MicroRNA-22 inhibits proliferation and promotes differentiation of satellite cells in porcine skeletal muscle

doi:10.1016/S2095-3119(19)62701-2

Journal of Integrative Agriculture ›› 2020, Vol. 19 ›› Issue (1): 225-233.DOI: 10.1016/S2095-3119(19)62701-2

所属专题：动物科学合辑Animal Science

收稿日期:2018-10-25 出版日期:2020-01-01 发布日期:2019-12-23

MicroRNA-22 inhibits proliferation and promotes differentiation of satellite cells in porcine skeletal muscle

Hong Quyen Dang^{1, 2}, XU Gu-li¹, HOU Lian-jie¹, XU Jian¹, HONG Guang-liang¹, Chingyuan Hu³, WANG Chong¹

¹ National Engineering Research Center for Breeding Swine Industry/Guangdong Provincial Key Laboratory of Agro-Animal Genomics and Molecular Breeding/College of Animal Science, South China Agricultural University, Guangzhou 510642, P.R.China
² Bac Giang Agricultural and Forestry University, Bac Giang 26000, Viet Nam
³ Department of Human Nutrition, Food and Animal Sciences, College of Tropical Agriculture and Human Resources, University of Hawaii at Manoa, Honolulu, HI 96822, USA

Received:2018-10-25 Online:2020-01-01 Published:2019-12-23
Contact: Correspondence WANG Chong, Tel: +86-20-85285031, Fax: +86-20-85280740, E-mail: betty@scau.edu.cn
About author:Hong Quyen Dang, Tel: +84-983816582, E-mail: quyendangbafu @gmail.com;
Supported by:
This work was supported by the Key Foundation for Basic and Application Research in Higher Education of Guangdong, China (2017KZDXM009), the China Postdoctoral Science Foundation (2018M640789) and the Provincial Agricultural Science Innovation and Promotion Project, China. (2018LM2150).

摘要/Abstract

Abstract:

Pig is an important economic animal in China. Improving meat quality and meat productivity is a long time issue in animal genetic breeding. MicroRNAs (miRNAs) are short non-coding RNAs that participate in various biological processes, such as muscle development and embryogenesis. miR-22 differentially expresses in embryonic and adult skeletal muscle. However, the underlying mechanism is unclear. In this study, we investigated miR-22 function in proliferation and differentiation of porcine satellite cells (PSCs) in skeletal muscle. Our data show that miR-22 expressed in both proliferation and differentiated PSCs and is significantly upregulated (P<0.05) during differentiation. After treated with the miR-22 inhibitor, PSCs proliferation was significantly increased (P<0.05), as indicated by the up-regulation (P<0.01) of cyclin D1 (CCND1), cyclin B1 (CCNB1) and down-regulation (P<0.05) of P21. Conversely, over-expression of miR-22 resulted in opposite results. Differentiation of PSCs was significantly suppressed (P<0.05), evidenced by two major myogenic markers: myogenin (MyoG) and myosin heavy chain (MyHC), after transfecting the PSCs with miR-22 inhibitor. Opposite results were demonstrated in the other way around by transfection with miR-22 mimics. In conclusion, the data from this study indicated that miR-22 inhibited the PSCs proliferation but promoted their differentiation.

Key words: miR-22 , skeletal muscle , porcine satellite cells , proliferation , differentiation

. [J]. Journal of Integrative Agriculture, 2020, 19(1): 225-233.

Hong Quyen Dang, XU Gu-li, HOU Lian-jie, XU Jian, HONG Guang-liang, Chingyuan Hu, WANG Chong. MicroRNA-22 inhibits proliferation and promotes differentiation of satellite cells in porcine skeletal muscle[J]. Journal of Integrative Agriculture, 2020, 19(1): 225-233.

