Exploring the Antimicrobial Properties Against Human Pathogens and Mode of Action of Various Extracts from Fredolia aretioides, an Endemic Medicinal Plant of Morocco and Algeria

Author(s): Btissam Bouchal, Mounia Elidrissi Errahhali, Manal Elidrissi Errahhali, Redouane Boulouiz, Meryem Ouarzane, Mariam Tajir, Katsuyoshi Matsunami, Mohammed Bellaoui*.

Journal Name: The Natural Products Journal

Volume 9 , Issue 4 , 2019

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Graphical Abstract:


Abstract:

Background: Developing new antimicrobial medicines is one of the strategic objectives of the global action plan adopted by the World Health Organization to tackle antimicrobial resistance.

Objective: Considering the fact that natural products derived from medicinal plants are an important source for discovering new antimicrobial compounds, we investigated here the antimicrobial properties and the mode of action of various extracts from Fredolia aretioides, an endemic medicinal plant of Morocco and Algeria, and belonging to the Chenopodiaceae family.

Methods: Various extracts from F. aretioides were prepared and evaluated for their antibacterial activity against six bacterial species, and their antifungal activity against five fungi species. Chemicalgenetic screens were performed using a collection of Saccharomyces cerevisiae viable haploid deletion mutants spanning diverse biological processes.

Results: The diethyl ether extract of roots was found to be active against Citobacter freundii, with a MIC of 400 µg/ml. Hydro-methanol, methanol and residual extracts from aerial parts and roots were active against all five fungi species tested. Our results showed that residual extracts were the most effective against the fungi tested. Residual extract from aerial parts was more potent than the residual root extract, with IC50’s of 60 µg/ml and 440 µg/ml, respectively. Chemical-genetic analysis in S. cerevisiae revealed that residual extracts might affect fatty acid and sphingolipid biosynthesis.

Conclusion: All these findings suggest that F. aretioides is a promising source for the isolation of novel antimicrobial agents with novel mechanisms of action against human pathogens.

Keywords: Fredolia aretioides, antibacterial, antifungal, chemical-genetic, sphingolipid, pathogens.

[1]
Jones, K.E.; Patel, N.G.; Levy, M.A.; Storeygard, A.; Balk, D.; Gittleman, J.L.; Daszak, P. Global trends in emerging infectious diseases. Nature, 2008, 451(7181), 990-993.
[http://dx.doi.org/10.1038/nature06536] [PMID: 18288193]
[2]
Dikid, T.; Jain, S.K.; Sharma, A.; Kumar, A.; Narain, J.P. Emerging & re-emerging infections in India: An overview. Indian J. Med. Res., 2013, 138(1), 19-31.
[PMID: 24056553]
[3]
Smith, K.F.; Goldberg, M.; Rosenthal, S.; Carlson, L.; Chen, J.; Chen, C.; Ramachandran, S. Global rise in human infectious disease outbreaks. J. R. Soc. Interface, 2014, 11(101)20140950
[http://dx.doi.org/10.1098/rsif.2014.0950] [PMID: 25401184]
[4]
Glaziou, P.; Floyd, K.; Raviglione, M.C. Global epidemiology of tuberculosis. Semin. Respir. Crit. Care Med., 2018, 39(3), 271-285.
[http://dx.doi.org/10.1055/s-0038-1651492] [PMID: 30071543]
[5]
Chilton, C.H.; Pickering, D.S.; Freeman, J. Microbiologic factors affecting Clostridium difficile recurrence. Clin. Microbiol. Infect., 2018, 24(5), 476-482.
[http://dx.doi.org/10.1016/j.cmi.2017.11.017] [PMID: 29208562]
[6]
Pillar, C.M.; Draghi, D.C.; Sheehan, D.J.; Sahm, D.F. Prevalence of multidrug-resistant, methicillin-resistant Staphylococcus aureus in the United States: Findings of the stratified analysis of the 2004 to 2005 LEADER Surveillance Programs. Diagn. Microbiol. Infect. Dis., 2008, 60(2), 221-224.
