Interactome study suggests multiple cellular functions of hepatoma-derived growth factor (HDGF)

Journal of Proteomics

Volumn 75, Issue 2, 2011, Pages 588-602

  Zhao, Jian ^a,b   Yu, Hongxiu ^b   Lin, Ling ^b   Tu, Jun ^b   Cai, Lili ^a,b   Chen, Yanmei ^a,b   Zhong, Fan ^b   Lin, Chengzhao ^b   He, Fuchu ^a,b,c   Yang, Pengyuan ^b  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c BEIJING INSTITUTE OF RADIATION MEDICINE   (China)

Author keywords

Hepatoma derived growth factor; Interactome; RNA co immunoprecipitation; Streptavidin binding peptide; Tandem affinity purification

Indexed keywords

HEPATOMA DERIVED GROWTH FACTOR; RNA; STREPTAVIDIN;

ARTICLE; BIOGENESIS; CELL FUNCTION; DNA DAMAGE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEOMICS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RIBOSOME; RNA PROCESSING; TANDEM MASS SPECTROMETRY; TRANSCRIPTION REGULATION;

CARRIER PROTEINS; HEK293 CELLS; HUMANS; IMMUNOPRECIPITATION; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; PROTEIN INTERACTION DOMAINS AND MOTIFS; TANDEM MASS SPECTROMETRY; TRANSCRIPTIONAL ACTIVATION;

EID: 82355183317     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.08.021     Document Type: Article

References (97)