参考文献

Andres V, Walsh K. 1996. Myogenin expression, cell cycle withdrawal, and phenotypic differentiation are temporally separable events that precede cell fusion upon myogenesis. Journal of Cell Biology, 132, 657–666.
Bartel D P. 2009. MicroRNAs: target recognition and regulatory functions. Cell, 136, 215–233.
Buckingham M, Montarras D, Relaix F, Cumano A, Mansouri A, Morgan J, Partridge T. 2006. Pax3 and Pax7 mark a major population of muscle progenitor cells that contribute to skeletal muscle formation and regeneration. Neuromuscular Disorders, 16, S48–S48.
Chen J F, Callis T E, Wang D Z. 2009. MicroRNAs and muscle disorders. Journal of Cell Science, 122, 13–20.
Chen J F, Mandel E M, Thomson J M, Wu Q, Callis T E, Hammond S M, Conlon F L, Wang D Z. 2006. The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nature Genetics, 38, 228–233.
Chen J F, Tao Y Z, Li J A, Deng Z L, Yan Z, Xiao X A, Wang D Z. 2010. MicroRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. Journal of Cell Biology, 190, 867–879.
Dey B K, Gagan J, Dutta A. 2011. miR-206 and -486 induce myoblast differentiation by downregulating Pax7. Molecular and Cellular Biology, 31, 1329–1329.
Fukada S, Yamaguchi M, Kokubo H, Ogawa R, Uezumi A, Yoneda T, Matev M M, Motohashi N, Ito T, Zolkiewska A, Johnson R L, Saga Y, Miyagoe-Suzuki Y, Tsujikawa K, Takeda S, Yamamoto H. 2011. Hesr1 and Hesr3 are essential to generate undifferentiated quiescent satellite cells and to maintain satellite cell numbers. Development, 138, 4609–4619.
Gagan J, Dey B K, Dutta A. 2012. MicroRNAs regulate and provide robustness to the myogenic transcriptional network. Current Opinion in Pharmacology, 12, 383–388.
Gagan J, Dey B K, Layer R, Yan Z, Dutta A. 2011. MicroRNA-378 targets the myogenic repressor MyoR during myoblast differentiation. The Journal of Biological Chemistry, 286, 19431–19438.
Ge Y J, Chen J. 2011. MicroRNAs in skeletal myogenesis. Cell Cycle, 10, 441–448.
Gopinathan L, Ratnacaram C K, Kaldis P. 2011. Established and novel Cdk/cyclin complexes regulating the cell cycle and development. Results and Problems in Cell Differentiation, 53, 365–389.
Guo M M, Hu L H, Wang Y Q, Chen P, Huang J G, Lu N, He J H, Liao C G. 2013. miR-22 is down-regulated in gastric cancer, and its overexpression inhibits cell migration and invasion via targeting transcription factor Sp1. Medical Oncology, 30, 542.
Guo S B, Bai R, Liu W L, Zhao A Q, Zhao Z Q, Wang Y X, Wang Y, Zhao W, Wang W X. 2014. miR-22 inhibits osteosarcoma cell proliferation and migration by targeting HMGB1 and inhibiting HMGB1-mediated autophagy. Tumor Biology, 35, 7025–7034.
Houbaviy H B, Murray M F, Sharp P A. 2003. Embryonic stem cell-specific microRNAs. Developmental Cell, 5, 351–358.
Huang S, Wang S H, Bian C J, Yang Z, Zhou H, Zeng Y, Li H L, Han Q, Zhao R C. 2012. Upregulation of miR-22
promotes osteogenic differentiation and inhibits adipogenic differentiation of human adipose tissue-derived mesenchymal stem cells by repressing HDAC6 protein expression. Stem Cells and Development, 21, 2531–2540.
Huang Z P, Wang D Z. 2014. miR-22 in cardiac remodeling and disease. Trends in Cardiovascular Medicine, 24, 267–272.
Iliopoulos D, Malizos K N, Oikonomou P, Tsezou A. 2008. Integrative microRNA and proteomic approaches identify novel osteoarthritis genes and their collaborative metabolic and inflammatory networks. PLoS ONE, 3, e3740.
Kim H K, Lee Y S, Sivaprasad U, Malhotra A, Dutta A. 2006. Muscle-specific microRNA miR-206 promotes muscle differentiation. Journal of Cell Biology, 174, 677–687.
Lee Y, Ahn C, Han J, Choi H, Kim J, Yim J, Lee J, Provost P, Radmark O, Kim S, Kim V N. 2003. The nuclear RNase III
Drosha initiates microRNA processing. Nature, 425, 415–419.
Lee Y, Kim M, Han J, Yeom K H, Lee S, Baek S H, Kim V N. 2004. MicroRNA genes are transcribed by RNA polymerase II.
The EMBO Journal, 23, 4051–4060.
Lenkala D, LaCroix B, Gamazon E R, Geeleher P, Im H K, Huang R S. 2014. The impact of microRNA expression on cellular proliferation. Human Genetics, 133, 931–938.
