Atg7-Mediated Autophagy Is Involved in the Neural Crest Cell Generation in Chick Embryo

Guang Wang, En-ni Chen, Chang Liang, Jianxin Liang, Lin-rui Gao, Manli Chuai, Andrea Münsterberg, Yongping Bao, Liu Cao (Lead / Corresponding author), Xuesong Yang (Lead / Corresponding author)

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Abstract

Autophagy plays a very important role in numerous physiological and pathological events. However, it still remains unclear whether Atg7-induced autophagy is involved in the regulation of neural crest cell production. In this study, we found the co-location of Atg7 and Pax7(+) neural crest cells in early chick embryo development. Upregulation of Atg7 with unilateral transfection of full-length Atg7 increased Pax7(+) and HNK-1(+) cephalic and trunk neural crest cell numbers compared to either Control-GFP transfection or opposite neural tubes, suggesting that Atg7 over-expression in neural tubes could enhance the production of neural crest cells. BMP4 in situ hybridization and p-Smad1/5/8 immunofluorescent staining demonstrated that upregulation of Atg7 in neural tubes suppressed the BMP4/Smad signaling, which is considered to promote the delamination of neural crest cells. Interestingly, upregulation of Atg7 in neural tubes could significantly accelerate cell progression into the S phase, implying that Atg7 modulates cell cycle progression. However, β-catenin expression was not significantly altered. Finally, we demonstrated that upregulation of the Atg7 gene could activate autophagy as did Atg8. We have also observed that similar phenotypes, such as more HNK-1(+) neural crest cells in the unilateral Atg8 transfection side of neural tubes, and the transfection with full-length Atg8-GFP certainly promote the numbers of BrdU(+) neural crest cells in comparison to the GFP control. Taken together, we reveal that Atg7-induced autophagy is involved in regulating the production of neural crest cells in early chick embryos through the modification of the cell cycle.

Original languageEnglish
Pages (from-to)3523-3536
Number of pages14
JournalMolecular Neurobiology
Volume55
Issue number4
Early online date16 May 2017
DOIs
Publication statusPublished - Apr 2018

Fingerprint

Neural Crest
Autophagy
Chick Embryo
Neural Tube
Transfection
Up-Regulation
Cell Cycle
Catenins
Bromodeoxyuridine
S Phase
Embryonic Development
In Situ Hybridization
Cell Count
Head
Staining and Labeling
Phenotype

Keywords

  • Atg7
  • Autophagy
  • Cell cycle
  • Neural crest

Cite this

Wang, Guang ; Chen, En-ni ; Liang, Chang ; Liang, Jianxin ; Gao, Lin-rui ; Chuai, Manli ; Münsterberg, Andrea ; Bao, Yongping ; Cao, Liu ; Yang, Xuesong. / Atg7-Mediated Autophagy Is Involved in the Neural Crest Cell Generation in Chick Embryo. In: Molecular Neurobiology. 2018 ; Vol. 55, No. 4. pp. 3523-3536.
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abstract = "Autophagy plays a very important role in numerous physiological and pathological events. However, it still remains unclear whether Atg7-induced autophagy is involved in the regulation of neural crest cell production. In this study, we found the co-location of Atg7 and Pax7(+) neural crest cells in early chick embryo development. Upregulation of Atg7 with unilateral transfection of full-length Atg7 increased Pax7(+) and HNK-1(+) cephalic and trunk neural crest cell numbers compared to either Control-GFP transfection or opposite neural tubes, suggesting that Atg7 over-expression in neural tubes could enhance the production of neural crest cells. BMP4 in situ hybridization and p-Smad1/5/8 immunofluorescent staining demonstrated that upregulation of Atg7 in neural tubes suppressed the BMP4/Smad signaling, which is considered to promote the delamination of neural crest cells. Interestingly, upregulation of Atg7 in neural tubes could significantly accelerate cell progression into the S phase, implying that Atg7 modulates cell cycle progression. However, β-catenin expression was not significantly altered. Finally, we demonstrated that upregulation of the Atg7 gene could activate autophagy as did Atg8. We have also observed that similar phenotypes, such as more HNK-1(+) neural crest cells in the unilateral Atg8 transfection side of neural tubes, and the transfection with full-length Atg8-GFP certainly promote the numbers of BrdU(+) neural crest cells in comparison to the GFP control. Taken together, we reveal that Atg7-induced autophagy is involved in regulating the production of neural crest cells in early chick embryos through the modification of the cell cycle.",
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author = "Guang Wang and En-ni Chen and Chang Liang and Jianxin Liang and Lin-rui Gao and Manli Chuai and Andrea M{\"u}nsterberg and Yongping Bao and Liu Cao and Xuesong Yang",
note = "This study was supported by NSFC grant (81571436, 31401230), Science and Technology Planning Project of Guangdong Province (2016B030229002), Science and Technology Program of Guangzhou (201710010054, 201510010073), Guangdong Natural Science Foundation (2016A030311044), Research Grant of Key Laboratory of Regenerative Medicine, Ministry of Education, Jinan University (Nos. ZSYX-M-00001 and ZSYX-T-00001), Fund for Science and Technology Innovation of Guangdong College Student (pdjh 2017b060) and Students Research Training Program Fund (CX16014, 16112011).",
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Wang, G, Chen, E, Liang, C, Liang, J, Gao, L, Chuai, M, Münsterberg, A, Bao, Y, Cao, L & Yang, X 2018, 'Atg7-Mediated Autophagy Is Involved in the Neural Crest Cell Generation in Chick Embryo', Molecular Neurobiology, vol. 55, no. 4, pp. 3523-3536. https://doi.org/10.1007/s12035-017-0583-6

Atg7-Mediated Autophagy Is Involved in the Neural Crest Cell Generation in Chick Embryo. / Wang, Guang; Chen, En-ni; Liang, Chang; Liang, Jianxin; Gao, Lin-rui; Chuai, Manli; Münsterberg, Andrea; Bao, Yongping; Cao, Liu (Lead / Corresponding author); Yang, Xuesong (Lead / Corresponding author).

