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Trim14 overexpression causes the same transcriptional changes in mouse embryonic stem cells and human HEK293 cells

  • Valentina V. NenashevaEmail author
  • Galina V. Kovaleva
  • Nella V. Khaidarova
  • Ekaterina V. Novosadova
  • Ekaterina S. Manuilova
  • Stanislav A. Antonov
  • Vyacheslav Z. Tarantul
Article
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Abstract

The trim14 (pub, KIAA0129) gene encodes the TRIM14 protein which is a member of the tripartite motif (TRIM) family. Previously, we revealed high expression levels of trim14 in HIV- or SIV-associated lymphomas and demonstrated the influence of trim14 on mesodermal differentiation of mouse embryonic stem cells (mESC). In the present work, to elucidate the role of trim14 in normal and pathological processes in the cell, we used two different types of cells transfected with trim14: mESC and human HEK293. Using subtractive hybridization and real-time PCR, we found a number of genes which expression was elevated in trim14-transfected mESC: hsp90ab1, prr13, pu.1, tnfrsf13c (baff-r), tnfrsf13b (taci), hlx1, hbp1, junb, and pdgfrb. A further analysis of the trim14-transfected mESC at the initial stage of differentiation (embryoid bodies (EB) formation) showed essential changes in the expression of these upregulated genes. The transfection of trim14 into HEK293 also induced an enhanced expression of the several genes upregulated in trim14-transfected mESC (hsp90ab1, prr13, pu.1, tnfrsf13c (baff-r), tnfrsf13b (taci), and hlx1). Summarizing, we found similar genes that participated in trim14-directed processes both in mESC and in HEK293. These results demonstrate the presence of the similar mechanism of trim14 gene action in different types of mammalian cells.

Keywords

Trim14 gene Mouse embryonic stem cells Differentiation Embryoid bodies Human HEK293 
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Notes

Acknowledgments

This work was supported by grants number 11-04-01337, 13-04-00598, and 13-04-00642 from the Russian Foundation for Basic Research and grant for Molecular and Cellular Biology from Russian Academy of Sciences.

