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Influence of autophagy, apoptosis and their interplay in filaricidal activity of C-cinnamoyl glycosides

Published online by Cambridge University Press:  28 June 2019

Priya Roy
Affiliation:
Parasitology Laboratory, Department of Zoology, Centre for Advanced Studies, Visva-Bharati, Santiniketan 731235, West Bengal, India Fishery and Ecotoxicology Revsearch Laboratory, Department of Zoology, The University of Burdwan, Bardhaman 713104, India
Anirban Sengupta
Affiliation:
Immunology Lab, Department of Zoology, University of Calcutta, 35, Ballygunge Circular Road, Kolkata 700019, India
Nikhilesh Joardar
Affiliation:
Parasitology Laboratory, Department of Zoology, Centre for Advanced Studies, Visva-Bharati, Santiniketan 731235, West Bengal, India
Arindam Bhattacharyya
Affiliation:
Immunology Lab, Department of Zoology, University of Calcutta, 35, Ballygunge Circular Road, Kolkata 700019, India
Nimai Chandra Saha
Affiliation:
Fishery and Ecotoxicology Revsearch Laboratory, Department of Zoology, The University of Burdwan, Bardhaman 713104, India
Anup Kumar Misra
Affiliation:
Division of Molecular Medicine, Bose Institute, P-1/12, C.I.T. Scheme VII-M, Kolkata 700054, India
Santi P. Sinha Babu*
Affiliation:
Parasitology Laboratory, Department of Zoology, Centre for Advanced Studies, Visva-Bharati, Santiniketan 731235, West Bengal, India
*
Author for correspondence: Santi P. Sinha Babu, E-mail: [email protected]

Abstract

The present work aims to explore the mechanism of action of C-cinnamoyl glycoside as an antifilarial agent against the bovine filarial nematode Setaria cervi. Both apoptosis and autophagy programmed cell death pathways play a significant role in parasitic death. The generation of reactive oxygen species, alteration of the level of antioxidant components and disruption of mitochondrial membrane potential may be the causative factors that drive the parasitic death. Monitoring of autophagic flux via the formation of autophagosome and autophagolysosome was detected via CYTO ID dye. The expression profiling of both apoptotic and autophagic marker proteins strongly support the initial findings of these two cell death processes. The increased interaction of pro-autophagic protein Beclin1 with BCL-2 may promote apoptotic pathway by suppressing anti-apoptotic protein BCL-2 from its function. This in turn partially restrains the autophagic pathway by engaging Beclin1 in the complex. But overall positive increment in autophagic flux was observed. Dynamic interaction and regulative balance of these two critical cellular pathways play a decisive role in controlling disease pathogenesis. Therefore, the present experimental work may prosper the chance for C-cinnamoyl glycosides to become a potential antifilarial therapeutic in the upcoming day after detail in vivo study and proper clinical trial.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2019 

