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Protein kinase D2 and heat shock protein 90 beta are required for BCL6-associated zinc finger protein mRNA stabilization induced by vascular endothelial growth factor-A

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Abstract

Vascular endothelial growth factor (VEGF) is a major angiogenic factor that activates pro-angiogenic molecules to generate new vessels. Recently, we identified a VEGF-A-induced pro-angiogenic gene, BCL-6 associated zinc finger protein (BAZF), in endothelial cells. BAZF interacts with CBF1, a transcriptional regulator of Notch signaling, and downregulates Notch signaling by inducing the degradation of CBF1. A signal inhibition assay with a combination of chemical inhibitors and siRNA revealed that the protein kinase D (PRKD) family, mainly PRKD2, mediated BAZF gene expression by VEGF-A stimulation. A luciferase reporter assay showed that the promoter activity of the BAZF gene was unchanged by VEGF-A stimulation. However, we found that the stability of BAZF mRNA increased in a VEGF-A/PRKD2-dependent manner. In further studies to investigate the underlying mechanism, we successfully identified heat shock protein 90 beta (HSP90β) as a molecule that interacts with and stabilizes BAZF mRNA following VEGF-A/PRKD2 activation. These data suggest that HSP90β may positively regulate angiogenesis, not only as a protein chaperone, but also as an mRNA stabilizer for pro-angiogenic genes, such as BAZF, in a PRKD2 activity-dependent manner.

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References

  1. Folkman J (2007) Angiogenesis: an organizing principle for drug discovery? Nat Rev Drug Discov 6:273–286

    Article  PubMed  CAS  Google Scholar 

  2. Hanahan D, Folkman J (1996) Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86:353–364

    Article  PubMed  CAS  Google Scholar 

  3. Dvorak HF (2002) Vascular permeability factor/vascular endothelial growth factor: a critical cytokine in tumor angiogenesis and a potential target for diagnosis and therapy. J Clin Oncol 20:4368–4380

    Article  PubMed  CAS  Google Scholar 

  4. Hicklin DJ, Ellis LM (2005) Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J Clin Oncol 23:1011–1027

    Article  PubMed  CAS  Google Scholar 

  5. Hellstrom M, Phng LK, Hofmann JJ, Wallgard E, Coultas L, Lindblom P, Alva J, Nilsson AK, Karlsson L, Gaiano N, Yoon K, Rossant J, Iruela-Arispe ML, Kalen M, Gerhardt H, Betsholtz C (2007) Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445:776–780

    Article  PubMed  Google Scholar 

  6. Jakobsson L, Franco CA, Bentley K, Collins RT, Ponsioen B, Aspalter IM, Rosewell I, Busse M, Thurston G, Medvinsky A, Schulte-Merker S, Gerhardt H (2010) Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol 12:943–953

    Article  PubMed  CAS  Google Scholar 

  7. Benedito R, Roca C, Sorensen I, Adams S, Gossler A, Fruttiger M, Adams RH (2009) The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137:1124–1135

    Article  PubMed  CAS  Google Scholar 

  8. Benedito R, Trindade A, Hirashima M, Henrique D, da Costa LL, Rossant J, Gill PS, Duarte A (2008) Loss of Notch signalling induced by Dll4 causes arterial calibre reduction by increasing endothelial cell response to angiogenic stimuli. BMC Dev Biol 8:117

    Article  PubMed  Google Scholar 

  9. Leslie JD, Ariza-McNaughton L, Bermange AL, McAdow R, Johnson SL, Lewis J (2007) Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134:839–844

    Article  PubMed  CAS  Google Scholar 

  10. Lobov IB, Renard RA, Papadopoulos N, Gale NW, Thurston G, Yancopoulos GD, Wiegand SJ (2007) Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci USA 104:3219–3224

    Article  PubMed  CAS  Google Scholar 

  11. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, Gale NW, Lin HC, Yancopoulos GD, Thurston G (2006) Blockade of Dll4 inhibits tumor growth by promoting non-productive angiogenesis. Nature 444:1032–1037

    Article  PubMed  CAS  Google Scholar 

  12. Ridgway J, Zhang G, Wu Y, Stawicki S, Liang WC, Chanthery Y, Kowalski J, Watts RJ, Callahan C, Kasman I, Singh M, Chien M, Tan C, Hongo JA, de Sauvage F, Plowman G, Yan M (2006) Inhibition of Dll4 signalling inhibits tumor growth by deregulating angiogenesis. Nature 444:1083–1087

