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Protein & Peptide Letters

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ISSN (Print): 0929-8665
ISSN (Online): 1875-5305

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Research Article

Water-soluble Moringa oleifera Seed Lectin Exhibits Monoaminergic Pathway-linked Anti-depressive-like Effects in Mice

Author(s): Leydianne Leite de Siqueira Patriota*, Barbara Raíssa Ferreira de Lima, Amanda de Oliveira Marinho, Jainaldo Alves da Costa, Luana Cassandra Breitenbach Barroso Coelho, Moacyr Jesus Barreto de Melo Rêgo, Maira Galdino da Rocha Pitta, Patrícia Maria Guedes Paiva, Michelly Cristiny Pereira, Thiago Henrique Napoleão and Michelle Melgarejo da Rosa

Volume 30, Issue 12, 2023

Published on: 21 November, 2023

Page: [1048 - 1057] Pages: 10

DOI: 10.2174/0109298665270366231031052629

Price: $65

Abstract

Objectives: The present study investigated the anti-depressive-like (anti-immobility) effect of a lectin from Moringa oleifera seeds (WSMoL) in mice.

Methods: To evaluate an acute effect, the animals were treated with WSMoL (1, 2, and 4 mg/kg, i.p.) 30 min before the tail suspension test (TST). To investigate the involvement of monoaminergic and nitrergic signaling, the mice were pre-treated with selective antagonists. The role of the WSMoL carbohydrate-recognizing domain (CRD) was verified using previous blockage with casein (0.5 mg/mL). The subacute anti-immobility effect was also evaluated by administering WSMoL (1, 2, and 4 mg/kg, i.p.) once a day for 7 d. Finally, an open field test (OFT) was performed to identify possible interferences of WSMoL on animal locomotory behavior.

Results: WSMoL reduced the immobility time of mice in the TST at all doses, and combined treatment with fluoxetine (5 mg/kg, i.p.) and WSMoL (1 mg/kg) was also effective. The CRD appeared to be involved in the anti-immobility effect since the solution of WSMoL (4 mg/kg) pre-incubated with casein showed no activity. The lectin effect was prevented by the pre-treatment of mice with ketanserin, yohimbine, and SCH 23390, thereby demonstrating the involvement of monoaminergic pathways. In contrast, pre-treatment with L-NAME, aminoguanidine, and L-arginine did not interfere with lectin action. WSMoL exhibited a subacute effect in the TST, thereby reducing immobility time and increasing agitation time even on the seventh day. OFT data revealed that the anti-immobility effect was not caused by interference with locomotor behavior.

Conclusion: WSMoL elicits an anti-depressant-like effect that is dependent on monoaminergic signaling.

Keywords: Moringa oleifera, lectin, anti-immobility effect, tail suspension test, monoaminergic signaling, nitrergic signaling.

