Spermidine promotes adipogenesis of 3T3-L1 cells by preventing interaction of ANP32 with HuR and PP2A

Biochemical Journal

Volumn 453, Issue 3, 2013, Pages 467-474

  Hyvönen, Mervi T ^a   Koponen, Taina ^a   Weisell, Janne ^a   Pietilä, Marko ^a   Khomutov, Alex R ^b   Vepsäläinen, Jouko ^a   Alhonen, Leena ^a   Keinänen, Tuomo A ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b ENGELHARDT INSTITUTE OF MOLECULAR BIOLOGY   (Russian Federation)

Author keywords

Differentiation; Difluoromethylornithine; Mitotic clonal expansion; Polyamine; Polyamine analogue

Indexed keywords

ACIDIC NUCLEAR PHOSPHOPROTEIN 32; CCAAT ENHANCER BINDING PROTEIN BETA; CYCLIN A; CYCLIN D; CYCLIN E; HU ANTIGEN; HUMAN ANTIGEN R; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; PHOSPHOPROTEIN; PHOSPHOPROTEIN PHOSPHATASE 2A; SPERMIDINE; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; UNCLASSIFIED DRUG;

ADIPOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL EXPANSION; CONTROLLED STUDY; DNA SYNTHESIS; ENZYME ACTIVITY; LIPID METABOLISM; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS;

3T3-L1 CELLS; ADIPOGENESIS; ANIMALS; EFLORNITHINE; FEMALE; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; MALE; MICE; NUCLEAR PROTEINS; POLYAMINES; PROTEIN PHOSPHATASE 2; RATS; RATS, WISTAR; SPERMIDINE;

EID: 84880061760     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130263     Document Type: Article

References (36)