    Article  PubMed  CAS  Google Scholar 

  13. Sainson RC, Aoto J, Nakatsu MN, Holderfield M, Conn E, Koller E, Hughes CC (2005) Cell-autonomous notch signaling regulated endothelial cell branching and proliferation during vascular tubulogenesis. FASEB J 19:1027–1029

    PubMed  CAS  Google Scholar 

  14. Siekmann AF, Lawson ND (2007) Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445:781–784

    Article  PubMed  CAS  Google Scholar 

  15. Suchting S, Freitas C, le Noble F, Benedito R, Breant C, Duarte A, Eichmann A (2007) The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad USA 104:3225–3230

    Article  CAS  Google Scholar 

  16. Tammela T, Zarkada G, Wallgard E, Murtomaki A, Suchting S, Wirzenius M, Waltari M, Hellstrom M, Schomber T, Peltonen R, Freitas C, Duarte A, Isoniemi H, Laakkonen P, Christofori G, Yla-Herttuala S, Shibuya M, Pytowski B, Eichmann A, Betsholtz C, Alitalo K (2008) Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454:656–660

    Article  PubMed  CAS  Google Scholar 

  17. Caolo V, van den Akker NM, Verbruggen S, Donners MM, Swennen G, Schulten H, Waltenberger J, Post MJ, Molin DG (2010) Feed-forward signaling by membrane-bound ligand receptor circuit: the case of NOTCH DELTA-like 4 ligand in endothelial cells. J Biol Chem 285:40681–40689

    Article  PubMed  CAS  Google Scholar 

  18. Roukens MG, Alloul-Ramdhani M, Baan B, Kobayashi K, Peterson-Maduro J, van Dam H, Schulte-Merker S, Baker DA (2010) Control of endothelial sprouting by a Tel-CtBP complex. Nat Cell Biol 12:933–942

    Article  PubMed  CAS  Google Scholar 

  19. Eilken HM, Adams RH (2010) Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr Opin Cell Biol 22:617–625

    Article  PubMed  CAS  Google Scholar 

  20. Ohnuki H, Inoue H, Takemori N, Nakayama H, Sakaue T, Fukuda S, Miwa D, Nishiwaki E, Hatano M, Tokuhisa T, Endo Y, Nose M, Higashiyama S (2012) BAZF, a novel component of cullin3-based E3 ligase complex, mediates VEGFR and Notch cross-signaling in angiogenesis. Blood 119:2688–2698

    Article  PubMed  CAS  Google Scholar 

  21. Dou GR, Wang YC, Hu XB, Hou LH, Wang CM, Xu JF, Wang YS, Liang YM, Yao LB, Yang AG, Han H (2008) RBP-J, the transcription factor downstream of Notch receptors, is essential for the maintenance of vascular homeostasis in adult mice. FASEB J. 22:1606–1617

    Article  PubMed  CAS  Google Scholar 

  22. Irie A, Harada K, Tsukamoto H, Kim JR, Araki N, Nishimura Y (2006) Protein kinase D2 contributes to either IL-2 promoter regulation or induction of cell death upon TCR stimulation depending on its activity in Jurkat cells. Int Immunol 18:1737–1747

    Article  PubMed  CAS  Google Scholar 

  23. Miura N, Takemori N, Kikugawa T, Tanji N, Higashiyama S, Yokoyama M (2012) Adseverin: a novel cisplatin-resistant marker in the human bladder cancer cell line HT1376 identified by quantitative proteomic analysis. Mol Oncol 6:311–322

    Article  PubMed  CAS  Google Scholar 

  24. Tenenbaum SA, Lager PJ, Carson CC, Keene JD (2002) Ribonomics: identifying mRNA subsets in mRNP complexes using antibodies to RNA-binding proteins and genomic arrays. Methods 26:191–19825

    Article  PubMed  CAS  Google Scholar 

  25. Yang E, van Nimwegen E, Zavolan M, Rajewsky N, Schroeder M, Magnasco M, Darnell JE Jr (2003) Decay of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res 13:1863–1872

    Article  PubMed  CAS  Google Scholar 

  26. Barreau C, Paillard L, Osborne HB (2005) AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 33:7138–7150

    Article  PubMed  CAS  Google Scholar 

  27. Khabar KS (2010) Post-transcriptional control during chronic inflammation and cancer: a focus on AU-rich elements. Cell Mol Life Sci 67:2937–2955

    Article  PubMed  CAS  Google Scholar 

  28. Cerchietti LC, Lopes EC, Yang SN, Hatzi K, Bunting KL, Tsikitas LA, Mallik A, Robles AI, Walling J, Varticovski L, Shaknovich R, Bhalla KN, Chiosis G, Melnick A (2009) A purine scaffold Hsp90 inhibitor destabilizes BCL-6 and has specific antitumor activity in BCL-6-dependent B cell lymphomas. Nat Med 15:1369–1376