1. Nakamura H., Kambe H., Egawa T., Kimura Y., Ito H., Hayashi E., et al. Partial purification and characterization of human hepatoma-derived growth factor. Clin Chim Acta 1989, 183:273-284.
2. Enomoto H., Yoshida K., Kishima Y., Okuda Y., Nakamura H. Participation of hepatoma-derived growth factor in the regulation of fetal hepatocyte proliferation. J Gastroenterol 2002, 37:158-161.
3. Enomoto H., Yoshida K., Kishima Y., Kinoshita T., Yamamoto M., Everett A.D., et al. Hepatoma-derived growth factor is highly expressed in developing liver and promotes fetal hepatocyte proliferation. Hepatology 2002, 36:1519-1527.
4. Enomoto H., Nakamura H., Liu W.D., Yoshida K., Okuda Y., Imanishi H., et al. Hepatoma-derived growth factor is induced in liver regeneration. Hepatol Res 2009, 39:988-997.
5. Oliver J.A., Al-Awqati Q. An endothelial growth factor involved in rat renal development. J Clin Invest 1998, 102:1208-1219.
6. Cilley R.E., Zgleszewski S.E., Chinoy M.R. Fetal lung development: airway pressure enhances the expression of developmental genes. J Pediatr Surg 2000, 35:113-118.
7. Everett A.D., Narron J.V., Stoops T., Nakamura H., Tucker A. Hepatoma-derived growth factor is a pulmonary endothelial cell-expressed angiogenic factor. Am J Physiol Lung Cell Mol Physiol 2004, 286:L1194-L1201.
8. Narron J.V., Stoops T.D., Barringhaus K., Matsumura M., Everett A.D. Hepatoma-derived growth factor is expressed after vascular injury in the rat and stimulates smooth muscle cell migration. Pediatr Res 2006, 59:778-783.
9. Everett A.D., Stoops T., McNamara C.A. Nuclear targeting is required for hepatoma-derived growth factor-stimulated mitogenesis in vascular smooth muscle cells. J Biol Chem 2001, 276:37564-37568.
10. Everett A.D., Lobe D.R., Matsumura M.E., Nakamura H., McNamara C.A. Hepatoma-derived growth factor stimulates smooth muscle cell growth and is expressed in vascular development. J Clin Invest 2000, 105:567-575.
11. Everett A.D. Identification, cloning, and developmental expression of hepatoma-derived growth factor in the developing rat heart. Dev Dyn 2001, 222:450-458.
12. Yoshida K., Tomita Y., Okuda Y., Yamamoto S., Enomoto H., Uyama H., et al. Hepatoma-derived growth factor is a novel prognostic factor for hepatocellular carcinoma. Ann Surg Oncol 2006, 13:159-167.
13. Huang J.S., Chao C.C., Su T.L., Yeh S.H., Chen D.S., Chen C.T., et al. Diverse cellular transformation capability of overexpressed genes in human hepatocellular carcinoma. Biochem Biophys Res Commun 2004, 315:950-958.
14. Hu T.H., Huang C.C., Liu L.F., Lin P.R., Liu S.Y., Chang H.W., et al. Expression of hepatoma-derived growth factor in hepatocellular carcinoma - a novel prognostic factor. Cancer 2003, 98:1444-1456.
15. Hu T.H., Huang C.C., Liu L.F., Lin P.R., Liu S.Y., Chang H.W., et al. Expression of hepatoma-derived growth factor in hepatocellular carcinoma. Cancer 2003, 98:1444-1456.
16. Yamamoto T., Nakamura H., Liu W., Cao K., Yoshikawa S., Enomoto H., et al. Involvement of hepatoma-derived growth factor in the growth inhibition of hepatocellular carcinoma cells by vitamin K-2. J Gastroenterol 2009, 44:228-235.
17. Yoshida K., Nakamura H., Okuda Y., Enomoto H., Kishima Y., Uyama H., et al. Expression of hepatoma-derived growth factor in hepatocarcinogenesis. J Gastroenterol Hepatol 2003, 18:1293-1301.
18. Nakamura H., Izumoto Y., Kambe H., Kuroda T., Mori T., Kawamura K., et al. Molecular-cloning of complementary-DNA for a novel human hepatoma-derived growth-factor - its homology with high-mobility group-1 protein. J Biol Chem 1994, 269:25143-25149.