1. Pegg, A. E. (2009) Mammalian polyamine metabolism and function. IUBMB Life 61, 880-894
2. Nishimura, K., Murozumi, K., Shirahata, A., Park, M. H., Kashiwagi, K. and Igarashi, K. (2005) Independent roles of eIF5A and polyamines in cell proliferation. Biochem. J. 385, 779-785 (Pubitemid 40208839)
3. Park, M. H., Nishimura, K., Zanelli, C. F. and Valentini, S. R. (2010) Functional significance of eIF5A and its hypusine modification in eukaryotes. Amino Acids 38, 491-500
4. Hyvönen, M. T., Keinänen, T. A., Cerrada-Gimenez, M., Sinervirta, R., Grigorenko, N., Khomutov, A. R., Vepsäläinen, J., Alhonen, L. and Jänne, J. (2007) Role of hypusinated eukaryotic translation initiation factor 5A in polyamine depletion-induced cytostasis. J. Biol. Chem. 282, 34700-34706
5. Hyvönen, M. T., Keinänen, T. A., Khomutov, M., Simonian, A., Vepsäläinen, J., Park, J. H., Khomutov, A. R., Alhonen, L. and Park, M. H. (2012) Effects of novel C-methylated spermidine analogs on cell growth via hypusination of eukaryotic translation initiation factor 5A. Amino Acids. 42, 685-695
6. Vuohelainen, S., Pirinen, E., Cerrada-Gimenez, M., Keinänen, T. A., Uimari, A., Pietilä, M., Khomutov, A. R., Jänne, J. and Alhonen, L. (2010) Spermidine is indispensable in differentiation of 3T3-L1 fibroblasts to adipocytes. J. Cell. Mol. Med. 14, 1683-1692
7. Cowherd, R. M., Lyle, R. E. and McGehee, Jr, R. E. (1999) Molecular regulation of adipocyte differentiation. Semin. Cell Dev. Biol. 10, 3-10 (Pubitemid 129505533)
8. Hyvönen, M. T., Keinänen, T. A., Khomutov, M., Simonian, A., Weisell, J., Kochetkov, S. N., Vepsäläinen, J., Alhonen, L. and Khomutov, A. R. (2011) The use of novel C-methylated spermidine derivatives to investigate the regulation of polyamine metabolism. J. Med. Chem. 54, 4611-4618
9. Grigorenko, N. A., Khomutov, A. R., Keinänen, T. A., Järvinen, A., Alhonen, L., Jänne, J. and Vepsäläinen, J. (2007) Synthesis of novel optical isomers of α-methylpolyamines. Tetrahedron 63, 2257-2263
10. Zhu, S., Oh, H. S., Shim, M., Sterneck, E., Johnson, P. F. and Smart, R. C. (1999) C/EBPβ modulates the early events of keratinocyte differentiation involving growth arrest and keratin 1 and keratin 10 expression. Mol. Cell. Biol. 19, 7181-7190 (Pubitemid 29441898)
11. Alhonen, L., Parkkinen, J. J., Keinänen, T., Sinervirta, R., Herzig, K. H. and Jänne, J. (2000) Activation of polyamine catabolism in transgenic rats induces acute pancreatitis. Proc. Natl. Acad. Sci. U.S.A. 97, 8290-8295 (Pubitemid 30639665)
12. Alhonen, L., Räsänen, T. L., Sinervirta, R., Parkkinen, J. J., Korhonen, V. P., Pietilä, M. and Jänne, J. (2002) Polyamines are required for the initiation of rat liver regeneration. Biochem. J. 362, 149-153 (Pubitemid 34174472)
13. Hyvönen, T., Keinänen, T. A., Khomutov, A. R., Khomutov, R. M. and Eloranta, T. O. (1992) Monitoring of the uptake and metabolism of aminooxy analogues of polyamines in cultured cells by high-performance liquid chromatography. J. Chromatogr. 574, 17-21
14. Hamm, J. K., Park, B. H. and Farmer, S. R. (2001) A role for C/EBPβ in regulating peroxisome proliferator-activated receptor γ activity during adipogenesis in 3T3-L1 preadipocytes. J. Biol. Chem. 276, 18464-18471
15. Kim, J. B., Wright, H. M., Wright, M. and Spiegelman, B. M. (1998) ADD1/SREBP1 activates PPARγ through the production of endogenous ligand. Proc. Natl. Acad. Sci. U.S.A. 95, 4333-4337 (Pubitemid 28207912)
16. Brennan, C. M., Gallouzi, I. E. and Steitz, J. A. (2000) Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 151, 1-14
17. Brennan, C. M. and Steitz, J. A. (2001) HuR and mRNA stability. Cell. Mol. Life Sci. 58, 266-277 (Pubitemid 32217358)
18. Gantt, K., Cherry, J., Tenney, R., Karschner, V. and Pekala, P. H. (2005) An early event in adipogenesis, the nuclear selection of the CCAAT enhancer-binding proteinß (C/EBPβ) mRNA by HuR and its translocation to the cytosol. J. Biol. Chem. 280, 24768-24774 (Pubitemid 40934567)
19. Zou, T., Mazan-Mamczarz, K., Rao, J. N., Liu, L., Marasa, B. S., Zhang, A. H., Xiao, L., Pullmann, R., Gorospe, M. and Wang, J. Y. (2006) Polyamine depletion increases cytoplasmic levels of RNA-binding protein HuR leading to stabilization of nucleophosmin and p53 mRNAs. J. Biol. Chem. 281, 19387-19394 (Pubitemid 44035444)
20. 11-diethylnorspermine. Mol. Pharmacol. 55, 693-698
21. Sureban, S. M., Murmu, N., Rodriguez, P., May, R., Maheshwari, R., Dieckgraefe, B. K., Houchen, C. W. and Anant, S. (2007) Functional antagonism between RNA binding proteins HuR and CUGBP2 determines the fate of COX-2 mRNA translation. Gastroenterology 132, 1055-1065 (Pubitemid 46440864)
22. Eberhardt, W., Doller, A. and Pfeilschifter, J. (2012) Regulation of the mRNA-binding protein HuR by posttranslational modification: spotlight on phosphorylation. Curr. Prot. Pept. Sci. 13, 380-390
23. Arnaud, L., Chen, S., Liu, F., Li, B., Khatoon, S., Grundke-Iqbal, I. and Iqbal, K. (2011) Mechanism of inhibition of PP2A activity and abnormal hyperphosphorylation of tau by I2(PP2A)/SET. FEBS Lett. 585, 2653-2659
24. Fries, B., Heukeshoven, J., Hauber, I., Gruttner, C., Stocking, C., Kehlenbach, R. H., Hauber, J. and Chemnitz, J. (2007) Analysis of nucleocytoplasmic trafficking of the HuR ligand APRIL and its influence on CD83 expression. J. Biol. Chem. 282, 4504-4515 (Pubitemid 47100928)
25. Keinänen, T. A., Järvinen, A., Uimari, A., Vepsälä inen, J., Khomutov, A. R., Grigorenko, N., Hyvönen, M. T., Cerrada-Gimenez, M., Alhonen, L. and Jänne, J. (2007) α-Methylated polyamines as potential drugs and experimental tools in enzymology. Minirev. Med. Chem. 7, 813-20
26. Lakanen, J. R., Coward, J. K. and Pegg, A. E. (1992) α-Methyl polyamines: metabolically stable spermidine and spermine mimics capable of supporting growth in cells depleted of polyamines. J. Med. Chem. 35, 724-734
27. Bethell, D. R. and Pegg, A. E. (1981) Polyamines are needed for the differentiation of 3T3-L1 fibroblasts into adipose cells. Biochem. Biophys. Res. Commun. 102, 272-278 (Pubitemid 12201936)
28. Oredsson, S. M. (2003) Polyamine dependence of normal cell-cycle progression. Biochem. Soc. Trans. 31, 366-370
29. Wang, W., Caldwell, M. C., Lin, S., Furneaux, H. and Gorospe, M. (2000) HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J. 19, 2340-2350 (Pubitemid 30259015)
30. Tanaka, T., Yoshida, N., Kishimoto, T. and Akira, S. (1997) Defective adipocyte differentiation in mice lacking the C/EBPβ and/or C/EBPδ gene. EMBO J. 16, 7432-7443 (Pubitemid 28010503)
31. Tang, Q. Q., Otto, T. C. and Lane, M. D. (2003) CCAAT/enhancer-binding protein β is required for mitotic clonal expansion during adipogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 850-855 (Pubitemid 36183919)
32. Srikantan, S. and Gorospe, M. (2012) HuR function in disease. Front. Biosci. 17, 189-205
33. Ray, R. M., Bhattacharya, S. and Johnson, L. R. (2005) Protein phosphatase 2A regulates apoptosis in intestinal epithelial cells. J. Biol. Chem. 280, 31091-31100 (Pubitemid 41291844)
34. Leroy, D., Heriche, J. K., Filhol, O., Chambaz, E. M. and Cochet, C. (1997) Binding of polyamines to an autonomous domain of the regulatory subunit of protein kinase CK2 induces a conformational change in the holoenzyme. A proposed role for the kinase stimulation. J. Biol. Chem. 272, 20820-20827 (Pubitemid 27355651)
35. 12-bis(ethyl)spermine. Biochemistry 34, 13423-13430
36. Wolff, E. C., Kang, K. R., Kim, Y. S. and Park, M. H. (2007) Posttranslational synthesis of hypusine: evolutionary progression and specificity of the hypusine modification. Amino Acids 33, 341-350 (Pubitemid 47222971) Research