Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (2): 390-402.doi: 10.3864/j.issn.0578-1752.2024.02.013

• ANIMAL SCIENCE·VETERINARY SCIENCE • Previous Articles     Next Articles

Cloning of PLZF Gene and Its Effects on the Proliferation of Undifferentiated Spermatogonia in Cattleyak

ZHANG Peng(), WANG MingXiu, JING KeMin, LI YuQian, TIAN Yuan, ZHONG JinCheng(), CAI Xin()   

  1. Key Laboratory of Qinghai-Tibetan Plateau Animal Genetic Resource Reservation and Utilization, Ministry of Education / Sichuan Province, Southwest Minzu University, Chengdu 610041
  • Received:2023-05-11 Accepted:2023-10-07 Online:2024-01-16 Published:2024-01-19
  • Contact: ZHONG JinCheng, CAI Xin

RichHTML

8

PDF

76

Abstract:

【Objective】 As the product of interspecific hybridization between yak and cattle, cattleyak has excellent production performance, but the further application of its heterosis is limited by the male sterility of cattleyak. The aim of the study was to clone the PLZF of cattleyak, and to identify its differential expression in the testicular tissue and undifferentiated spermatogonia of cattleyak and yak, and to further reveal the effect of expressing this gene on the activity of undifferentiated spermatogonia of cattleyak. This study could provide a theoretical basis for clarifying the mechanism of spermatogenesis stagnation in cattleyaks. 【Method】 In this study, 24-month-old male Maiwa yak and F1 generation male cattleyak were used as experimental animals, and the CDS sequences of PLZF in cattleyak were cloned by RT-PCR and analyzed by bioinformatics. The differential expression of PZLF in the testis tissues of cattleyak and yak was analyzed by RT-qPCR. The expression vector of PLZF was constructed by homologous recombination, and the overexpression efficiency and the expression of downstream target genes were detected by RT-qPCR. The effect of overexpression of PLZF on the undifferentiated spermatogonia of cattleyak was detected by PDT, CCK-8, EdU, and immunofluorescence. 【Result】 The CDS region of the PLZF was cloned, and it was found by bioinformatics analysis that the protein sequence encoded by the gene did not contain transmembrane domain and signal peptide sequence, and its tertiary structure was mainly α helix and random curl. Phylogenetic tree analysis showed that the PLZF of cattleyak was more closely related to the PLZF of cattle. The prediction of tertiary structure showed that although the tertiary structure of PLZF protein of cattleyak, yak and cattle was highly similar, the PLZF protein of yak was quite different from that of cattleyak and cattle at amino acids 531-540. RT-qPCR found that the expression levels of PLZF gene in the testis tissue and undifferentiated spermatogonia of cattleyak were significantly lower than that in yak (P<0.05). After overexpression of PLZF, the expression of PLZF in the undifferentiated spermatogonia of the cattleyak was up-regulated by 13.8 times (P<0.01), and the proliferation activity of the undifferentiated spermatogonia of the cattleyak was significantly increased (P<0.05), which showed that the down-regulation of PLZF expression affected the proliferation activity of undifferentiated spermatogonia of cattleyak. In addition, after overexpression of PLZF, the proliferation activity of undifferentiated spermatogonia was significantly increased All proliferation-related genes (Etv5, Bcl6b, Pcna and c-fos) were significantly up-regulated (P<0.05), and all differentiation-related genes (Stra8, Kit, Dmrt1 and Sohlh2) were significantly down-regulated (P<0.05), indicating that PLZF could promote the proliferation of undifferentiated spermatogonia by up-regulating the expression of proliferation-related genes and down-regulating the expression of differentiation-related genes.【Conclusion】 The abnormal expression of PLZF in cattleyak undifferentiated spermatogonia reduced the proliferative activity of cattleyak undifferentiated spermatogonia, resulting in its decrease in number and affecting the spermatogenesis of cattleyak. This study provided a theoretical basis for further elucidation of the mechanism of spermatogenesis and stagnation in cattleyak, and a new idea for solving the problem of male sterility in cattleyak.