Li B, Song Y, Liu T J, Cui Y B, Jiang Y, Xie Z S, Xie S L. 2013. miRNA-22 suppresses colon cancer cell migration and invasion by inhibiting the expression of T-cell lymphoma invasion and metastasis 1 and matrix metalloproteinases 2 and 9. Oncology Reports, 29, 1932–1938.
Ling B, Wang G X, Long G, Qiu J H, Hu Z L. 2012. Tumor suppressor miR-22 suppresses lung cancer cell progression through post-transcriptional regulation of ErbB3. Journal of Cancer Research and Clinical Oncology, 138, 1355–1361.
Liu N, Williams A H, Kim Y, McAnally J, Bezprozvannaya S, Sutherland L B, Richardson J A, Bassel-Duby R, Olson E N. 2007. An intragenic MEF2-dependent enhancer directs muscle-specific expression of microRNAs 1 and 133. Proceedings of the National Academy of Sciences of the United States of America, 104, 20844–20849.
Maliszewska-Cyna E, Bawa D, Eubanks J H. 2010. Diminished prevalence but preserved synaptic distribution of N-methyl-D-aspartate receptor subunits in the methyl CpG binding protein 2 (MeCP2)-null mouse brain. Neuroscience, 168, 624–632.
Mauro A. 1961. Satellite cell of skeletal muscle fibers. Journal of Biophysical and Biochemical Cytology, 9, 493–495.
Muinos-Gimeno M, Espinosa-Parrilla Y, Guidi M, Kagerbauer B, Sipila T, Maron E, Pettai K, Kananen L, Navines R, Martin-Santos R, Gratacos M, Metspalu A, Hovatta I, Estivill X. 2011. Human microRNAs miR-22, miR-138-2, miR-148a, and miR-488 are associated with panic disorder and regulate several anxiety candidate genes and related pathways. Biological Psychiatry, 69, 526–533.
Qin L, Xu J, Wu Z, Zhang Z, Li J, Wang C, Long Q. 2013. Notch1-mediated signaling regulates proliferation of porcine satellite cells (PSCs). Cellular Signalling, 25, 561–569.
Qin L L, Li X K, Xu J, Mo D L, Tong X, Pan Z C, Li J Q, Chen Y S, Zhang Z, Wang C, Long Q M. 2012. Mechano growth factor (MGF) promotes proliferation and inhibits differentiation of porcine satellite cells (PSCs) by down-regulation of key myogenic transcriptional factors. Molecular and Cellular Biochemistry, 370, 221–230.
Rao P K, Kumar R M, Farkhondeh M, Baskerville S, Lodish H F. 2006. Myogenic factors that regulate expression of muscle-specific, microRNAs. Proceedings of the National Academy of Sciences of United States of America, 103, 8721–8726.
Rosenberg M I, Georges S A, Asawachaicharn A, Analau E, Tapscott SJ. 2006. MyoD inhibits Fstl1 and Utrn expression by inducing transcription of miR-206. Journal of Cell Biology, 175, 77–85.
Sarkar F H. 2010. (Part I) Recent trends in anti-cancer drug discovery. Mini Reviews in Medicinal Chemistry, 10, 357–358.
Townley-Tilson W H, Callis T E, Wang D. 2010. MicroRNAs 1, 133, and 206: critical factors of skeletal and cardiac muscle development, function, and disease. International Journal of Biochemistry and Cell Biology, 42, 1252–1255.
van Rooij E, Liu N, Olson E N. 2008. MicroRNAs flex their muscles. Trends in Genetics, 24, 159–166.
Wang X, Yu H, Lu X, Zhang P, Wang M, Hu Y. 2014. MiR-22 suppresses the proliferation and invasion of gastric cancer cells by inhibiting CD151. Biochemical and Biophysical Research Communications, 445, 175–179.
Williams A H, Liu N, van Rooij E, Olson E N. 2009. MicroRNA control of muscle development and disease. Current Opinion in Cell Biology, 21, 461–469.
Xu X D, Song X W, Li Q, Wang G K, Jing Q, Qin Y W. 2012. Attenuation of microRNA-22 derepressed PTEN to effectively protect rat cardiomyocytes from hypertrophy. Journal of Cellular Physiology, 227, 1391–1398.
Zhang G, Xia S, Tian H, Liu Z, Zhou T. 2012. Clinical significance of miR-22 expression in patients with colorectal cancer. Medical Oncology, 29, 3108–3112.
Zhang J, Yang Y, Yang T, Liu Y, Li A, Fu S, Wu M, Pan Z, Zhou W. 2010. MicroRNA-22, downregulated in hepatocellular carcinoma and correlated with prognosis, suppresses cell proliferation and tumourigenicity. British Journal of Cancer, 103,1215–1220.
Zhang J, Ying Z Z, Tang Z L, Long L Q, Li K. 2012. MicroRNA-148a promotes myogenic differentiation by targeting the ROCK1 gene. The Journal of Biological Chemistry, 287, 21093–21101.

MicroRNA-22 inhibits proliferation and promotes differentiation of satellite cells in porcine skeletal muscle

PDF

可视化

摘要/Abstract

引用本文

使用本文

参考文献

相关文章 0

编辑推荐

Metrics