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Graphical Abstract

[1]
Van Dammes, E.J.M.; Fouquaert, E.; Lannoo, N.; Vandenborre, G.; Schouppe, D.; Peumans, W.J. Novel concepts about the role of lectins in the plant cell. Adv. Exp. Med. Biol., 2011, 705, 271-294.
[http://dx.doi.org/10.1007/978-1-4419-7877-6_13] [PMID: 21618113]
[2]
Fontenelle, T.P.C.; Lima, G.C.; Mesquita, J.X.; Lopes, J.L.S.; de Brito, T.V.; Vieira Júnior, F.C.; Sales, A.B.; Aragão, K.S.; Souza, M.H.L.P.; Barbosa, A.L.R.; Freitas, A.L.P. Lectin obtained from the red seaweed Bryothamnion triquetrum: Secondary structure and anti-inflammatory activity in mice. Int. J. Biol. Macromol., 2018, 112, 1122-1130.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.02.058] [PMID: 29452186]
[3]
Pires, A.F.; Marques, G.F.O.; Alencar, N.M.N.D.; Martins, M.G.Q.; Silva, M.T.L.D.; Nascimento, K.S.D.; Cavada, B.S.; Assreuy, A.M.S. Inhibitory effect of Lonchocarpus araripensis lectin in rat acute models of inflammation. An. Acad. Bras. Cienc., 2019, 91(2), e20180991.
[http://dx.doi.org/10.1590/0001-3765201920180991] [PMID: 31241705]
[4]
Leal, R.B.; Pinto-Junior, V.R.; Osterne, V.J.S.; Wolin, I.A.V.; Nascimento, A.P.M.; Neco, A.H.B.; Araripe, D.A.; Welter, P.G.; Neto, C.C.; Correia, J.L.A.; Rocha, C.R.C.; Nascimento, K.S.; Cavada, B.S. Crystal structure of DlyL, a mannose-specific lectin from Dioclea lasiophylla Mart. Ex Benth seeds that display cytotoxic effects against C6 glioma cells. Int. J. Biol. Macromol., 2018, 114, 64-76.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.03.080] [PMID: 29559315]
[5]
Cunha, C.R.A.; Silva, L.C.N.; Almeida, F.J.F.; Ferraz, M.S.; Varejão, N.; Cartaxo, M.F.S.; Miranda, R.C.M.; Aguiar, F.C.A.; Santos, N.P.S.; Coelho, L.C.B.B.; Santos-Magalhães, N.S.; Correia, M.T.S. Encapsulation into stealth liposomes enhances the anti- tumor action of recombinant Cratylia mollis lectin expressed in Escherichia coli. Front. Microbiol., 2016, 7, 1355.
[http://dx.doi.org/10.3389/fmicb.2016.01355] [PMID: 27695439]
[6]
de Freitas Pires, A.; Bezerra, M.M.; Amorim, R.M.F.; do Nascimento, F.L.F.; Marinho, M.M.; Moura, R.M.; Silva, M.T.L.; Correia, J.L.A.; Cavada, B.S.; Assreuy, A.M.S.; Nascimento, K.S. Lectin purified from Lonchocarpus campestris seeds inhibits inflammatory nociception. Int. J. Biol. Macromol., 2019, 125, 53-60.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.11.233] [PMID: 30500503]
[7]
Alves, S.M.; Freitas, R.S.; do Val, D.R.; Vieira, L.V.; de Assis, E.L.; Gomes, F.I.F.; Gadelha, C.A.A.; Gadelha, T.S.; de Lacerda, J.T.J.G.; Clemente-Napimoga, J.T.; Pinto, V.P.T.; Cristino Filho, G.; Bezerra, M.M.; Chaves, H.V. The efficacy of a lectin from Abelmoschus Esculentus depends on central opioid receptor activation to reduce temporomandibular joint hypernociception in rats. Biomed. Pharmacother., 2018, 101, 478-484.
[http://dx.doi.org/10.1016/j.biopha.2018.02.117] [PMID: 29501769]
[8]
Russi, M.A.; Vandresen-Filho, S.; Rieger, D.K.; Costa, A.P.; Lopes, M.W.; Cunha, R.M.S.; Teixeira, E.H.; Nascimento, K.S.; Cavada, B.S.; Tasca, C.I.; Leal, R.B. ConBr, a lectin from Canavalia brasiliensis seeds, protects against quinolinic acid-induced seizures in mice. Neurochem. Res., 2012, 37(2), 288-297.
[http://dx.doi.org/10.1007/s11064-011-0608-x] [PMID: 21948344]
[9]
Araújo, J.R.C.; Campos, A.R.; de Barros M V Damasceno, M.; Santos, S.A.A.R.; Ferreira, M.K.A.; de Azevedo Moreira, R.; de O Monteiro-Moreira, A.C. Neuropharmacological characterization of Dioclea altissima seed lectin (DAL) in mice: Evidence of anxiolytic- like effect mediated by serotonergic, GABAergic receptors and NO pathway. Curr. Pharm. Des., 2020, 26(31), 3895-3904. a
[http://dx.doi.org/10.2174/1381612826666200331093207] [PMID: 32228418]
[10]
