Molecular and Cellular Biochemistry

, Volume 401, Issue 1–2, pp 209–218 | Cite as

CCAAT-enhancer binding protein (C/EBP) β regulates insulin-like growth factor (IGF) 1 expression in porcine liver during prenatal and postnatal development

  • Yiting Tang
  • Kai Xiong
  • Ming Shen
  • Yulian Mu
  • Kui Li
  • Honglin Liu
Article

Abstract

IGF1 expression regulation attracts numerous interests because of its important role during mammalian growth and development. Domestic pig can be used as a valuable animal model to investigate human development since they share the high similarity in general physiology and metabolism. In this study, we examined the expression pattern of IGF1 and found it associated with liver C/EBP β expression pattern in porcine liver during embryonic and postnatal development. Both IGF1 and C/EBP β expression in liver maintained at low levels before birth and increased after birth. Correspondingly, C/EBP β demonstrated high binding activity to two sites at IGF1 promoter region in liver after birth. Additionally, IGF1 expression can be activated by C/EBP β overexpression in porcine primary hepatocytes. These results indicated that C/EBP β can activate IGF1 expression after birth by binding to IGF1 promoter. Our study may contribute to a better understanding of mammalian development and bring a novel anti-aging pathway in human.

Keywords

C/EBP β IGF1 Liver Transcription factor Porcine 

Notes

Acknowledgments

This study was supported by Grants from the following Projects: Study on the regulation of IGF1 gene in pig liver (National Natural Science Foundation of China 31472073 2015-2019); Cultivating New Varieties by Transgenic Technology (#2012ZX08006-003); and China Scholarship Council.

Supplementary material

11010_2014_2308_MOESM1_ESM.jpg (44 kb)
Supplementary material 1 (PDF 44 kb)

