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Parental Neuropathic Pain Influences Emotion-Related Behavior in Offspring Through Maternal Feeding Associated with DNA Methylation of Amygdale in Rats

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Abstract

Chronic neuropathic pain has currently become a remarkable public health concern, considerably damaging not only the physiological but also the psychological aspects of humans. This study investigated whether neuropathic pain affects maternal care and assessed the effect of parental neuropathic pain on the development of neuropathic pain and emotion among offspring. Our results showed that mother rats suffered from chronic constriction injury (CCI) exhibited defective maternal care. The offspring fed by CCI mother rats (own or cross-fed) showed a significant increase in anxiety and anxiety-related behavior compared with that fed by sham-operated mother rats. The offspring fed by CCI mother rats also displayed decreased oxytocin expression in their supraoptic nucleus than that fed by sham-operated mother rats. Moreover, DNA methyltransferase (DNMT)1 expression in the amygdale was increased, whereas DNMT3a and DNMT3b expressions remained the same in offspring fed by CCI mother rats, as detected with immunohistochemistry and western blot analysis. In addition, the total DNA methylation in amygdale was upregulated in offspring fed by CCI mother rats. Considering the above findings, the data of this study suggest that parental neuropathic pain influences emotion-related behavior in offspring through maternal feeding behavior rather than through genetic factors and pregnancy experience that was associated with DNA methylation of amygdale in offspring.

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Abbreviations

CCI:

Chronic constriction injury

DNMT:

DNA methyltransferase

HPA:

Hypothalamic–pituitary–gonadal axis

PWT:

Paw withdrawal threshold

PWL:

Paw withdrawal latency

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Acknowledgments

This work was supported by a grant from the Science and Technology Department Foundation of Hunan (#2013SK3006) to Dr. Yang.

Conflict of interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. Department of Anesthesiology, Xiangya Hospital, Central South University, 87 Xiangya Road, Changsha, 410008, Hunan, China

    Tao Zhong, Yanfeng Zhang, Qulian Guo, Yong Yang & Jianqin Yan

  2. Department of Anesthesiology, The Second Xiangya Hospital, Central South University, Changsha, 410013, Hunan, China

    Ruping Dai

  3. Department of Medical Oncology, Hunan Cancer Hospital, Affiliated Cancer Hospital of Xiangya School of Medicine, Central South University, Changsha, 410006, Hunan, China

    Hui Wu

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  1. Tao Zhong
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  2. Yanfeng Zhang
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  3. Qulian Guo
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  4. Yong Yang
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Correspondence to Yong Yang.

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11064_2015_1578_MOESM1_ESM.tif

Fig. S1 Comparison of emotion in parental rats among the four groups. (A) Anxiety was examined by conducting the elevated plus maze test; (B) Anxiety-related behavior was assessed by performing an open-field test. C1, male rats with CCI; C2, female rats with CCI; S1, male sham-operated rats; and S2, female sham-operated rats. * p < 0.05 vs. C1 and & p < 0.05 vs.C2. (TIFF 200 kb)

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Zhong, T., Zhang, Y., Guo, Q. et al. Parental Neuropathic Pain Influences Emotion-Related Behavior in Offspring Through Maternal Feeding Associated with DNA Methylation of Amygdale in Rats. Neurochem Res 40, 1179–1187 (2015). https://doi.org/10.1007/s11064-015-1578-1

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  • DOI: https://doi.org/10.1007/s11064-015-1578-1

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