Natural Products and Bioprospecting    2024, Vol. 14 Issue (2) : 4-4     DOI: 10.1007/s13659-024-00439-x
ORIGINAL ARTICLES |
Petrosamine isolated from marine sponge Petrosia sp. demonstrates protection against neurotoxicity in vitro and in vivo
Joana Ribeiro1, Henrique Araújo-Silva1, Mário Fernandes1, Joilna Alves da Silva2, Francisco das Chagas L. Pinto3, Otília Deusdenia L. Pessoa3, Hélcio Silva Santos2,3, Jane Eire Silva Alencar de Menezes2, Andreia C. Gomes1
1. CBMA (Centre of Molecular and Environmental Biology)/Aquatic Research Network (ARNET) Associate Laboratory, Department of Biology, University of Minho, Campus de Gualtar, 4710-057, Braga, Portugal;
2. Program in Natural Sciences, Natural Products Chemistry Laboratory, State University of Ceará, Fortaleza, Ceará, Brazil;
3. Department of Organic and Inorganic Chemistry, Science Center, Federal University of Ceará, Fortaleza, Ceará, Brazil
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Abstract  According to The World Alzheimer Report 2023 by Alzheimer’s Disease International (ADI) estimates that 33 to 38.5 million people worldwide suffer from Alzheimer’s Disease (AD). A crucial hallmark associated with this disease is associated with the deficiency of the brain neurotransmitter acetylcholine, due to an affected acetylcholinesterase (AChE) activity. Marine organisms synthesize several classes of compounds, some of which exhibit significant AChE inhibition, such as petrosamine, a coloured pyridoacridine alkaloid. The aim of this work was to characterize the activity of petrosamine isolated for the first time from a Brazilian marine sponge, using two neurotoxicity models with aluminium chloride, as exposure to aluminium is associated with the development of neurodegenerative diseases. The in vitro model was based in a neuroblastoma cell line and the in vivo model exploited the potential of zebrafish (Danio rerio) embryos in mimicking hallmarks of AD. To our knowledge, this is the first report on petrosamine’s activity over these parameters, either in vitro or in vivo, in order to characterize its full potential for tackling neurotoxicity.
Keywords Petrosamine      Petrosia sp.      Neuroprotection      Aluminium-induced neurotoxicity     
Fund:This work was supported by the “Contrato-Programa” UIDB/04050/2020 funded by national funds through the FCT I.P. https://doi.org/10.54499/UIDB/04050/2020. MF (SFRH/BD/147819/2019) holds a scholarship from FCT. FUNCAP-INTERNACIONALIZAÇÃO (Grant ITR-0214-00060.01.00/23), CNPq-Universal (Grant 406119/2021-0).
Corresponding Authors: Jane Eire Silva Alencar de Menezes,E-mail:jane.menezes@uece.br;Andreia C. Gomes,E-mail:agomes@bio.uminho.pt     E-mail: jane.menezes@uece.br;agomes@bio.uminho.pt
Issue Date: 16 May 2024
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Joana Ribeiro
Henrique Araú
jo-Silva
rio Fernandes
Joilna Alves da Silva
Francisco das Chagas L. Pinto
Otí
lia Deusdenia L. Pessoa
lcio Silva Santos
Jane Eire Silva Alencar de Menezes
Andreia C. Gomes
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Joana Ribeiro,Henrique Araú,jo-Silva, et al. Petrosamine isolated from marine sponge Petrosia sp. demonstrates protection against neurotoxicity in vitro and in vivo[J]. Natural Products and Bioprospecting, 2024, 14(2): 4-4.
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http://npb.kib.ac.cn/EN/10.1007/s13659-024-00439-x     OR     http://npb.kib.ac.cn/EN/Y2024/V14/I2/4
[1] Wilson DM, Cookson MR, VanDen Bosch L, Zetterberg H, Holtzman DM, Dewachter I. Hallmarks of neurodegenerative diseases. Cell. 2023;186(4):693-714. https://doi.org/10.1016/j.cell.2022.12.032.
[2] Forrest SL, Kovacs GG. Current concepts of mixed pathologies in neurodegenerative diseases. Can J Neurol Sci. 2022. https://doi.org/10.1017/cjn.2022.34.
[3] Li X, Feng X, Sun X, Hou N, Han F, Liu Y. Global, regional, and national burden of Alzheimer’s disease and other dementias, 1990-2019. Front Aging Neurosci. 2022;14: 937486. https://doi.org/10.3389/fnagi.2022.937486.
