Scientia Agricultura Sinica ›› 2022, Vol. 55 ›› Issue (10): 2057-2066.doi: 10.3864/j.issn.0578-1752.2022.10.015

• ANIMAL SCIENCE·VETERINARY SCIENCE·RESOURCE INSECT • Previous Articles     Next Articles

LKB1 Regulates Steroids Synthesis Related Genes Expression in Bovine Granulosa Cells

ZHANG Jing1,3(),ZHANG JiYue1,3,YUE YongQi1,3,ZHAO Dan1,3,FAN YiLing1,3,MA Yan1,3,XIONG Yan1,2,3(),XIONG XianRong1,2,3,ZI XiangDong1,2,3,LI Jian1,2,3,YANG LiXue1,2()   

  1. 1Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Ministry of Education,Chengdu 610041
    2Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Chengdu 610041
    3Key Laboratory of Animal Science of State Ethnic Affairs Commission, Southwest Minzu University, Chengdu 610041
  • Received:2021-04-07 Accepted:2022-03-29 Online:2022-05-16 Published:2022-06-02
  • Contact: Yan XIONG,LiXue YANG E-mail:zjing2513338252@163.com;xiongyan0910@126.com;yanglixue_79@163.com

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Abstract:

【Background】 The Steroids synthesis capacity of ovarian granulosa cells plays the important roles in the development and maturation of follicles, however, the key regulators were involved in this process remains largely unknown. Our previously research reported that Liver kinase B1 (LKB1) influenced the cellular lipid metabolism, which is close associated with steroids synthesis. Further, another study showed that knockout of LKB1 caused premature ovarian failure in mice. 【Objective】 The aim of this study was to study the expression pattern of LKB1 in bovine follicle and its regulation on steroid synthesis related genes expression in granulosa cells (GCs),and provided a theoretical basis for the research of the reproductive physiological regulation in the cow.【Method】The expression pattern of LKB1 in follicle was detected by immunohistochemically assay. Then the primary follicular granulosa cells were isolated and identified by immunofluorescence staining incubated by follicle stimulating hormone receptor (FSHR) antibody. Next, these verified granulosa cells were used as the cell model. On one hand, LKB1 loss-of-function was mediated by siRNAs. qRT-PCR was performed to measure LKB1 regulation of steroid hormone synthesis related genes expression. On the other hand, LKB1 gain-of-function was mediated by adenovirus. qRT-PCR and ELISA analysis were carried out to confirm the changes of above detected genes influenced by LKB1 and estradiol (E2) secretion, respectively. 【Result】 The data showed that: 1) LKB1 protein expressed in all cell types of follicles and the positive signal in granulosa cells is significantly higher than that of theca cells, which is verified by quantitative analysis. 2) The morphology of isolated bovine follicular granulosa cells was shape of round, which were specifically labeled by follicle stimulating hormone receptor (FSHR) using immunofluorescence staining, with 95% of positive cells. 3) The interference efficiency of LKB1 treated by siRNA1 and siRNA2 was respectively 48% (P<0.05) and 52% (P<0.05) to that of control. Knockdown of LKB1 significantly down-regulated mRNA levels of STAR (P<0.01), CYP11A1 (P<0.01) and CYP19A1 (P<0.05), with the 60%, 80% and 50% decrease to those of the control. 4) The highly infected efficiency was observed infected by LKB1-OE and control adenovirus. In contrast, overexpression of LKB1 dramatically increased mRNA levels of STAR (P<0.01), CYP11A1 (P<0.01) and CYP19A1 (P<0.05), which was associated with elevation of E2 secretion. 【Conclusion】In summary, LKB1 was highly expressed in follicular granulosa cells, which promoted the expression of steroids synthesis related genes and E2 secretion. This result provides directly theoretical evidence for the LKB1 regulation of steroids hormone synthesis in bovine.

Key words: LKB1, bovine, granulosa cells, steroid hormone, ovary

Table 1

siRNA sequence targeting LKB1"

siRNA名称 siRNA name 序列(5'-3') Sequence(5'-3')
LKB1-siRNA-1 F: CCAAGCUCAUCGGAAAGUACCUGAU
R: AUCAGGUACUUUCCGAUGAGCUUGG
LKB1-siRNA-2 F: GACAUUGAGGACGACGUCAUCUACA
R: UGUAGAUGACGUCGUCCUCAAUGUC

Table 2

The primer sequence of detected genes by qPCR"

基因名称 Gene symbol 引物序(5’-3’) Primer sequence
LKB1 F: AAGCGGTTCTCCATACAGCA
R: CCTCCAGGTAGGGCATCACT
ACTIN F: CTTCAACACCCCTGCCAT
R: CTCGGCTGTGGTGGTGAAG
CYP11A1 F: CTACCAGGACCTGAGACGGA
R: CCTGCCAGCATCTCCGTAAT
CYP17A1 F: AACCATCAGTGACCGGAACC
R: GATGGCGAGATGAGTTGCGT
CYP19A1 F: TCCCCTTGGATGAAAGTGCC
R: TGTCTTCCAGCTTCTCTGCTG
STAR F: TGGAAGTCCCTCAAGGACCA
R: GCAAGTTGGCCTTCAACACC

Fig. 1

Immunohistochemistry of LKB1 protein in the bovine follicles A-D: The immunohistochemistry staining of LKB1 protein in antral follicle. A: The diameter of the follicle is 2 mm, B: the diameter of the follicle is 3 mm, C: the diameter of the follicle is 5 mm, and D: the diameter of the follicle is 7 mm. Blue arrows: bovine ovarian granulosa cells; Red arrows: theca cells. E: The morphology of different diameter follicle. F: The quantitatively analysis of LKB1 stained signal in bovine ovarian granulosa cells and theca cells. Error bars: S.E.M. ** P < 0.01, two-tailed Student’s t test. Scale bar of section: 500 µm"

Fig. 2

Identification of ovarian granulosa cells by immunofluorescence staining A: The morphology of primary granulosa cells; B: Green fluorescence labeled FSHR protein and DAPI labeled nucleus"

Fig. 3

The detection of knockdown efficiency for LKB1 gene Error bars: S.E.M, * P < 0.05, two-tailed Student’s t test"

Fig. 4

LKB1 regulation on steroidogenesis gene expression Two-tailed Student’s t test. The same as below"

Fig. 5

Overexpression of LKB1 in granulosa cells mediated by adenovirus A: The GFP expression in Control and LKB1 overexpressed (LKB1-OE) granulosa cells; B: The overexpression efficiency of LKB1"

Fig. 6

Overexpression of LKB1 regulation on steroidogenesis gene expression and E2 secretion"

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