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Qing Zhu
Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, Sichuan Agricultural University, Chengdu 611130, China

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Journal article
Published: 13 August 2021 in Animals
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Skeletal muscle plays important roles in animal locomotion, metabolism, and meat production in farm animals. Current studies showed that non-coding RNAs, especially the circular RNA (circRNA) play an indispensable role in skeletal muscle development. Our previous study revealed that several differentially expressed circRNAs among fast muscle growing broilers (FMGB) and slow muscle growing layers (SMGL) may regulate muscle development in the chicken. In this study, a novel differentially expressed circPPP1R13B was identified. Molecular mechanism analysis indicated that circPPP1R13B targets miR-9-5p and negatively regulates the expression of miR-9-5p, which was previously reported to be an inhibitor of skeletal muscle development. In addition, circPPP1R13B positively regulated the expression of miR-9-5p target gene insulin like growth factor 2 mRNA binding protein 3 (IGF2BP3) and further activated the downstream insulin like growth factors (IGF)/phosphatidylinositol 3-kinase (PI3K)/AKT serine/threonine kinase (AKT) signaling pathway. The results also showed that the knockdown of circPPP1R13B inhibits chicken skeletal muscle satellite cells (SMSCs) proliferation and differentiation, and the overexpression of circPPP1R13B promotes the proliferation and differentiation of chicken SMSCs. Furthermore, the overexpression of circPPP1R13B could block the inhibitory effect of miR-9-5p on chicken SMSC proliferation and differentiation. In summary, our results suggested that circPPP1R13B promotes chicken SMSC proliferation and differentiation by targeting miR-9-5p and activating IGF/PI3K/AKT signaling pathway.

ACS Style

Xiaoxu Shen; Yuanhang Wei; Guishuang You; Wei Liu; Felix Kwame Amevor; Yao Zhang; Haorong He; Menggen Ma; Yun Zhang; Diyan Li; Qing Zhu; Huadong Yin. Circular PPP1R13B RNA Promotes Chicken Skeletal Muscle Satellite Cell Proliferation and Differentiation via Targeting miR-9-5p. Animals 2021, 11, 2396 .

AMA Style

Xiaoxu Shen, Yuanhang Wei, Guishuang You, Wei Liu, Felix Kwame Amevor, Yao Zhang, Haorong He, Menggen Ma, Yun Zhang, Diyan Li, Qing Zhu, Huadong Yin. Circular PPP1R13B RNA Promotes Chicken Skeletal Muscle Satellite Cell Proliferation and Differentiation via Targeting miR-9-5p. Animals. 2021; 11 (8):2396.

Chicago/Turabian Style

Xiaoxu Shen; Yuanhang Wei; Guishuang You; Wei Liu; Felix Kwame Amevor; Yao Zhang; Haorong He; Menggen Ma; Yun Zhang; Diyan Li; Qing Zhu; Huadong Yin. 2021. "Circular PPP1R13B RNA Promotes Chicken Skeletal Muscle Satellite Cell Proliferation and Differentiation via Targeting miR-9-5p." Animals 11, no. 8: 2396.

Journal article
Published: 08 July 2021 in Animal Biotechnology
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Skeletal muscle also plays a vital role in regulating the movement energy storage and health of metabolism. In order to investigate the expression profile of protein and phosphor-proteins in chicken skeletal muscle during embryonic development, we performed phosphor-proteomics analysis by label-free and TiO2 enrichment strategy in chicken leg muscle tissues of at embryonic age embryo day 7(E7), E12, E17 and 3-day post-hatch (D3). The study led to the identification of 4332 proteins in the proteome and 1043 phosphorylation modification sites in the phosphorylated proteome, corresponding to 718 proteins (FC ≥ 2 or FC ≤ 0.5 and p < 0.05). The DEP-associated biological processes were involved in Focal adhesion, Glycolysis/gluconeogenesis, Arginine and proline metabolism by KEGG analysis. PPI analyses revealed that these DEPs TNNC1, TNNC2, TNNT2, TNNT3 and phosphorylated DEPs MYLPF interacted with involved pathways. Integrative analysis of proteome and phosphoproteome data found 324 common proteins, corresponding to 521 modification sites and Focal adhesion was the only pathway significantly enriched. These results provide a basis for further understanding the proteome and phosphoproteome and their regulatory biochemical pathways during the development of embryonic chicken skeletal muscle.

ACS Style

Can Cui; Huadong Yin; Shunshun Han; Yao Zhang; Yun Zhang; Qing Zhu. Quantitative proteomic and phosphoproteomic analysis of chicken skeletal muscle during embryonic development. Animal Biotechnology 2021, 1 -12.

AMA Style

Can Cui, Huadong Yin, Shunshun Han, Yao Zhang, Yun Zhang, Qing Zhu. Quantitative proteomic and phosphoproteomic analysis of chicken skeletal muscle during embryonic development. Animal Biotechnology. 2021; ():1-12.

Chicago/Turabian Style

Can Cui; Huadong Yin; Shunshun Han; Yao Zhang; Yun Zhang; Qing Zhu. 2021. "Quantitative proteomic and phosphoproteomic analysis of chicken skeletal muscle during embryonic development." Animal Biotechnology , no. : 1-12.

Journal article
Published: 04 April 2021 in Animals
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Skeletal muscle satellite cell growth and development is a complicated process driven by multiple genes. The PDZ and LIM domain 5 (PDLIM5) gene has been proven to function in C2C12 myoblast differentiation and is involved in the regulation of skeletal muscle development. The role of PDLIM5 in chicken skeletal muscle satellite cells, however, is unclear. In this study, in order to determine whether the PDLIM5 gene has a function in chicken skeletal muscle satellite cells, we examined the changes in proliferation and differentiation of chicken skeletal muscle satellite cells (SMSCs) after interfering and overexpressing PDLIM5 in cells. In addition, the molecular pathways of the PDLIM5 gene regulating SMSC proliferation and differentiation were analyzed by transcriptome sequencing. Our results show that PDLIM5 can promote the proliferation and differentiation of SMSCs; furthermore, through transcriptome sequencing, it can be found that the differential genes are enriched in the MAPK signaling pathway after knocking down PDLIM5. Finally, it was verified that PDLIM5 played an active role in the proliferation and differentiation of chicken SMSCs by activating the p38-MAPK signaling pathway. These results indicate that PDLIM5 may be involved in the growth and development of chicken skeletal muscle.

