Nicotinamide mononucleotide ameliorates ionizing radiation-induced spermatogenic dysfunction in mice by modulating the glycolytic pathway

Radiotherapy, a common cancer treatment, leads to infertility in male cancer survivors, particularly young and middle-aged patients. Nicotinamide mononucleotide (NMN), a precursor of nicotinamide adenine dinucleotide (NAD<sup>+</sup>), plays crucial roles in energy metabolism, DNA repair...

Full description

Saved in:
Bibliographic Details
Main Authors: Yang Wenqin, Nong Weihua, Liu Ke, Lei Xiaocan, Chen Xiaping, Jiang Pei, Tang Jiayi, Hu Cong, Hu Zecheng, Li Meixiang
Format: Article
Language:English
Published: China Science Publishing & Media Ltd. 2024-10-01
Series:Acta Biochimica et Biophysica Sinica
Subjects:
Online Access:https://www.sciengine.com/doi/10.3724/abbs.2024167
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850085074588925952
author Yang Wenqin
Nong Weihua
Liu Ke
Lei Xiaocan
Chen Xiaping
Jiang Pei
Tang Jiayi
Hu Cong
Hu Zecheng
Li Meixiang
author_facet Yang Wenqin
Nong Weihua
Liu Ke
Lei Xiaocan
Chen Xiaping
Jiang Pei
Tang Jiayi
Hu Cong
Hu Zecheng
Li Meixiang
author_sort Yang Wenqin
collection DOAJ
description Radiotherapy, a common cancer treatment, leads to infertility in male cancer survivors, particularly young and middle-aged patients. Nicotinamide mononucleotide (NMN), a precursor of nicotinamide adenine dinucleotide (NAD<sup>+</sup>), plays crucial roles in energy metabolism, DNA repair, and gene expression. The purpose of this study is to investigate the protective effects and underlying mechanisms of NMN against ionizing radiation (IR)-induced testicular injury and spermatogenic dysfunction in an adult male mouse model. To assess the effects of NMN, single whole-body γ-ray irradiation is used to induce testicular injury and spermatogenic dysfunction in adult male mice. NMN is orally administered at <sc>500 mg/kg</sc> before and after IR exposure. The structural and cellular damage to the testes caused by 5 Gy γ-ray irradiation, as well as the protective effect of NMN on testicular spermatogenic dysfunction, are evaluated. The serum hormone testosterone, LH, and FSH levels, as well as testicular NAD<sup>+</sup>, lactate, and pyruvate levels, are detected. Furthermore, the expressions of the apoptosis-related genes Bcl-2, Bax, and Caspase-3 and the rate-limiting enzymes HK2, PKM2, and LDHA, which are potentially associated with the mechanism of injury, are examined. The results demonstrate that <sc>5 Gy</sc> γ-ray irradiation exposure causes a decrease in the serum testosterone, LH, and FSH levels in adult male mice, as well as in the testicular NAD<sup>+</sup>, lactate, and pyruvate levels, and causes damage to the testicular structure and cells. Morphometric analysis reveal a decrease in the testis mass, seminiferous tubule diameter, and height of the germinal epithelium. The sperm quantity, motility, and testicular volume are reduced in the <sc>5 Gy</sc> group but are restored by NMN supplementation. NMN intervention downregulates the expressions of proapoptotic genes (Bax and Caspase-3) and upregulates the expression of an antiapoptotic gene (Bcl-2). Sertoli cells marker genes (WT-1, GATA-4, SOX9, and vimentin) and glycolysis rate-limiting enzyme-encoding genes (HK2, PKM2, and LDHA) are significantly upregulated. In summary, NMN has a positive regulatory effect on testicular spermatogenic dysfunction in male mice induced by ionizing radiation. This positive effect is likely achieved by promoting the proliferation of spermatogenic cells and activating glycolytic pathways. These findings suggest that NMN supplementation may be a potential protective strategy to prevent reproductive damage to male subjects from ionizing radiation.
format Article
id doaj-art-7eebe99ead924eecbdd6a87ae7e68817
institution DOAJ
issn 1672-9145
language English
publishDate 2024-10-01
publisher China Science Publishing & Media Ltd.
