Two new isoforms of the human hepatoma-derived growth factor interact with components of the cytoskeleton
-
Jessica Nüße
, Ursula Mirastschijski , Mario Waespy , Janina Oetjen , Nadine Brandes , Osmond Rebello , Federico Paroni , Sørge Kelm und Frank Dietz
Abstract
Hepatoma-derived growth factor (HDGF) is involved in diverse, apparently unrelated processes, such as cell proliferation, apoptosis, DNA-repair, transcriptional control, ribosome biogenesis and cell migration. Most of the interactions of HDGF with diverse molecules has been assigned to the hath region of HDGF. In this study we describe two previously unknown HDGF isoforms, HDGF-B and HDGF-C, generated via alternative splicing with structurally unrelated N-terminal regions of their hath region, which is clearly different from the well described isoform, HDGF-A. In silico modeling revealed striking differences near the PHWP motif, an essential part of the binding site for glycosaminoglycans and DNA/RNA. This observation prompted the hypothesis that these isoforms would have distinct interaction patterns with correspondingly diverse roles on cellular processes. Indeed, we discovered specific associations of HDGF-B and HDGF-C with cytoskeleton elements, such as tubulin and dynein, suggesting previously unknown functions of HDGF in retrograde transport, site directed localization and/or cytoskeleton organization. In contrast, the main isoform HDGF-A does not interact directly with the cytoskeleton, but via RNA with messenger ribonucleoprotein (mRNP) complexes. In summary, the discovery of HDGF splice variants with their discrete binding activities and subcellular distributions opened new avenues for understanding its biological function and importance.
Funding source: European Research Council
Award Identifier / Grant number: FP7/2007-2013
Funding statement: Our sincerest gratitude goes to Ajinkya Kulkarni, Department of Microbial Ecophysiology, University of Bremen for help and advice with the Zeiss ApoTome microscope and Prof. Michael Friedrich as head of the group for enabling the use. We would like to thank Prof. Jörn Bullerdiek, Centre for Human Genetics, University of Bremen, Germany and Prof. Dr. Martin Götte, Department of Gynecology and Obstetrics, University Medical Centre Münster, Germany for providing the cell lines MCF-7 and MDA-MB-231, respectively. The research leading to these results has received – in part – funding from the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 243195.
Acknowledgments:
Our sincerest gratitude goes to Ajinkya Kulkarni, Department of Microbial Ecophysiology, University of Bremen for help and advice with the Zeiss ApoTome microscope and Prof. Michael Friedrich as head of the group for enabling the use. We would like to thank Prof. Jörn Bullerdiek, Centre for Human Genetics, University of Bremen, Germany and Prof. Dr. Martin Götte, Department of Gynecology and Obstetrics, University Medical Centre Münster, Germany for providing the cell lines MCF-7 and MDA-MB-231, respectively. The research leading to these results has received – in part – funding from the European Research Council under the European Community’s Seventh Framework Programme (FP7/2007-2013)/ERC grant agreement no. 243195.