References

  1. Abujarour R.; Efe J.; Ding S. Genome-wide gain-of-function screen identifies novel regulators of pluripotency. Stem Cells 28: 1487–1497; 2010.PubMedCrossRefGoogle Scholar
  2. Alexaki V.-I.; Notas G.; Pelekanou V.; Kampa M.; Valkanou M.; Theodoropoulos P.; Stathopoulos E. N.; Tsapis A.; Castanas E. Adipocytes as immune cells: differential expression of TWEAK, BAFF, and APRIL and their receptors (Fn14, BAFF-R, TACI, and BCMA) at different stages of normal and pathological adipose tissue development. J. Immunol. 183: 5948–5956; 2009.PubMedCrossRefGoogle Scholar
  3. Canfield A. E.; Sutton A. B.; Hoyland J. A.; Schor A. M. Association of thrombospondin-1 with osteogenic differentiation of retinal pericytes in vitro. J. Cell Sci. 109(Pt 2): 343–353; 1996.PubMedGoogle Scholar
  4. Gabet Y.; Baniwal S. K.; Leclerc N.; Shi Y.; Kohn-Gabet A. E.; Cogan J.; Dixon A.; Bachar M.; Guo L.; Turman Jr. J. E.; Frenkel B. Krox20/EGR2 deficiency accelerates cell growth and differentiation in the monocytic lineage and decreases bone mass. Blood 116: 3964–3971; 2010.PubMedCrossRefGoogle Scholar
  5. Gallant S.; Gilkeson G. ETS transcription factors and regulation of immunity. Arch. Immunol. Ther. Exp. (Warsz.) 54: 149–163; 2006.CrossRefGoogle Scholar
  6. Haasper C.; Jagodzinski M.; Drescher M.; Meller R.; Wehmeier M.; Krettek C.; Hesse E. Cyclic strain induces FosB and initiates osteogenic differentiation of mesenchymal cells. Exp. Toxicol. Pathol. 59: 355–363; 2008.PubMedCrossRefGoogle Scholar
  7. Halene S.; Gaines P.; Sun H.; Zibello T.; Lin S.; Khanna-Gupta A.; Williams S. C.; Perkins A.; Krause D.; Berliner N. C/EBPepsilon directs granulocytic-vs-monocytic lineage determination and confers chemotactic function via Hlx. Exp. Hematol. 38: 90–103; 2010.PubMedCentralPubMedCrossRefGoogle Scholar
  8. Hamdan R.; Zhou Z.; Kleinerman E. S. SDF-1α induces PDGF-B expression and the differentiation of bone marrow cells into pericytes. Mol. Cancer Res. 9: 1462–1470; 2011.PubMedCentralPubMedCrossRefGoogle Scholar
  9. Herquel B.; Ouararhni K.; Khetchoumian K.; Ignat M.; Teletin M.; Mark M.; Béchade G.; Van Dorsselaer A.; Sanglier-Cianférani S.; Hamiche A.; Cammas F.; Davidson I.; Losson R. Transcription cofactors TRIM24, TRIM28, and TRIM33 associate to form regulatory complexes that suppress murine hepatocellular carcinoma. Proc. Natl. Acad. Sci. U. S. A. 108: 8212–8217; 2011.PubMedCentralPubMedCrossRefGoogle Scholar
  10. Hewitt K. J.; Shamis Y.; Knight E.; Smith A.; Maione A.; Alt-Holland A.; Sheridan S. D.; Haggarty S. J.; Garlick J. A. PDGFRβ expression and function in fibroblasts derived from pluripotent cells is linked to DNA demethylation. J. Cell Sci. 125(Pt 9): 2276–87; 2012.PubMedCrossRefGoogle Scholar
  11. Hirose S.; Nishizumi H.; Sakano H. Pub, a novel PU.1 binding protein, regulates the transcriptional activity of PU.1. Biochem. Biophys. Res. Commun. 311: 351–360; 2003.PubMedCrossRefGoogle Scholar
  12. Kawai T.; Akira S. Regulation of innate immune signaling pathways by the tripartite motif (TRIM) family proteins. EMBO Mol. Med. 3: 513–527; 2011.PubMedCentralPubMedCrossRefGoogle Scholar
  13. Lang S. A.; Moser C.; Fichnter-Feigl S.; Schachtschneider P.; Hellerbrand C.; Schmitz V.; Schlitt H. J.; Geissler E. K.; Stoeltzing O. Targeting heat-shock protein 90 improves efficacy of rapamycin in a model of hepatocellular carcinoma in mice. Hepatology 49: 523–532; 2009.PubMedCrossRefGoogle Scholar