Key words: cattleyak, PLZF, undifferentiated spermatogonia, proliferation

Table 1

Primers for PLZF cloning"

基因 Gene 登录号 Accession NO. 引物序列 Primer sequence (5’→3’)
PLZF XM_005891907 F: CTAGCGTTTAAACTTAAGCTTATGGATCTGACAAAGATGGGCA
R: CCACACTGGACTAGTGGATCCTCACACGTAGCACAGATAGAGGTACG

Table 2

Primer sequence for RT-qPCR"

基因
Gene		 登录号
Accession No.		 引物序列
Primer sequences (5′→3′)		 引物长度
Primer Length (bp)		 退火温度
Tm (℃)		 产物长度
Product size (bp)
Bcl6b XM_005906036 F：GAAAACGCATAGCCGCATCC
R：GACTCTTGTGCCGGAAATGC		 20
20		 60.32
59.32		 248
Etv5 XM_005910750 F：ACCGGCAAATGTCAGAACCT
R：CGTCAAAGTACAACCGGGGA		 20
20		 59.89
59.97		 276
c-fos XM_005900989 F：GCCCGGACCTACAATGGCTA
R：CTCTGCCTCCTGTCATGGTTT		 20
21		 61.69
60.00		 150
Pcna XM_005906528 F：AGCTGAAGATAACGCAGACAC
R：ATCTCGGCATATACGTGCAA		 21
20		 58.39
57.19		 178
Dmrt1 XM_005900007 F：CCCGTGCCTGATGATTGAGA
R：GTACGGAAACAGAGACGGCT		 20
20		 59.82
59.76		 211
Sohlh2 XM_002691802 F：CTATCCGTCCCAGGCATGAT
R：ACCGATAGCCTTCTCTGACG		 20
20		 59.02
58.97		 189
Kit NM_001166484 F：AGAAAACGACACGCTGGTTC
R：CTCGCGCTTCACATTTCTGA		 20
20		 59.06
58.93		 151
Stra8 XM_005906930 F：TGTGGCAAGTTTCCTGGACA
R：TCTCCGTGCACCTCAACATT		 20
20		 59.74
59.60		 215
Plzf XM_005891907 F：GTTCCATGCCCACCGGACT
R：TGGCCTCCGTGTCATTGTCA		 19
20		 63.16
55.00		 275
β-actin DQ838049 F：CCCTGGAGAAGAGCTACGAG
R：TAGTTTCGTGAATGCCGCAG		 20
20		 58.97
58.92		 129

Table 3

Reaction program of RT-qPCR"

阶段
Stage		 循环数
Number of cycles		 温度
Temperature (℃)		 时间
Time
(s)
预变性Predenaturation 1 95 10
循环反应
Cyclic reaction		 40 95 10
60 30
溶解曲线
Melting curve		 1 95 15
60 60
95 15

Fig. 1

The amplification of the target fragment of PLZF of cattleyak P and M represent PLZF and Marker, respectively"

Table 4

Sequence comparison of CDS region of PLZF in different species"

物种
Specics		 登录号
Accession No.		 CDS区长度
Length of CDS region (bp)		 相似性
Percent identity (%)
牦牛 Bos Mutus XM_005891907 2 019 98.96
黄牛 Bos Taurus XM_005215851 2 022 99.80
瘤牛 Bos indicus XM_019974560 2 022 99.75
猪 Sus scrofa XM_021062870 2 022 94.07
山羊 Capra hircus XM_018058857 2 022 97.23

Fig. 2

Sequence comparison of CDS region of PLZF in different species"

Fig. 3

Characteristic information analysis, structural analysis and phylogenetic tree of PLZF protein of cattleyak (A) Prediction analysis of transmembrane structure domain. (B) Prediction analysis of hydrophobicity and hydrophilicity. (C) Signal peptide sequence prediction analysis. (D) Prediction analysis of secondary structure in protein. (E) The phylogenetic tree of PLZF gene sequence"