References
Abouzied, M.M., Baader, S.L., Dietz, F., Kappler, J., Gieselmann, V., and Franken, S. (2004). Expression patterns and different subcellular localization of the growth factors HDGF (hepatoma-derived growth factor) and HRP-3 (HDGF-related protein-3) suggest functions in addition to their mitogenic activity. Biochem. J. 378, 169–176.10.1042/bj20030916Suche in Google Scholar PubMed PubMed Central
Aizawa, H., Kawasaki, H., Murofushi, H., Kotani, S., Suzuki, K., and Sakai, H. (1989). A common amino acid sequence in 190-kDa microtubule-associated protein and tau for the promotion of microtubule assembly. J. Biol. Chem. 264, 5885–5890.10.1016/S0021-9258(18)83632-8Suche in Google Scholar
Bianco, A., Dienstbier, M., Salter, H.K., Gatto, G., and Bullock, S.L. (2010). Bicaudal-D regulates fragile X mental retardation protein levels, motility, and function during neuronal morphogenesis. Curr. Biol. 20, 1487–1492.10.1016/j.cub.2010.07.016Suche in Google Scholar PubMed PubMed Central
Bremer, S., Klein, K., Sedlmaier, A., Abouzied, M., Gieselmann, V., and Franken, S. (2013). Hepatoma-derived growth factor and nucleolin exist in the same ribonucleoprotein complex. BMC Biochem. 14, 1–1.10.1186/1471-2091-14-2Suche in Google Scholar PubMed PubMed Central
Canutescu, A.A., Shelenkov, A.A., and Dunbrack, R.L., Jr. (2003). A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci. 12, 2001–2014.10.1110/ps.03154503Suche in Google Scholar PubMed PubMed Central
Chang, K.-C., Tai, M.-H., Lin, J.-W., Wang, C.-C., Huang, C.-C., Hung, C.-H., Chen, C.-H., Lu, S.-N., Lee, C.-M., Changchien, C.-S., et al. (2007). Hepatoma-derived growth factor is a novel prognostic factor for gastrointestinal stromal tumors. Int. J. Cancer 121, 1059–1065.10.1002/ijc.22803Suche in Google Scholar PubMed
Chen, C.Y., Gherzi, R., Andersen, J.S., Gaietta, G., Jürchott, K., Royer, H.D., Mann, M., and Karin, M. (2000). Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Gene. Dev. 14, 1236–1248.10.1101/gad.14.10.1236Suche in Google Scholar
Chen, F.F., Lin, W.H., Lin, S.C., Kuo, J.H., Chu, H.Y., Huang, W.C., Chuang, Y.J., Lee, S.C., and Sue, S.C. (2012a). Significance of heparin binding to basic residues in homologous to the amino terminus of hepatoma-derived growth factor and related proteins. Glycobiology 22, 649–661.10.1093/glycob/cwr191Suche in Google Scholar PubMed
Chen, J., Guo, K., and Kastan, M.B. (2012b). Interactions of Nucleolin and Ribosomal Protein L26 (RPL26) in Translational Control of Human p53 mRNA. J. Biol. Chem. 287, 16467–16476.10.1074/jbc.M112.349274Suche in Google Scholar PubMed PubMed Central
Chernov, K.G., Mechulam, A., Popova, N.V., Pastre, D., Nadezhdina, E.S., Skabkina, O.V., Shanina, N.A., Vasiliev, V.D., Tarrade, A., Melki, J., et al. (2008). YB-1 promotes microtubule assembly in vitro through interaction with tubulin and microtubules. BMC Biochem. 9, 23–16.10.1186/1471-2091-9-23Suche in Google Scholar PubMed PubMed Central
Dietz, F., Franken, S., Yoshida, K., Nakamura, H., Kappler, J., and Gieselmann, V. (2002). The family of hepatoma-derived growth factor proteins: characterization of a new member HRP-4 and classification of its subfamilies. Biochem. J. 366, 491–500.10.1042/bj20011811Suche in Google Scholar