ACS Style

Haorong He; Huadong Yin; Xueke Yu; Yao Zhang; Menggen Ma; Diyan Li; Qing Zhu. PDLIM5 Affects Chicken Skeletal Muscle Satellite Cell Proliferation and Differentiation via the p38-MAPK Pathway. Animals 2021, 11, 1016 .

AMA Style

Haorong He, Huadong Yin, Xueke Yu, Yao Zhang, Menggen Ma, Diyan Li, Qing Zhu. PDLIM5 Affects Chicken Skeletal Muscle Satellite Cell Proliferation and Differentiation via the p38-MAPK Pathway. Animals. 2021; 11 (4):1016.

Chicago/Turabian Style

Haorong He; Huadong Yin; Xueke Yu; Yao Zhang; Menggen Ma; Diyan Li; Qing Zhu. 2021. "PDLIM5 Affects Chicken Skeletal Muscle Satellite Cell Proliferation and Differentiation via the p38-MAPK Pathway." Animals 11, no. 4: 1016.

Journal article
Published: 10 March 2021 in Toxins
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Zearalenone (ZEA) is a nonsteroidal estrogenic mycotoxin found in several food commodities worldwide. ZEA causes reproductive disorders, genotoxicity, and testicular toxicity in animals. However, little is known about the functions of apoptosis and autophagy after exposure to ZEA in granulosa cells. This study investigated the effects of ZEA on chicken granulosa cells. The results show that ZEA at different doses significantly inhibited the growth of chicken granulosa cells by inducing apoptosis. ZEA treatment up-regulated Bax and downregulated Bcl-2 expression, promoted cytochrome c release into the cytosol, and triggered mitochondria-mediated apoptosis. Consequently, caspase-9 and downstream effector caspase-3 were activated, resulting in chicken granulosa cells apoptosis. ZEA treatment also upregulated LC3-II and Beclin-1 expression, suggesting that ZEA induced a high level of autophagy. Pretreatment with chloroquine (an autophagy inhibitor) and rapamycin (an autophagy inducer) increased and decreased the rate of apoptosis, respectively, in contrast with other ZEA-treated groups. Autophagy delayed apoptosis in the ZEA-treated cells. Therefore, autophagy may prevent cells from undergoing apoptosis by reducing ZEA-induced cytotoxicity. In addition, our results further show that the autophagy was stimulated by ZEA through PI3K-AKT-mTOR and MAPK signaling pathways in chicken granulosa cells.

ACS Style

Yifeng Zhu; Heng Wang; Jianping Wang; Shunshun Han; Yao Zhang; Menggen Ma; Qing Zhu; Keying Zhang; Huadong Yin. Zearalenone Induces Apoptosis and Cytoprotective Autophagy in Chicken Granulosa Cells by PI3K-AKT-mTOR and MAPK Signaling Pathways. Toxins 2021, 13, 199 .

AMA Style

Yifeng Zhu, Heng Wang, Jianping Wang, Shunshun Han, Yao Zhang, Menggen Ma, Qing Zhu, Keying Zhang, Huadong Yin. Zearalenone Induces Apoptosis and Cytoprotective Autophagy in Chicken Granulosa Cells by PI3K-AKT-mTOR and MAPK Signaling Pathways. Toxins. 2021; 13 (3):199.

Chicago/Turabian Style

Yifeng Zhu; Heng Wang; Jianping Wang; Shunshun Han; Yao Zhang; Menggen Ma; Qing Zhu; Keying Zhang; Huadong Yin. 2021. "Zearalenone Induces Apoptosis and Cytoprotective Autophagy in Chicken Granulosa Cells by PI3K-AKT-mTOR and MAPK Signaling Pathways." Toxins 13, no. 3: 199.

Journal article
Published: 09 March 2021 in Gene
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Skeletal muscle is the most abundant tissue in the human and animal body, loss of its function can lead to muscle aging and various myogenic diseases. The skeletal muscle development is a complex and tightly regulated process, which is driven by a variety of many factors, signaling pathways and regulatory mechanisms. Plectin (Plec), a cytolinker protein, is ubiquitously expressed in various tissues such as skin, muscle, plasma membrane, and most types of cells. Although known isoforms of Plec is well-characterized in muscle dystrophy, very little is known on the function of Plec in the skeletal muscle development. Here, we found that Plec plays a vital role in promoting C2C12 myoblasts differentiation and proliferation, but inhibits their apoptosis. Also, Plec regulates the expression of atrophy-related genes (atrogin-1 and muRF-1) to rescue muscle atrophy. Furthermore, we have demonstrated that Plec binds to Dishevelled-2 (Dvl-2) and forms a protein complex, which is then activate the canonical Wnt signaling. We also observed that Plec resists ubiquitination by stabilizing Dvl-2 and reduces the level of LC3-labeled Dvl-2 and antagonizes the autophagy system. In conclusion, our findings suggest that Plec regulates canonical Wnt signaling mediated skeletal development by stabilizing Dvl-2 and downregulating the cellular autophagic degradation system.

ACS Style

Huadong Yin; Shunshun Han; Can Cui; Yan Wang; Diyan Li; Qing Zhu. Plectin regulates Wnt signaling mediated-skeletal muscle development by interacting with Dishevelled-2 and antagonizing autophagy. Gene 2021, 783, 145562 .

AMA Style

Huadong Yin, Shunshun Han, Can Cui, Yan Wang, Diyan Li, Qing Zhu. Plectin regulates Wnt signaling mediated-skeletal muscle development by interacting with Dishevelled-2 and antagonizing autophagy. Gene. 2021; 783 ():145562.

Chicago/Turabian Style

Huadong Yin; Shunshun Han; Can Cui; Yan Wang; Diyan Li; Qing Zhu. 2021. "Plectin regulates Wnt signaling mediated-skeletal muscle development by interacting with Dishevelled-2 and antagonizing autophagy." Gene 783, no. : 145562.

Erratum
Published: 07 December 2020 in Animals
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The authors wish to make the following corrections to their paper

ACS Style

Jing Zhao; Xiaoxu Shen; Xinao Cao; Haorong He; Shunshun Han; Yuqi Chen; Can Cui; Yuanhang Wei; Yan Wang; Diyan Li; Qing Zhu; Huadong Yin. Erratum: Zhao, J.; Shen, X.; Cao, X.; He, H.; Han, S.; Chen, Y.; Cui, C.; Wei, Y.; Wang, Y.; Li, D.; Zhu, Q.; Yin, H. HDAC4 Regulates the Proliferation, Differentiation and Apoptosis of Chicken Skeletal Muscle Satellite Cells. Animals 2020, 10, 84. Animals 2020, 10, 2322 .