Fig. 4

Tertiary structure prediction and protein structure difference analysis of PLZF protein in cattleyak, yak and cattle (A-B) Analysis of amino acid sequence differences of PLZF among cattleyak, yak and cattle. (C-E) Prediction of tertiary structure of PLZF protein in cattle, yak and cattleyak. (F-K) Analysis of structural differences of PLZF protein among cattle, yak and cattleyak"

Fig. 5

Expression of PLZF in testis of yak and cattleyak YK represents yak, CY represents cattleyak (the same below). ** means P<0.01"

Fig. 6

Identification of PLZF expression vector by enzyme digestion and overexpression efficiency (A) Identification of PLZF expression vector by enzyme digestion. M, 1, 2, and 3 represent Marker, expression vector by double enzyme digestion, PLZF gene cloning, and linear pcDNA3.1(+) empty vector, respectively. (B) PLZF gene overexpression efficiency. Bars that do not share the same letters are significantly different from each other (P<0.05). CY-PLZF represents the overexpression of PLZF gene in the undifferentiated spermatogonia of cattleyak. The same as below"

Fig. 7

Effect of overexpression of PLZF gene on undifferentiated spermatogonia of cattleyak A: Population doubling times of the cells for YK, CY-PLZF and CY groups; B: The proliferation of YK, CY-PLZF, CY-TAF4b and CY was detected by CCK-8 under different conditions; C: Proliferation of CY, CY-PLZF and YK undifferentiated spermatogonia were detected by EdU. Red image indicates “EdU”, blue image indicates “H33342”, and “Merge” indicated the merged image; D: Proliferation of CY, CY-PLZF and YK undifferentiated spermatogonia were detected by immunofluorescence of DDX4. Green image indicated “DDX4”, blue image indicated “DAPI”, and “Merge” indicated the merged image"

Fig. 8

Expression of PLZF target genes in undifferentiated spermatogonia of cattleyak"

Fig. 9

Effects of PLZF on proliferation of undifferentiated spermatogonia in cattleyak"

[1]
吴周林, 左玲, 徐弘扬, 王健蓉, 张仕民, 赵莉, 罗海艳. 犏牛杂种优势研究进展. 当代畜牧, 2018(6): 23-25.
WU Z L, ZUO L, XU H Y, WANG J R, ZHANG S M, ZHAO L, LUO H Y. The research progress on heterosis in cattle-yak. Contemporary Animal Husbandry, 2018(6): 23-25. (in Chinese)
[2]
NIAYALE R, CUI Y, ADZITEY F. Male hybrid sterility in the cattle-yak and other bovines: a review. Biology of Reproduction, 2021, 104(3): 495-507.

doi: 10.1093/biolre/ioaa207 pmid: 33185248
[3]
陈会友, 张建敏, 李柏森, 邓永琳, 张龚炜. 犏牛雄性不育的减数分裂基因表达与表观遗传调控研究进展. 遗传, 2020, 42(11): 1081-1092.
CHEN H Y, ZHANG J M, LI B S, DENG Y L, ZHANG G W. Progress on meiotic gene expression and epigenetic regulation of male sterility in Dzo cattle. Hereditas(Beijing), 2020, 42(11): 1081-1092. (in Chinese)
[4]
张鹏, 王明秀, 敬科民, 彭巍, 田园, 李雨谦, 付长其, 舒适, 钟金城, 蔡欣. FGFs/FGFRs及其介导信号通路基因的异常表达影响犏牛未分化精原细胞增殖活性. 畜牧兽医学报, 2023: 1-15. (2023-03-14). https://kns.cnki.net/kcms/detail/11.1985.s.20230311.1755.004.html.
ZHANG P, WANG M X, JING K M, PENG W, TIAN Y, LI Y Q, FU C Q, SHU S, ZHONG J C, CAI X. Abnormal expression of FGFs/FGFRs and their mediated signaling pathway genes affect the proliferative activity of undifferentiated spermatogonia in Cattleyak. Acta Veterinaria et Zootechnica Sinica, 2023: 1-15. (2023-03-14). https://kns.cnki.net/kcms/detail/11.1985.s.20230311.1755.004.html. (in Chinese)
[5]
DAVID G, ALLAND L, HONG S H, WONG C W, DEPINHO R A, DEJEAN A. Histone deacetylase associated with mSin3A mediates repression by the acute promyelocytic leukemia-associated PLZF protein. Oncogene, 1998, 16(19): 2549-2556.