    Article  PubMed  CAS  Google Scholar 

  29. He H, Zatorska D, Kim J, Aguirre J, Liauger L, She Y, Wu N, Immormino RM, Gewirth DT, Chiosis G (2006) Identification of potent water soluble purine-scaffold inhibitors of the heat shock protein 90. J Med Chem 49:381–390

    Article  PubMed  CAS  Google Scholar 

  30. Whitesell L, Mimnaugh EG, De Costa B, Myers CE, Neckers LM (1994) Inhibition of heat shock protein HSP90-pp 60v-src heteroprotein complex formation by benzoquinone ansamycins: essential role for stress proteins in oncogenic transformation. Proc Natl Acad Sci USA 91:8324–8328

    Article  PubMed  CAS  Google Scholar 

  31. Johannes FJ, Prestle J, Eis S, Oberhagemann P, Pfizenmaier K (1994) PKCμ is a novel, atypical member of the protein kinase C family. J Biol Chem 269:6140–6148

    PubMed  CAS  Google Scholar 

  32. Valverde AM, Sinnett-Smith J, Van Lint J, Rozengurt E (1994) Molecular cloning and characterization of protein kinase D: a target for diacylglycerol and phorbol esters with a distinctive catalytic domain. Proc Natl Acad Sci USA 91:8572–8576

    Article  PubMed  CAS  Google Scholar 

  33. Sturany S, Van Lint J, Muller F, Wilda M, Hameister H, Hocker M, Brey A, Gern U, Vandenheede J, Gress T, Adler G, Seufferlein T (2001) Molecular cloning and characterization of the human protein kinase D2. A novel member of the protein kinase D family of serine threonine kinases. J Biol Chem 276:3310–3318

    Article  PubMed  CAS  Google Scholar 

  34. Hayashi A, Seki N, Hattori A, Kozuma S, Saito T (1999) PKCnu, a new member of the protein kinase C family, composes a fourth subfamily with PKCmu. Biochim Biophys Acta 1450:99–106

    Article  PubMed  CAS  Google Scholar 

  35. Manning G, Whyte DB, Martinez R, Hunter T, Sudarsanam S (2002) The protein kinase complement of the human genome. Science 298:1912–1934

    Article  PubMed  CAS  Google Scholar 

  36. Rykx A, De Kimpe L, Mikhalap S, Vantus T, Seufferlein T, Vandenheede JR, Van Lint J (2003) Protein kinase D: a family affair. FEBS Lett 546:81–86

    Article  PubMed  CAS  Google Scholar 

  37. Rozengurt E, Rey O, Waldron RT (2005) Protein kinase D signaling. J Biol Chem 280:13205–13208

    Article  PubMed  CAS  Google Scholar 

  38. Rousseau S, Houle F, Landry J, Huot J (1997) p38 MAP kinase activation by vascular endothelial growth factor mediates actin reorganization and cell migration in human endothelial cells. Oncogene 15:2169–2177

    Article  PubMed  CAS  Google Scholar 

  39. Evans IM, Britton G, Zachary IC (2008) Vascular endothelial growth factor induces heat shock protein (HSP) 27 serine 82 phosphorylation and endothelial tubulogenesis via protein kinase D and independent of p38 kinase. Cell Signal 20:1375–1384

    Article  PubMed  CAS  Google Scholar 

  40. Hao Q, Wang L, Zhao ZJ, Tang H (2009) Identification of protein kinase D2 as a pivotal regulator of endothelial cell proliferation, migration, and angiogenesis. J Biol Chem 284:799–806

    Article  PubMed  CAS  Google Scholar 

  41. Chen CY, Shyu AB (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20:465–470

    Article  PubMed  CAS  Google Scholar 

  42. Halees AS, El-Badrawi R, Khabar KS (2008) ARED Organism: expansion of ARED reveals AU-rich element cluster variations between human and mouse. Nucleic Acids Res 36:D137–D140

    Article  PubMed  CAS  Google Scholar 

  43. Bakheet T, Williams BR, Khabar KS (2006) ARED 3.0: the large and diverse AU-rich transcriptome. Nucleic Acids Res 34:D111–D114

    Article  PubMed  CAS  Google Scholar 

  44. Claffey KP, Shih SC, Mullen A, Dziennis S, Cusick JL, Abrams KR, Lee SW, Detmar M (1998) Identification of a human VPF/VEGF 3′ untranslated region mediating hypoxia-induced mRNA stability. Mol Biol Cell 9:469–481