19. Kishima Y., Yoshida K., Enomoto H., Yamamoto M., Kuroda T., Okuda Y., et al. Antisense oligonucleotides of hepatoma-derived growth factor (HDGF) suppress the proliferation of hepatoma cells. Hepatogastroenterology 2002, 49:1639-1644.
20. Kishima Y., Yamamoto H., Izumoto Y., Yoshida K., Enomoto H., Yamamoto M., et al. Hepatoma-derived growth factor stimulates cell growth after translocation to the nucleus by nuclear localization signals. J Biol Chem 2002, 277:10315-10322.
21. Yamamoto S., Tomita Y., Hoshida Y., Takiguchi S., Fujiwara Y., Yasuda T., et al. Expression of hepatoma-derived growth factor is correlated watch lymph node metastasis and prognosis of gastric carcinoma. Clin Cancer Res 2006, 12:117-122.
22. Chang K.C., Tai M.H., Lin J.W., Wang C.C., Huang C.C., Hung C.H., et al. Hepatoma-derived growth factor is a novel prognostic factor for gastrointestinal stromal tumors. Int J Cancer 2007, 121:1059-1065.
23. Mao J.S., Xu Z.F., Fang Y.M., Wang H.J., Xu J.H., Ye J.J., et al. Hepatoma-derived growth factor involved in the carcinogenesis of gastric epithelial cells through promotion of cell proliferation by Erk1/2 activation. Cancer Sci 2008, 99:2120-2127.
24. Lepourcelet M., Tou L., Cai L., Sawada J., Lazar A.J., Glickman J.N., et al. 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 2005, 132:415-427.
25. Yamamoto S., Tomita Y., Hoshida Y., Takiguchi S., Fujiwara Y., Yasuda T., et al. Expression of hepatoma-derived growth factor is correlated with lymph node metastasis and prognosis of gastric carcinoma. Clin Cancer Res 2006, 12:117-122.
26. Ren H., Tang X., Lee J.J., Feng L., Everett A.D., Hong W.K., et al. Expression of hepatoma-derived growth factor is a strong prognostic predictor for patients with early-stage non-small-cell lung cancer. J Clin Oncol 2004, 22:3230-3237.
27. Zhang J., Ren H.N., Yuan P., Lang W.H., Zhang L., Mao L. Down-regulation of hepatoma-derived growth factor inhibits anchorage-independent growth and invasion of non-small cell lung cancer cells. Cancer Res 2006, 66:18-23.
28. Uyama H., Tomita Y., Nakamura H., Nakamori S., Zhang B.L., Hoshida Y., et al. Hepatoma-derived growth factor is a novel prognostic factor for patients with pancreatic cancer. Clin Cancer Res 2006, 12:6043-6048.
29. Uyama H., Nakamura H. Hepatoma-derived growth factor is a novel prognostic factor for patients with pancreatic cancer. Gastroenterology 2008, 134:A695-A.
30. Yamamoto S., Tomita Y., Hoshida Y., Morii E., Yasuda T., Doki Y., et al. Expression level of hepatoma-derived growth factor correlates with tumor recurrence of esophageal carcinoma. Ann Surg Oncol 2007, 14:2141-2149.
31. Dietz F., Franken S., Yoshida K., Nakamura H., Kappler J., Gieselmann V. The family of hepatoma-derived growth factor proteins: characterization of a new member HRP-4 and classification of its subfamilies. Biochem J 2002, 366:491-500.
32. Sue S.C., Lee W.T., Tien S.C., Lee S.C., Yu J.G., Wu W.J., et al. PWWP module of human hepatoma-derived growth factor forms a domain-swapped dimer with much higher affinity for heparin. J Mol Biol 2007, 367:456-472.
33. Sue S.C., Chen J.Y., Lee S.C., Wu W.G., Huang T.H. Solution structure and heparin interaction of human hepatoma-derived growth factor. J Mol Biol 2004, 343:1365-1377.
34. Nameki N., Tochio N., Koshiba S., Inoue M., Yabuki T., Aoki M., et al. Solution structure of the PWWP domain of the hepatoma-derived growth factor family. Protein Sci 2005, 14:756-764.
35. Stec I., Nagl S.B., van Ommen G.J.B., den Dunnen J.T. The PWWP domain: a potential protein-protein interaction domain in nuclear proteins influencing differentiation?. FEBS Lett 2000, 473:1-5.