AMA Style

Jing Zhao, Xiaoxu Shen, Xinao Cao, Haorong He, Shunshun Han, Yuqi Chen, Can Cui, Yuanhang Wei, Yan Wang, Diyan Li, Qing Zhu, Huadong Yin. Erratum: Zhao, J.; Shen, X.; Cao, X.; He, H.; Han, S.; Chen, Y.; Cui, C.; Wei, Y.; Wang, Y.; Li, D.; Zhu, Q.; Yin, H. HDAC4 Regulates the Proliferation, Differentiation and Apoptosis of Chicken Skeletal Muscle Satellite Cells. Animals 2020, 10, 84. Animals. 2020; 10 (12):2322.

Chicago/Turabian Style

Jing Zhao; Xiaoxu Shen; Xinao Cao; Haorong He; Shunshun Han; Yuqi Chen; Can Cui; Yuanhang Wei; Yan Wang; Diyan Li; Qing Zhu; Huadong Yin. 2020. "Erratum: Zhao, J.; Shen, X.; Cao, X.; He, H.; Han, S.; Chen, Y.; Cui, C.; Wei, Y.; Wang, Y.; Li, D.; Zhu, Q.; Yin, H. HDAC4 Regulates the Proliferation, Differentiation and Apoptosis of Chicken Skeletal Muscle Satellite Cells. Animals 2020, 10, 84." Animals 10, no. 12: 2322.

Original research article
Published: 06 November 2020 in Frontiers in Cell and Developmental Biology
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Circular RNAs (circRNAs) are recognized as functional non-coding transcripts; however, emerging evidence has revealed that some synthetic circRNAs generate functional peptides or proteins. Additionally, the diverse biological functions of circRNAs include acting as miRNA-binding sponges, RNA-binding protein regulators, and protein translation templates. Previously, we found that circular RNA circFAM188B is a stable circular RNA and differentially expressed between broiler chickens and layers during embryonic skeletal muscle development. In this study, we found that circFAM188B exhibited a unique pattern of sharply decreased expression from embryonic day 10 (E10) to Day 35 (D35) after hatching. Our experimental results showed that circFAM188B promotes the proliferation, but inhibits the differentiation of chicken skeletal muscle satellite cells (SMSCs). Bioinformatic analysis revealed circFAM188B contain an opening reading frame (ORF) which translate into circFAM188B-103aa, internal ribosome entry site (IRES) analysis further confirmed the coding potential of circFAM188B. In addition, western blot assay detected a flag tagged circFAM188B-103aa, and several peptides of circFAM188B-103aa were detected by LC-MS/MS analysis. We further verified that the role of circFAM188B-103aa in chicken myogenesis is consistent with that of its parent transcript circFAM188B, which facilitates proliferation, but represses differentiation of chicken SMSC. Taken together, these results suggested that a novel protein circFAM188B-103aa encoded by circFAM188B that promotes the proliferation but inhibits the differentiation of chicken SMSCs.

ACS Style

Huadong Yin; Xiaoxu Shen; Jing Zhao; Xinao Cao; Haorong He; Shunshun Han; Yuqi Chen; Can Cui; Yuanhang Wei; Yan Wang; Diyan Li; Qing Zhu. Circular RNA CircFAM188B Encodes a Protein That Regulates Proliferation and Differentiation of Chicken Skeletal Muscle Satellite Cells. Frontiers in Cell and Developmental Biology 2020, 8, 1 .

AMA Style

Huadong Yin, Xiaoxu Shen, Jing Zhao, Xinao Cao, Haorong He, Shunshun Han, Yuqi Chen, Can Cui, Yuanhang Wei, Yan Wang, Diyan Li, Qing Zhu. Circular RNA CircFAM188B Encodes a Protein That Regulates Proliferation and Differentiation of Chicken Skeletal Muscle Satellite Cells. Frontiers in Cell and Developmental Biology. 2020; 8 ():1.

Chicago/Turabian Style

Huadong Yin; Xiaoxu Shen; Jing Zhao; Xinao Cao; Haorong He; Shunshun Han; Yuqi Chen; Can Cui; Yuanhang Wei; Yan Wang; Diyan Li; Qing Zhu. 2020. "Circular RNA CircFAM188B Encodes a Protein That Regulates Proliferation and Differentiation of Chicken Skeletal Muscle Satellite Cells." Frontiers in Cell and Developmental Biology 8, no. : 1.

Journal article
Published: 22 August 2020 in Animals
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Fibromodulin (Fmod), which is an extracellular matrix protein, belongs to the extracellular matrix small-leucine-rich proteoglycan family. Fmod is abundantly expressed in muscles and connective tissues and is involved in biological regulation processes, including cell apoptosis, cell adhesion, and modulation of cytokine activity. Fmod is the main regulator of myostatin, which controls the development of muscle cells, but its regulatory path is unknown. Chicken models are ideal for studying embryonic skeletal muscle development; therefore, to investigate the mechanism of Fmod in muscle development, Fmod-silenced and Fmod-overexpressed chicken myoblasts were constructed. The results showed that Fmod plays a positive role in differentiation by detecting the expression of myogenic differentiation markers, immunofluorescence of MyHC protein, and myotube formation in myoblasts. Fmod regulates expression of atrophy-related genes to alleviate muscle atrophy, which was confirmed by histological analysis of breast muscles in Fmod-modulated chicks in vivo. Additionally, genes differentially expressed between Fmod knockdown and normal myoblasts were enriched in the signaling pathway of transforming growth factor β (TGF-β). Both Fmod-silenced and Fmod-overexpressed myoblasts regulated the expression of TGFBR1 and p-Smad3. Thus, Fmod can promote differentiation but not proliferation of myoblasts by regulating the TGF-β signaling pathway, which may serve a function in muscular atrophy.

ACS Style

Huadong Yin; Can Cui; Shunshun Han; Yuqi Chen; Jing Zhao; Haorong He; Diyan Li; Qing Zhu. Fibromodulin Modulates Chicken Skeletal Muscle Development via the Transforming Growth Factor-β Signaling Pathway. Animals 2020, 10, 1477 .