[http://dx.doi.org/10.1016/j.diagmicrobio.2007.08.007] [PMID: 17976944]
[7]
Tacconelli, E. Antimicrobial use: Risk driver of multidrug resistant microorganisms in healthcare settings. Curr. Opin. Infect. Dis., 2009, 22(4), 352-358.
[http://dx.doi.org/10.1097/QCO.0b013e32832d52e0] [PMID: 19461514]
[8]
Davies, J.; Davies, D. Origins and evolution of antibiotic resistance. Microbiol. Mol. Biol. Rev., 2010, 74(3), 417-433.
[http://dx.doi.org/10.1128/MMBR.00016-10] [PMID: 20805405]
[9]
Pendleton, J.N.; Gorman, S.P.; Gilmore, B.F. Clinical relevance of the ESKAPE pathogens. Expert Rev. Anti Infect. Ther., 2013, 11(3), 297-308.
[http://dx.doi.org/10.1586/eri.13.12] [PMID: 23458769]
[10]
Gandra, S.; Barter, D.M.; Laxminarayan, R. Economic burden of antibiotic resistance: How much do we really know? Clin. Microbiol. Infect., 2014, 20(10), 973-980.
[http://dx.doi.org/10.1111/1469-0691.12798] [PMID: 25273968]
[11]
Watkins, R.R.; Bonomo, R.A. Overview: Global and local impact of antibiotic resistance. Infect. Dis. Clin. North Am., 2016, 30(2), 313-322.
[http://dx.doi.org/10.1016/j.idc.2016.02.001] [PMID: 27208761]
[12]
Ravensbergen, S.J.; Lokate, M.; Cornish, D.; Kloeze, E.; Ott, A.; Friedrich, A.W.; Van Hest, R.; Akkerman, O.W.; De Lange, W.C.; Van der Werf, T.S.; Bathoorn, E.; Stienstra, Y. High prevalence of infectious diseases and drug-resistant microorganisms in asylum seekers admitted to hospital; No carbapenemase producing enterobacteriaceae until September 2015. PLoS One, 2016, 11(5)e0154791
[http://dx.doi.org/10.1371/journal.pone.0154791] [PMID: 27144599]
[13]
Tao, N.N.; He, X.C.; Zhang, X.X.; Liu, Y.; Yu, C.B.; Li, H.C. Drug-resistant tuberculosis among children, China, 2006-2015. Emerg. Infect. Dis., 2017, 23(11), 1800-1805.
[http://dx.doi.org/10.3201/eid2311.170234] [PMID: 29047424]
[14]
La Fauci, V.; Alessi, V. Antibiotic resistance: Where are we going? Ann. Ig., 2018, 30(4), 52-57.
[PMID: 30062381]
[15]
Enoch, D.A.; Ludlam, H.A.; Brown, N.M. Invasive fungal infections: A review of epidemiology and management options. J. Med. Microbiol., 2006, 55(Pt 7), 809-818.
[http://dx.doi.org/10.1099/jmm.0.46548-0] [PMID: 16772406]
[16]
Vandeputte, P.; Ferrari, S.; Coste, A.T. Antifungal resistance and new strategies to control fungal infections. Int. J. Microbiol., 2012, 2012713687
[http://dx.doi.org/10.1155/2012/713687] [PMID: 22187560]
[17]
Pfaller, M.A. Antifungal drug resistance: Mechanisms, epidemiology, and consequences for treatment. Am. J. Med., 2012, 125(1), S3-S13.
[http://dx.doi.org/10.1016/j.amjmed.2011.11.001] [PMID: 22196207]
[18]
Hope, W.; Natarajan, P.; Goodwin, L. Invasive fungal infections. Clin. Med. (Lond.), 2013, 13(5), 507-510.