  14. Lih C. J.; Wei W.; Cohen S. N. Txr1: a transcriptional regulator of thrombospondin-1 that modulates cellular sensitivity to taxanes. Genes Dev. 20: 2082–2095; 2006.PubMedCrossRefGoogle Scholar
  15. Lloberas J.; Solier C.; Celada A. The key role of PU.1/SPI-1 in B cells, myeloid cells and macrophages. Immunol. Today 20: 184–189; 1999.PubMedCrossRefGoogle Scholar
  16. Lord K. A.; Abdollahi A.; Hoffman-Liebermann B.; Liebermann D. A. Proto-oncogenes of the fos/jun family of transcription factors are positive regulators of myeloid differentiation. Mol. Cell. Biol. 13: 841–851; 1993.PubMedCentralPubMedGoogle Scholar
  17. Lüscher B.; Vervoorts J. Regulation of gene transcription by the oncoprotein MYC. Gene 494: 145–160; 2012.PubMedCrossRefGoogle Scholar
  18. McNab F. W.; Rajsbaum R.; Stoye J. P.; O’Garra A. Tripartite-motif proteins and innate immune regulation. Curr. Opin. Immunol. 23: 46–56; 2011.PubMedCrossRefGoogle Scholar
  19. Morceau F.; Buck I.; Dicato M.; Diederich M. Radicicol-mediated inhibition of Bcr-Abl in K562 cells induced p38-MAPK dependent erythroid differentiation and PU.1 down-regulation. Biofactors 34: 313–29; 2008.PubMedCrossRefGoogle Scholar
  20. Munir M. TRIM proteins: another class of viral victims. Sci. Signal. 3(118): jc2; 2010. doi: 10.1126/scisignal.3118jc2.PubMedCrossRefGoogle Scholar
  21. Nagy A.; Rossant J.; Nagy R.; Abramow-Newerly W.; Roder J. C. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 90: 8424–8428; 1993.PubMedCentralPubMedCrossRefGoogle Scholar
  22. Nenasheva V.; Maksimov V.; Nikolaev A.; Tarantul V. Comparative analysis of the level of gene transcription in two types of HIV-associated lymphoma. Mol. Gen. Mikrobiol. Virusol. 4: 27–31; 2001.PubMedGoogle Scholar
  23. Nenasheva V. V.; Nikolaev A. I.; Martynenko A. V.; Kaplanskaya I. B.; Bodemer W.; Hunsmann G.; Tarantul V. Z. Differential gene expression in HIV/SIV-associated and spontaneous lymphomas. Int. J. Med. Sci. 2: 122–128; 2005.PubMedCentralPubMedCrossRefGoogle Scholar
  24. Nisole S.; Stoye J. P.; Saib A. TRIM family proteins: retroviral restriction and antiviral defense. Nat. Rev. Microbiol. 3: 799–808; 2005.PubMedCrossRefGoogle Scholar
  25. Novosadova E.; Khaydarova N.; Manuilova E.; Arsenyeva E.; Lebedev A.; Tarantul V.; Grivennikov I. Similar effects of mouse and human pub gene on proliferation and embryoid bodies formation in mouse embryonic stem cells in vitro. Stem Cell Discov. 2: 78–83; 2012.Google Scholar
  26. Novosadova E.; Manuilova E.; Arsenyeva E.; Lebedev A.; Khaydarova N.; Tarantul V.; Grivennikov I. Influence of pub gene expression on differentiation of mouse embryonic stem cells into derivatives of ecto-, meso-, and endoderm in vitro. Acta Naturae 1: 93–97; 2009.PubMedCentralPubMedGoogle Scholar
  27. Novosadova E. V.; Manuilova E. S.; Arsen’eva E. L.; Khaidarova N. V.; Dolotov O. V.; Inozemtseva L. S.; Kozachenkov K. Y.; Tarantul V. Z.; Grivennikov I. A. Different effects of enhanced and reduced expression of pub gene on the formation of embryoid bodies by cultured embryonic mouse stem cell. Bull. Exp. Biol. Med. 140: 153–158; 2005.Google Scholar
  28. Okawa Y.; Hideshima T.; Steed P.; Vallet S.; Hall S.; Huang K.; Rice J.; Barabasz A.; Foley B.; Ikeda H.; Raje N.; Kiziltepe T.; Yasui H.; Enatsu S.; Anderson K. C. SNX-2112, a selective Hsp90 inhibitor, potently inhibits tumor cell growth, angiogenesis, and osteoclastogenesis in multiple myeloma and other hematologic tumors by abrogating signaling via Akt and ERK. Blood 113: 846–855; 2009.PubMedCrossRefGoogle Scholar