AMA Style

Huadong Yin, Can Cui, Shunshun Han, Yuqi Chen, Jing Zhao, Haorong He, Diyan Li, Qing Zhu. Fibromodulin Modulates Chicken Skeletal Muscle Development via the Transforming Growth Factor-β Signaling Pathway. Animals. 2020; 10 (9):1477.

Chicago/Turabian Style

Huadong Yin; Can Cui; Shunshun Han; Yuqi Chen; Jing Zhao; Haorong He; Diyan Li; Qing Zhu. 2020. "Fibromodulin Modulates Chicken Skeletal Muscle Development via the Transforming Growth Factor-β Signaling Pathway." Animals 10, no. 9: 1477.

Journal article
Published: 04 August 2020 in International Journal of Molecular Sciences
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MicroRNAs (miRNAs) are evolutionarily conserved, small noncoding RNAs that post-transcriptionally regulate expression of their target genes. Emerging evidence demonstrates that miRNAs are important regulators in the development of skeletal muscle satellite cells (SMSCs). Our previous research showed that gga-miR-3525 is differentially expressed in breast muscle of broilers (high growth rate) and layers (low growth rate). In this study, we report a new role for gga-miR-3525 as a myogenic miRNA that regulates skeletal muscle development in chickens. Exogenous increases in the expression of gga-miR-3525 significantly inhibited proliferation and differentiation of SMSCs, whereas the opposite effects were observed in gga-miR-3525 knockdown SMSCs. We confirmed that PDLIM3 (PDZ and LIM domain 3) is a target gene of gga-miR-3525 that can promote proliferation and differentiation of SMSCs. We found that PDLIM3 overexpression elevated the abundance of phosphorylated (p-)p38 protein but that the gga-miR-3525 mimic and p38-MAPK inhibitor (SB203580) weakened the activation of p-p38. Furthermore, treatment with SB203580 reduced the promoting effect of PDLIM3 on SMSC proliferation and differentiation. Overall, our results indicate that gga-miR-3525 regulates the proliferation and differentiation of SMSCs by targeting PDLIM3 via the p38/MAPK signaling pathway in chickens.

ACS Style

Huadong Yin; Jing Zhao; Haorong He; Yuqi Chen; Yan Wang; Diyan Li; Qing Zhu. Gga-miR-3525 Targets PDLIM3 through the MAPK Signaling Pathway to Regulate the Proliferation and Differentiation of Skeletal Muscle Satellite Cells. International Journal of Molecular Sciences 2020, 21, 5573 .

AMA Style

Huadong Yin, Jing Zhao, Haorong He, Yuqi Chen, Yan Wang, Diyan Li, Qing Zhu. Gga-miR-3525 Targets PDLIM3 through the MAPK Signaling Pathway to Regulate the Proliferation and Differentiation of Skeletal Muscle Satellite Cells. International Journal of Molecular Sciences. 2020; 21 (15):5573.

Chicago/Turabian Style

Huadong Yin; Jing Zhao; Haorong He; Yuqi Chen; Yan Wang; Diyan Li; Qing Zhu. 2020. "Gga-miR-3525 Targets PDLIM3 through the MAPK Signaling Pathway to Regulate the Proliferation and Differentiation of Skeletal Muscle Satellite Cells." International Journal of Molecular Sciences 21, no. 15: 5573.

Original research article
Published: 04 June 2020 in Frontiers in Genetics
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As bioinformatic approaches have been developed, it has been demonstrated that microRNAs (miRNAs) are involved in the formation of muscles and play important roles in regulation of muscle cell proliferation and differentiation. Previously, it has been demonstrated that miR-148a-3p is one of the most abundant miRNAs in chicken skeletal muscle. Here, we build on that work and demonstrate that miR-148a-3p is important in the control of differentiation of chicken skeletal muscle satellite cells (SMSCs). Elevated expression of miR-148a-3p significantly promoted differentiation and inhibited apoptosis of SMSCs but did not affect proliferation. Furthermore, it was observed that the mesenchyme homeobox 2 (Meox2) is a target gene of miR-148a-3p and that miR-148a-3p can down-regulate expression of Meox2, which promote differentiation of SMSCs and suppress apoptosis. Furthermore, miR-148a-3p overexpression encouraged activation of the PI3K/AKT signaling pathway, which could be recovered by overexpression of Meox2. Overall, these findings suggest that microRNA-148a-3p is a potent promoter of myogenesis via direct targeting of Meox2 and increase of the PI3K/AKT signaling pathway in chicken SMSCs.

ACS Style

Huadong Yin; Haorong He; Xinao Cao; Xiaoxu Shen; Shunshun Han; Can Cui; Jing Zhao; Yuanhang Wei; Yuqi Chen; Lu Xia; Yan Wang; Diyan Li; Qing Zhu. MiR-148a-3p Regulates Skeletal Muscle Satellite Cell Differentiation and Apoptosis via the PI3K/AKT Signaling Pathway by Targeting Meox2. Frontiers in Genetics 2020, 11, 1 .

AMA Style

Huadong Yin, Haorong He, Xinao Cao, Xiaoxu Shen, Shunshun Han, Can Cui, Jing Zhao, Yuanhang Wei, Yuqi Chen, Lu Xia, Yan Wang, Diyan Li, Qing Zhu. MiR-148a-3p Regulates Skeletal Muscle Satellite Cell Differentiation and Apoptosis via the PI3K/AKT Signaling Pathway by Targeting Meox2. Frontiers in Genetics. 2020; 11 ():1.

Chicago/Turabian Style

Huadong Yin; Haorong He; Xinao Cao; Xiaoxu Shen; Shunshun Han; Can Cui; Jing Zhao; Yuanhang Wei; Yuqi Chen; Lu Xia; Yan Wang; Diyan Li; Qing Zhu. 2020. "MiR-148a-3p Regulates Skeletal Muscle Satellite Cell Differentiation and Apoptosis via the PI3K/AKT Signaling Pathway by Targeting Meox2." Frontiers in Genetics 11, no. : 1.