Eidahl, J.O., Crowe, B.L., North, J.A., McKee, C.J., Shkriabai, N., Feng, L., Plumb, M., Graham, R.L., Gorelick, R.J., Hess, S., et al. (2013). Structural basis for high-affinity binding of LEDGF PWWP to mononucleosomes. Nucleic Acids Res. 41, 3924–3936.10.1093/nar/gkt074Suche in Google Scholar PubMed PubMed Central
El-tahir, H.M., Abouzied, M.M., Gallitzendoerfer, R., Gieselmann, V., and Franken, S. (2009). Hepatoma-derived growth factor-related protein-3 interacts with microtubules and promotes neurite outgrowth in mouse cortical neurons. J. Biol. Chem. 284, 11637–11651.10.1074/jbc.M901101200Suche in Google Scholar PubMed PubMed Central
Enomoto, H. (2002). Hepatoma-derived growth factor is highly expressed in developing liver and promotes fetal hepatocyte proliferation. Hepatology 36, 1519–1527.10.1002/hep.1840360629Suche in Google Scholar
Evdokimova, V.M. and Ovchinnikov, L.P. (1999). Translational regulation by Y-box transcription factor: involvement of the major mRNA-associated protein, p50. Int. J. Biochem. Cell Biol. 31, 139–149.10.1016/S1357-2725(98)00137-XSuche in Google Scholar PubMed
Everett, A.D. (2001). Identification, cloning, and developmental expression of hepatoma-derived growth factor in the developing rat heart. Dev. Dyn. 222, 450–458.10.1002/dvdy.1204Suche in Google Scholar PubMed
Everett, A.D., Lobe, D.R., Matsumura, M.E., Nakamura, H., and McNamara, C.A. (2000). Hepatoma-derived growth factor stimulates smooth muscle cell growth and is expressed in vascular development. J. Clin. Invest. 105, 567–575.10.1172/JCI7497Suche in Google Scholar PubMed PubMed Central
Everett, A.D., Stoops, T., and McNamara, C.A. (2001). Nuclear targeting is required for hepatoma-derived growth factor-stimulated mitogenesis in vascular smooth muscle cells. J. Biol. Chem. 276, 37564–37568.10.1074/jbc.M105109200Suche in Google Scholar PubMed
Fähling, M., Steege, A., Perlewitz, A., Nafz, B., Mrowka, R., Persson, P.B., and Thiele, B.J. (2005). Role of nucleolin in posttranscriptional control of MMP-9 expression. Biochim. Biophys. Acta Gene Struct. Expr. 1731, 32–40.10.1016/j.bbaexp.2005.08.005Suche in Google Scholar PubMed
Giannakakou, P., Nakano, M., Nicolaou, K.C., O’Brate, A., Yu, J., Blagosklonny, M.V., Greber, U.F., and Fojo, T. (2002). Enhanced microtubule-dependent trafficking and p53 nuclear accumulation by suppression of microtubule dynamics. Proc. Natl. Acad. Sci. USA 99, 10855–10860.10.1073/pnas.132275599Suche in Google Scholar PubMed PubMed Central
Giannakakou, P., Sackett, D.L., Ward, Y., Webster, K.R., Blagosklonny, M.V., and Fojo, T. (2000). p53 is associated with cellular microtubules and is transported to the nucleus by dynein. Nat. Cell Biol. 2, 709–717.10.1038/35036335Suche in Google Scholar PubMed
Guo, C. (2011). Various effects of hepatoma-derived growth factor on cell growth, migration and invasion of breast cancer and prostate cancer cells. Oncol. Rep. 26, 511–517.10.3892/or.2011.1295Suche in Google Scholar PubMed
Guo, S., Liu, H.-D., Liu, Y.-F., Liu, L., Sun, Q., and Cui, X.-J. (2014). Hepatoma-derived growth factor: a novel prognostic biomarker in intrahepatic cholangiocarcinoma. Tumor Biol. 36, 353–364.10.1007/s13277-014-2651-0Suche in Google Scholar PubMed
Gurland, G. and Gundersen, G.G. (1995). Stable, detyrosinated microtubules function to localize vimentin intermediate filaments in fibroblasts. J. Cell Biol. 131, 1275–1290.10.1083/jcb.131.5.1275Suche in Google Scholar PubMed PubMed Central