36. Lukasik S.M., Cierpicki T., Borloz M., Grembecka J., Everett A., Bushweller J.H. High resolution structure of the HDGF PWWP domain: a potential DNA binding domain. Protein Sci 2006, 15:314-323.
37. Yang J., Everett A.D. Hepatoma-derived Growth Factor Represses SET and MYND Domain Containing 1 Gene Expression through Interaction with C-terminal Binding Protein. J Mol Biol 2009, 386:938-950.
38. Yang J., Everett A.D. Hepatoma-derived growth factor binds DNA through the N-terminal PWWP domain. BMC Mol Biol 2007, 8:101.
39. Morgenstern J.P., Land H. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res 1990, 18:3587-3596.
40. Hellman L.M., Fried M.G. Electrophoretic mobility shift assay (EMSA) for detecting protein-nucleic acid interactions. Nat Protoc 2007, 2:1849-1861.
41. Shevchenko A., Tomas H., Havlis J., Olsen J.V., Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 2006, 1:2856-2860.
42. Kocher T., Superti-Furga G. Mass spectrometry-based functional proteomics: from molecular machines to protein networks. Nat Methods 2007, 4:807-815.
43. Rigaut G., Shevchenko A., Rutz B., Wilm M., Mann M., Seraphin B. A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 1999, 17:1030-1032.
44. Puig O., Caspary F., Rigaut G., Rutz B., Bouveret E., Bragado-Nilsson E., et al. The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 2001, 24:218-229.
45. Xu X.L., Song Y., Li Y.H., Chang J.F., Zhang H., An L.Z. The tandem affinity purification method: an efficient system for protein complex purification and protein interaction identification. Protein Expr Purif 2010, 72:149-156.
46. Gloeckner C.J., Boldt K., Schumacher A., Roepman R., Ueffing M. A novel tandem affinity purification strategy for the efficient isolation and characterisation of native protein complexes. Proteomics 2007, 7:4228-4234.
47. Terpe K. Overview of tag protein fusions: from molecular and biochemical fundamentals to commercial systems. Appl Microbiol Biotechnol 2003, 60:523-533.
48. Belotserkovskaya R., Reinberg D. Facts about FACT and transcript elongation through chromatin. Curr Opin Genet Dev 2004, 14:139-146.
49. Mongelard F., Bouvet P. Nucleolin: a multiFACeTed protein. Trends Cell Biol 2007, 17:80-86.
50. Wegierski T., Billy E., Nasr F., Filipowicz W. Bms1p, a G-domain-containing protein, associates with Rcl1p and is required for 18S rRNA biogenesis in yeast. Rna Pub Rna Soc 2001, 7:1254-1267.
51. Yang H., Zhou J., Ochs R.L., Henning D., Jin R., Valdez B.C. Down-regulation of RNA helicase II/Gu results in the depletion of 18 and 28 S rRNAs in Xenopus oocyte. J Biol Chem 2003, 278:38847-38859.
52. Romanova L., Grand A., Zhang L.Y., Rayner S., Katoku-Kikyo N., Kellner S., et al. Critical role of nucleostemin in Pre-rRNA processing. J Biol Chem 2009, 284:4968-4977.
53. Cartegni L., Chew S.L., Krainer A.R. Listening to silence and understanding nonsense: exonic mutations that affect splicing. Nat Rev Genet 2002, 3:285-298.
54. Zhang Z., Krainer A.R. Involvement of SR proteins in mRNA surveillance. Mol Cell 2004, 16:597-607.
55. Huang Y.Q., Gattoni R., Stevenin J., Steitz J.A. SR splicing factors serve as adapter proteins for TAP-dependent mRNA export. Mol Cell 2003, 11:837-843.
56. Sanford J.R., Gray N.K., Beckmann K., Caceres J.F. A novel role for shuttling SR proteins in mRNA translation. Genes Dev 2004, 18:755-768.
57. Karni R., de Stanchina E., Lowe S.W., Sinha R., Mu D., Krainer A.R. The gene encoding the splicing factor SF2/ASF is a proto-oncogene. Nat Struct Mol Biol 2007, 14:185-193.
58. Krecic A.M., Swanson M.S. hnRNP complexes: composition, structure, and function. Curr Opin Cell Biol 1999, 11:363-371.
59. House A.E., Lynch K.W. Regulation of alternative splicing: more than just the ABCs. J Biol Chem 2008, 283:1217-1221.
