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Astaxanthin and DHA Supplementation Modulates the Maternal Undernutrition-induced Impairment of Cognitive Behavior and Synaptic Plasticity in Adult Life of Offspring’s -Exploring the Molecular Mechanism

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Abstract

Maternal nutrition was recognized as a significant part of brain growth and maturation in most mammalian species. Timely intervention with suitable nutraceuticals would provide long-term health benefits. We aim to unravel the molecular mechanisms of perinatal undernutrition-induced impairments in cognition and synaptic plasticity, employing animal model based on dietary nutraceutical supplementation. We treated undernourished dams at their gestational, lactational, and at both the time point with Astaxanthin (AsX) and Docosahexaenoic acid (DHA), and their pups were used as experimental animals. We evaluated the cognitive function by subjecting the pups to behavioral tests in their adult life. In addition, we assessed the expression of genes in the hippocampus related to cognitive function and synaptic plasticity. Our results showed downregulation of Brain-derived neurotrophic factor (BDNF), Neurotrophin-3 (NT-3), cAMP response-element-binding protein (CREB), and uncoupling protein-2 (UCP2) gene expression in pups born to undernourished dams in their adult life, which AsX and DHA modulated. Maternal AsX and DHA supplementation ameliorated the undernutrition-induced learning impairment in novel object recognition (NOR) tests and partially baited radial arm maze (RAM) tasks in offspring’s. The expressions of Synapsin-1 and PSD-95 decreased in perinatally undernourished groups compared to control and AsX-DHA treated groups at CA1, CA2, CA3, and DG. AsX and DHA supplementation upregulated BDNF, NT-3, CREB, and UCP2 gene expressions in perinatally undernourished rats, which are involved in intracellular signaling cascades like Ras, PI3K, and PLC. The results of our study give new insights into neuronal differentiation, survival, and plasticity, indicating that the perinatal period is the critical time for reversing maternal undernutrition-induced cognitive impairment in offspring’s.

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Data Availability

The datasets generated during and/or analyzed during the current study are included in the manuscript and supplementary file.

Abbreviations

ABSR:

Adaptive Bbio-energetic Stress Response

AsX:

Astaxanthin

BDNF:

Brain Derived Neurotrophic Factor

BSI:

Brain Somatic Index

C:

Control

DC:

Drug Control

CREB:

Cyclic AMP Response Element-Binding Protein

DHA:

Docosahexaenoic Acid

DI:

Discrimination Index

NOR:

Novel Object Recognition

NT-3:

Neurotrophin-3

n-3PUFAs:

N-3 long-chain Polyunsaturated Fatty Acids

PD:

Postnatal Day

PeriUN-AD:

Perinatally Undernourished Rats Supplemented with Astaxanthin and Docosahexaenoic Acid

%CC:

Percentage Correct Choice

Peri UN:

Perinatally Undernourished Rats

PostUN-AD:

Postnatally Undernourished Rats Supplemented with Astaxanthin and Docosahexaenoic Acid

PostUN:

Postnatally Undernourished Rats

PreUN-AD:

Prenatally Undernourished Rats Supplemented with Astaxanthin and Docosahexaenoic Acid

PreUN:

Prenatally Undernourished Rats

PSD-95:

Postsynaptic Density Protein 95

PUFAs:

Polyunsaturated Fatty Acids

RAM:

Radial Arm Maze

RMEs:

Reference Memory Errors

ROS:

Reactive Oxygen Species

TAC:

Total Antioxidant Capacity

UCP2:

Uncoupling Protein-2

VC:

Vehicle Control

VCUN:

Perinatally Undernourished Rats Supplemented with Vehicle (Olive Oil)

WMEs:

Working Memory Errors

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Acknowledgements

The authors acknowledge the support of the institutional animal care facility, Nitte (Deemed to be University) and laboratory facilities at Nitte University Centre for Science Education and Research, and Biotechnology Unit, Dept of Biosciences, Mangalore University. Auhors acknowledge the financial support from Indian Council of Medical Research (No. 5/9/1220/2019-Nut.).

Authors also acknowledge the constructive recommendations of the honorable reviwers.

Funding

This study was supported by grants from the Indian Council of Medical Research (No. 5/9/1220/2019-Nut.). Corresponding Author, Damodara Gowda K M has received research support from Indian Council of Medical Research.

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Authors and Affiliations

  1. Nitte (Deemed to be University), Department of Physiology, KS Hegde Medical Academy, Deralakatte, Mangalore, Karnataka, 575018, India

    Megha Bhat Agni, Pramukh Subrahmanya Hegde & Damodara Gowda K M

  2. Nitte (Deemed to be University), Department of Infectious Diseases & Microbial Genomics, Nitte University Centre for Science Education and Research (NUCSER), Mangalore, Karnataka, 575018, India

    Praveen Rai

  3. Biotechnology Unit, Department of Biosciences, Mangalore University, Mangalagangothri, 574199, Karnataka, India

    Monika Sadananda

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Contributions

All authors contributed to the study's conception and design. M.B.A. and P.S. H. carried out animal handling and treatment experiments, performed statistical analysis and preparation of figures and tables, and contributed to the drafting and editing of the manuscript. D.G. K M., P. R., and M.S. provided scientific advice and contributed to designing the research work, conceptualizing the ideas, preparing tables and figures, reviewing the analyzed data, and drafting and editing the manuscript. M.S. supervised behavioral experiments. D.G.K. M. led the entire research. All the authors read and approved the final manuscript.

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Correspondence to Damodara Gowda K M.

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Animal experiments were approved by the Institutional Animal Ethics Committee, KS Hegde Medical Academy, Nitte (Deemed to be University), Mangalore (approval number Ref. KSHEMA/IAEC/05/2019).

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Agni, M.B., Hegde, P.S., Rai, P. et al. Astaxanthin and DHA Supplementation Modulates the Maternal Undernutrition-induced Impairment of Cognitive Behavior and Synaptic Plasticity in Adult Life of Offspring’s -Exploring the Molecular Mechanism. Mol Neurobiol (2024). https://doi.org/10.1007/s12035-024-04147-y

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