References

  1. 1.
    Christoforidis A, Maniadaki I, Stanhope R (2005) Growth hormone/insulin-like growth factor-1 axis during puberty. Pediatr Endocrinol Rev PER 3:5–10Google Scholar
  2. 2.
    Miura Y, Kato H, Noguchi T (1992) Effect of dietary proteins on insulin-like growth factor-1 (IGF-1) messenger ribonucleic acid content in rat liver. Br J Nutr 67:257–265PubMedCrossRefGoogle Scholar
  3. 3.
    Ohlsson C, Mohan S, Sjögren K, Tivesten Å, Isgaard J, Isaksson O et al (2009) The role of liver-derived insulin-like growth factor-I. Endocr Rev 30:494–535PubMedCentralPubMedCrossRefGoogle Scholar
  4. 4.
    Tannenbaum G, Guyda HJ, Posner BI (1983) Insulin-like growth factors: a role in growth hormone negative feedback and body weight regulation via brain. Science 220:77–79PubMedCrossRefGoogle Scholar
  5. 5.
    Baker J, Liu J-P, Robertson EJ, Efstratiadis A (1993) Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75:73–82PubMedCrossRefGoogle Scholar
  6. 6.
    Jones JI, Clemmons DR (1995) Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 16:3–34PubMedGoogle Scholar
  7. 7.
    Clemmons DR (1997) Insulin-like growth factor binding proteins and their role in controlling IGF actions. Cytokine Growth Factor Rev 8:45–62PubMedCrossRefGoogle Scholar
  8. 8.
    Annunziata M, Granata R, Ghigo E (2011) The IGF system. Acta Diabetol 48:1–9PubMedCrossRefGoogle Scholar
  9. 9.
    Li S, Yakar S, Brodt P (2011) Role of the IGF-axis in liver metastasis: experimental and clinical evidence. liver metastasis: biology and clinical management. Springer, Dordecht, pp 233–271CrossRefGoogle Scholar
  10. 10.
    Liu J-P, Baker J, Perkins AS, Robertson EJ, Efstratiadis A (1993) Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75:59–72PubMedGoogle Scholar
  11. 11.
    Loughna PT, Mason P, Bates PC (1992) Regulation of insulin-like growth factor 1 gene expression in skeletal muscle. Symposia of the Society for Experimental Biology, p. 319Google Scholar
  12. 12.
    Rosenbloom AL (2007) The role of recombinant insulin-like growth factor I in the treatment of the short child. Curr Opin Pediatr 19:458–464PubMedCrossRefGoogle Scholar
  13. 13.
    Vaught J, Contreras P, Glicksman M, Neff N (2008) Potential utility of rhlGF-1 in neuromuscular and/or degenerative. Growth Factors Drugs Neurol Sens Disord 777:18Google Scholar
  14. 14.
    Pan Z, Zhang J, Zhang J, Zhou B, Chen J, Jiang Z et al (2012) Expression profiles of the insulin-like growth factor system components in liver tissue during embryonic and postnatal growth of Erhualian and Yorkshire reciprocal cross F-1 pigs. Asian Aust J Anim Sci 25:903–912CrossRefGoogle Scholar
  15. 15.
    Hiney JK, Ojeda S, Dees WL (1991) Insulin-like growth factor I: a possible metabolic signal involved in the regulation of female puberty. Neuroendocrinology 54:420–423PubMedCrossRefGoogle Scholar
  16. 16.
    Laron Z, Klinger B (1998) Effect of insulin-like growth factor-I treatment on serum androgens and testicular and penile size in males with Laron syndrome (primary growth hormone resistance). Eur J Endocrinol 138:176–180PubMedCrossRefGoogle Scholar
  17. 17.
    Argente J, Barrios V, Pozo J, Munoz M, Hervas F, Stene M et al (1993) Normative data for insulin-like growth factors (IGFs), IGF-binding proteins, and growth hormone-binding protein in a healthy Spanish pediatric population: age-and sex-related changes. J Clin Endocrinol Metab 77:1522–1528PubMedGoogle Scholar
  18. 18.
    Kitanaka S (2008) Role of HNF-1α and HNF-1β on insulin, IGF-1 and other potential target genes. Expert Rev Endocrinol Metabol. doi: 10.1586/17446651.3.4.441 Google Scholar
  19. 19.
    Wolfrum C, Besser D, Luca E, Stoffel M (2003) Insulin regulates the activity of forkhead transcription factor Hnf-3β/Foxa-2 by Akt-mediated phosphorylation and nuclear/cytosolic localization. Proc Natl Acad Sci 100:11624–11629PubMedCentralPubMedCrossRefGoogle Scholar
  20. 20.
    LaVoie HA, Nguyen JB, Kordus RJ, Hui YY (2010) GATA6 depletion reduces cyclic AMP-stimulated IGF1 mRNA and free protein levels in luteinizing porcine granulosa cells. Biology of Reproduction, Soc Study Reproduction 1603 MONROE ST, Madison, WI 53711-2021 USA, pp. 185–185Google Scholar
  21. 21.
    LaVoie HA, Kordus RJ, Nguyen JB, Barth JL, Hui YY (2010) GATA depletion impacts insulin-like growth factor 1 mRNA and protein levels in luteinizing porcine granulosa cells. Biol Reprod 83:1015–1026PubMedCentralPubMedCrossRefGoogle Scholar
  22. 22.
    Joung Y-H, Lee M-Y, Lim E-J, Kim M-S, Hwang TS, Kim S-Y et al (2007) Hypoxia activates the IGF-1 expression through STAT5b in human HepG2 cells. Biochem Biophys Res Commun 358:733–738PubMedCrossRefGoogle Scholar
  23. 23.
