β-Catenin regulates ovarian granulosa cell cycle and proliferation in laying hens by interacting with TCF4

ABSTRACT: Ovarian follicle development depends on the proliferation and differentiation of granulosa cells and is a complex biological process. The Wnt/β-catenin signaling pathway can regulate ovarian follicle development, and β-catenin, encoded by catenin beta 1 (CTNNB1), is the core component of t...

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Main Authors: Xueying Ma, Xu Han, Wenwen Wang, Qin Zhang, Hui Tang
Format: Article
Language:English
Published: Elsevier 2024-03-01
Series:Poultry Science
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0032579123008970
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author Xueying Ma
Xu Han
Wenwen Wang
Qin Zhang
Hui Tang
author_facet Xueying Ma
Xu Han
Wenwen Wang
Qin Zhang
Hui Tang
author_sort Xueying Ma
collection DOAJ
description ABSTRACT: Ovarian follicle development depends on the proliferation and differentiation of granulosa cells and is a complex biological process. The Wnt/β-catenin signaling pathway can regulate ovarian follicle development, and β-catenin, encoded by catenin beta 1 (CTNNB1), is the core component of this pathway. Although several studies of the mechanisms by which the Wnt/β-catenin pathway regulates cell proliferation in humans and mammals have reported, it remains unclear how β-catenin functions in poultry. To investigate the function of β-catenin in laying hens' follicle development, we evaluated the effect of CTNNB1 on cell cycle, proliferation, and apoptosis in ovarian granulosa cells (GCs) isolated from laying hens. We demonstrated that CTNNB1 significantly affected the expression of cyclin D1 (CCND1) and v-myc avian myelocytomatosis viral oncogene homolog (c-Myc) (P < 0.01 and P < 0.05), key genes related to cell cycle and proliferation, to promote cell cycle progression from G1 to S phase, and thus accelerate granulosa cell proliferation. CTNNB1 did not however affect apoptosis or the expression of related genes baculoviral IAP repeat containing 5 (BIRC5) and BCL2 apoptosis regulator (Bcl-2). Overexpression of transcription factor 7-like 2 (TCF4) resulted in increased expression of CCND1, accelerated cell cycle progression, and granulosa cell proliferation. Direct physical interaction between β-catenin and TCF4 was demonstrated by immunofluorescence and coimmunoprecipitation. The proliferation of granulosa cells was inhibited by silencing CCND1; overexpression of TCF4 in CCND1-silenced cells restored their proliferation rate to normal levels. These results indicate that the interaction of TCF4 and β-catenin promotes CCND1 expression which in turn accelerates the cell cycle process of laying hen hierarchical follicular granulosa cells.
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spelling doaj.art-39d226f05dd24c94b5d20b26bb0790912024-02-29T05:17:10ZengElsevierPoultry Science0032-57912024-03-011033103377β-Catenin regulates ovarian granulosa cell cycle and proliferation in laying hens by interacting with TCF4Xueying Ma0Xu Han1Wenwen Wang2Qin Zhang3Hui Tang4Department of Animal Genetics and Breeding, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, Shandong 271018, China; Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Tai'an, Shandong 271018, China; Key Laboratory of Efficient Utilization of Non-grain Feed Resources (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Tai'an, Shandong 271018, ChinaDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, Shandong 271018, China; Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Tai'an, Shandong 271018, China; Key Laboratory of Efficient Utilization of Non-grain Feed Resources (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Tai'an, Shandong 271018, ChinaDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, Shandong 271018, China; Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Tai'an, Shandong 271018, China; Key Laboratory of Efficient Utilization of Non-grain Feed Resources (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Tai'an, Shandong 271018, ChinaDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, Shandong 271018, China; Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Tai'an, Shandong 271018, China; Key Laboratory of Efficient Utilization of Non-grain Feed Resources (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Tai'an, Shandong 271018, ChinaDepartment of Animal Genetics and Breeding, College of Animal Science and Technology, Shandong Agricultural University, Tai'an, Shandong 271018, China; Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, Tai'an, Shandong 271018, China; Key Laboratory of Efficient Utilization of Non-grain Feed Resources (Co-construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Tai'an, Shandong 271018, China; Corresponding author:ABSTRACT: Ovarian follicle development depends on the proliferation and differentiation of granulosa cells and is a complex biological process. The Wnt/β-catenin signaling pathway can regulate ovarian follicle development, and β-catenin, encoded by catenin beta 1 (CTNNB1), is the core component of this pathway. Although several studies of the mechanisms by which the Wnt/β-catenin pathway regulates cell proliferation in humans and mammals have reported, it remains unclear how β-catenin functions in poultry. To investigate the function of β-catenin in laying hens' follicle development, we evaluated the effect of CTNNB1 on cell cycle, proliferation, and apoptosis in ovarian granulosa cells (GCs) isolated from laying hens. We demonstrated that CTNNB1 significantly affected the expression of cyclin D1 (CCND1) and v-myc avian myelocytomatosis viral oncogene homolog (c-Myc) (P < 0.01 and P < 0.05), key genes related to cell cycle and proliferation, to promote cell cycle progression from G1 to S phase, and thus accelerate granulosa cell proliferation. CTNNB1 did not however affect apoptosis or the expression of related genes baculoviral IAP repeat containing 5 (BIRC5) and BCL2 apoptosis regulator (Bcl-2). Overexpression of transcription factor 7-like 2 (TCF4) resulted in increased expression of CCND1, accelerated cell cycle progression, and granulosa cell proliferation. Direct physical interaction between β-catenin and TCF4 was demonstrated by immunofluorescence and coimmunoprecipitation. The proliferation of granulosa cells was inhibited by silencing CCND1; overexpression of TCF4 in CCND1-silenced cells restored their proliferation rate to normal levels. These results indicate that the interaction of TCF4 and β-catenin promotes CCND1 expression which in turn accelerates the cell cycle process of laying hen hierarchical follicular granulosa cells.http://www.sciencedirect.com/science/article/pii/S0032579123008970laying henβ-cateningranulosa cellTCF4CCND1
spellingShingle Xueying Ma
Xu Han
Wenwen Wang
Qin Zhang
Hui Tang
β-Catenin regulates ovarian granulosa cell cycle and proliferation in laying hens by interacting with TCF4
Poultry Science
laying hen
β-catenin
granulosa cell
TCF4
CCND1
title β-Catenin regulates ovarian granulosa cell cycle and proliferation in laying hens by interacting with TCF4
title_full β-Catenin regulates ovarian granulosa cell cycle and proliferation in laying hens by interacting with TCF4
title_fullStr β-Catenin regulates ovarian granulosa cell cycle and proliferation in laying hens by interacting with TCF4
title_full_unstemmed β-Catenin regulates ovarian granulosa cell cycle and proliferation in laying hens by interacting with TCF4
title_short β-Catenin regulates ovarian granulosa cell cycle and proliferation in laying hens by interacting with TCF4
title_sort β catenin regulates ovarian granulosa cell cycle and proliferation in laying hens by interacting with tcf4
topic laying hen
β-catenin
granulosa cell
TCF4
CCND1
url http://www.sciencedirect.com/science/article/pii/S0032579123008970
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