Journal article
Published: 05 May 2020 in International Journal of Molecular Sciences
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MicroRNAs (miRNAs) are evolutionarily conserved, small noncoding RNAs that play critical post-transcriptional regulatory roles in skeletal muscle development. Chicken is an optimal model to study skeletal muscle formation because its developmental anatomy is similar to that of mammals. In this study, we identified potential miRNAs in the breast muscle of broilers and layers at embryonic day 10 (E10), E13, E16, and E19. We detected 1836 miRNAs, 233 of which were differentially expressed between broilers and layers. In particular, miRNA-200a-3p was significantly more highly expressed in broilers than layers at three time points. In vitro experiments showed that miR-200a-3p accelerated differentiation and proliferation of chicken skeletal muscle satellite cells (SMSCs) and inhibited SMSCs apoptosis. The transforming growth factor 2 (TGF-β2) was identified as a target gene of miR-200a-3p, and which turned out to inhibit differentiation and proliferation, and promote apoptosis of SMSCs. Exogenous TGF-β2 increased the abundances of phosphorylated SMAD2 and SMAD3 proteins, and a miR-200a-3p mimic weakened this effect. The TGF-β2 inhibitor treatment reduced the promotional and inhibitory effects of miR-200a-3p on SMSC differentiation and apoptosis, respectively. Our results indicate that miRNAs are abundantly expressed during embryonic skeletal muscle development, and that miR-200a-3p promotes SMSC development by targeting TGF-β2 and regulating the TGF-β2/SMAD signaling pathway.

ACS Style

Huadong Yin; Haorong He; Xiaoxu Shen; Shuyue Tang; Jing Zhao; Xinao Cao; Shunshun Han; Can Cui; Yuqi Chen; Yuanhang Wei; Yan Wang; Diyan Li; Qing Zhu. MicroRNA Profiling Reveals an Abundant miR-200a-3p Promotes Skeletal Muscle Satellite Cell Development by Targeting TGF-β2 and Regulating the TGF-β2/SMAD Signaling Pathway. International Journal of Molecular Sciences 2020, 21, 3274 .

AMA Style

Huadong Yin, Haorong He, Xiaoxu Shen, Shuyue Tang, Jing Zhao, Xinao Cao, Shunshun Han, Can Cui, Yuqi Chen, Yuanhang Wei, Yan Wang, Diyan Li, Qing Zhu. MicroRNA Profiling Reveals an Abundant miR-200a-3p Promotes Skeletal Muscle Satellite Cell Development by Targeting TGF-β2 and Regulating the TGF-β2/SMAD Signaling Pathway. International Journal of Molecular Sciences. 2020; 21 (9):3274.

Chicago/Turabian Style

Huadong Yin; Haorong He; Xiaoxu Shen; Shuyue Tang; Jing Zhao; Xinao Cao; Shunshun Han; Can Cui; Yuqi Chen; Yuanhang Wei; Yan Wang; Diyan Li; Qing Zhu. 2020. "MicroRNA Profiling Reveals an Abundant miR-200a-3p Promotes Skeletal Muscle Satellite Cell Development by Targeting TGF-β2 and Regulating the TGF-β2/SMAD Signaling Pathway." International Journal of Molecular Sciences 21, no. 9: 3274.

Journal article
Published: 04 May 2020 in Toxins
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Aflatoxin B1 (AFB1) leads to a major risk to poultry and its residues in meat products can also pose serious threat to human health. In this study, after feeding 165-day-old Roman laying hens for 35 days, the toxic effects of aflatoxin B1 at different concentrations were evaluated. The purpose of this study was to explore the mechanism of liver toxicosis responses to AFB1. We found that highly toxic group exposure resulted in liver fat deposition, increased interstitial space, and hepatocyte apoptosis in laying hens. Furthermore, a total of 164 differentially expressed lnRNAs and 186 differentially expressed genes were found to be highly correlated (Pearson Correlation Coefficient > 0.80, p-value < 0.05) by sequencing the transcriptome of control (CB) and highly toxic group (TB3) chickens. We also identify 29 differentially expressed genes and 19 miRNAs that have targeted regulatory relationships. Based on the liver cell apoptosis and fatty liver syndrome that this research focused on, we found that the highly toxic AFB1 led to dysregulation of the expression of PPARG and BCL6. They are cis-regulated by TU10057 and TU45776, respectively. PPARG was the target gene of gga-miR-301a-3p, gga-miR-301b-3p, and BCL6 was the target gene of gga-miR-190a-3p. In summary, highly toxic AFB1 affects the expression levels of protein-coding genes and miRNAs in the liver of Roman layer hens, as well as the expression level of long non-coding RNA in the liver, which upregulates the expression of PPARG and downregulates the expression of Bcl-6. Our study provides information on possible genetic regulatory networks in AFB1-induced hepatic fat deposition and hepatocyte apoptosis.

ACS Style

Xueqin Liu; Shailendra Kumar Mishra; Tao Wang; Zhongxian Xu; Xiaoling Zhao; Yan Wang; Huadong Yin; Xiaolan Fan; Bo Zeng; Mingyao Yang; Deying Yang; Qingyong Ni; Yan Li; Mingwang Zhang; Qing Zhu; Feng Chen; Diyan Li. AFB1 Induced Transcriptional Regulation Related to Apoptosis and Lipid Metabolism in Liver of Chicken. Toxins 2020, 12, 290 .

AMA Style

Xueqin Liu, Shailendra Kumar Mishra, Tao Wang, Zhongxian Xu, Xiaoling Zhao, Yan Wang, Huadong Yin, Xiaolan Fan, Bo Zeng, Mingyao Yang, Deying Yang, Qingyong Ni, Yan Li, Mingwang Zhang, Qing Zhu, Feng Chen, Diyan Li. AFB1 Induced Transcriptional Regulation Related to Apoptosis and Lipid Metabolism in Liver of Chicken. Toxins. 2020; 12 (5):290.

Chicago/Turabian Style

Xueqin Liu; Shailendra Kumar Mishra; Tao Wang; Zhongxian Xu; Xiaoling Zhao; Yan Wang; Huadong Yin; Xiaolan Fan; Bo Zeng; Mingyao Yang; Deying Yang; Qingyong Ni; Yan Li; Mingwang Zhang; Qing Zhu; Feng Chen; Diyan Li. 2020. "AFB1 Induced Transcriptional Regulation Related to Apoptosis and Lipid Metabolism in Liver of Chicken." Toxins 12, no. 5: 290.