[4] García-Ayllón M-S. Revisiting the role of acetylcholinesterase in Alzheimer’s disease: cross-talk with P-tau and β-amyloid. Front Mol Neurosci. 2011. https://doi.org/10.3389/fnmol.2011.00022.
[5] Marucci G, Buccioni M, Ben DD, Lambertucci C, Volpini R, Amenta F. Efficacy of acetylcholinesterase inhibitors in Alzheimer’s disease. Neuropharmacology. 2021;190: 108352. https://doi.org/10.1016/j.neuropharm.2020.108352.
[6] Sharma NS, Karan A, Lee D, Yan Z, Xie J. Advances in modeling Alzheimer’s disease in vitro. Adv NanoBiomed Res. 2021;1(12):2100097. https://doi.org/10.1002/anbr.202100097.
[7] Lima E, Medeiros J. Marine organisms as alkaloid biosynthesizers of potential anti-alzheimer agents. Mar Drugs. 2022;20(1):75. https://doi.org/10.3390/md20010075.
[8] Ibrahim SRM, Mohamed GA. Marine pyridoacridine alkaloids: biosynthesis and biological activities. Chem Biodivers. 2016;13(1):37-47. https://doi.org/10.1002/cbdv.201400434.
[9] Nukoolkarn VS, Saen-oon S, Rungrotmongkol T, Hannongbua S, Ingkaninan K, Suwanborirux K. Petrosamine, a potent anticholinesterase pyridoacridine alkaloid from a Thai marine sponge Petrosia n. sp. Bioorg Med Chem. 2008;16(13):6560-7. https://doi.org/10.1016/j.bmc.2008.05.027.
[10] Gartshore CJ, Wang X, Su Y, Molinski TF. Petrosamine. Revisited experimental and computational investigation of solvatochromism, tautomerism and free energy landscapes of a pyridoacridinium quaternary salt. Mar Drugs. 2023;21(8):446. https://doi.org/10.3390/md21080446.
[11] Konrath EL, Passos CDS, Klein-Júnior LC, Henriques AT. Alkaloids as a source of potential anticholinesterase inhibitors for the treatment of Alzheimer’s disease. J Pharm Pharmacol. 2013;65(12):1701-25. https://doi.org/10.1111/jphp.12090.
[12] Huat TJ, Camats-Perna J, Newcombe EA, Valmas N, Kitazawa M, Medeiros R. Metal toxicity links to Alzheimer’s disease and neuroinflammation. J Mol Biol. 2016;431(9):1843-68. https://doi.org/10.1016/j.jmb.2019.01.018.
[13] Wang Z, et al. Chronic exposure to aluminum and risk of Alzheimer’s disease: a meta-analysis. Neurosci Lett. 2016;610:200-6. https://doi.org/10.1016/j.neulet.2015.11.014.
[14] Kandimalla R, Vallamkondu J, Corgiat EB, Gill KD. Understanding aspects of aluminum exposure in Alzheimer’s disease development: aluminum exposure in Alzheimer’s disease. Brain Pathol. 2016;26(2):139-54. https://doi.org/10.1111/bpa.12333.
[15] Fish PV, Steadman D, Bayle ED, Whiting P. New approaches for the treatment of Alzheimer’s disease. Bioorg Med Chem Lett. 2019;29(2):125-33. https://doi.org/10.1016/j.bmcl.2018.11.034.
[16] Tatulian SA. Challenges and hopes for Alzheimer’s disease. Drug Discov Today. 2022;27(4):1027-43. https://doi.org/10.1016/j.drudis.2022.01.016.
[17] Cuerva JM, Cárdenas DJ, Echavarren AM. New synthesis of pyridoacridines based on an intramolecular aza-Diels-Alder reaction followed by an unprecedented rearrangement?. Chem Commun. 1999;17:1721-2. https://doi.org/10.1039/a905234h.
[18] Munekata PES, et al. Marine alkaloids: compounds with in vivo activity and chemical synthesis. Mar Drugs. 2021;19(7):374. https://doi.org/10.3390/md19070374.
[19] Monaco A, Grimaldi MC, Ferrandino I. Aluminium chloride-induced toxicity in zebrafish larvae. J Fish Dis. 2017;40(5):629-35. https://doi.org/10.1111/jfd.12544.