doi: 10.1038/sj.onc.1202043 pmid: 9627120
[6]
FISCHER S, KOHLHASE J, BÖHM D, SCHWEIGER B, HOFFMANN D, HEITMANN M, HORSTHEMKE B, WIECZOREK D. Biallelic loss of function of the promyelocytic leukaemia zinc finger (PLZF) gene causes severe skeletal defects and genital hypoplasia. Journal of Medical Genetics, 2008, 45(11): 731-737.

doi: 10.1136/jmg.2008.059451 pmid: 18611983
[7]
BUAAS F W, KIRSH A L, SHARMA M, MCLEAN D J, MORRIS J L, GRISWOLD M D, DE ROOIJ D G, BRAUN R E. Plzf is required in adult male germ cells for stem cell self-renewal. Nature Genetics, 2004, 36(6): 647-652.

doi: 10.1038/ng1366 pmid: 15156142
[8]
PHILLIPS B T, GASSEI K, ORWIG K E. Spermatogonial stem cell regulation and spermatogenesis. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 2010, 365(1546): 1663-1678.
[9]
BABATABAR DARZI M, NEMATI F, AZIZI H, DEHPOUR JOUYBARI A. Immunohistochemistry and immunocytochemistry analysis of PLZF and VASA in mice testis during spermatogenesis. Zygote, 2023, 31(3): 273-280.

doi: 10.1017/S0967199423000047
[10]
MIPAM T, CHEN X M, ZHAO W S, ZHANG P, CHAI Z X, YUE B L, LUO H, WANG J K, WANG H B, WU Z J, WANG J B, WANG M X, WANG H, ZHANG M, WANG H Y, JING K M, ZHONG J C, CAI X. Single-cell transcriptome analysis and in vitro differentiation of testicular cells reveal novel insights into male sterility of the interspecific hybrid cattle-yak. BMC Genomics, 2023, 24(1): 149.

doi: 10.1186/s12864-023-09251-2
[11]
CHAN A L, LA H M, LEGRAND J M D, MÄKELÄ J A, EICHENLAUB M, DE SERAM M, RAMIALISON M, HOBBS R M. Germline stem cell activity is sustained by SALL4-dependent silencing of distinct tumor suppressor genes. Stem Cell Reports, 2017, 9(3): 956-971.

doi: 10.1016/j.stemcr.2017.08.001
[12]
OATLEY J M, AVARBOCK M R, TELARANTA A I, FEARON D T, BRINSTER R L. Identifying genes important for spermatogonial stem cell self-renewal and survival. Proceedings of the National Academy of Sciences of the United States of America, 2006, 103(25): 9524-9529.
[13]
HOBBS R M, SEANDEL M, FALCIATORI I, RAFII S, PANDOLFI P P. Plzf regulates germline progenitor self-renewal by opposing mTORC1. Cell, 2010, 142(3): 468-479.

doi: 10.1016/j.cell.2010.06.041 pmid: 20691905
[14]
MU H L, LI N, WU J, ZHENG L M, ZHAI Y X, LI B, SONG W C, WANG J L, ZHU H J, LI G P, HUA J L. PLZF-induced upregulation of CXCR4 promotes dairy goat male germline stem cell proliferation by targeting Mir146a. Journal of Cellular Biochemistry, 2016, 117(4): 844-852.