[http://dx.doi.org/10.7861/clinmedicine.13-5-507] [PMID: 24115712]
[19]
Wiederhold, N.P.; Patterson, T.F. Emergence of azole resistance in Aspergillus. Semin. Respir. Crit. Care Med., 2015, 36(5), 673-680.
[http://dx.doi.org/10.1055/s-0035-1562894] [PMID: 26398534]
[20]
Perlin, D.S. Mechanisms of echinocandin antifungal drug resistance. Ann. N. Y. Acad. Sci., 2015, 1354(1), 1-11.
[http://dx.doi.org/10.1111/nyas.12831] [PMID: 26190298]
[21]
Chowdhary, A.; Voss, A.; Meis, J.F. Multidrug-resistant Candida auris: ‘New kid on the block’ in hospital-associated infections? J. Hosp. Infect., 2016, 94(3), 209-212.
[http://dx.doi.org/10.1016/j.jhin.2016.08.004] [PMID: 27634564]
[22]
Salari, S.; Khosravi, A.R.; Mousavi, S.A.; Nikbakht-Brojeni, G.H. Mechanisms of resistance to fluconazole in Candida albicans clinical isolates from Iranian HIV-infected patients with oropharyngeal candidiasis. J. Mycol. Med., 2016, 26(1), 35-41.
[http://dx.doi.org/10.1016/j.mycmed.2015.10.007] [PMID: 26627124]
[23]
Perlin, D.S.; Rautemaa-Richardson, R.; Alastruey-Izquierdo, A. The global problem of antifungal resistance: Prevalence, mechanisms, and management. Lancet Infect. Dis., 2017, 17(12), e383-e392.
[http://dx.doi.org/10.1016/S1473-3099(17)30316-X] [PMID: 28774698]
[24]
Limper, A.H.; Adenis, A.; Le, T.; Harrison, T.S. Fungal infections in HIV/AIDS. Lancet Infect. Dis., 2017, 17(11), e334-e343.
[http://dx.doi.org/10.1016/S1473-3099(17)30303-1] [PMID: 28774701]
[25]
Denning, D.W.; Kneale, M.; Sobel, J.D.; Rautemaa-Richardson, R. Global burden of recurrent vulvovaginal candidiasis: A systematic review. Lancet Infect. Dis., 2018, 18(11), e339-e347.
[http://dx.doi.org/10.1016/S1473-3099(18)30103-8] [PMID: 30078662]
[26]
O’Neill, J. The review on antimicrobial resistance.Antimicrobial resistance: Tackling a crisis for the health and wealth of nations; Antimicrobial Resistance: London, 2014.
[27]
World Health Organization. Global action plan on antimicrobial resistance. Available from:,, http://www.who.int/iris/handle/10665/ 193736 (Accessed June 21, 2018)
[28]
Tacconelli, E.; Peschel, A.; Autenrieth, I.B. Translational research strategy: An essential approach to fight the spread of antimicrobial resistance. J. Antimicrob. Chemother., 2014, 69(11), 2889-2891.
[http://dx.doi.org/10.1093/jac/dku244] [PMID: 25011653]
[29]
Fedorenko, V.; Genilloud, O.; Horbal, L.; Marcone, G.L.; Marinelli, F.; Paitan, Y.; Ron, E.Z. Antibacterial discovery and development: From gene to product and back. BioMed Res. Int., 2015, 2015591349
[http://dx.doi.org/10.1155/2015/591349] [PMID: 26339625]
[30]
Gibbons, S. Plants as a source of bacterial resistance modulators and anti-infective agents. Phytochem. Rev., 2005, 4(1), 63-78.
[http://dx.doi.org/10.1007/s11101-005-2494-9]
[31]
Arif, T.; Bhosale, J.D.; Kumar, N.; Mandal, T.K.; Bendre, R.S.; Lavekar, G.S.; Dabur, R. Natural products-antifungal agents derived from plants. J. Asian Nat. Prod. Res., 2009, 11(7), 621-638.