record_format Article
series Acta Biochimica et Biophysica Sinica
spelling doaj-art-7eebe99ead924eecbdd6a87ae7e688172025-08-20T02:43:49ZengChina Science Publishing & Media Ltd.Acta Biochimica et Biophysica Sinica1672-91452024-10-015727428510.3724/abbs.202416720d259ccNicotinamide mononucleotide ameliorates ionizing radiation-induced spermatogenic dysfunction in mice by modulating the glycolytic pathwayYang Wenqin0Nong Weihua1Liu Ke2Lei Xiaocan3Chen Xiaping4Jiang Pei5Tang Jiayi6Hu Cong7Hu Zecheng8Li Meixiang9["Institute of Clinical Anatomy & Reproductive Medicine, Department of Histology and Embryology, Hengyang Medical School, University of South China, Hengyang 421001, China"]["Department of Obstetrics and Gynecology, Affiliated Hospital of Youjiang Medical University for Nationalities, Key Laboratory of Research on Clinical Molecular Diagnosis for High Incidence Diseases in Western Guangxi, Baise 533300, China"]["Institute of Clinical Anatomy & Reproductive Medicine, Department of Histology and Embryology, Hengyang Medical School, University of South China, Hengyang 421001, China"]["Institute of Clinical Anatomy & Reproductive Medicine, Department of Histology and Embryology, Hengyang Medical School, University of South China, Hengyang 421001, China","Department of Obstetrics and Gynecology, Affiliated Hospital of Youjiang Medical University for Nationalities, Key Laboratory of Research on Clinical Molecular Diagnosis for High Incidence Diseases in Western Guangxi, Baise 533300, China"]["Institute of Clinical Anatomy & Reproductive Medicine, Department of Histology and Embryology, Hengyang Medical School, University of South China, Hengyang 421001, China"]["Institute of Clinical Anatomy & Reproductive Medicine, Department of Histology and Embryology, Hengyang Medical School, University of South China, Hengyang 421001, China"]["Institute of Clinical Anatomy & Reproductive Medicine, Department of Histology and Embryology, Hengyang Medical School, University of South China, Hengyang 421001, China"]["Institute of Clinical Anatomy & Reproductive Medicine, Department of Histology and Embryology, Hengyang Medical School, University of South China, Hengyang 421001, China"]["the First Affiliated Hospital, Department of Breast and Thyroid Surgery, Hengyang Medical School, University of South China, Hengyang 421001, China"]["Institute of Clinical Anatomy & Reproductive Medicine, Department of Histology and Embryology, Hengyang Medical School, University of South China, Hengyang 421001, China"]Radiotherapy, a common cancer treatment, leads to infertility in male cancer survivors, particularly young and middle-aged patients. Nicotinamide mononucleotide (NMN), a precursor of nicotinamide adenine dinucleotide (NAD<sup>+</sup>), plays crucial roles in energy metabolism, DNA repair, and gene expression. The purpose of this study is to investigate the protective effects and underlying mechanisms of NMN against ionizing radiation (IR)-induced testicular injury and spermatogenic dysfunction in an adult male mouse model. To assess the effects of NMN, single whole-body γ-ray irradiation is used to induce testicular injury and spermatogenic dysfunction in adult male mice. NMN is orally administered at <sc>500 mg/kg</sc> before and after IR exposure. The structural and cellular damage to the testes caused by 5 Gy γ-ray irradiation, as well as the protective effect of NMN on testicular spermatogenic dysfunction, are evaluated. The serum hormone testosterone, LH, and FSH levels, as well as testicular NAD<sup>+</sup>, lactate, and pyruvate levels, are detected. Furthermore, the expressions of the apoptosis-related genes Bcl-2, Bax, and Caspase-3 and the rate-limiting enzymes HK2, PKM2, and LDHA, which are potentially associated with the mechanism of injury, are examined. The results demonstrate that <sc>5 Gy</sc> γ-ray irradiation exposure causes a decrease in the serum testosterone, LH, and FSH levels in adult male mice, as well as in the testicular NAD<sup>+</sup>, lactate, and pyruvate levels, and causes