doi: 10.1002/jcb.25371 pmid: 26365432
[15]
DI GIACOMO M, COMAZZETTO S, SAINI H, DE FAZIO S, CARRIERI C, MORGAN M, VASILIAUSKAITE L, BENES V, ENRIGHT A J, O’CARROLL D. Multiple epigenetic mechanisms and the PiRNA pathway enforce LINE1 silencing during adult spermatogenesis. Molecular Cell, 2013, 50(4): 601-608.

doi: 10.1016/j.molcel.2013.04.026 pmid: 23706823
[16]
ZHANG P, WANG M X, CHEN X M, JING K M, LI Y Q, LIU X R, RAN H B, QIN J, ZHONG J C, CAI X. Dysregulated genes in undifferentiated spermatogonia and Sertoli cells are associated with the spermatogenic arrest in cattleyak. Molecular Reproduction and Development, 2022, 89(12): 632-645.

doi: 10.1002/mrd.23653 pmid: 36409004
[17]
孙军伟. GDNF对奶山羊雄性生殖干细胞自我更新的调控[D]. 杨凌: 西北农林科技大学, 2011: 19-20.
SUN J W. The mechanism of GDNF mediates self-renewal of dairy goat male germ-line stem cells[D]. Yangling: Northwest A & F University, 2011: 19-20. (in Chinese)
[18]
SHAMHARI A, JEFFERI N E S, ABD HAMID Z, BUDIN S B, IDRIS M H M, TAIB I S. The role of promyelocytic leukemia zinc finger (PLZF) and glial-derived neurotrophic factor family receptor alpha 1 (GFRα1) in the cryopreservation of spermatogonia stem cells. International Journal of Molecular Sciences, 2023, 24(3): 1945.

doi: 10.3390/ijms24031945
[19]
AZIZI H, KORUJI M, SKUTELLA T. Comparison of PLZF gene expression between pluripotent stem cells and testicular germ cells. Cell Journal, 2020, 22(1): 60-65.
[20]
ISHII K, KANATSU-SHINOHARA M, TOYOKUNI S, SHINOHARA T. FGF2 mediates mouse spermatogonial stem cell self-renewal via upregulation of Etv5 and Bcl6b through MAP2K1 activatio. Development, 2012, 139(10): 1734-1743.

doi: 10.1242/dev.076539
[21]
OATLEY J M, AVARBOCK M R, BRINSTER R L. Glial cell line-derived neurotrophic factor regulation of genes essential for self-renewal of mouse spermatogonial stem cells is dependent on Src family kinase signaling. The Journal of Biological Chemistry, 2007, 282(35): 25842-25851.

doi: 10.1074/jbc.M703474200
[22]
WU S X, MIPAM T, XU C F, ZHAO W S, ALI SHAH M, YI C P, LUO H, CAI X, ZHONG J C. Testis transcriptome profiling identified genes involved in spermatogenic arrest of cattleyak. PLoS ONE, 2020, 15(2): e0229503.

doi: 10.1371/journal.pone.0229503
[23]
SONG W X, SHI X L, XIA Q, YUAN M, LIU J X, HAO K Y, QIAN Y J, ZHAO X D, ZOU K. PLZF suppresses differentiation of mouse spermatogonial progenitor cells via binding of differentiation associated genes. Journal of Cellular Physiology, 2020, 235(3): 3033-3042.

doi: 10.1002/jcp.29208 pmid: 31541472
[24]
KOTAJA N, SASSONE-CORSI P. Plzf pushes stem cells. Nature Genetics, 2004, 36(6): 551-553.

pmid: 15167928
[25]
SUZUKI H, AHN H W, CHU T J, BOWDEN W, GASSEI K, ORWIG K, RAJKOVIC A. SOHLH1 and SOHLH2 coordinate spermatogonial differentiation. Developmental Biology, 2012, 361(2): 301-312.