[http://dx.doi.org/10.1080/10286020902942350] [PMID: 20183299]
[32]
Taye, B.; Giday, M.; Animut, A.; Seid, J. Antibacterial activities of selected medicinal plants in traditional treatment of human wounds in Ethiopia. Asian Pac. J. Trop. Biomed., 2011, 1(5), 370-375.
[http://dx.doi.org/10.1016/S2221-1691(11)60082-8] [PMID: 23569795]
[33]
Martins, N.; Barros, L.; Henriques, M.; Silva, S.; Ferreira, I.C. Activity of phenolic compounds from plant origin against Candida species. Ind. Crops Prod., 2015, 2015(74), 648-670.
[http://dx.doi.org/10.1016/j.indcrop.2015.05.067]
[34]
Vu, T.T.; Kim, H.; Tran, V.K.; Le Dang, Q.; Nguyen, H.T.; Kim, H.; Kim, I.S.; Choi, G.J.; Kim, J.C. In vitro antibacterial activity of selected medicinal plants traditionally used in Vietnam against human pathogenic bacteria. BMC Complement. Altern. Med., 2016, 16, 32.
[http://dx.doi.org/10.1186/s12906-016-1007-2] [PMID: 26819218]
[35]
Swamy, M.K.; Akhtar, M.S.; Sinniah, U.R. Antimicrobial properties of plant essential oils against human pathogens and their mode of action: An updated review. Evid. Based Complement. Alternat. Med., 2016, 20163012462
[http://dx.doi.org/10.1155/2016/3012462] [PMID: 28090211]
[36]
Dongmo, W.; Kechia, F.; Tchuenguem, R.; Nangwat, C.; Yves, I.; Kuiate, J.R.; Dzoyem, J.P. In vitro antifungal susceptibility of environmental isolates of Cryptococcus spp. from the west region of Cameroon. Ethiop. J. Health Sci., 2016, 26(6), 555-560.
[http://dx.doi.org/10.4314/ejhs.v26i6.8] [PMID: 28450771]
[37]
Soberón, J.R.; Sgariglia, M.A.; Pastoriza, A.C.; Soruco, E.M.; Jäger, S.N.; Labadie, G.R.; Sampietro, D.A.; Vattuone, M.A. Antifungal activity and cytotoxicity of extracts and triterpenoid saponins obtained from the aerial parts of Anagallis arvensis L. J. Ethnopharmacol., 2017, 203(203), 233-240.
[http://dx.doi.org/10.1016/j.jep.2017.03.056] [PMID: 28389355]
[38]
Lamola, S.M.; Dzoyem, J.P.; Botha, F.; Van Wyk, C. Anti-bacterial, free radical scavenging activity and cytotoxicity of acetone extracts of Grewia flava. Afr. Health Sci., 2017, 17(3), 790-796.
[http://dx.doi.org/10.4314/ahs.v17i3.22] [PMID: 29085407]
[39]
Lu, M.; Li, T.; Wan, J.; Li, X.; Yuan, L.; Sun, S. Antifungal effects of phytocompounds on Candida species alone and in combination with fluconazole. Int. J. Antimicrob. Agents, 2017, 49(2), 125-136.
[http://dx.doi.org/10.1016/j.ijantimicag.2016.10.021] [PMID: 28040409]
[40]
Barbieri, R.; Coppo, E.; Marchese, A.; Daglia, M.; Sobarzo-Sánchez, E.; Nabavi, S.F.; Nabavi, S.M. Phytochemicals for human disease: An update on plant-derived compounds antibacterial activity. Microbiol. Res., 2017, 196, 44-68.
[http://dx.doi.org/10.1016/j.micres.2016.12.003] [PMID: 28164790]
[41]
Romha, G.; Admasu, B.; Hiwot Gebrekidan, T.; Aleme, H.; Gebru, G. Antibacterial activities of five medicinal plants in Ethiopia against some human and animal pathogens. Evid. Based Complement. Alternat. Med., 2018, 20182950758
[http://dx.doi.org/10.1155/2018/2950758] [PMID: 29552081]
[42]
Fennane, M.; Tattou, M.I. Statistiques et commentaires sur l’inventaire actuel de la flore vasculaire du Maroc. Bulletin de l’Institut Scientifique, 2012, 34(1), 1-9.
