtual screening of B-Raf kinase inhibitors: a combination of pharmacophore modelling, molecular docking, 3D-QSAR model and binding free energy calculation studies. Comput Biol Chem, 2017; 70:186- 90. https://doi.org/10.1016/j.compbiolchem.2017.08.017

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