5.9
CiteScore
5.9
Impact Factor
Volume 44 Issue 12
Dec.  2017
Turn off MathJax
Article Contents

Essential roles of stat5.1/stat5b in controlling fish somatic growth

doi: 10.1016/j.jgg.2017.07.006
More Information
  • Corresponding author: E-mail address: jmei@mail.hzau.edu.cn (Jie Mei); E-mail address: jfgui@ihb.ac.cn (Jian-Fang Gui)
  • Received Date: 2017-05-05
  • Accepted Date: 2017-07-19
  • Rev Recd Date: 2017-06-21
  • Available Online: 2017-11-16
  • Publish Date: 2017-12-20
  • Signal transducer and activator of transcription 5b (STAT5b) has been identified as a key downstream mediator of growth hormone (GH) signaling in somatic growth of mammalian. However, the corresponding homologue gene of Stat5b is unknown in fish species. In this study, we generated loss-of-function mutants in stat5.1 and stat5.2, two stat5 homologues existing in zebrafish. In stat5.1-deficient zebrafish, a significant reduction of body length and body weight was detected in the embryos/larvae and adults compared with the wild-type control fish, and sexual size dimorphism in adult zebrafish was also eliminated. However, the stat5.2-deficient zebrafish displayed a normal developmental phenotype during all lifespan. Chromatin immunoprecipitation combined with deep sequencing (ChIP-seq) method was adopted to further investigate the potential transcriptional targets of Stat5 protein and cast much light upon the biological function of Stat5. We identified more than 800 genes as transcriptional targets of Stat5 during zebrafish embryogenesis. KEGG analysis indicated that the Stat5 target gene network is predominantly linked to the metabolic pathways, neuroactive ligand-receptor interaction and JAK-STAT signaling pathways. Further validation studies suggested that Stat5.1 protein could directly regulate the expression of gh1, and stat5.1-mutated zebrafish showed a reduction of gh1 mRNA level. In the present study, stat5.1 was revealed as the corresponding homologue gene of Stat5b in fish species. Additionally, we found a novel molecular interaction between Stat5.1/Stat5b and GH, and unraveled a positive feedback loop Stat5.1-GH-Stat5.1 which is necessary for somatic growth and body development in zebrafish.
  • loading
  • [1]
    Ahmed, A.S., Xiong, F., Pang, S.C. et al. Activation of GH signaling and GH-independent stimulation of growth in zebrafish by introduction of a constitutively activated GHR construct Transgenic Res., 20 (2011),pp. 557-567
    [2]
    Ahmed, S.F., Farquharson, C. The effect of GH and IGF1 on linear growth and skeletal development and their modulation by SOCS proteins J. Endocrinol., 206 (2010),pp. 249-259
    [3]
    Charlton, H.M., Clark, R.G., Robinson, I.C. et al. Growth hormone-deficient dwarfism in the rat: a new mutation J. Endocrinol., 119 (1988),pp. 51-58
    [4]
    Chen, Z., Ballar, P., Fu, Y. et al. The E3 ubiquitin ligase gp78 protects against ER stress in zebrafish liver J. Genet. Genomics, 41 (2014),pp. 357-368
    [5]
    Cruz, E.M.V., Brown, C.L., Luckenbach, J.A. et al. Aquaculture, 251 (2006),pp. 585-595
    [6]
    Dan, C., Mei, J., Wang, D. et al. Genetic differentiation and efficient sex-specific marker development of a pair of Y- and X-linked markers in yellow catfish Int. J. Biol. Sci., 9 (2013),pp. 1043-1049
    [7]
    , Sherman, B.T., Hosack, D.A., Yang, J. et al. DAVID: database for annotation, visualization, and integrated discovery Genome Biol., 4 (2003),p. R60
    [8]
    Do, A., Menon, V., Zhi, X. et al. Thyroxine modifies the effects of growth hormone in Ames dwarf mice Aging (Albany NY), 7 (2015),pp. 241-255
    [9]
    Elo, L.L., Jarvenpaa, H., Tuomela, S. et al. Genome-wide profiling of interleukin-4 and STAT6 transcription factor regulation of human Th2 cell programming Immunity, 32 (2010),pp. 852-862
    [10]
    Fan, Y., Menon, R.K., Cohen, P. et al. Liver-specific deletion of the growth hormone receptor reveals essential role of growth hormone signaling in hepatic lipid metabolism J. Biol. Chem., 284 (2009),pp. 19937-19944
    [11]
    Greenhalgh, C.J., Bertolino, P., Asa, S.L. et al. Growth enhancement in suppressor of cytokine signaling 2 (SOCS-2)-deficient mice is dependent on signal transducer and activator of transcription 5b (STAT5b) Mol. Endocrinol., 16 (2002),pp. 1394-1406
    [12]
    Heinz, S., Benner, C., Spann, N. et al. Mol. Cell, 38 (2010),pp. 576-589
    [13]
    Jing, J., Xiong, S., Li, Z. et al. A feedback regulatory loop involving p53/miR-200 and growth hormone endocrine axis controls embryo size of zebrafish Sci. Rep., 5 (2015),p. 15906
    [14]
    Johnston, I.A., de la Serrana, D.G., Devlin, R.H. Muscle fibre size optimisation provides flexibility for energy budgeting in calorie-restricted coho salmon transgenic for growth hormone J. Exp. Biol., 217 (2014),pp. 3392-3395