  29. Ozato K.; Shin D. M.; Chang T. H.; Morse 3rd H. C. TRIM family proteins and their emerging roles in innate immunity. Nat. Rev. Immunol. 8: 849–860; 2008.PubMedCentralPubMedCrossRefGoogle Scholar
  30. Rajaraman G.; Murthi P.; Quinn L.; Brennecke S. P.; Kalionis B. Homeodomain protein HLX is expressed primarily in cytotrophoblast cell types in the early pregnancy human placenta. Reprod. Fertil. Dev. 20: 357–367; 2008.PubMedCrossRefGoogle Scholar
  31. Reymond A.; Meroni G.; Fantozzi A.; Merla G.; Cairo S.; Luzi L.; Riganelli D.; Zanaria E.; Messali S.; Cainarca S.; Guffanti A.; Minucci S.; Pelicci P. G.; Ballabio A. The tripartite motif family identifies cell compartments. EMBO J. 20: 2140–2151; 2001.PubMedCrossRefGoogle Scholar
  32. Sambrook J.; Fritsch E. F.; Maniatis T. Cold Spring, Molecular Cloning, a laboratory manual. 2nd ed. Cold Spring Harbor Laboratory Press, New York; 1989.Google Scholar
  33. Sardiello M.; Cairo S.; Fontanella B.; Ballabio A.; Meroni G. Genomic analysis of the TRIM family reveals two groups of genes with distinct evolutionary properties. BMC Evol. Biol. 8: 225; 2008.PubMedCentralPubMedCrossRefGoogle Scholar
  34. Scheef E. A.; Sorenson C. M.; Sheibani N. Attenuation of proliferation and migration of retinal pericytes in the absence of thrombospondin-1. Am. J. Physiol. Cell Physiol. 296: C724–C734; 2009.PubMedCrossRefGoogle Scholar
  35. Steidl U.; Rosenbauer F.; Verhaak R. G. W.; Gu X.; Ebralidze A.; Out H. H.; Klippel S.; Steidl C.; Bruns I.; Costa D. B.; Wagner K.; Aivado M.; Kobbe G.; Valk P. J.; Passegué E.; Libermann T. A.; Delwel R.; Tenen D. G. Essential role of Jun family transcription factors in PU.1 knockdown-induced leukemic stem cells. Nat. Genet. 38: 1269–1278; 2006.PubMedCrossRefGoogle Scholar
  36. Tarantul V. Z.; Nikolaev A. I.; Martynenko A.; Hannig H.; Hunsmann G.; Bodemer W. Differential gene expression in B-cell non-Hodgkin’s lymphoma of SIV-infected monkey. AIDS Res. Hum. Retroviruses 16: 173–179; 2000.PubMedCrossRefGoogle Scholar
  37. Thieu V. T.; Yu Q.; Chang H.-C.; Yeh N.; Nguyen E. T.; Sehra S.; Kaplan M. H. Signal transducer and activator of transcription 4 is required for the transcription factor T-bet to promote T helper 1 cell-fate determination. Immunity 29: 679–690; 2008.PubMedCentralPubMedCrossRefGoogle Scholar
  38. Torok M.; Etkin L. D. Two B or not two B? Overview of the rapidly expanding B-box family of proteins. Differentiation 67: 63–71; 2001.PubMedCrossRefGoogle Scholar
  39. Yao C. J.; Works K.; Romagnoli P. A.; Austin G. E. Effects of overexpression of HBP1 upon growth and differentiation of leukemic myeloid cells. Leukemia 19: 1958–1968; 2005.PubMedCrossRefGoogle Scholar

Copyright information

© The Society for In Vitro Biology 2013

Authors and Affiliations

  • Valentina V. Nenasheva
    • 1
    Email author
  • Galina V. Kovaleva
    • 1
  • Nella V. Khaidarova
    • 1
  • Ekaterina V. Novosadova
    • 1
  • Ekaterina S. Manuilova
    • 1
  • Stanislav A. Antonov
    • 1
  • Vyacheslav Z. Tarantul
    • 1
  1. 1.Department of viral and cellular molecular genetics, Institute of Molecular GeneticsRussian Academy of SciencesMoscowRussia

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