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Footnotes

*

These authors contributed equally to this work

References

Cao, S, Huang, Y, Zhang, Q, Lu, F, Donkor, PO, Zhu, Y, Qiu, F and Kang, N (2018) Molecular mechanisms of apoptosis and autophagy elicited by combined treatment with oridonin and cetuximab in laryngeal squamous cell carcinoma. Apoptosis. https://doi.org/10.1007/s10495-018-1497-0.Google Scholar
Chan, LLY, Shen, D, Wilkinson, AR, Patton, W, Lai, N and Chan, E (2012) A novel image-based cytometry method for autophagy detection in living cells. Autophagy 8, 13711382.Google Scholar
Dhananjeyan, MR, Milev, YP, Kron, MA and Nair, MG (2005) Synthesis and activity of substituted anthraquinones against a human filarial parasite, Brugia malayi. Journal of Medicinal Chemistry 48, 28222830.Google Scholar
Dreyer, G, Noroes, J, Fiqueredo-Silva, J and Piessens, WF (2000) Pathogenesis of lymphatic disease in bancroftian filariasis: a clinical perspective. Parasitology Today 16, 544548.Google Scholar
Fimia, GM, Kroemer, G and Piacentini, M (2013) Molecular mechanisms of selective autophagy. Cell Death & Differentiation 20, 12.Google Scholar
Gucchait, A, Joardar, N, Parida, PK, Roy, P, Mukherjee, N, Dutta, A, Yesuvadian, R, Sinha Babu, SP, Jana, K and Misra, AK (2018) Development of novel anti-filarial agents using carbamo(dithioperoxo)thioate derivatives. European Journal of Medicinal Chemistry 148, 598610.Google Scholar
Iwai-Kanai, E, Yuan, H, Huang, C, Sayen, MR, Perry-Garza, CN, Kim, L and Gottlieb, RA (2008) A method to measure cardiac autophagic flux in vivo. Autophagy 4, 322329.Google Scholar
James, CE, Hudson, AL and Davey, MW (2009) Drug resistance mechanisms in helminths: is it survival of the fittest? Trends in Parasitology 25, 328335.Google Scholar
Joardar, N, Mukherjee, S and Sinha Babu, SP (2018) Thioredoxin reductase from the bovine flarial parasite Setaria cervi: studies on its localization and optimization of the extraction. International Journal of Biological Macromolecules 107, 23752384.Google Scholar
Koukourakis, MI, Kalamida, D, Giatromanolaki, A, Zois, CE, Sivridis, E, Pouliliou, S, Mitrakas, A, Gatter, KC and Harris, AL (2015) Autophagosome proteins LC3A, LC3B and LC3C have distinct subcellular distribution kinetics and expression in cancer cell lines. PLoS One 10, e0137675.Google Scholar
Liang, J, Cao, R, Wang, X, Zhang, Y, Wang, P, Gao, H, Li, C, Yang, F, Zeng, R, Wei, P, Li, D, Li, W and Yang, W (2017) Mitochondrial PKM2 regulates oxidative stress-induced apoptosis by stabilizing Bcl2. Cell Research 27, 329335.Google Scholar
Mukherjee, N, Mukherjee, S, Saini, P, Roy, P and Sinha Babu, SP (2014) Antifilarial effects of polyphenol rich ethanolic extract from the leaves of Azadirachta indica through molecular and biochemical approaches describing reactive oxygen species (ROS) mediated apoptosis of Setaria cervi. Experimental Parasitology 136, 4158.Google Scholar
Mukherjee, N, Joardar, N and Sinha Babu, SP (2018 a) Antifilarial activity of azadirachtin fuelled through reactive oxygen species induced apoptosis: a thorough molecular study on Setaria cervi. Journal of Helminthology 93, 519528.Google Scholar
Mukherjee, S, Joardar, N, Mondal, S, Schiefer, A, Hoerauf, A, Pfarr, K and Sinha Babu, SP (2018 b) Quinolone fused cyclic sulfonamide as a novel benign antifilarial agent. Scientific Reports 8, 12073.Google Scholar
Munafo, DB and Colombo, MI (2001) A novel assay to study autophagy: regulation of autophagosome vacuole size by amino acid deprivation. Journal of Cell Science 114, 36193629.Google Scholar
Munafo, DB and Colombo, MI (2002) Induction of autophagy causes dramatic changes in the subcellular distribution of GFP-Rab24. Traffic 3, 472482.Google Scholar
