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Phycoerythrin averts intracellular ROS generation and physiological functional decline in eukaryotes under oxidative stress

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Abstract

In vitro antioxidant virtue and life-prolonging effect of phycoerythrin (PE; a pigment protein isolated from Phormidium sp. A09DM) have been revealed in our previous reports (Sonani et al. in Age 36:9717, 2014a; Sonani et al. in Process Biochem 49:1757–1766, 2014b). It has been hypothesized that the PE expands life span of Caenorhabditis elegans (bears large resemblance with human aging pathways) due to its antioxidant virtue. This hypothesis is tested in present study by checking the effect of PE on intracellular reactive oxygen species (ROS) generation and associated physiological deformities using mouse and human skin fibroblasts, C. elegans, and Drosophila melanogaster Oregon R + and by divulging PE’s structural attributes responsible for its antioxidant asset. PE treatment displayed noteworthy decrease of 67, 48, and 77 % in ROS level in mouse fibroblast (3T3-L1), human fibroblast, and C. elegans N2, respectively, arisen under chemical-induced oxidative stress. PE treatment delayed the development of paraquat-induced Alzheimer phenotype by 14.5 % in C. elegans CL4176. Furthermore, PE improved the locomotion of D. melanogaster Oregon R + under oxidative stress with simultaneous up-regulation in super-oxide dismutase and catalase activities. The existence of 52 Glu + Asp + His + Thr residues (having metal ion sequestration capacity), 5 phycoerythrobilin chromophores (potential electron exchangers) in PE’s primary structure, and significant hydrophobic patches on the surface of its α- and β-subunits are supposed to collectively contribute in the antioxidant virtues of PE. Altogether, results support the hypothesis that it is the PE’s antioxidant asset, which is responsible for its life-prolonging effect and thus could be exploited in the therapeutics of ROS-associated abnormalities including aging and neurodegeneration in eukaryotes.

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Acknowledgments

Datta Madamwar acknowledges University Grant Commission (UGC), New Delhi for financial help in form of CENTRE OF ADVANCED STUDY (CAS) program. Ravi R Sonani is highly thankful to the Department of Science and Technology (DST), New Delhi, and Indo-French Centre for the Promotion of Advance Research (IFCPAR) for the financial support in form of INSPIRE (IF120712) and Raman-Charpak bi-national fellowships, respectively. Rajesh P. Rastogi is thankful to the University Grant Commission (UGC), New Delhi, India, for Dr. D.S. Kothari Postdoctoral Research Grant. Niraj Kumar Singh acknowledges the Department of Science and Technology (DST), New Delhi, for financial support in the form of DST (SERB) Fast track young scientist project (SB/YS/LS-290/2013). Jitendra Kumar acknowledges the DST for young scientist award (SB/YS/LS-166/2014) and DBT-Patna University-IPLS Program (BT/PR4577/INF/22/149/2012) for the financial support.

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Author notes

  1. Ravi R. Sonani

    Present address: Commission of Atomic and Alternative Energy, Institute of Biology and Technology of Saclay, 91191, Gif/Yvette, France

  2. Jitendra Kumar

    Present address: DBT-PU-IPLS Programme, Department of Botany/Biotechnology, Patna University, Patna, Bihar, 800005, India

Authors and Affiliations

  1. Post-Graduate Department of Biosciences, UGC-Centre of Advanced Study, Sardar Patel University, Vadtal Road, Satellite Campus, Bakrol, Anand, Gujarat, 388 315, India

    Ravi R. Sonani, Rajesh P. Rastogi & Datta Madamwar

  2. Department of Biotechnology, Shri A. N. Patel PG Institute, Anand, Gujarat, 388001, India

    Niraj K. Singh & Puja J. Patel

  3. Division of Phytotherapeutics and Metabolic Endocrinology, Department of Zoology, Faculty of Science, The Maharaja Sayajirao University of Baroda, Vadodara, Gujarat, 390002, India

    Jaymesh Thadani & Ranjitsinh V. Devkar

  4. The Buck Institute for Research on Aging, 8001 Redwood Boulevard, Novato, CA, 94945, USA

    Jitendra Kumar

  5. School of Biological Sciences and Biotechnology, Indian Institute of Advanced Research, Koba, Gandhinagar, Gujarat, 382007, India

    Anand K. Tiwari

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Sonani, R.R., Rastogi, R.P., Singh, N.K. et al. Phycoerythrin averts intracellular ROS generation and physiological functional decline in eukaryotes under oxidative stress. Protoplasma 254, 849–862 (2017). https://doi.org/10.1007/s00709-016-0996-5

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