[43]
Alves-Silva, J.M.; Romane, A.; Efferth, T.; Salgueiro, L. North African medicinal plants traditionally used in cancer therapy. Front. Pharmacol., 2017, 8, 383.
[http://dx.doi.org/10.3389/fphar.2017.00383] [PMID: 28694778]
[44]
Barkaoui, M.; Katiri, A.; Boubaker, H.; Msanda, F. Ethnobotanical survey of medicinal plants used in the traditional treatment of diabetes in Chtouka Ait Baha and Tiznit (Western Anti-Atlas), Morocco. J. Ethnopharmacol., 2017, 198, 338-350.
[http://dx.doi.org/10.1016/j.jep.2017.01.023] [PMID: 28109915]
[45]
Jamila, F.; Mostafa, E. Ethnobotanical survey of medicinal plants used by people in Oriental Morocco to manage various ailments. J. Ethnopharmacol., 2014, 154(1), 76-87.
[http://dx.doi.org/10.1016/j.jep.2014.03.016] [PMID: 24685583]
[46]
Bouyahya, A.; Abrini, J.; Et-Touys, A.; Bakri, Y.; Dakka, N. Indigenous knowledge of the use of medicinal plants in the North-West of Morocco and their biological activities. Eur. J. Integr. Med., 2017, 13, 9-25.
[http://dx.doi.org/10.1016/j.eujim.2017.06.004]
[47]
El-Rhaffari, L.; Zaid, A. Pratique de la phytothérapie dans le sud-est du Maroc (Tafilalet). Un savoir empirique pour une pharmacopée rénovée. From the sources of knowledge to the medicines of the future. Proceedings of the 4th European Congress on Ethnopharmocology, Tafilalt, Morocco2002, pp. 293-318.
[48]
Farid, O.; Hajji, L.; Eddouks, M. Aqueous extract of Anabasis aretioides ameliorates streptozotocin induced diabetes mellitus in rats. Nat. Prod. J., 2018, 8(2), 139-146.
[http://dx.doi.org/10.2174/2210315507666170927163450]
[49]
Cheriti, A.; Talhi, M.F.; Belboukhari, N.; Taleb, S. Copper ions biosorption properties of biomass derived from Algerian Sahara plants, Expanding issues in desalination, Robert Y. Ning, In: Tech Open. Available from: https://www.intechopen.com/books/expanding-issues-in-desalination/copper-ions-biosorption-properties-of-biomass-derived-from-algerian-sahara-plants
[50]
Abrigach, F.; Bouchal, B.; Riant, O.; Macé, Y.; Takfaoui, A.; Radi, S.; Oussaid, A.; Bellaoui, M.; Touzani, R. New, N. N. N′, N′-tetradentate pyrazoly agents: Synthesis and evaluation of their antifungal and antibacterial activities. Med. Chem., 2016, 12(1), 83-89.
[http://dx.doi.org/10.2174/1573406411666150519111800] [PMID: 25985861]
[51]
Biyiti, L.; Meko’o, D.; Tamzc, V.; Amvam Zollo, P. Recherche de l’activité antibactérienne de quatre plantes médicinales camerounaises. Pharm. Med. Trad. Afr., 2004, 13, 11-20.
[52]
Ennadir, J.; Hassikou, R.; Bouazza, F.; Arahou, M.; Al Askari, G.; Khedid, K. Évaluation in vitro de l’activité antibactérienne des extraits aqueux et organiques des graines de Nigella sativa L. et de Foeniculum vulgare Mill. Phytotherapie, 2014, 12(5), 302-308.