Journal article
Published: 29 March 2020 in Genes
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Noncoding RNAs, especially microRNAs (miRNAs), have been reported to play important roles during skeletal muscle development and regeneration. Our previous sequencing data revealed that miR-99a-5p is one of the most abundant miRNAs in chicken breast muscle. The purpose of this study was to reveal the regulatory mechanism of miR-99a-5p in the proliferation and differentiation of chicken skeletal muscle satellite cells (SMSCs). Through the investigation of cell proliferation activity, cell cycle progression, and 5-ethynyl-29-deoxyuridine (EdU) assay, we found that miR-99a-5p can significantly promote the proliferation of SMSCs. Moreover, we found that miR-99a-5p can inhibit myotube formation by decreasing the expression of muscle cell differentiation marker genes. After miR-99a-5p target gene scanning, we confirmed that miR-99a-5p directly targets the 3′ untranslated region (UTR) of myotubularin-related protein 3 (MTMR3) and regulates its expression level during chicken SMSC proliferation and differentiation. We also explored the role of MTMR3 in muscle development and found that its knockdown significantly facilitates the proliferation but represses the differentiation of SMSCs, which is opposite to the effects of miR-99a-5p. Overall, we demonstrated that miR-99a-5p regulates the proliferation and differentiation of SMSCs by targeting MTMR3.

ACS Style

Xinao Cao; Shuyue Tang; Fei Du; Hao Li; Xiaoxu Shen; Diyan Li; Yan Wang; Zhichao Zhang; Lu Xia; Qing Zhu; Huadong Yin. miR-99a-5p Regulates the Proliferation and Differentiation of Skeletal Muscle Satellite Cells by Targeting MTMR3 in Chicken. Genes 2020, 11, 369 .

AMA Style

Xinao Cao, Shuyue Tang, Fei Du, Hao Li, Xiaoxu Shen, Diyan Li, Yan Wang, Zhichao Zhang, Lu Xia, Qing Zhu, Huadong Yin. miR-99a-5p Regulates the Proliferation and Differentiation of Skeletal Muscle Satellite Cells by Targeting MTMR3 in Chicken. Genes. 2020; 11 (4):369.

Chicago/Turabian Style

Xinao Cao; Shuyue Tang; Fei Du; Hao Li; Xiaoxu Shen; Diyan Li; Yan Wang; Zhichao Zhang; Lu Xia; Qing Zhu; Huadong Yin. 2020. "miR-99a-5p Regulates the Proliferation and Differentiation of Skeletal Muscle Satellite Cells by Targeting MTMR3 in Chicken." Genes 11, no. 4: 369.

Original article
Published: 17 March 2020 in 3 Biotech
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The Src homology 3 and cysteine-rich domain 3 gene (STAC3) encodes a protein containing both a cysteine-rich domain and two Src (sarcoma) homology 3 domains (SH3). STAC3 is specifically expressed in skeletal muscle and plays an important role in skeletal muscle development, but the explicit sequence and function of chicken SATC3 remain unknown. In the current study, we found the full-length chicken STAC3 cDNA to be 1383 bp long, with a 1092 bp open reading frame that harbors one cysteine-rich C1 domain and two SH3 domains. Tissue distribution analysis reveals chicken STAC3 mRNA only in skeletal muscle among 12 chicken tissues examined by reverse transcription PCR. Both cholecystokinin octapeptide analysis and a 5-ethynyl-2′-deoxyuridine assay suggest that neither STAC3 overexpression nor knockdown has any effect on the proliferation of chicken skeletal muscle satellite cells. However, STAC3 knockdown significantly increases the mRNA expression of MyoG, MyoD, Mb, and MyHC, and the protein abundance of MyHC and MyoG, whereas the opposite result is found in STAC3 overexpressed cells. We conclude that the STAC3 gene is expressed specifically in skeletal muscle and is a negative regulator of skeletal muscle satellite cell differentiation in chicken.

ACS Style

Huadong Yin; Jing Zhao; Shunshun Han; Can Cui; Yan Wang; Diyan Li; Qing Zhu. Molecular characterization, tissue distribution, and functional analysis of the STAC3 gene in chicken. 3 Biotech 2020, 10, 1 -10.

AMA Style

Huadong Yin, Jing Zhao, Shunshun Han, Can Cui, Yan Wang, Diyan Li, Qing Zhu. Molecular characterization, tissue distribution, and functional analysis of the STAC3 gene in chicken. 3 Biotech. 2020; 10 (4):1-10.

Chicago/Turabian Style

Huadong Yin; Jing Zhao; Shunshun Han; Can Cui; Yan Wang; Diyan Li; Qing Zhu. 2020. "Molecular characterization, tissue distribution, and functional analysis of the STAC3 gene in chicken." 3 Biotech 10, no. 4: 1-10.

Journal article
Published: 28 February 2020 in International Journal of Molecular Sciences
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MicroRNAs are evolutionarily conserved, small non-coding RNAs that play critical post-transcriptional regulatory roles in skeletal muscle development. We previously found that miR-9-5p is abundantly expressed in chicken skeletal muscle. Here, we demonstrate a new role for miR-9-5p as a myogenic microRNA that regulates skeletal muscle development. The overexpression of miR-9-5p significantly inhibited the proliferation and differentiation of skeletal muscle satellite cells (SMSCs), whereas miR-9-5p inhibition had the opposite effect. We show that insulin-like growth factor 2 mRNA-binding protein 3 (IGF2BP3) is a target gene of miR-9-5p, using dual-luciferase assays, RT-qPCR, and Western Blotting, and that it promotes proliferation and differentiation of SMSCs. In addition, we found that IGF2BP3 regulates IGF-2 expression, using overexpression and knockdown studies. We show that Akt is activated by IGF2BP3 and is essential for IGF2BP3-induced cell development. Together, our results indicate that miR-9-5p could regulate the proliferation and differentiation of myoblasts by targeting IGF2BP3 through IGF-2 and that this activity results in the activation of the PI3K/Akt signaling pathway in skeletal muscle cells.

ACS Style

Huadong Yin; Haorong He; Xiaoxu Shen; Jing Zhao; Xinao Cao; Shunshun Han; Can Cui; Yuqi Chen; Yuanhang Wei; Lu Xia; Yan Wang; Diyan Li; Qing Zhu. miR-9-5p Inhibits Skeletal Muscle Satellite Cell Proliferation and Differentiation by Targeting IGF2BP3 through the IGF2-PI3K/Akt Signaling Pathway. International Journal of Molecular Sciences 2020, 21, 1655 .

AMA Style

Huadong Yin, Haorong He, Xiaoxu Shen, Jing Zhao, Xinao Cao, Shunshun Han, Can Cui, Yuqi Chen, Yuanhang Wei, Lu Xia, Yan Wang, Diyan Li, Qing Zhu. miR-9-5p Inhibits Skeletal Muscle Satellite Cell Proliferation and Differentiation by Targeting IGF2BP3 through the IGF2-PI3K/Akt Signaling Pathway. International Journal of Molecular Sciences. 2020; 21 (5):1655.