doi: 10.1016/j.ydbio.2011.10.027 pmid: 22056784
[26]
穆海龙. PLZF通过靶向抑制miR-146a促进CXCR4表达调控奶山羊精原干细胞增殖[D]. 杨凌: 西北农林科技大学, 2015: 29.
MU H L. PLZF up-regulatiion CXCR4 to promote dairy goat male germline stem cells proliferation via targeting miR-146a[D]. Yangling: Northwest A & F University, 2015: 29. (in Chinese)
[27]
ORNITZ D M, ITOH N. The fibroblast growth factor signaling pathway. Wiley Interdisciplinary Reviews Developmental Biology, 2015, 4(3): 215-266.

doi: 10.1002/wdev.2015.4.issue-3
[28]
MENG X, LINDAHL M, HYVÖNEN M E, PARVINEN M, DE ROOIJ D G, HESS M W, RAATIKAINEN-AHOKAS A, SAINIO K, RAUVALA H, LAKSO M, PICHEL J G, WESTPHAL H, SAARMA M, SARIOLA H. Regulation of cell fate decision of undifferentiated spermatogonia by GDNF. Science, 2000, 287(5457): 1489-1493.

doi: 10.1126/science.287.5457.1489 pmid: 10688798
[29]
GOERTZ M J, WU Z R, GALLARDO T D, HAMRA F K, CASTRILLON D H. Foxo1 is required in mouse spermatogonial stem cells for their maintenance and the initiation of spermatogenesis. The Journal of Clinical Investigation, 2011, 121(9): 3456-3466.

doi: 10.1172/JCI57984
[30]
LOVASCO L A, GUSTAFSON E A, SEYMOUR K A, DE ROOIJ D G, FREIMAN R N. TAF4b is required for mouse spermatogonial stem cell development. Stem Cells, 2015, 33(4): 1267-1276.

doi: 10.1002/stem.1914 pmid: 25727968
[31]
SNIPPERT H J, VAN DER FLIER L G, SATO T, VAN ES J H, VAN DEN BORN M, KROON-VEENBOER C, BARKER N, KLEIN A M, VAN RHEENEN J, SIMONS B D, CLEVERS H. Intestinal crypt homeostasis results from neutral competition between symmetrically dividing Lgr5 stem cells. Cell, 2010, 143(1): 134-144.