damage to the testicular structure and cells. Morphometric analysis reveal a decrease in the testis mass, seminiferous tubule diameter, and height of the germinal epithelium. The sperm quantity, motility, and testicular volume are reduced in the <sc>5 Gy</sc> group but are restored by NMN supplementation. NMN intervention downregulates the expressions of proapoptotic genes (Bax and Caspase-3) and upregulates the expression of an antiapoptotic gene (Bcl-2). Sertoli cells marker genes (WT-1, GATA-4, SOX9, and vimentin) and glycolysis rate-limiting enzyme-encoding genes (HK2, PKM2, and LDHA) are significantly upregulated. In summary, NMN has a positive regulatory effect on testicular spermatogenic dysfunction in male mice induced by ionizing radiation. This positive effect is likely achieved by promoting the proliferation of spermatogenic cells and activating glycolytic pathways. These findings suggest that NMN supplementation may be a potential protective strategy to prevent reproductive damage to male subjects from ionizing radiation.https://www.sciengine.com/doi/10.3724/abbs.2024167ionizing radiationnicotinamide mononucleotidespermatogenic dysfunctionglycolysisapoptosissertoli cell
spellingShingle Yang Wenqin
Nong Weihua
Liu Ke
Lei Xiaocan
Chen Xiaping
Jiang Pei
Tang Jiayi
Hu Cong
Hu Zecheng
Li Meixiang
Nicotinamide mononucleotide ameliorates ionizing radiation-induced spermatogenic dysfunction in mice by modulating the glycolytic pathway
Acta Biochimica et Biophysica Sinica
ionizing radiation
nicotinamide mononucleotide
spermatogenic dysfunction
glycolysis
apoptosis
sertoli cell
title Nicotinamide mononucleotide ameliorates ionizing radiation-induced spermatogenic dysfunction in mice by modulating the glycolytic pathway
title_full Nicotinamide mononucleotide ameliorates ionizing radiation-induced spermatogenic dysfunction in mice by modulating the glycolytic pathway
title_fullStr Nicotinamide mononucleotide ameliorates ionizing radiation-induced spermatogenic dysfunction in mice by modulating the glycolytic pathway
title_full_unstemmed Nicotinamide mononucleotide ameliorates ionizing radiation-induced spermatogenic dysfunction in mice by modulating the glycolytic pathway
title_short Nicotinamide mononucleotide ameliorates ionizing radiation-induced spermatogenic dysfunction in mice by modulating the glycolytic pathway
title_sort nicotinamide mononucleotide ameliorates ionizing radiation induced spermatogenic dysfunction in mice by modulating the glycolytic pathway
topic ionizing radiation
nicotinamide mononucleotide
spermatogenic dysfunction
glycolysis
apoptosis
sertoli cell
url https://www.sciengine.com/doi/10.3724/abbs.2024167
work_keys_str_mv AT yangwenqin nicotinamidemononucleotideamelioratesionizingradiationinducedspermatogenicdysfunctioninmicebymodulatingtheglycolyticpathway
AT nongweihua nicotinamidemononucleotideamelioratesionizingradiationinducedspermatogenicdysfunctioninmicebymodulatingtheglycolyticpathway
AT liuke nicotinamidemononucleotideamelioratesionizingradiationinducedspermatogenicdysfunctioninmicebymodulatingtheglycolyticpathway
AT leixiaocan nicotinamidemononucleotideamelioratesionizingradiationinducedspermatogenicdysfunctioninmicebymodulatingtheglycolyticpathway
AT chenxiaping nicotinamidemononucleotideamelioratesionizingradiationinducedspermatogenicdysfunctioninmicebymodulatingtheglycolyticpathway
AT jiangpei nicotinamidemononucleotideamelioratesionizingradiationinducedspermatogenicdysfunctioninmicebymodulatingtheglycolyticpathway
AT tangjiayi nicotinamidemononucleotideamelioratesionizingradiationinducedspermatogenicdysfunctioninmicebymodulatingtheglycolyticpathway
AT hucong nicotinamidemononucleotideamelioratesionizingradiationinducedspermatogenicdysfunctioninmicebymodulatingtheglycolyticpathway
AT huzecheng nicotinamidemononucleotideamelioratesionizingradiationinducedspermatogenicdysfunctioninmicebymodulatingtheglycolyticpathway
AT limeixiang nicotinamidemononucleotideamelioratesionizingradiationinducedspermatogenicdysfunctioninmicebymodulatingtheglycolyticpathway