    PubMed  CAS  Google Scholar 

  45. Levy NS, Chung S, Furneaux H, Levy AP (1998) Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J Biol Chem 273:6417–6423

    Article  PubMed  CAS  Google Scholar 

  46. King PH (2000) RNA-binding analyses of HuC and HuD with the VEGF and c-myc 3′-untranslated regions using a novel ELISA-based assay. Nucleic Acids Res 28:E20

    Article  PubMed  CAS  Google Scholar 

  47. Dixon DA, Tolley ND, King PH, Nabors LB, McIntyre TM, Zimmerman GA, Prescott SM (2001) Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Invest. 108:1657–1665

    PubMed  CAS  Google Scholar 

  48. Onesto C, Berra E, Grepin R, Pages G (2004) Poly(A)-binding protein-interacting protein 2, a strong regulator of vascular endothelial growth factor mRNA. J Biol Chem 279:34217–34226

    Article  PubMed  CAS  Google Scholar 

  49. Touriol C, Morillon A, Gensac MC, Prats H, Prats AC (1999) Expression of human fibroblast growth factor 2 mRNA is post-transcriptionally controlled by a unique destabilizing element present in the 3′-untranslated region between alternative polyadenylation sites. J Biol Chem 274:21402–21408

    Article  PubMed  CAS  Google Scholar 

  50. Kim TW, Yim S, Choi BJ, Jang Y, Lee JJ, Sohn BH, Yoo HS, Yeom YI, Park KC (2010) Tristetraprolin regulates the stability of HIF-1alpha mRNA during prolonged hypoxia. Biochem Biophys Res Commun 391:963–968

    Article  PubMed  CAS  Google Scholar 

  51. Lai PF, Mohamed F, Monge JC, Stewart DJ (2003) Downregulation of eNOS mRNA expression by TNFalpha: identification and functional characterization of RNA-protein interactions in the 3′UTR. Cardiovasc Res 59:160–168

    Article  PubMed  CAS  Google Scholar 

  52. Ristimaki A, Narko K, Hla T (1996) Down-regulation of cytokine-induced cyclo-oxygenase-2 transcript isoforms by dexamethasone: evidence for post-transcriptional regulation. Biochem. J. 318(Pt 1):325–331

    PubMed  CAS  Google Scholar 

  53. Gou Q, Liu CH, Ben-Av P, Hla T (1998) Dissociation of basal turnover and cytokine-induced transcript stabilization of the human cyclooxygenase-2 mRNA by mutagenesis of the 3′-untranslated region. Biochem Biophys Res Commun 242:508–512

    Article  PubMed  CAS  Google Scholar 

  54. Xu K, Robida AM, Murphy TJ (2000) Immediate-early MEK-1-dependent stabilization of rat smooth muscle cell cyclooxygenase-2 mRNA by Galpha(q)-coupled receptor signaling. J Biol Chem 275:23012–23019

    Article  PubMed  CAS  Google Scholar 

  55. Sengupta S, Jang BC, Wu MT, Paik JH, Furneaux H, Hla T (2003) The RNA-binding protein HuR regulates the expression of cyclooxygenase-2. J Biol Chem 278:25227–25233

    Article  PubMed  CAS  Google Scholar 

  56. Takayama S, Reed JC, Homma S (2003) Heat-shock proteins as regulators of apoptosis. Oncogene 22:9041–9047

    Article  PubMed  CAS  Google Scholar 

  57. Pearl LH, Prodromou C (2001) Structure, function, and mechanism of the Hsp90 molecular chaperone. Adv Protein Chem 59:157–186

    Article  PubMed  CAS  Google Scholar 

  58. Picard D (2002) Heat-shock protein 90, a chaperone for folding and regulation. Cell Mol Life Sci 59:1640–1648

    Article  PubMed  CAS  Google Scholar 

  59. Pratt WB, Toft DO (2003) Regulation of signaling protein function and trafficking by the hsp90/hsp70-based chaperone machinery. Exp Biol Med (Maywood) 228:111–133

    CAS  Google Scholar 

  60. Whitesell L, Bagatell R, Falsey R (2003) The stress response: implications for the clinical development of hsp90 inhibitors. Curr Cancer Drug Targets 3:349–358

    Article  PubMed  CAS  Google Scholar 

  61. Isaacs JS (2005) Heat-shock protein 90 inhibitors in antineoplastic therapy: is it all wrapped up? Expert Opin Investig Drugs 14:569–589

    Article  PubMed  CAS  Google Scholar 

  62. Powers MV, Workman P (2006) Targeting of multiple signaling pathways by heat shock protein 90 molecular chaperone inhibitors. Endocr Relat Cancer 13(Suppl 1):S125–S135