[20] De HPS, Cesário F, et al. Anxiolytic-like effect of brominated compounds from the marine sponge Aplysina fulva on adult zebrafish (Danio rerio): involvement of the GABAergic system. Neurochem Int. 2021;146: 105021. https://doi.org/10.1016/j.neuint.2021.105021.
[21] Drummond E, Wisniewski T. Alzheimer’s disease: experimental models and reality. Acta Neuropathol. 2017;133(2):155-75. https://doi.org/10.1007/s00401-016-1662-x.
[22] Goel P, Chakrabarti S, Goel K, Bhutani K, Chopra T, Bali S. Neuronal cell death mechanisms in Alzheimer’s disease: an insight. Front Mol Neurosci. 2022;15: 937133. https://doi.org/10.3389/fnmol.2022.937133.
[23] Mustafa Rizvi SH, Parveen A, Verma AK, Ahmad I, Arshad M, Mahdi AA. Aluminium induced endoplasmic reticulum stress mediated cell death in SH-SY5Y neuroblastoma cell line is independent of p53. PLoS ONE. 2014;9(5): e98409. https://doi.org/10.1371/journal.pone.0098409.
[24] Yang M-H, et al. Reduction of aluminum ion neurotoxicity through a small peptide application—NAP treatment of Alzheimer’s disease. J Food Drug Anal. 2019;27(2):551-64. https://doi.org/10.1016/j.jfda.2018.11.009.
[25] Biswas K, Alexander K, Francis MM. Reactive oxygen species: angels and demons in the life of a neuron. NeuroSci. 2022;3(1):130-45. https://doi.org/10.3390/neurosci3010011.
[26] Su L-J, et al. Reactive oxygen species-induced lipid peroxidation in apoptosis, autophagy, and ferroptosis. Oxid Med Cell Longev. 2019. https://doi.org/10.1155/2019/5080843.
[27] David B, Schneider P, Schäfer P, Pietruszka J, Gohlke H. Discovery of new acetylcholinesterase inhibitors for Alzheimer’s disease: virtual screening and in vitro characterisation. J Enzyme Inhibit Med Chem. 2021;36(1):491-6. https://doi.org/10.1080/14756366.2021.1876685.
[28] Kawahara M, Kato-Negishi M. Link between aluminum and the pathogenesis of Alzheimer’s disease: the integration of the aluminum and amyloid cascade hypotheses. Int J Alzheimer’s Dis. 2011. https://doi.org/10.4061/2011/276393.
[29] Kimmel CB, Ballard WW, Kimmel SR, Ullmann B, Schilling TF. Stages of embryonic development of the zebrafish. Dev Dyn. 1995;203(3):253-310. https://doi.org/10.1002/aja.1002030302.
[30] Capriello T, Monteiro SM, Félix LM, Donizetti A, Aliperti V, Ferrandino I. Apoptosis, oxidative stress and genotoxicity in developing zebrafish after aluminium exposure. Aquat Toxicol. 2021;236: 105872. https://doi.org/10.1016/j.aquatox.2021.105872.
[31] Bruce AEE. Zebrafish epiboly: spreading thin over the yolk. Dev Dyn. 2016;245(3):244-58. https://doi.org/10.1002/dvdy.24353.
[32] Sant KE, Timme-Laragy AR. Zebrafish as a model for toxicological perturbation of yolk and nutrition in the early embryo. Curr Environ Health Rpt. 2018;5(1):125-33. https://doi.org/10.1007/s40572-018-0183-2.
[33] Aldavood SJ, et al. Effect of cadmium and nickel exposure on early development in zebrafish (Danio rerio) embryos. Water. 2020;12(11):3005. https://doi.org/10.3390/w12113005.
[34] Santoso F, et al. An overview of methods for cardiac rhythm detection in zebrafish. Biomedicines. 2020;8(9):329. https://doi.org/10.3390/biomedicines8090329.
[35] Winbo A, Ashton JL, Montgomery JM. Neuroscience in the heart: recent advances in neurocardiac communication and its role in cardiac arrhythmias. Int J Biochem Cell Biol. 2020;122: 105737. https://doi.org/10.1016/j.biocel.2020.105737.
[36] Gouva E, Nathanailides C, Skoufos I, Paschos I, Athanassopoulou F, Pappas IS. Comparative study of the effects of heavy metals on embryonic development of zebrafish. Aquac Res. 2020;51(8):3255-67. https://doi.org/10.1111/are.14660.