In: Molecular Neurobiology, Vol. 55, No. 4, 04.2018, p. 3523-3536.

Research output: Contribution to journalArticle

TY - JOUR

T1 - Atg7-Mediated Autophagy Is Involved in the Neural Crest Cell Generation in Chick Embryo

AU - Wang, Guang

AU - Chen, En-ni

AU - Liang, Chang

AU - Liang, Jianxin

AU - Gao, Lin-rui

AU - Chuai, Manli

AU - Münsterberg, Andrea

AU - Bao, Yongping

AU - Cao, Liu

AU - Yang, Xuesong

N1 - This study was supported by NSFC grant (81571436, 31401230), Science and Technology Planning Project of Guangdong Province (2016B030229002), Science and Technology Program of Guangzhou (201710010054, 201510010073), Guangdong Natural Science Foundation (2016A030311044), Research Grant of Key Laboratory of Regenerative Medicine, Ministry of Education, Jinan University (Nos. ZSYX-M-00001 and ZSYX-T-00001), Fund for Science and Technology Innovation of Guangdong College Student (pdjh 2017b060) and Students Research Training Program Fund (CX16014, 16112011).

PY - 2018/4

Y1 - 2018/4

N2 - Autophagy plays a very important role in numerous physiological and pathological events. However, it still remains unclear whether Atg7-induced autophagy is involved in the regulation of neural crest cell production. In this study, we found the co-location of Atg7 and Pax7(+) neural crest cells in early chick embryo development. Upregulation of Atg7 with unilateral transfection of full-length Atg7 increased Pax7(+) and HNK-1(+) cephalic and trunk neural crest cell numbers compared to either Control-GFP transfection or opposite neural tubes, suggesting that Atg7 over-expression in neural tubes could enhance the production of neural crest cells. BMP4 in situ hybridization and p-Smad1/5/8 immunofluorescent staining demonstrated that upregulation of Atg7 in neural tubes suppressed the BMP4/Smad signaling, which is considered to promote the delamination of neural crest cells. Interestingly, upregulation of Atg7 in neural tubes could significantly accelerate cell progression into the S phase, implying that Atg7 modulates cell cycle progression. However, β-catenin expression was not significantly altered. Finally, we demonstrated that upregulation of the Atg7 gene could activate autophagy as did Atg8. We have also observed that similar phenotypes, such as more HNK-1(+) neural crest cells in the unilateral Atg8 transfection side of neural tubes, and the transfection with full-length Atg8-GFP certainly promote the numbers of BrdU(+) neural crest cells in comparison to the GFP control. Taken together, we reveal that Atg7-induced autophagy is involved in regulating the production of neural crest cells in early chick embryos through the modification of the cell cycle.

AB - Autophagy plays a very important role in numerous physiological and pathological events. However, it still remains unclear whether Atg7-induced autophagy is involved in the regulation of neural crest cell production. In this study, we found the co-location of Atg7 and Pax7(+) neural crest cells in early chick embryo development. Upregulation of Atg7 with unilateral transfection of full-length Atg7 increased Pax7(+) and HNK-1(+) cephalic and trunk neural crest cell numbers compared to either Control-GFP transfection or opposite neural tubes, suggesting that Atg7 over-expression in neural tubes could enhance the production of neural crest cells. BMP4 in situ hybridization and p-Smad1/5/8 immunofluorescent staining demonstrated that upregulation of Atg7 in neural tubes suppressed the BMP4/Smad signaling, which is considered to promote the delamination of neural crest cells. Interestingly, upregulation of Atg7 in neural tubes could significantly accelerate cell progression into the S phase, implying that Atg7 modulates cell cycle progression. However, β-catenin expression was not significantly altered. Finally, we demonstrated that upregulation of the Atg7 gene could activate autophagy as did Atg8. We have also observed that similar phenotypes, such as more HNK-1(+) neural crest cells in the unilateral Atg8 transfection side of neural tubes, and the transfection with full-length Atg8-GFP certainly promote the numbers of BrdU(+) neural crest cells in comparison to the GFP control. Taken together, we reveal that Atg7-induced autophagy is involved in regulating the production of neural crest cells in early chick embryos through the modification of the cell cycle.

KW - Atg7

KW - Autophagy

KW - Cell cycle

KW - Neural crest

U2 - 10.1007/s12035-017-0583-6

DO - 10.1007/s12035-017-0583-6

M3 - Article

C2 - 28509082

VL - 55

SP - 3523

EP - 3536

JO - Molecular Neurobiology

JF - Molecular Neurobiology

SN - 0893-7648

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ER -