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Transgenerational Inheritance of Paternal Neurobehavioral Phenotypes: Stress, Addiction, Ageing and Metabolism

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Abstract

Epigenetic modulation is found to get involved in multiple neurobehavioral processes. It is believed that different types of environmental stimuli could alter the epigenome of the whole brain or related neural circuits, subsequently contributing to the long-lasting neural plasticity of certain behavioral phenotypes. While the maternal influence on the health of offsprings has been long recognized, recent findings highlight an alternative way for neurobehavioral phenotypes to be passed on to the next generation, i.e., through the male germ line. In this review, we focus specifically on the transgenerational modulation induced by environmental stress, drugs of abuse, and other physical or mental changes (e.g., ageing, metabolism, fear) in fathers, and recapitulate the underlying mechanisms potentially mediating the alterations in epigenome or gene expression of offsprings. Together, these findings suggest that the inheritance of phenotypic traits through male germ-line epigenome may represent the unique manner of adaptation during evolution. Hence, more attention should be paid to the paternal health, given its equivalently important role in affecting neurobehaviors of descendants.

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Funding

The work is supported by “Hundred Talents program”, “Qing Lan Project” of Nanjing Normal University, Jiangsu Provincial Natural Science Foundation (#BK20140917), National Natural Science Foundation of China (#81501164, # 81501171), Hong Kong Health and Medical Research Fund, and by funds of Leading Talents of Guangdong (2013), and Programme of Introducing Talents of Discipline to Universities (B14036).

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    Authors and Affiliations

    1. School of Psychology, Nanjing Normal University, Nanjing, China

      Ti-Fei Yuan

    2. Guangdong-Hong Kong-Macau Institute of CNS Regeneration (GHMICR), Guangdong Key Laboratory of Brain Function and Diseases, Jinan University, Guangzhou, China

      Ang Li, Xin Sun, Huan Ouyang & Kwok Fai So

    3. Polytechnic Institute of Porto, School of Health Technologies, Porto, Portugal

      Carlos Campos & Nuno B. F. Rocha

    4. Unidad de Trastornos del Movimiento y Sueño (TMS), Hospital General Dr. Manuel Gea González/IFC-UNAM, Mexico City, Mexico

      Oscar Arias-Carrión

    5. Laboratory of Panic and Respiration, Institute of Psychiatry, Federal University of Rio de Janeiro (IPUB/UFRJ), Rio de Janeiro, Brazil

      Sergio Machado

    6. Physical Activity Neuroscience, Physical Activity Sciences Postgraduate Program, Salgado de Oliveira University, Niterói, Brazil

      Sergio Machado

    7. Institute of Cognitive Neuroscience and Department of Psychology, Zhejiang Sci-Tech University, Hangzhou, China

      Gonglin Hou

    8. Department of Ophthalmology, LFS Faculty of Medicine, The University of Hong Kong, Hong Kong SAR, China

      Kwok Fai So

    9. State Key Laboratory of Brain and Cognitive Sciences, The University of Hong Kong, Hong Kong SAR, China

      Kwok Fai So

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    1. Ti-Fei Yuan
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    2. Ang Li
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    3. Xin Sun
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    Correspondence to Ti-Fei Yuan, Ang Li, Gonglin Hou or Kwok Fai So.

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    Ti-Fei Yuan, Ang Li and Xin Sun contributed equally to this work.

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    Yuan, TF., Li, A., Sun, X. et al. Transgenerational Inheritance of Paternal Neurobehavioral Phenotypes: Stress, Addiction, Ageing and Metabolism. Mol Neurobiol 53, 6367–6376 (2016). https://doi.org/10.1007/s12035-015-9526-2

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