Lima, B.R.F.; Patriota, L.L.S.; Marinho, A.O.; Costa, J.A.; Napoleão, T.H.; Rosa, M.M.; Paiva, P.M.G. The anxiolytic activity of Schinus terebinthifolia leaf lectin (SteLL) is dependent on monoaminergic signaling although independent of the carbohydrate-binding domain of the lectin. Pharmaceuticals, 2022, 15(11), 1364.
[http://dx.doi.org/10.3390/ph15111364] [PMID: 36355536]
[11]
Patriota, L.L.S.; de Lima, B.R.F.; Marinho, A.O.; da Costa, J.A.; Coelho, L.C.B.B.; Paiva, P.M.G.; da Rosa, M.M.; Napoleão, T.H. The anxiolytic-like activity of water-soluble Moringa oleifera Lam. lectin is mediated via serotoninergic, noradrenergic, and dopaminergic neurotransmission. Brain Disorders, 2023, 9, 100066.
[http://dx.doi.org/10.1016/j.dscb.2023.100066]
[12]
Araújo, J.R.C.; Coelho, C.B.; Campos, A.R.; de Azevedo Moreira, R.; de Oliveira Monteiro-Moreira, A.C. Animal galectins and plant lectins as tools for studies in neurosciences. Curr. Neuropharmacol., 2020, 18(3), 202-215. b
[http://dx.doi.org/10.2174/1570159X17666191016092221] [PMID: 31622208]
[13]
Raíssa Ferreira de Lima, B.; Leite de Siqueira Patriota, L.; de Oliveira Marinho, A.; Alves da Costa, J.; Henrique Napoleão, T.; Melgarejo da Rosa, M.; Maria Guedes Paiva, P. The lectin from Schinus terebinthifolia leaf (SteLL) reduces immobility of mice on the tail suspension test dependent on the monoaminergic and nitric oxide signaling. Neurosci. Lett., 2023, 801, 137092.
[http://dx.doi.org/10.1016/j.neulet.2023.137092] [PMID: 36690060]
[14]
Cavada, B.; Barbosa, T.; Arruda, S.; Grangeiro, T.; Barral-Netto, M. Revisiting proteus: Do minor changes in lectin structure matter in biological activity? Lessons from and potential biotechnological uses of the Diocleinae subtribe lectins. Curr. Protein Pept. Sci., 2001, 2(2), 123-135.
[http://dx.doi.org/10.2174/1389203013381152] [PMID: 12370020]
[15]
Yagi, H.; Kato, K. Functional roles of glycoconjugates in the maintenance of stemness and differentiation process of neural stem cells. Glycoconj. J., 2017, 34(6), 757-763.
[http://dx.doi.org/10.1007/s10719-016-9707-x] [PMID: 27350557]
[16]
de Moura, K.S.; da Silva, H.R.C.; Dornelles, L.P.; Coelho, L.C.B.B.; Napoleão, T.H.; de Oliveira, M.D.L.; Paiva, P.M.G. Coagulant activity of water-Soluble Moringa oleifera lectin is linked to lowering of electrical resistance and inhibited by monosaccharides and magnesium ions. Appl. Biochem. Biotechnol., 2016, 180(7), 1361-1371.
[http://dx.doi.org/10.1007/s12010-016-2172-y] [PMID: 27351986]
[17]
Coelho, J.S.; Santos, N.D.L.; Napoleão, T.H.; Gomes, F.S.; Ferreira, R.S.; Zingali, R.B.; Coelho, L.C.B.B.; Leite, S.P.; Navarro, D.M.A.F.; Paiva, P.M.G. Effect of Moringa oleifera lectin on development and mortality of Aedes aegypti larvae. Chemosphere, 2009, 77(7), 934-938.
[http://dx.doi.org/10.1016/j.chemosphere.2009.08.022] [PMID: 19747711]
[18]
Coriolano, M.C.; de Santana Brito, J.; de Siqueira Patriota, L.L.; de Araujo Soares, A.K.; de Lorena, V.M.B.; Paiva, P.M.G.; Napoleão, T.H.; Coelho, L.C.B.B.; de Melo, C.M.L. Immunomodulatory effects of the water-soluble lectin from moringa oleifera seeds (WSMoL) on human peripheral blood mononuclear cells (PBMC). Protein Pept. Lett., 2018, 25(3), 295-301.
[http://dx.doi.org/10.2174/0929866525666180130141736] [PMID: 29384049]
[19]
World Health Organization. Depressive disorder (depression) fact sheets; WHO: Geneva, 2023. Available from: https://www.who.int/ news-room/factsheets/detail/depression (cited 2023 Jul 1).
[20]
Ferrari, F.; Villa, R.F. The neurobiology of depression: An integrated overview from biological theories to clinical evidence. Mol. Neurobiol., 2017, 54(7), 4847-4865.
[http://dx.doi.org/10.1007/s12035-016-0032-y] [PMID: 27510505]
[21]
Mekonen, T.; Chan, G.C.K.; Connor, J.P.; Hides, L.; Leung, J. Estimating the global treatment rates for depression: A systematic review and meta-analysis. J. Affect. Disord., 2021, 295, 1234-1242.
[http://dx.doi.org/10.1016/j.jad.2021.09.038] [PMID: 34665135]
[22]