[37] Manuel R, Iglesias Gonzalez AB, Habicher J, Koning HK, Boije H. Characterization of individual projections reveal that neuromasts of the zebrafish lateral line are innervated by multiple inhibitory efferent cells. Front Neuroanat. 2021;15: 666109. https://doi.org/10.3389/fnana.2021.666109.
[38] Closset M, Cailliau K, Slaby S, Marin M. Effects of aluminium contamination on the nervous system of freshwater aquatic vertebrates: a review. IJMS. 2021;23(1):31. https://doi.org/10.3390/ijms23010031.
[39] Senger MR, Seibt KJ, Ghisleni GC, Dias RD, Bogo MR, Bonan CD. Aluminum exposure alters behavioral parameters and increases acetylcholinesterase activity in zebrafish (Danio rerio) brain. Cell Biol Toxicol. 2011;27(3):199-205. https://doi.org/10.1007/s10565-011-9181-y.
[40] Oliveira VM, et al. Aluminium sulfate exposure: a set of effects on hydrolases from brain, muscle and digestive tract of juvenile Nile tilapia (Oreochromis niloticus). Comp Biochem Physiol C: Toxicol Pharmacol. 2017;191:101-8. https://doi.org/10.1016/j.cbpc.2016.10.002.
[41] Duan Z, et al. Barrier function of zebrafish embryonic chorions against microplastics and nanoplastics and its impact on embryo development. J Hazard Mater. 2020;395: 122621. https://doi.org/10.1016/j.jhazmat.2020.122621.
[42] Lin J, et al. Fucoxanthin, a marine carotenoid, reverses scopolamine-induced cognitive impairments in mice and inhibits acetylcholinesterase in vitro. Mar Drugs. 2016;14(4):67. https://doi.org/10.3390/md14040067.
[43] Pan H, et al. Fascaplysin derivatives are potent multitarget agents against Alzheimer’s disease: in vitro and in vivo evidence. ACS Chem Neurosci. 2019;10(11):4741-56. https://doi.org/10.1021/acschemneuro.9b00503.
[44] Nie Y, et al. Marine fungal metabolite butyrolactone I prevents cognitive deficits by relieving inflammation and intestinal microbiota imbalance on aluminum trichloride-injured zebrafish. J Neuroinflamm. 2022;19(1):39. https://doi.org/10.1186/s12974-022-02403-3.
[45] Vrabec R, Blunden G, Cahlíková L. Natural alkaloids as multi-target compounds towards factors implicated in Alzheimer’s disease. IJMS. 2023;24(5):4399. https://doi.org/10.3390/ijms24054399.
[46] Vitale RM, et al. In silico identification and experimental validation of novel anti-Alzheimer’s multitargeted ligands from a marine source featuring a “2-aminoimidazole plus aromatic group” scaffold. ACS Chem Neurosci. 2018;9(6):1290-303. https://doi.org/10.1021/acschemneuro.7b00416.
[47] Langjae R, Bussarawit S, Yuenyongsawad S, Ingkaninan K, Plubrukarn A. Acetylcholinesterase-inhibiting steroidal alkaloid from the sponge Corticium sp. Steroids. 2007;72(9-10):682-5. https://doi.org/10.1016/j.steroids.2007.05.005.
[48] Kowal NM, Di X, Omarsdottir S, Olafsdottir ES, Flustramine Q. A novel marine origin acetylcholinesterase inhibitor from Flustra foliacea. Fut Pharmacol. 2023;3(1):38-47. https://doi.org/10.3390/futurepharmacol3010003.
[49] Fernandes M, et al. Novel concept of exosome-like liposomes for the treatment of Alzheimer’s disease. J Control Release. 2021;336:130-43. https://doi.org/10.1016/j.jconrel.2021.06.018.
[50] Ellman GL, Courtney KD, Andres V, Featherstone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 1961;7(2):88-95. https://doi.org/10.1016/0006-2952(61)90145-9.
[51] Gravato C, Abe FR, de Oliveira DP, Soares AMVM, Domingues I. Acetylcholinesterase (AChE) activity in embryos of zebrafish. Toxicity assessment, 2240, In: Palmeira CMM, de Oliveira DP, Dorta DJ, editors. Methods in molecular biology, 2240. New York, NY: Springer US; 2021, pp. 119-124. https://doi.org/10.1007/978-1-0716-1091-6_10.
[52] Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes Text with EEA relevance.
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