60. Smith G.C.M., Jackson S.P. The DNA-dependent protein kinase. Genes Dev 1999, 13:916-934.
61. Burkle A. Physiology and pathophysiology of poly(ADP-ribosyl)ation. Bioessays 2001, 23:795-806.
62. Kim M.Y., Zhang T., Kraus W.L. Poly(ADP-ribosyl)ation by PARP-1: 'PAR-laying' NAD+ into a nuclear signal. Genes Dev 2005, 19:1951-1967.
63. Burkle A. PARP-1: a regulator of genomic stability linked with mammalian longevity. Chembiochem 2001, 2:725-728.
64. Ng H.H., Bird A. Histone deacetylases: silencers for hire. Trends Biochem Sci 2000, 25:121-126.
65. Cress W.D., Seto E. Histone deacetylases, transcriptional control, and cancer. J Cell Physiol 2000, 184:1-16.
66. Belotserkovskaya R., Oh S., Bondarenko V.A., Orphanides G., Studitsky V.M., Reinberg D. FACT facilitates transcription-dependent nucleosome alteration. Science 2003, 301:1090-1093.
67. Orphanides G., Wu W.H., Lane W.S., Hampsey M., Reinberg D. The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 1999, 400:284-288.
68. Angelov D., Bondarenko V.A., Almagro S., Menoni H., Mongelard F., Hans F., et al. Nucleolin is a histone chaperone with FACT-like activity and assists remodeling of nucleosomes. EMBO J 2006, 25:1669-1679.
69. Edwards T.K., Saleem A., Shaman J.A., Dennis T., Gerigk C., Oliveros E., et al. Role for nucleolin/Nsr1 in the cellular localization of topoisomerase I. J Biol Chem 2000, 275:36181-36188.
70. Buszczak M., Spradling A.C. The Drosophila P68 RNA helicase regulates transcriptional deactivation by promoting RNA release from chromatin. Genes Dev 2006, 20:977-989.
71. Tavner F.J., Simpson R., Tashiro S., Favier D., Jenkins N.A., Gilbert D.J., et al. Molecular cloning reveals that the p160 Myb-binding protein is a novel, predominantly nucleolar protein which may play a role in transactivation by Myb. Mol Cell Biol 1998, 18:989-1002.
72. Jones L.C., Okino S.T., Gonda T.J., Whitlock J.P. Myb-binding protein 1a augments AhR-dependent gene expression. J Biol Chem 2002, 277:22515-22519.
73. Fan M., Rhee J., St-Pierre J., Handschin C., Puigserver P., Lin J.D., et al. Suppression of mitochondrial respiration through recruitment of p160 myb binding protein to PGC-1 alpha: modulation by p38 MAPK. Genes Dev 2004, 18:278-289.
74. Diaz V.M., Mori S., Longobardi E., Menendez G., Ferrai C., Keough R.A., et al. p160 Myb-binding protein interacts with Prep1 and inhibits its transcriptional activity. Mol Cell Biol 2007, 27:7981-7990.
75. Hara Y., Onishi Y., Oishi K., Miyazaki K., Fukamizu A., Ishida N. Molecular characterization of Mybbp1a as a co-repressor on the Period2 promoter. Nucleic Acids Res 2009, 37:1115-1126.
76. Owen H.R., Elser M., Cheung E., Gersbach M., Kraus W.L., Hottiger M.O. MYBBP1a is a novel repressor of NF-kappa B. J Mol Biol 2007, 366:725-736.
77. Wilson B.J., Bates G.J., Nicol S.M., Gregory D.J., Perkins N.D., Fuller-Pace F.V. The p68 and p72 DEAD box RNA helicases interact with HDACI and repress transcription in a promoter-specific manner. BMC Mol Biol 2004, 5.
78. Wortham N.C., Ahamed E., Nicol S.M., Thomas R.S., Periyasamy M., Jiang J., et al. The DEAD-box protein p72 regulates ER alpha-/oestrogen-dependent transcription and cell growth, and is associated with improved survival in ER alpha-positive breast cancer. Oncogene 2009, 28:4053-4064.
79. Endoh H., Maruyama K., Masuhiro Y., Kobayashi Y., Goto M., Tai H., et al. Purification and identification of p68 RNA helicase acting as a transcriptional coactivator specific for the activation function 1 of human estrogen receptor alpha. Mol Cell Biol 1999, 19:5363-5372.