Gyoeva, F.K. and Gelfand, V.I. (1991). Coalignment of vimentin intermediate filaments with microtubules depends on kinesin. Nature 353, 445–448.10.1038/353445a0Suche in Google Scholar PubMed
Helfand, B.T., Mikami, A., Vallee, R.B., and Goldman, R.D. (2002). A requirement for cytoplasmic dynein and dynactin in intermediate filament network assembly and organization. J. Cell Biol. 157, 795–806.10.1083/jcb.200202027Suche in Google Scholar PubMed PubMed Central
Hsu, S.-S., Chen, C.-H., Liu, G.-S., Tai, M.-H., Wang, J.-S., Wu, J.-C., Kung, M.-L., Chan, E.C., and Liu, L.-F. (2012). Tumorigenesis and prognostic role of hepatoma-derived growth factor in human gliomas. J. Neurooncol. 107, 101–109.10.1007/s11060-011-0733-zSuche in Google Scholar PubMed
Hu, T.-H., Huang, C.-C., Liu, L.-F., Lin, P.-R., Liu, S.-Y., Chang, H.-W., Changchien, C.-S., Lee, C.-M., Chuang, J.-H., and Tai, M.-H. (2003). Expression of hepatoma-derived growth factor in hepatocellular carcinoma. Cancer 98, 1444–1456.10.1002/cncr.11653Suche in Google Scholar PubMed
Hung, Y.-L., Lee, H.-J., Jiang, I., Lin, S.-C., Lo, W.-C., Lin, Y.-J., and Sue, S.-C. (2015). The first residue of the PWWP motif modulates HATH domain binding, Stability, and Protein–Protein Interaction. Biochemistry 54, 406374.10.1021/acs.biochem.5b00454Suche in Google Scholar PubMed
Iwasaki, T., Nakagawa, K., Nakamura, H., Takada, Y., Matsui, K., and Kawahara, K. (2005). Hepatoma-derived growth factor as a prognostic marker in completely resected non-small-cell lung cancer. Oncol. Rep. 13, 1075–1080.10.3892/or.13.6.1075Suche in Google Scholar
Izumoto, Y., Kuroda, T., Harada, H., Kishimoto, T., and Nakamura, H. (1997). Hepatoma-derived growth factor belongs to a gene family in mice showing significant homology in the amino terminus. Biochem. Biophy. Res. Co. 238, 26–32.10.1006/bbrc.1997.7233Suche in Google Scholar PubMed
Jones, D.T. (1999). Protein secondary structure prediction based on position-specific scoring matrices. J. Mol. Biol. 292, 195–202.10.1006/jmbi.1999.3091Suche in Google Scholar PubMed
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., et al. (2012). Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.10.1093/bioinformatics/bts199Suche in Google Scholar PubMed PubMed Central
King, R.D. and Sternberg, M.J. (1996). Identification and application of the concepts important for accurate and reliable protein secondary structure prediction. Protein Sci. 5, 2298–2310.10.1002/pro.5560051116Suche in Google Scholar PubMed PubMed Central
Kishima, Y., Yamamoto, H., Izumoto, Y., Yoshida, K., Enomoto, H., Yamamoto, M., Kuroda, T., Ito, H., Yoshizaki, K., and Nakamura, H. (2002). Hepatoma-derived growth factor stimulates cell growth after translocation to the nucleus by nuclear localization signals. J. Biol. Chem. 277, 10315–10322.10.1074/jbc.M111122200Suche in Google Scholar PubMed
Krieger, E., Joo, K., Lee, J., Lee, J., Raman, S., Thompson, J., Tyka, M., Baker, D., and Karplus, K. (2009). Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: four approaches that performed well in CASP8. Proteins 77, 114–122.10.1002/prot.22570Suche in Google Scholar PubMed PubMed Central
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.10.1038/227680a0Suche in Google Scholar PubMed