[http://dx.doi.org/10.1007/s10298-014-0885-z]
[53]
Bendaha, H.; Yu, L.; Touzani, R.; Souane, R.; Giaever, G.; Nislow, C.; Boone, C.; El-Kadiri, S.; Brown, G.W.; Bellaoui, M. New azole antifungal agents with novel modes of action: Synthesis and biological studies of new tridentate ligands based on pyrazole and triazole. Eur. J. Med. Chem., 2011, 46(9), 4117-4124.
[http://dx.doi.org/10.1016/j.ejmech.2011.06.012] [PMID: 21723647]
[54]
Yu, L.; Lopez, A.; Anaflous, A.; El-Bali, B.; Hamal, A.; Ericson, E.; Heisler, L.E.; McQuibban, A.; Giaever, G.; Nislow, C.; Boone, C.; Brown, G.W.; Bellaoui, M. Chemical-genetic profiling of imidazo[1,2-a]pyridines and -pyrimidines reveals target pathways conserved between yeast and human cells. PLoS Genet., 2008, 4(11)e1000284
[http://dx.doi.org/10.1371/journal.pgen.1000284] [PMID: 19043571]
[55]
Winzeler, E.A.; Shoemaker, D.D.; Astromoff, A.; Liang, H.; Anderson, K.; Andre, B.; Bangham, R.; Benito, R.; Boeke, J.D.; Bussey, H.; Chu, A.M.; Connelly, C.; Davis, K.; Dietrich, F.; Dow, S.W.; El-Bakkoury, M.; Foury, F.; Friend, S.H.; Gentalen, E.; Giaever, G.; Hegemann, J.H.; Jones, T.; Laub, M.; Liao, H.; Liebundguth, N.; Lockhart, D.J.; Lucau-Danila, A.; Lussier, M.; M’Rabet, N.; Menard, P.; Mittmann, M.; Pai, C.; Rebischung, C.; Revuelta, J.L.; Riles, L.; Roberts, C.J.; Ross-MacDonald, P.; Scherens, B.; Snyder, M.; Sookhai-Mahadeo, S.; Storms, R.K.; Véronneau, S.; Voet, M.; Volckaert, G.; Ward, T.R.; Wysocki, R.; Yen, G.S.; Yu, K.; Zimmermann, K.; Philippsen, P.; Johnston, M.; Davis, R.W. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science, 1999, 285(5429), 901-906.
[http://dx.doi.org/10.1126/science.285.5429.901] [PMID: 10436161]
[56]
Ríos, J.L.; Recio, M.C. Medicinal plants and antimicrobial activity. J. Ethnopharmacol., 2005, 100(1-2), 80-84.
[http://dx.doi.org/10.1016/j.jep.2005.04.025] [PMID: 15964727]
[57]
Cos, P.; Vlietinck, A.J.; Berghe, D.V.; Maes, L. Anti-infective potential of natural products: How to develop a stronger in vitro ‘proof-of-concept’. J. Ethnopharmacol., 2006, 106(3), 290-302.
[http://dx.doi.org/10.1016/j.jep.2006.04.003] [PMID: 16698208]
[58]
Bentabet, N.; Boucherit-Otmani, Z.; Boucherit, K. Composition chimique et activité antioxydante d’extraits organiques des racines de Fredolia aretioides de la région de Béchar en Algérie. Phytotherapie, 2014, 12(6), 364-371.
[http://dx.doi.org/10.1007/s10298-014-0834-x]
[59]
Parsons, A.B.; Lopez, A.; Givoni, I.E.; Williams, D.E.; Gray, C.A.; Porter, J.; Chua, G.; Sopko, R.; Brost, R.L.; Ho, C.H.; Wang, J.; Ketela, T.; Brenner, C.; Brill, J.A.; Fernandez, G.E.; Lorenz, T.C.; Payne, G.S.; Ishihara, S.; Ohya, Y.; Andrews, B.; Hughes, T.R.; Frey, B.J.; Graham, T.R.; Andersen, R.J.; Boone, C. Exploring the mode-of-action of bioactive compounds by chemical-genetic profiling in yeast. Cell, 2006, 126(3), 611-625.