doi: 10.1016/j.cell.2010.09.016 pmid: 20887898
[1] GUO YunPeng, TAN HaoYun, GUO Hong, FU MengYun, LI Xin, HU DeBao, ZHANG LinLin, DING XiangBin, GUO YiWen. LNC721 Targeted Regulation MMP9 Affects Bovineskeletal Muscle Satellite Cell Proliferation and Differentiation [J]. Scientia Agricultura Sinica, 2023, 56(24): 4944-4955.
[2] WANG Peng, LIU ZiYi, LIU YuFang, CHU MingXing. miR-535 Targets the GAB2 Gene to Promote Goat Granulosa Cell Proliferation Through Activation of the PI3K/AKT Signaling Pathway [J]. Scientia Agricultura Sinica, 2023, 56(23): 4757-4771.
[3] LIU PeiPei, DING ShiJie, SONG WenJuan, TANG ChangBo, LI HuiXia, TANG Hong. NAC Affects Proliferation and Differentiation of Adipose-Derived Mesenchymal Stem Cells by Regulating Reactive Oxygen Species [J]. Scientia Agricultura Sinica, 2023, 56(21): 4330-4343.
[4] WEI Yao, ZHANG RuiMen, AN Qiang, WANG LeYi, ZHANG YongWang, ZOU ChaoXia, ZHANG ErKang, MO BiYun, SHI DeShun, YANG SuFang, DENG YanFei, WEI YingMing. CircCEP85L Regulates the Proliferation and Myogenic Differentiation of Bovine MuSCs [J]. Scientia Agricultura Sinica, 2023, 56(18): 3670-3681.
[5] YANG XinRan,MA XinHao,DU JiaWei,ZAN LinSen. Expression Pattern of m6A Methylase-Related Genes in Bovine Skeletal Muscle Myogenesis [J]. Scientia Agricultura Sinica, 2023, 56(1): 165-178.
[6] WANG JiaMin,SHI JiaChen,MA FangFang,CAI Yong,QIAO ZiLin. Effects of Soy Isoflavones on the Proliferation and Apoptosis of Yak Ovarian Granulosa Cells [J]. Scientia Agricultura Sinica, 2022, 55(8): 1667-1675.
[7] HU RongRong,DING ShiJie,GUO Yun,ZHU HaoZhe,CHEN YiChun,LIU Zheng,DING Xi,TANG ChangBo,ZHOU GuangHong. Effects of Trolox on Proliferation and Differentiation of Pig Muscle Stem Cells [J]. Scientia Agricultura Sinica, 2021, 54(24): 5290-5301.
[8] FENG YunKui,WANG Jian,MA JinLiang,ZHANG LiuMing,LI YongJun. Effects of miR-31-5p on the Proliferation and Apoptosis of Hair Follicle Stem Cells in Goat [J]. Scientia Agricultura Sinica, 2021, 54(23): 5132-5143.
[9] LI Yu,WANG Fang,WENG ZeBin,SONG HaiZhao,SHEN XinChun. Preparation of Soybean Protein-Derived Pro-osteogenic Peptides via Enzymatic Hydrolysis [J]. Scientia Agricultura Sinica, 2021, 54(13): 2885-2894.
[10] LAI YuTing,ZHU FeiFei,WANG YiMin,GUO Hong,ZHANG LinLin,LI Xin,GUO YiWen,DING XiangBin. Effects of PSMB5 on the Proliferation and Myogenic Differentiation of Skeletal Muscle Satellite Cells [J]. Scientia Agricultura Sinica, 2020, 53(20): 4287-4296.
[11] LI Yan,CHEN MingMing,ZHANG JunXing,ZHANG LinLin,LI Xin,GUO Hong,DING XiangBin,LIU XinFeng. Effects of Bovine LncRNA-133a on the Proliferation and Differentiation of Skeletal Muscle Satellite Cells [J]. Scientia Agricultura Sinica, 2019, 52(1): 143-153.
[12] YANG Qiang, XU Pan, JIANG Kai, QIAO ChuanMin, REN Jun, HUANG LuSheng, XING YuYun. Targeted Editing of BMPR-IB Gene in Porcine Fetal Fibroblasts via Lentivirus Mediated CRISPR/Cas9 Technology and Its Effects on Expression of Genes in the BMPs Signaling Pathway [J]. Scientia Agricultura Sinica, 2018, 51(7): 1378-1389.
[13] SHI Hong-yan, HE Qi, CHENG Min, SUN Ying-ning, LI Hui, WANG Ning. Effect of HOPX Gene Overexpression on Chicken Preadipocyte Proliferation [J]. Scientia Agricultura Sinica, 2015, 48(8): 1624-1631.
[14] LIN Kai, YU De-bing, XIE Xiao-dong, YU Min-li, LI Dong-feng, DU Wen-xing. The Regulated Mechanism of Follistatin on the Proliferation Process of Duck Skeletal Muscle Satellite Cell Involved in TGF-β / Smad Signaling Pathway [J]. Scientia Agricultura Sinica, 2015, 48(12): 2460-2468.
[15] WEI Cai-hong, WU Ming-ming, LIU Rui-zao, ZHAO Fu-ping, ZHANG Li, DU Li-xin. Research Progress in Muscular Growth and Development of Long Noncoding RNAs [J]. Scientia Agricultura Sinica, 2014, 47(20): 4078-4085.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
京ICP备09089781号-30
Copyright 2018 © Editorial office of Scientia Agricultura Sinica
Tel: 86-010-82106279    E-mail: zgnykx@mail.caas.net.cn
Supported by Beijing Magtech Co.Ltd