    Hemati N, Ross SE, Erickson RL, Groblewski GE, MacDougald OA (1997) Signaling pathways through which insulin regulates CCAAT/enhancer binding protein α (C/EBPα) phosphorylation and gene expression in 3T3-L1 adipocytes correlation with GLUT4 gene Expression. J Biol Chem 272:25913–25919PubMedCrossRefGoogle Scholar
  24. 24.
    Li F, Zhao R, Xu Q, Chen W, Ma Y, Chen J (2003) Characteristics of testosterone secretion in male Erhualian and Large White pigs in different developmental stages. J Nanjing Agric Univ 26:117–119Google Scholar
  25. 25.
    Sjögren K, Liu J-L, Blad K, Skrtic S, Vidal O, Wallenius V et al (1999) Liver-derived insulin-like growth factor I (IGF-I) is the principal source of IGF-I in blood but is not required for postnatal body growth in mice. Proc Natl Acad Sci 96:7088–7092PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.
    Kovács KA, Steinmann M, Magistretti PJ, Halfon O, Cardinaux J-R (2003) CCAAT/enhancer-binding protein family members recruit the coactivator CREB-binding protein and trigger its phosphorylation. J Biol Chem 278:36959–36965PubMedCrossRefGoogle Scholar
  27. 27.
    Ramji D, Foka P (2002) CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem J 365:561–575PubMedCentralPubMedGoogle Scholar
  28. 28.
    Ruffell D, Mourkioti F, Gambardella A, Kirstetter P, Lopez RG, Rosenthal N et al (2009) A CREB-C/EBPβ cascade induces M2 macrophage-specific gene expression and promotes muscle injury repair. Proc Natl Acad Sci 106:17475–17480PubMedCentralPubMedCrossRefGoogle Scholar
  29. 29.
    Harries LW, Pilling LC, Hernandez LDG, Bradley-Smith R, Henley W, Singleton AB et al (2012) CCAAT-enhancer-binding protein-beta expression in vivo is associated with muscle strength. Aging Cell 11:262–268PubMedCentralPubMedCrossRefGoogle Scholar
  30. 30.
    Wessells J, Yakar S, Johnson PF (2004) Critical prosurvival roles for C/EBPβ and insulin-like growth factor I in macrophage tumor cells. Mol Cell Biol 24:3238–3250PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    Umayahara Y, Kajimoto Y, Fujitani Y, Gorogawa S-I, Yasuda T, Kuroda A et al (2002) Protein kinase C-dependent, CCAAT/enhancer-binding protein β-mediated expression of insulin-like growth factor I gene. J Biol Chem 277:15261–15270PubMedCrossRefGoogle Scholar
  32. 32.
    Staiger J, Lueben MJ, Berrigan D, Malik R, Perkins SN, Hursting SD et al (2009) C/EBPβ regulates body composition, energy balance-related hormones and tumor growth. Carcinogenesis 30:832–840PubMedCentralPubMedCrossRefGoogle Scholar
  33. 33.
    Cesi V, Giuffrida ML, Vitali R, Tanno B, Mancini C, Calabretta B et al (2005) C/EBP α and β mimic retinoic acid activation of IGFBP-5 in neuroblastoma cells by a mechanism independent from binding to their site. Exp Cell Res 305:179–189PubMedCrossRefGoogle Scholar
  34. 34.
    Barzilai N, Bartke A (2009) Biological approaches to mechanistically understand the healthy life span extension achieved by calorie restriction and modulation of hormones. J Gerontol Ser A 64:187–191CrossRefGoogle Scholar
  35. 35.
    Bartke A (2011) Single-gene mutations and healthy ageing in mammals. Philos Trans R Soc B 366:28–34CrossRefGoogle Scholar
  36. 36.
    Suh Y, Atzmon G, Cho M-O, Hwang D, Liu B, Leahy DJ et al (2008) Functionally significant insulin-like growth factor I receptor mutations in centenarians. Proc Natl Acad Sci 105:3438–3442PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Van Heemst D, Beekman M, Mooijaart SP, Heijmans BT, Brandt BW, Zwaan BJ et al (2005) Reduced insulin/IGF-1 signalling and human longevity. Aging Cell 4:79–85PubMedCrossRefGoogle Scholar
  38. 38.
    Pawlikowska L, Hu D, Huntsman S, Sung A, Chu C, Chen J et al (2009) Association of common genetic variation in the insulin/IGF1 signaling pathway with human longevity. Aging Cell 8:460–472PubMedCentralPubMedCrossRefGoogle Scholar
  39. 39.
    Guevara-Aguirre J, Balasubramanian P, Guevara-Aguirre M, Wei M, Madia F, Cheng C-W et al (2011) Growth hormone receptor deficiency is associated with a major reduction in pro-aging signaling, cancer and diabetes in humans. Sci Transl Med 3:70ra13PubMedCentralPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Yiting Tang
    • 1
    • 2
  • Kai Xiong
    • 1
    • 3
  • Ming Shen
    • 1
  • Yulian Mu
    • 2
  • Kui Li
    • 2
  • Honglin Liu
    • 1
  1. 1.College of Animal Science and TechnologyNanjing Agricultural UniversityNanjingPeople’s Republic of China
  2. 2.Department of Gene and Cell Engineering, Institute of Animal ScienceChinese Academy of Agricultural SciencesBeijingPeople’s Republic of China
  3. 3.Department of Veterinary Clinical and Animal SciencesUniversity of CopenhagenFrederiksberg CDenmark

Personalised recommendations