Nayak, A, Gayen, P, Saini, P, Maitra, S and Sinha Babu, SP (2011) Albendazole induces apoptosis in adults and microfilariae of Setaria cervi. Experimental Parasitology 128, 236242.Google Scholar
Nayak, A, Gayen, P, Saini, P, Mukherjee, N and Sinha Babu, SP (2012) Molecular evidence of curcumin-induced apoptosis in the filarial worm Setariacervi. Parasitology Research 111, 11731186.Google Scholar
Perera, M, Whitehead, M, Molyneux, D, Weerasooriya, M and Gunatilleke, G (2007) Neglected patients with a neglected disease? A qualitative study of lymphatic filariasis. PLOS Neglected Tropical Diseases 1, e128.Google Scholar
Ray, AS, Joardar, N, Mukherjee, S, Rahaman, CH and Sinha Babu, SP (2018) Polyphenol enriched ethanolic extract of Cajanus scarabaeoides (L.) Thouars exerts potential antifilarial activity by inducing oxidative stress and programmed cell death. PLoS ONE 13, e0208201.Google Scholar
Rodrigues, F, Canac, Y and Lubineau, A (2000) A convenient, one-step, synthesis of β-C-glycosidic ketones in aqueous media. Chemical Communications 20, 20492050.Google Scholar
Roy, P, Dhara, D, Parida, PK, Kar, RK, Bhunia, A, Jana, K, Sinha Babu, SP and Misra, AK (2016) C-cinnamoyl glycosides as a new class of anti-filarial agents. European Journal of Medicinal Chemistry 114, 308317.Google Scholar
Roy, P, Saha, SK, Gayen, P, Chowdhury, P and Sinha Babu, SP (2018) Exploration of antifilarial activity of gold nanoparticle against human and bovine filarial parasites: a nanomedicinal mechanistic approach. Colloids and Surfaces B: Biointerfaces 161, 236243.Google Scholar
Saha, SK, Roy, P, Saini, P, Mondal, MK, Chowdhury, P and Sinha Babu, SP (2016) Carbohydrate polymer inspired silver nanoparticles for filaricidal and mosquitocidal activities: a comprehensive view. Carbohydrate Polymers 137, 390401.Google Scholar
Saha, SK, Roy, P, Mondal, MK, Roy, D, Gayen, P, Chowdhury, P and Sinha Babu, SP (2017) Development of chitosan based gold nanomaterial as an efficient antifilarial agent: a mechanistic approach. Carbohydrate Polymers 157, 16661676.Google Scholar
Saini, P, Saha, SK, Roy, P, Chowdhury, P and Sinha Babu, SP (2016) Evidence of reactive oxygen species (ROS) mediated apoptosis in Setaria cervi induced by green silver nanoparticles from Acacia auriculiformis at a very low dose. Experimental Parasitology 160, 3948.Google Scholar
Sashidhara, KV, Rao, KB, Kushwaha, V, Modukuri, RK, Verma, R and Murthy, PK (2014) Synthesis and antifilarial activity of chalcone-thiazole derivatives against a human lymphatic filarial parasite, Brugia malayi. European Journal of Medicinal Chemistry 81, 473480.Google Scholar
Shvets, E, Fass, E and Elazar, Z (2008) Utilizing flow cytometry to monitor autophagy in living mammalian cells. Autophagy 4, 621628.Google Scholar
Singh, BK, Mishra, M, Saxena, N, Yadav, GP, Maulik, PR, Sahoo, MK, Gaur, RL, Murthy, PK and Tripathi, RP (2008) Synthesis of 2-sulfanyl-6-methyl-1,4-dihydropyrimidines as a new class of antifilarial agents. European Journal of Medicinal Chemistry 43, 27172723.Google Scholar
Srivastava, S, Chauhan, PM, Bhaduri, AP, Murthy, PK and Chatterjee, RK (2000) Secondary amines as new pharmacophores for macrofilaricidal drug design. Bioorganic & Medicinal Chemistry Letters 10, 313314.Google Scholar
World Health Organization (2016) Available at http://www.who.int/mediacentre/factsheets/fs102/en/.Google Scholar
Yoshida, Y, Umeno, A and Shichiri, M (2013) Lipid peroxidation biomarkers for evaluating oxidative stress and assessing antioxidant capacity in vivo. Journal of Clinical Biochemistry and Nutrition 52, 916.Google Scholar