Lepourcelet, M. (2005). Insights into developmental mechanisms and cancers in the mammalian intestine derived from serial analysis of gene expression and study of the hepatoma-derived growth factor (HDGF). Development 132, 415–427.10.1242/dev.01579Suche in Google Scholar PubMed
Lewis, S.A., Wang, D.H., and Cowan, N.J. (1988). Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein. Science 242, 936–939.10.1126/science.3142041Suche in Google Scholar PubMed
Liao, F., Dong, W., and Fan, L. (2009). Apoptosis of human colorectal carcinoma cells is induced by blocking hepatoma-derived growth factor. Med. Oncol. 27, 1219–1226.10.1007/s12032-009-9362-1Suche in Google Scholar PubMed
Liu, Y.-F., Zhao, R., Guo, S., Wang, X.-Q., Lian, P.-L., Chen, Y.-G., and Xu, K.-S. (2010). Expression and clinical significance of hepatoma-derived growth factor as a prognostic factor in human hilar cholangiocarcinoma. Ann. Surg. Oncol. 18, 872–879.10.1245/s10434-010-1303-xSuche in Google Scholar PubMed
Lukasik, S.M. (2006). High resolution structure of the HDGF PWWP domain: a potential DNA binding domain. Prot. Sci. 15, 314–323.10.1110/ps.051751706Suche in Google Scholar PubMed PubMed Central
Maher-Laporte, M., Berthiaume, F., Moreau, M., Julien, L.-A., Lapointe, G., Mourez, M., and DesGroseillers, L. (2010). Molecular Composition of Staufen2-Containing Ribonucleoproteins in Embryonic Rat Brain. PLoS One 5, e11350.10.1371/journal.pone.0011350Suche in Google Scholar PubMed PubMed Central
Mallik, R. and Gross, S.P. (2004). Molecular motors: strategies to get along. Curr. Biol. 14, R971–R982.10.1016/j.cub.2004.10.046Suche in Google Scholar PubMed
Mandelkow, E. and Mandelkow, E.M. (1995). Microtubules and microtubule-associated proteins. Curr. Opin. Cell Biol. 7, 72–81.10.1016/0955-0674(95)80047-6Suche in Google Scholar PubMed
Meng, J., Xie, W., Cao, L., Hu, C., and Zhen, Z. (2009). shRNA targeting HDGF suppressed cell growth and invasion of squamous cell lung cancer. Acta Biochim. Biophys. 42, 52–57.10.1093/abbs/gmp102Suche in Google Scholar PubMed
Nakamura, H., Izumoto, Y., Kambe, H., Kuroda, T., Mori, T., Kawamura, K., Yamamoto, H., and Kishimoto, T. (1994). Molecular cloning of complementary DNA for a novel human hepatoma-derived growth factor. Its homology with high mobility group-1 protein. J. Biol. Chem. 269, 25143–25149.10.1016/S0021-9258(17)31509-0Suche in Google Scholar
Nameki, N. (2005). Solution structure of the PWWP domain of the hepatoma-derived growth factor family. Prot. Sci. 14, 756–764.10.1110/ps.04975305Suche in Google Scholar PubMed PubMed Central
Narron, J.V., Stoops, T.D., Barringhaus, K., Matsumura, M., and Everett, A.D. (2006). Hepatoma-derived growth factor is expressed after vascular injury in the rat and stimulates smooth muscle cell migration. Pediatr. Res. 59, 778–783.10.1203/01.pdr.0000219299.24435.4fSuche in Google Scholar PubMed
Oliver, J.A. and Al-Awqati, Q. (1998). An endothelial growth factor involved in rat renal development. J. Clin. Invest. 102, 1208–1219.10.1172/JCI785Suche in Google Scholar PubMed PubMed Central
Pfaffl, M.W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.10.1093/nar/29.9.e45Suche in Google Scholar PubMed PubMed Central
Pradeepa, M.M., Sutherland, H.G., Ule, J., Grimes, G.R., and Bickmore, W.A. (2012). Psip1/Ledgf p52 binds methylated histone H3K36 and splicing factors and contributes to the regulation of alternative splicing. PLoS Genet. 8, e1002717.10.1371/journal.pgen.1002717Suche in Google Scholar PubMed PubMed Central