[http://dx.doi.org/10.1016/j.cell.2006.06.040] [PMID: 16901791]
[60]
Qaddouri, B.; Guaadaoui, A.; Bellirou, A.; Hamal, A.; Melhaoui, A.; Brown, G.W.; Bellaoui, M. The budding yeast Saccharomyces cerevisiae as a drug discovery tool to identify plant-derived natural products with anti-proliferative properties. Evid. Based Complement. Alternat. Med., 2011, 2011954140
[http://dx.doi.org/10.1093/ecam/nep069] [PMID: 19596744]
[61]
Andrusiak, K.; Piotrowski, J.S.; Boone, C. Chemical-genomic profiling: Systematic analysis of the cellular targets of bioactive molecules. Bioorg. Med. Chem., 2012, 20(6), 1952-1960.
[http://dx.doi.org/10.1016/j.bmc.2011.12.023] [PMID: 22261022]
[62]
Rubilar-Hernández, C.; Hicks, G.R.; Norambuena, L. Chemical genomics screening for biomodulators of endomembrane system trafficking. Methods Mol. Biol., 2014, 1209, 251-264.
[http://dx.doi.org/10.1007/978-1-4939-1420-3_19] [PMID: 25117289]
[63]
Chaillot, J.; Tebbji, F.; Remmal, A.; Boone, C.; Brown, G.W.; Bellaoui, M.; Sellam, A. The monoterpene carvacrol generates endoplasmic reticulum stress in the pathogenic fungus Candida albicans. Antimicrob. Agents Chemother., 2015, 59(8), 4584-4592.
[http://dx.doi.org/10.1128/AAC.00551-15] [PMID: 26014932]
[64]
García, R.; Botet, J.; Rodríguez-Peña, J.M.; Bermejo, C.; Ribas, J.C.; Revuelta, J.L.; Nombela, C.; Arroyo, J. Genomic profiling of fungal cell wall-interfering compounds: Identification of a common gene signature. BMC Genomics, 2015, 16, 683.
[http://dx.doi.org/10.1186/s12864-015-1879-4] [PMID: 26341223]
[65]
Suresh, S.; Schlecht, U.; Xu, W.; Bray, W.; Miranda, M.; Davis, R.W.; Nislow, C.; Giaever, G.; Lokey, R.S.; St Onge, R.P. Systematic mapping of chemical-genetic interactions in Saccharomyces cerevisiae Cold Spring Harb. Protoc 2016, 2016(9), pdbtop077701.,
[http://dx.doi.org/10.1101/pdb.top077701] [PMID: 27587783]
[66]
Suresh, S.; Schlecht, U.; Xu, W.; Miranda, M.; Davis, R.W.; Nislow, C.; Giaever, G.; St. Onge, R.P. Identification of chemicalgenetic interactions via parallel analysis of barcoded yeast strains. Cold Spring Harb. Protoc., 2016, 2016(9), pdb-rot088054.
[http://dx.doi.org/10.1101/pdb.prot088054] [PMID: 27587778]
[67]
Piotrowski, J.S.; Li, S.C.; Deshpande, R.; Simpkins, S.W.; Nelson, J.; Yashiroda, Y.; Barber, J.M.; Safizadeh, H.; Wilson, E.; Okada, H.; Gebre, A.A.; Kubo, K.; Torres, N.P.; LeBlanc, M.A.; Andrusiak, K.; Okamoto, R.; Yoshimura, M.; DeRango-Adem, E.; Van Leeuwen, J.; Shirahige, K.; Baryshnikova, A.; Brown, G.W.; Hirano, H.; Costanzo, M.; Andrews, B.; Ohya, Y.; Osada, H.; Yoshida, M.; Myers, C.L.; Boone, C. Functional annotation of chemical libraries across diverse biological processes. Nat. Chem. Biol., 2017, 13(9), 982-993.