Chicago/Turabian Style

Huadong Yin; Haorong He; Xiaoxu Shen; Jing Zhao; Xinao Cao; Shunshun Han; Can Cui; Yuqi Chen; Yuanhang Wei; Lu Xia; Yan Wang; Diyan Li; Qing Zhu. 2020. "miR-9-5p Inhibits Skeletal Muscle Satellite Cell Proliferation and Differentiation by Targeting IGF2BP3 through the IGF2-PI3K/Akt Signaling Pathway." International Journal of Molecular Sciences 21, no. 5: 1655.

Journal article
Published: 29 January 2020 in Toxins
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T-2 toxin is type A trichothecenes mycotoxin, which produced by fusarium species in cereal grains. T-2 toxin has been shown to induce a series of toxic effects on the health of human and animal, such as immunosuppression and carcinogenesis. Previous study has proven that T-2 toxin caused hepatotoxicity in chicken, but the regulatory mechanism is unclear. In the present study, we assessed the toxicological effect of T-2 toxin on apoptosis and autophagy in hepatocytes. The total of 120 1-day-old healthy broilers were allocated randomly into four groups and reared for 21 day with complete feed containing 0 mg/kg, 0.5 mg/kg, 1 mg/kg or 2 mg/kg T-2 toxin, respectively. The results showed that the apoptosis rate and pathological changes degree hepatocytes were aggravated with the increase of T-2 toxin. At the molecular mechanism level, T-2 toxin induced mitochondria-mediated apoptosis by producing reactive oxygen species, promoting cytochrome c translocation between the mitochondria and cytoplasm, and thus promoting apoptosomes formation. Meanwhile, the expression of the autophagy-related protein, ATG5, ATG7 and Beclin-1, and the LC3-II/LC3-I ratio were increased, while p62 was downregulated, suggesting T-2 toxin caused autophagy in hepatocytes. Further experiments demonstrated that the PI3K/AKT/mTOR signal may be participated in autophagy induced by T-2 toxin in chicken hepatocytes. These data suggest a possible underlying molecular mechanism for T-2 toxin that induces apoptosis and autophagy in chicken hepatocytes

ACS Style

Huadong Yin; Shunshun Han; Yuqi Chen; Yan Wang; Diyan Li; Qing Zhu. T-2 Toxin Induces Oxidative Stress, Apoptosis and Cytoprotective Autophagy in Chicken Hepatocytes. Toxins 2020, 12, 90 .

AMA Style

Huadong Yin, Shunshun Han, Yuqi Chen, Yan Wang, Diyan Li, Qing Zhu. T-2 Toxin Induces Oxidative Stress, Apoptosis and Cytoprotective Autophagy in Chicken Hepatocytes. Toxins. 2020; 12 (2):90.

Chicago/Turabian Style

Huadong Yin; Shunshun Han; Yuqi Chen; Yan Wang; Diyan Li; Qing Zhu. 2020. "T-2 Toxin Induces Oxidative Stress, Apoptosis and Cytoprotective Autophagy in Chicken Hepatocytes." Toxins 12, no. 2: 90.

Journal article
Published: 23 January 2020 in International Journal of Molecular Sciences
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CSRP3/MLP (cysteine-rich protein 3/muscle Lim protein), a member of the cysteine-rich protein family, is a muscle-specific LIM-only factor specifically expressed in skeletal muscle. CSRP3 is critical in maintaining the structure and function of normal muscle. To investigate the mechanism of disease in CSRP3 myopathy, we performed siRNA-mediated CSRP3 knockdown in chicken primary myoblasts. CSRP3 silencing resulted in the down-regulation of the expression of myogenic genes and the up-regulation of atrophy-related gene expressions. We found that CSRP3 interacted with LC3 protein to promote the formation of autophagosomes during autophagy. CSRP3-silencing impaired myoblast autophagy, as evidenced by inhibited autophagy-related ATG5 and ATG7 mRNA expression levels, and inhibited LC3II and Beclin-1 protein accumulation. In addition, impaired autophagy in CSRP3-silenced cells resulted in increased sensitivity to apoptosis cell death. CSRP3-silenced cells also showed increased caspase-3 and caspase-9 cleavage. Moreover, apoptosis induced by CSRP3 silencing was alleviated after autophagy activation. Together, these results indicate that CSRP3 promotes the correct formation of autophagosomes through its interaction with LC3 protein, which has an important role in skeletal muscle remodeling and maintenance.

ACS Style

Can Cui; Shunshun Han; Shuyue Tang; Haorong He; Xiaoxu Shen; Jing Zhao; Yuqi Chen; Yuanhang Wei; Yan Wang; Qing Zhu; Diyan Li; And Huadong Yin. The Autophagy Regulatory Molecule CSRP3 Interacts with LC3 and Protects Against Muscular Dystrophy. International Journal of Molecular Sciences 2020, 21, 749 .

AMA Style

Can Cui, Shunshun Han, Shuyue Tang, Haorong He, Xiaoxu Shen, Jing Zhao, Yuqi Chen, Yuanhang Wei, Yan Wang, Qing Zhu, Diyan Li, And Huadong Yin. The Autophagy Regulatory Molecule CSRP3 Interacts with LC3 and Protects Against Muscular Dystrophy. International Journal of Molecular Sciences. 2020; 21 (3):749.

Chicago/Turabian Style

Can Cui; Shunshun Han; Shuyue Tang; Haorong He; Xiaoxu Shen; Jing Zhao; Yuqi Chen; Yuanhang Wei; Yan Wang; Qing Zhu; Diyan Li; And Huadong Yin. 2020. "The Autophagy Regulatory Molecule CSRP3 Interacts with LC3 and Protects Against Muscular Dystrophy." International Journal of Molecular Sciences 21, no. 3: 749.

Journal article
Published: 04 January 2020 in Animals
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The development of skeletal muscle satellite cells (SMSCs) is a complex process that could be regulated by many genes. Previous studies have shown that Histone Deacetylase 4 (HDAC4) plays a critical role in cell proliferation, differentiation, and apoptosis in mouse. However, the function of HDAC4 in chicken muscle development is still unknown. Given that chicken is a very important meat-producing animal that is also an ideal model to study skeletal muscle development, we explored the functions of HDAC4 in chicken SMSCs after the interference of HDAC4. The results showed that HDAC4 was enriched in embryonic skeletal muscle, and it was highly expressed in embryonic muscle than in postnatal muscles. Meanwhile, knockdown of HDAC4 could significantly inhibit the proliferation and differentiation of chicken SMSCs but had no effect on the apoptosis of SMSCs as observed in a series of experiment conducted in vitro. These results indicated that HDAC4 might play a positive role in chicken skeletal muscle growth and development.