Prahlad, V., Yoon, M., Moir, R.D., Vale, R.D., and Goldman, R.D. (1998). Rapid movements of vimentin on microtubule tracks: kinesin-dependent assembly of intermediate filament networks. J. Cell Biol. 143, 159–170.10.1083/jcb.143.1.159Suche in Google Scholar PubMed PubMed Central
Qin, S. and Min, J. (2014). Structure and function of the nucleosome-binding PWWP domain. Trends Biochem. Sci. 39, 536–547.10.1016/j.tibs.2014.09.001Suche in Google Scholar PubMed
Qiu, J. and Elber, R. (2006). SSALN: an alignment algorithm using structure-dependent substitution matrices and gap penalties learned from structurally aligned protein pairs. Proteins 62, 881–891.10.1002/prot.20854Suche in Google Scholar PubMed
Ren, H. (2004). Expression of hepatoma-derived growth factor is a strong prognostic predictor for patients with early-stage non-small-cell lung cancer. J. Clin. Oncol. 22, 3230–3237.10.1200/JCO.2004.02.080Suche in Google Scholar PubMed
Ren, H., Chu, Z., and Mao, L. (2009). Antibodies targeting hepatoma-derived growth factor as a novel strategy in treating lung cancer. Mol. Cancer Ther. 8, 1106–1112.10.1158/1535-7163.MCT-08-0779Suche in Google Scholar PubMed PubMed Central
Rodriguez, O.C., Schaefer, A.W., Mandato, C.A., Forscher, P., Bement, W.M., and Waterman-Storer, C.M. (2003). Conserved microtubule-actin interactions in cell movement and morphogenesis. Nat. Cell Biol. 5, 599–609.10.1038/ncb0703-599Suche in Google Scholar PubMed
Sardar, P., Kumar, A., Bhandari, A., and Goswami, C. (2012). Conservation of Tubulin-Binding Sequences in TRPV1 throughout Evolution. PLoS One 7, e31448–10.10.1371/journal.pone.0031448Suche in Google Scholar PubMed PubMed Central
Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850–858.10.1021/ac950914hSuche in Google Scholar PubMed
Singh, D.P., Kimura, A., Chylack, L.T., and Shinohara, T. (2000). Lens epithelium-derived growth factor (LEDGF/p75) and p52 are derived from a single gene by alternative splicing. Gene 242, 265–273.10.1016/S0378-1119(99)00506-5Suche in Google Scholar
Stec, I., Nagl, S.B., van Ommen, G.J., and den Dunnen, J.T. (2000). The PWWP domain: a potential protein-protein interaction domain in nuclear proteins influencing differentiation? FEBS Lett. 473, 1–5.10.1016/S0014-5793(00)01449-6Suche in Google Scholar
Sue, S.-C., Chen, J.-Y., and Huang, T.-H. (2004a). Sequence specific 1H, 13C and 15N resonance assignments of the hath-domain of human hepatoma-derived growth factor. J. Biomol. NMR 29, 95–96.10.1023/B:JNMR.0000019467.57276.05Suche in Google Scholar PubMed
Sue, S.-C., Chen, J.-Y., Lee, S.-C., Wu, W.-G., and Huang, T.-H. (2004b). Solution Structure and Heparin Interaction of Human Hepatoma-derived Growth Factor. J. Mol. Biol. 343, 1365–1377.10.1016/j.jmb.2004.09.014Suche in Google Scholar PubMed
Sue, S.-C., Lee, W.-T., Tien, S.-C., Lee, S.-C., Yu, J.-G., Wu, W.-J., Wu, W.-G., and Huang, T.-H. (2007). PWWP module of human hepatoma-derived growth factor forms a domain-swapped dimer with much higher affinity for heparin. J. Mol. Biol. 367, 456–472.10.1016/j.jmb.2007.01.010Suche in Google Scholar PubMed