Laemmli, U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 1970, 227(5259), 680-685.
[http://dx.doi.org/10.1038/227680a0] [PMID: 5432063]
[23]
Lowry, O.; Rosebrough, N.; Farr, A.L.; Randall, R. Protein measurement with the Folin phenol reagent. J. Biol. Chem., 1951, 193(1), 265-275.
[http://dx.doi.org/10.1016/S0021-9258(19)52451-6] [PMID: 14907713]
[24]
de Siqueira Patriota, L.L.; Procópio, T.F.; de Santana Brito, J.; Sebag, V.; de Oliveira, A.P.S.; de Araújo Soares, A.K.; Moreira, L.R.; de Albuquerque Lima, T.; Soares, T.; da Silva, T.D.; Paiva, P.M.G.; de Lorena, V.M.B.; de Melo, C.M.L.; de Albuquerque, L.P.; Napoleão, T.H. Microgramma vacciniifolia (Polypodiaceae) fronds contain a multifunctional lectin with immunomodulatory properties on human cells. Int. J. Biol. Macromol., 2017, 103, 36-46.
[http://dx.doi.org/10.1016/j.ijbiomac.2017.05.037] [PMID: 28501598]
[25]
Steru, L.; Chermat, R.; Thierry, B.; Simon, P. The tail suspension test: A new method for screening antidepressants in mice. Psychopharmacology, 1985, 85(3), 367-370.
[http://dx.doi.org/10.1007/BF00428203] [PMID: 3923523]
[26]
Teegarden, S. Behavioral phenotyping in rats and mice. Mat. Meth., 2012, 2, 122.
[http://dx.doi.org/10.13070/mm.en.2.122]
[27]
Wang, Q.; Timberlake, M.A., II; Prall, K.; Dwivedi, Y. The recent progress in animal models of depression. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2017, 77, 99-109.
[http://dx.doi.org/10.1016/j.pnpbp.2017.04.008] [PMID: 28396255]
[28]
Araújo, J.R.C.; Júnior, J.M.A.M.; Damasceno, M.B.M.V.; Santos, S.A.A.R.; Vieira-Neto, A.E.; Lobo, M.D.P.; Campos, A.R.; Moreira, R.A.; Monteiro-Moreira, A.C.O. Neuropharmacological characterization of frutalin in mice: Evidence of an antidepressant-like effect mediated by the NMDA receptor/NO/cGMP pathway. Int. J. Biol. Macromol., 2018, 112, 548-554.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.01.180] [PMID: 29408007]
[29]
Carola, V.; D’Olimpio, F.; Brunamonti, E.; Mangia, F.; Renzi, P. Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice. Behav. Brain Res., 2002, 134(1-2), 49-57.
[http://dx.doi.org/10.1016/S0166-4328(01)00452-1] [PMID: 12191791]
[30]
Iqbal, S.; Ghanimi Fard, M.; Everest-Dass, A.; Packer, N.H.; Parker, L.M. Understanding cellular glycan surfaces in the central nervous system. Biochem. Soc. Trans., 2019, 47(1), 89-100.
[http://dx.doi.org/10.1042/BST20180330] [PMID: 30559272]
[31]
Fakhoury, M. Revisiting the serotonin hypothesis: Implications for major depressive disorders. Mol. Neurobiol., 2016, 53(5), 2778-2786.
[http://dx.doi.org/10.1007/s12035-015-9152-z] [PMID: 25823514]
[32]
Fakhoury, M. Optogenetics: A revolutionary approach for the study of depression. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2021, 106, 110094.
[http://dx.doi.org/10.1016/j.pnpbp.2020.110094] [PMID: 32890694]
[33]
Barauna, S.; Kaster, M.; Heckert, B.; Donascimento, K.; Rossi, F.; Teixeira, E.; Cavada, B.; Rodrigues, A.; Leal, R. Antidepressant‐like effect of lectin from Canavalia brasiliensis (ConBr) administered centrally in mice. Pharmacol. Biochem. Behav., 2006, 85(1), 160-169.
[http://dx.doi.org/10.1016/j.pbb.2006.07.030] [PMID: 16950503]
[34]
Rieger, D.K.; Costa, A.P.; Budni, J.; Moretti, M.; Barbosa, S.G.R.; Nascimento, K.S.; Teixeira, E.H.; Cavada, B.S.; Rodrigues, A.L.S.; Leal, R.B.; Leal, R.B. Antidepressant-like effect of Canavalia brasiliensis (ConBr) lectin in mice: Evidence for the involvement of the glutamatergic system. Pharmacol. Biochem. Behav., 2014, 122, 53-60.
[http://dx.doi.org/10.1016/j.pbb.2014.03.008] [PMID: 24650588]
[35]
Joca, S.R.L.; Sartim, A.G.; Roncalho, A.L.; Diniz, C.F.A.; Wegener, G. Nitric oxide signalling and antidepressant action revisited. Cell Tissue Res., 2019, 377(1), 45-58.
[http://dx.doi.org/10.1007/s00441-018-02987-4] [PMID: 30649612]

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