    Article  PubMed  CAS  Google Scholar 

  63. Neckers L (2002) Hsp90 inhibitors as novel cancer chemotherapeutic agents. Trends Mol Med 8:S55–S61

    Article  PubMed  CAS  Google Scholar 

  64. Grenert JP, Johnson BD, Toft DO (1999) The importance of ATP binding and hydrolysis by hsp90 in formation and function of protein heterocomplexes. J Biol Chem 274:17525–17533

    Article  PubMed  CAS  Google Scholar 

  65. Obermann WM, Sondermann H, Russo AA, Pavletich NP, Hartl FU (1998) In vivo function of Hsp90 is dependent on ATP binding and ATP hydrolysis. J Cell Biol 143:901–910

    Article  PubMed  CAS  Google Scholar 

  66. Weikl T, Muschler P, Richter K, Veit T, Reinstein J, Buchner J (2000) C-terminal regions of Hsp90 are important for trapping the nucleotide during the ATPase cycle. J Mol Biol 303:583–592

    Article  PubMed  CAS  Google Scholar 

  67. Isaacs JS, Xu W, Neckers L (2003) Heat shock protein 90 as a molecular target for cancer therapeutics. Cancer Cell 3:213–217

    Article  PubMed  CAS  Google Scholar 

  68. Whitesell L, Lindquist SL (2005) HSP90 and the chaperoning of cancer. Nat Rev Cancer 5:761–772

    Article  PubMed  CAS  Google Scholar 

  69. Matsui H, Asou H, Inaba T (2007) Cytokines direct the regulation of Bim mRNA stability by heat-shock cognate protein 70. Mol Cell 25:99–112

    Article  PubMed  CAS  Google Scholar 

  70. Mimnaugh EG, Worland PJ, Whitesell L, Neckers LM (1995) Possible role for serine/threonine phosphorylation in the regulation of the heteroprotein complex between the hsp90 stress protein and the pp 60v tyrosine kinase. J Biol Chem 270:28654–28659

    Article  PubMed  CAS  Google Scholar 

  71. Zhao YG, Gilmore R, Leone G, Coffey MC, Weber B, Lee PW (2001) Hsp90 phosphorylation is linked to its chaperoning function. Assembly of the retrovirus cell attachment protein. J Biol Chem 276:32822–32827

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We would like to thank Drs. Yoshimura (Keio University), Nishimura (Kumamoto University), and Miyoshi (RIKEN BioResource Center) for kindly providing the plasmids used in this study. We gratefully appreciate discussions with Drs. Matsushita, Ohnuki, and Nakayama of Ehime University. This study was supported by a grant from Ehime University (D.M.: 054402060) and a Grant-in-Aid for Scientific Research (23112513 to S. Higashiyama, 22590501 to H. Inoue) from the Ministry of Education, Culture, Sports, Science, and Technology, Japan.

Conflict of interest

The authors declare that there are no conflicts of interest that would prejudice the impartiality of this scientific work.

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Authors and Affiliations

  1. Department of Biochemistry and Molecular Genetics, Ehime University Graduate School of Medicine, Shitsukawa, Toon, Ehime, 791-0295, Japan

    Daisuke Miwa, Hirofumi Inoue, Maki Kurokawa, Shinji Fukuda & Shigeki Higashiyama

  2. Department of Cell Growth and Tumor Regulation, Ehime University, Shitsukawa, Toon, Ehime, 791-0295, Japan

    Tomohisa Sakaue, Hirofumi Inoue & Shigeki Higashiyama

  3. Ehime-NIKON Bioimaging Core-Laboratory, Ehime University, Shitsukawa, Toon, Ehime, 791-0295, Japan

    Hirofumi Inoue

  4. Proteomics Core-Laboratory, Ehime Proteo-Medicine Research Center (ProMRes), Ehime University, Shitsukawa, Toon, Ehime, 791-0295, Japan

    Nobuaki Takemori

  5. Fujirebio Inc., 2-62-5 Nihonbashi-Hamacho, Chuo-ku, Tokyo, 103-0007, Japan

    Daisuke Miwa, Kazuya Omi & Katsutoshi Goishi

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  1. Daisuke Miwa
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Miwa, D., Sakaue, T., Inoue, H. et al. Protein kinase D2 and heat shock protein 90 beta are required for BCL6-associated zinc finger protein mRNA stabilization induced by vascular endothelial growth factor-A. Angiogenesis 16, 675–688 (2013). https://doi.org/10.1007/s10456-013-9345-x

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