Thakar, K., Kröcher, T., Savant, S., Gollnast, D., Kelm, S., and Dietz, F. (2010). Secretion of hepatoma-derived growth factor is regulated by N-terminal processing. Biol. Chem. 391, 1–10.10.1515/bc.2010.147Suche in Google Scholar
Thakar, K., Niedenthal, R., Okaz, E., Franken, S., Jakobs, A., Gupta, S., Kelm, S., and Dietz, F. (2008). SUMOylation of the hepatoma-derived growth factor negatively influences its binding to chromatin. FEBS J. 275, 1411–1426.10.1111/j.1742-4658.2008.06303.xSuche in Google Scholar PubMed
Thakar, K., Votteler, I., Kelkar, D., Shidore, T., Gupta, S., Kelm, S., and Dietz, F. (2012). Interaction of HRP-2 isoforms with HDGF. Chromatin binding of a specific heteromer. FEBS J. 279, 737–751.10.1111/j.1742-4658.2011.08464.xSuche in Google Scholar PubMed
Tichopad, A. (2003). Standardized determination of real-time PCR efficiency from a single reaction set-up. Nucleic Acids Res. 31, e122.10.1093/nar/gng122Suche in Google Scholar PubMed PubMed Central
Tsang, T.Y., Tang, W.Y., Tsang, W.P., Co, N.N., Kong, S.K., and Kwok, T.T. (2008). Downregulation of hepatoma-derived growth factor activates the Bad-mediated apoptotic pathway in human cancer cells. Apoptosis 13, 1135–1147.10.1007/s10495-008-0241-6Suche in Google Scholar PubMed
Uyama, H., Tomita, Y., Nakamura, H., Nakamori, S., Zhang, B., Hoshida, Y., Enomoto, H., Okuda, Y., Sakon, M., Aozasa, K., et al. (2006). Hepatoma-derived growth factor is a novel prognostic factor for patients with pancreatic cancer. Clin. Cancer Res. 12, 6043–6048.10.1158/1078-0432.CCR-06-1064Suche in Google Scholar PubMed
van Nuland, R., van Schaik, F.M., Simonis, M., van Heesch, S., Cuppen, E., Boelens, R., Timmers, H.M., and van Ingen, H. (2013). Nucleosomal DNA binding drives the recognition of H3K36-methylated nucleosomes by the PSIP1-PWWP domain. Epigenetics Chromatin 6, 1–1.10.1186/1756-8935-6-12Suche in Google Scholar PubMed PubMed Central
Villace, P. (2004). The composition of Staufen-containing RNA granules from human cells indicates their role in the regulated transport and translation of messenger RNAs. Nucleic Acids Res. 32, 2411–2420.10.1093/nar/gkh552Suche in Google Scholar PubMed PubMed Central
Wang, C.-H., Davamani, F., Sue, S.-C., Lee, S.-C., Wu, P.-L., Tang, F.-M., Shih, C., Huang, T.-H., and Wu, W.-G. (2011). Cell surface heparan sulfates mediate internalization of the PWWP/HATH domain of HDGF via macropinocytosis to fine-tune cell signalling processes involved in fibroblast cell migration. Biochem. J. 433, 127–138.10.1042/BJ20100589Suche in Google Scholar PubMed
Wu, H., Zeng, H., Lam, R., Tempel, W., Amaya, M.F., Xu, C., Dombrovski, L., Qiu, W., Wang, Y., and Min, J. (2011). Structural and histone binding ability characterizations of human PWWP domains. PLoS One 6, e18919.10.1371/journal.pone.0018919Suche in Google Scholar PubMed PubMed Central
Yamamoto, S. (2006). Expression of hepatoma-derived growth factor is correlated with lymph node metastasis and prognosis of gastric carcinoma. Clin. Cancer Res. 12, 117–122.10.1158/1078-0432.CCR-05-1347Suche in Google Scholar PubMed
Yang, J. and Everett, A.D. (2007). Hepatoma derived growth factor binds DNA through the N-terminal PWWP domain. BMC Mol. Biol. 8, 101–109.10.1186/1471-2199-8-101Suche in Google Scholar PubMed PubMed Central