[http://dx.doi.org/10.1038/nchembio.2436] [PMID: 28759014]
[68]
Mandala, S.M.; Thornton, R.A.; Frommer, B.R.; Curotto, J.E.; Rozdilsky, W.; Kurtz, M.B.; Giacobbe, R.A.; Bills, G.F.; Cabello, M.A.; Martín, I. The discovery of australifungin, a novel inhibitor of sphinganine N-acyltransferase from Sporormiella australis. Producing organism, fermentation, isolation, and biological activity. J. Antibiot. (Tokyo), 1995, 48(5), 349-356.
[http://dx.doi.org/10.7164/antibiotics.48.349] [PMID: 7797434]
[69]
Nickels, J.T.; Broach, J.R. A ceramide-activated protein phosphatase mediates ceramide-induced G1 arrest of Saccharomyces cerevisiae. Genes Dev., 1996, 10(4), 382-394.
[http://dx.doi.org/10.1101/gad.10.4.382] [PMID: 8600023]
[70]
Ogretmen, B.; Hannun, Y.A. Biologically active sphingolipids in cancer pathogenesis and treatment. Nat. Rev. Cancer, 2004, 4(8), 604-616.
[http://dx.doi.org/10.1038/nrc1411] [PMID: 15286740]
[71]
El-Alwani, M.; Wu, B.X.; Obeid, L.M.; Hannun, Y.A. Bioactive sphingolipids in the modulation of the inflammatory response. Pharmacol. Ther., 2006, 112(1), 171-183.
[http://dx.doi.org/10.1016/j.pharmthera.2006.04.004] [PMID: 16759708]
[72]
Huang, F.C. The role of sphingolipids on innate immunity to intestinal salmonella infection. Int. J. Mol. Sci., 2017, 18(8), 1720.
[http://dx.doi.org/10.3390/ijms18081720] [PMID: 28783107]
[73]
Ortega, J.A.; Arencibia, J.M.; La Sala, G.; Borgogno, M.; Bauer, I.; Bono, L.; Braccia, C.; Armirotti, A.; Girotto, S.; Ganesan, A.; De Vivo, M. Pharmacophore identification and scaffold exploration to discover novel, potent, and chemically stable inhibitors of acid ceramidase in melanoma Cells. J. Med. Chem., 2017, 60(13), 5800-5815.
[http://dx.doi.org/10.1021/acs.jmedchem.7b00472] [PMID: 28603987]
[74]
Abdjul, D.B.; Yamazaki, H.; Kanno, S.I.; Tomizawa, A.; Rotinsulu, H.; Wewengkang, D.S.; Sumilat, D.A.; Ukai, K.; Kapojos, M.M.; Namikoshi, M. An anti-mycobacterial bisfunctionalized sphingolipid and new bromopyrrole alkaloid from the Indonesian marine sponge Agelas sp. J. Nat. Med., 2017, 71(3), 531-536.
[http://dx.doi.org/10.1007/s11418-017-1085-6] [PMID: 28364227]
[75]
Zweerink, M.M.; Edison, A.M.; Wells, G.B.; Pinto, W.; Lester, R.L. Characterization of a novel, potent, and specific inhibitor of serine palmitoyltransferase. J. Biol. Chem., 1992, 267(35), 25032-25038.
[PMID: 1460005]
[76]
Olsen, I.; Jantzen, E. Sphingolipids in bacteria and fungi. Anaerobe, 2001, 7(2), 103-112.
[http://dx.doi.org/10.1006/anae.2001.0376]
[77]
Moye, Z.D.; Valiuskyte, K.; Dewhirst, F.E.; Nichols, F.C.; Davey, M.E. Synthesis of sphingolipids impacts survival of Porphyromonas gingivalis and the presentation of surface polysaccharides. Front. Microbiol., 2016, 7, 1919.
[http://dx.doi.org/10.3389/fmicb.2016.01919] [PMID: 27965646]


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VOLUME: 9
ISSUE: 4
Year: 2019
Page: [321 - 329]
Pages: 9
DOI: 10.2174/2210315509666190117144936
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