    [15]
    Kaneko, G., Furukawa, S., Kurosu, Y. et al. J. Fish. Biol., 79 (2011),pp. 854-874
    [16]
    Kofoed, E.M., Hwa, V., Little, B. et al. N. Engl. J. Med., 349 (2003),pp. 1139-1147
    [17]
    Langmead, B., Trapnell, C., Pop, M. et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome Genome Biol., 10 (2009),p. R25
    [18]
    Laz, E.V., Sugathan, A., Waxman, D.J. Mol. Endocrinol., 23 (2009),pp. 1242-1254
    [19]
    Lewis, R.S., Ward, A.C. Gene, 338 (2004),pp. 65-74
    [20]
    Li, X.Y., Liu, X.L., Ding, M. et al. Sci. Bull., 62 (2017),pp. 528-536
    [21]
    Liu, X., Robinson, G.W., Wagner, K.U. et al. Stat5a is mandatory for adult mammary gland development and lactogenesis Genes Dev., 11 (1997),pp. 179-186
    [22]
    Lupu, F., Terwilliger, J.D., Lee, K. et al. Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth Dev. Biol., 229 (2001),pp. 141-162
    [23]
    Ma, W., Wu, J., Zhang, J. et al. Sci. China Life Sci., 59 (2016),pp. 431-433
    [24]
    Makrigiannakis, A., Vrekoussis, T., Zoumakis, E. et al. CRH receptors in human reproduction Curr. Mol. Pharmacol., 10 (2017),pp. 1-7
    [25]
    Mansfield, M.J., Beardsworth, D.E., Loughlin, J.S. et al. Long-term treatment of central precocious puberty with a long-acting analogue of luteinizing hormone-releasing hormone. Effects on somatic growth and skeletal maturation N. Engl. J. Med., 309 (1983),pp. 1286-1290
    [26]
    McMenamin, S.K., Minchin, J.E., Gordon, T.N. et al. Endocrinology, 154 (2013),pp. 1476-1487
    [27]
    Mei, J., Gui, J.F. Genetic basis and biotechnological manipulation of sexual dimorphism and sex determination in fish Sci. China Life Sci., 58 (2015),pp. 124-136
    [28]
    Mei, J., Zhang, Q.Y., Li, Z. et al. C1q-like inhibits p53-mediated apoptosis and controls normal hematopoiesis during zebrafish embryogenesis Dev. Biol., 319 (2008),pp. 273-284
    [29]
    Peng, J.X., Xie, J.L., Zhou, L. et al. J. Exp. Zool. B Mol. Dev. Evol., 312 (2009),pp. 855-871
    [30]
    Reich, N.C. STATs get their move on JAKSTAT, 2 (2013),p. e27080
    [31]
    Siveen, K.S., Sikka, S., Surana, R. et al. Targeting the STAT3 signaling pathway in cancer: role of synthetic and natural inhibitors Biochim. Biophys.Acta, 1845 (2014),pp. 136-154
    [32]
    Udy, G.B., Towers, R.P., Snell, R.G. et al. Requirement of STAT5b for sexual dimorphism of body growth rates and liver gene expression Proc. Natl. Acad. Sci. U. S. A., 94 (1997),pp. 7239-7244
    [33]
    Vasilatos-Younken, R., Zhou, Y., Wang, X. et al. J. Endocrinol., 166 (2000),pp. 609-620
    [34]
    Wang, Y., Zhou, L., Yao, B. et al. Differential expression of thyroid-stimulating hormone β subunit in gonads during sex reversal of orange-spotted and red-spotted groupers Mol. Cell. Endocrinol., 220 (2004),pp. 77-88
    [35]
    Williams, T.M., Carroll, S.B. Genetic and molecular insights into the development and evolution of sexual dimorphism Nat. Rev. Genet., 10 (2009),p. 883
    [36]
    Xiong, S.T., Wu, J.J., Jing, J. et al. Loss of stat3 function leads to spine malformation and immune disorder in zebrafish Sci. Bull., 62 (2017),pp. 185-196
    [37]
    Yang, Y.J., Wang, Y., Li, Z. et al. Genetics, 205 (2017),pp. 1551-1572
    [38]
    Zhang, D.C., Huang, Y.Q., Shao, Y.Q. et al. Gen. Comp. Endocrinol., 148 (2006),pp. 203-212
    [39]
    Zhang, D.W., Wang, J., Zhou, C. et al. Mech. Dev., 143 (2017),pp. 42-52
    [40]
    Zhang, J., Ma, W., He, Y. et al. Sex biased expression of ghrelin and GHSR associated with sexual size dimorphism in yellow catfish Gene, 578 (2016),pp. 169-176
    [41]
    Zhang, Y., Laz, E.V., Waxman, D.J. Dynamic, sex-differential STAT5 and BCL6 binding to sex-biased, growth hormone-regulated genes in adult mouse liver Mol. Cell. Biol., 32 (2012),pp. 880-896
    [42]
    Zhang, Y., Liu, T., Meyer, C.A. et al. Model-based analysis of ChIP-seq (MACS) Genome Biol., 9 (2008),p. R137
    [43]
    Zhong, H., Zhou, Y., Liu, S. et al. Elevated expressions of GH/IGF axis genes in triploid crucian carp Gen. Comp. Endocrinol., 178 (2012),pp. 291-300
    [44]
    Zhu, B.M., Kang, K., Yu, J.H. et al. Genome-wide analyses reveal the extent of opportunistic STAT5 binding that does not yield transcriptional activation of neighboring genes Nucleic Acids Res., 40 (2012),pp. 4461-4472
    [45]
    Zhu, T., Zhang, T., Wang, Y. et al. Effects of growth hormone (GH) transgene and nutrition on growth and bone development in common carp J. Exp. Zool. A. Ecol. Genet. Physiol., 319 (2013),pp. 451-460
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (96) PDF downloads (2) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return