Yang, J. and Everett, A.D. (2009). Hepatoma-derived growth factor represses SET and MYND domain containing 1 gene expression through interaction with C-terminal binding protein. J. Mol. Biol. 386, 938–950.10.1016/j.jmb.2008.12.080Suche in Google Scholar PubMed PubMed Central
Yoshida, K., Nakamura, H., Okuda, Y., Enomoto, H., Kishima, Y., Uyama, H., Ito, H., Hirasawa, T., Inagaki, S., and Kawase, I. (2003). Expression of hepatoma-derived growth factor in hepatocarcinogenesis. J. Gastroenterol. Hepatol. 18, 1293–1301.10.1046/j.1440-1746.2003.03191.xSuche in Google Scholar PubMed
Yu, Y., Shen, H., Yu, H., Zhong, F., Zhang, Y., Zhang, C., Zhao, J., Li, H., Chen, J., Liu, Y., et al. (2011). Systematic proteomic analysis of human hepotacellular carcinoma cells reveals molecular pathways and networks involved in metastasis. Mol. Biosyst. 7, 1908–1916.10.1039/c0mb00265hSuche in Google Scholar PubMed
Zhang, J. (2006). Down-regulation of hepatoma-derived growth factor inhibits anchorage-independent growth and invasion of non-small cell lung cancer cells. Cancer Res. 66, 18–23.10.1158/0008-5472.CAN-04-3905Suche in Google Scholar PubMed
Zhao, J., Yu, H., Lin, L., Tu, J., Cai, L., Chen, Y., Zhong, F., Lin, C., He, F., and Yang, P. (2011). Interactome study suggests multiple cellular functions of hepatoma-derived growth factor (HDGF). J. Proteomics 75, 588–602.10.1016/j.jprot.2011.08.021Suche in Google Scholar PubMed
Supplemental Material:
The online version of this article (DOI: 10.1515/hsz-2015-0273) offers supplementary material, available to authorized users.
©2016 by De Gruyter
Artikel in diesem Heft
- Frontmatter
- Review
- Nrf2 activation in the treatment of neurodegenerative diseases: a focus on its role in mitochondrial bioenergetics and function
- Research Articles/Short Communications
- Protein Structure and Function
- Effect of molecular chaperones on aberrant protein oligomers in vitro: super-versus sub-stoichiometric chaperone concentrations
- Two new isoforms of the human hepatoma-derived growth factor interact with components of the cytoskeleton
- Cell Biology and Signaling
- Activation of corticotropin releasing factor receptors up regulates collagen production by hepatic stellate cells via promoting p300 expression
- On the regulative role of the glutamate receptor in mitochondria
- Proteolysis
- Biomechanical and biochemical regulation of cathepsin K expression in endothelial cells converge at AP-1 and NF-κB
- New insights into the substrate specificity of macrophage elastase MMP-12
Artikel in diesem Heft
- Frontmatter
- Review
- Nrf2 activation in the treatment of neurodegenerative diseases: a focus on its role in mitochondrial bioenergetics and function
- Research Articles/Short Communications
- Protein Structure and Function
- Effect of molecular chaperones on aberrant protein oligomers in vitro: super-versus sub-stoichiometric chaperone concentrations
- Two new isoforms of the human hepatoma-derived growth factor interact with components of the cytoskeleton
- Cell Biology and Signaling
- Activation of corticotropin releasing factor receptors up regulates collagen production by hepatic stellate cells via promoting p300 expression
- On the regulative role of the glutamate receptor in mitochondria
- Proteolysis
- Biomechanical and biochemical regulation of cathepsin K expression in endothelial cells converge at AP-1 and NF-κB
- New insights into the substrate specificity of macrophage elastase MMP-12