ACS Style

Jing Zhao; Xiaoxu Shen; Xinao Cao; Haorong He; Shunshun Han; Yuqi Chen; Can Cui; Yuanhang Wei; Yan Wang; Diyan Li; Qing Zhu; Huadong Yin. HDAC4 Regulates the Proliferation, Differentiation and Apoptosis of Chicken Skeletal Muscle Satellite Cells. Animals 2020, 10, 84 .

AMA Style

Jing Zhao, Xiaoxu Shen, Xinao Cao, Haorong He, Shunshun Han, Yuqi Chen, Can Cui, Yuanhang Wei, Yan Wang, Diyan Li, Qing Zhu, Huadong Yin. HDAC4 Regulates the Proliferation, Differentiation and Apoptosis of Chicken Skeletal Muscle Satellite Cells. Animals. 2020; 10 (1):84.

Chicago/Turabian Style

Jing Zhao; Xiaoxu Shen; Xinao Cao; Haorong He; Shunshun Han; Yuqi Chen; Can Cui; Yuanhang Wei; Yan Wang; Diyan Li; Qing Zhu; Huadong Yin. 2020. "HDAC4 Regulates the Proliferation, Differentiation and Apoptosis of Chicken Skeletal Muscle Satellite Cells." Animals 10, no. 1: 84.

Journal article
Published: 16 October 2019 in International Journal of Molecular Sciences
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Myoferlin (MyoF), which is a calcium/phospholipid-binding protein expressed in cardiac and muscle tissues, belongs to the ferlin family. While MyoF promotes myoblast differentiation, the underlying mechanisms remain poorly understood. Here, we found that MyoF not only promotes C2C12 myoblast differentiation, but also inhibits muscle atrophy and autophagy. In the present study, we found that myoblasts fail to develop into mature myotubes due to defective differentiation in the absence of MyoF. Meanwhile, MyoF regulates the expression of atrophy-related genes (Atrogin-1 and MuRF1) to rescue muscle atrophy. Furthermore, MyoF interacts with Dishevelled-2 (Dvl-2) to activate canonical Wnt signaling. MyoF facilitates Dvl-2 ubiquitination resistance by reducing LC3-labeled Dvl-2 levels and antagonizing the autophagy system. In conclusion, we found that MyoF plays an important role in myoblast differentiation during skeletal muscle atrophy. At the molecular level, MyoF protects Dvl-2 against autophagy-mediated degradation, thus promoting activation of the Wnt/β-catenin signaling pathway. Together, our findings suggest that MyoF, through stabilizing Dvl-2 and preventing autophagy, regulates Wnt/β-catenin signaling-mediated skeletal muscle development.

ACS Style

Shunshun Han; Can Cui; Haorong He; Xiaoxu Shen; Yuqi Chen; Yan Wang; Diyan Li; Qing Zhu; Huadong Yin. Myoferlin Regulates Wnt/β-Catenin Signaling-Mediated Skeletal Muscle Development by Stabilizing Dishevelled-2 Against Autophagy. International Journal of Molecular Sciences 2019, 20, 5130 .

AMA Style

Shunshun Han, Can Cui, Haorong He, Xiaoxu Shen, Yuqi Chen, Yan Wang, Diyan Li, Qing Zhu, Huadong Yin. Myoferlin Regulates Wnt/β-Catenin Signaling-Mediated Skeletal Muscle Development by Stabilizing Dishevelled-2 Against Autophagy. International Journal of Molecular Sciences. 2019; 20 (20):5130.

Chicago/Turabian Style

Shunshun Han; Can Cui; Haorong He; Xiaoxu Shen; Yuqi Chen; Yan Wang; Diyan Li; Qing Zhu; Huadong Yin. 2019. "Myoferlin Regulates Wnt/β-Catenin Signaling-Mediated Skeletal Muscle Development by Stabilizing Dishevelled-2 Against Autophagy." International Journal of Molecular Sciences 20, no. 20: 5130.

Original article
Published: 04 October 2019 in 3 Biotech
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Chinese indigenous chickens have experienced strong selective pressure in genes or genomic regions controlling critical agricultural traits. To exploit the genetic features that may be useful in agriculture and are caused by artificial selection, we performed whole-genome sequencing of six Pengxian Yellow Chickens and downloaded the sequence data of five Red Jungle fowls from the NCBI. Through selective sweep analysis, we detected several regions with strong selection signals, containing 497 protein-coding genes. These genes were involved in developmental processes, metabolic processes, the response to external stimuli and other biological processes including digestion (ABCG5, ABCG8 and ADRB1), muscle development and growth (SMPD3, NELL1, and BICC1) and reduced immune function (CD86 and MTA3). Interestingly, we identified several genes with extremely strong selection signals associated with the loss of visual capability of domestic chickens relative to their wild ancestors. Amongst them, we propose that CTNND2 is involved in the evolutionary changes of domestic chickens toward reduced visual ability through the diopter system. VAT1 was also likely to contribute to these processes through its regulation of mitochondrial fusion. In summary, these data illustrate the patterns of genetic changes in Pengxian yellow chickens during domestication and provide valuable genetic resources that facilitate the utilization of chickens in agricultural production.

ACS Style

Huadong Yin; Diyan Li; Yan Wang; Qing Zhu. Whole-genome resequencing analysis of Pengxian Yellow Chicken to identify genome-wide SNPs and signatures of selection. 3 Biotech 2019, 9, 1 -10.

AMA Style

Huadong Yin, Diyan Li, Yan Wang, Qing Zhu. Whole-genome resequencing analysis of Pengxian Yellow Chicken to identify genome-wide SNPs and signatures of selection. 3 Biotech. 2019; 9 (11):1-10.

Chicago/Turabian Style

Huadong Yin; Diyan Li; Yan Wang; Qing Zhu. 2019. "Whole-genome resequencing analysis of Pengxian Yellow Chicken to identify genome-wide SNPs and signatures of selection." 3 Biotech 9, no. 11: 1-10.