80. Watanabe M., Yanagisawa J., Kitagawa H., Takeyama K., Ogawa S., Arao Y., et al. A subfamily of RNA-binding DEAD-box proteins acts as an estrogen receptor alpha coactivator through the N-terminal activation domain (AF-1) with an RNA coactivator, SRA. EMBO J 2001, 20:1341-1352.
81. Bates G.J., Nicol S.M., Wilson B.J., Jacobs A.M.F., Bourdon J.C., Wardrop J., et al. The DEAD box protein p68: a novel transcriptional coactivator of the p53 tumour suppressor. EMBO J 2005, 24:543-553.
82. Caretti G., Schiltz R.L., Dilworth F.J., Di Padova M., Zhao P., Ogryzko V., et al. The RNA helicases p68/p72 and the noncoding RNA SRA are coregulators of MyoD and skeletal muscle differentiation. Dev Cell 2006, 11:547-560.
83. Caretti G., Lei E.P., Sartorelli V. The DEAD-box p68/p72 proteins and the noncoding RNA steroid receptor activator SRA - Eclectic regulators of disparate biological functions. Cell Cycle 2007, 6:1172-1176.
84. Jensen E.D., Niu L., Caretti G., Nicol S.M., Teplyuk N., Stein G.S., et al. p68 (Ddx5) interacts with Runx2 and regulates osteoblast differentiation. J Cell Biochem 2008, 103:1438-1451.
85. Jacobs A.M.F., Nicol S.M., Hislop R.G., Jaffray E.G., Hay R.T., Fuller-Pace F.V. SUMO modifcation of the DEAD box protein p68modulates its transcriptional activity and promotes its interaction with HDAC1. Oncogene 2007, 26:5866-5876.
86. Westermarck J., Weiss C., Saffrich R., Kast J., Musti A.M., Wessely M., et al. The DEXD/H-box RNA helicase RHII/Gu is a co-factor for c-Jun-activated transcription. EMBO J 2002, 21:451-460.
87. Sijin L., Ziwei C., Yajun L., Meiyu D., Hongwei Z., Guofa H., et al. The effect of knocking-down nucleostemin gene expression on the in vitro proliferation and in vivo tumorigenesis of HeLa cells. J Exp Clin Cancer Res 2004, 23:529-538.
88. Ma H., Pederson T. Nucleostemin: a multiplex regulator of cell-cycle progression. Trends Cell Biol 2008, 18:575-579.
89. Henning D., So R.B., Jin R., Lau L.F., Valdez B.C. Silencing of RNA helicase II/Gualpha inhibits mammalian ribosomal RNA production. J Biol Chem 2003, 278:52307-52314.
90. Elser M., Borsig L., Hassa P.O., Erener S., Messner S., Valovka T., et al. Poly(ADP-ribose) polymerase 1 promotes tumor cell survival by coactivating hypoxia-inducible factor-1-dependent gene expression. Mol Cancer Res 2008, 6:282-290.
91. Hudson M.E., Pozdnyakova I., Haines K., Mor G., Snyder M. Identification of differentially expressed proteins in ovarian cancer using high-density protein microarrays. Proc Natl Acad Sci USA 2007, 104:17494-17499.
92. Hertel L., Foresta P., Barbiero G., Ying G.G., Bonelli G., Baccino F.M., et al. Decreased expression of the high-mobility group protein T160 by antisense RNA impairs the growth of mouse fibroblasts. Biochimie 1997, 79:717-723.
93. Tsang T.Y., Tang W.Y., Tsang W.P., Co N.N., Kong S.K., Kwok T.T. Downregulation of hepatoma-derived growth factor activates the Bad-mediated apoptotic pathway in human cancer cells. Apoptosis 2008, 13:1135-1147.
94. Tsang T.Y., Tanga W.Y., Tsang W.P., Co N.N., Kong S.K., Kwok T.T. Mechanistic study on growth suppression and apoptosis induction by targeting hepatoma-derived growth factor in human hepatocellular carcinoma HepG2 cells. Cell Physiol Biochem 2009, 24:253-262.
95. Liao F., Dong W., Fan L. Apoptosis of human colorectal carcinoma cells is induced by blocking hepatoma-derived growth factor. Med Oncol 2009, 27:1219-1226.
96. Zhang J., Tsaprailis G., Bowden G.T. Nucleolin stabilizes Bcl-X-L messenger RNA in response to UVA irradiation. Cancer Res 2008, 68:1046-1054.
97. Fogal V., Sugahara K.N., Ruoslahti E., Christian S. Cell surface nucleolin antagonist causes endothelial cell apoptosis and normalization of tumor vasculature. Angiogenesis 2009, 12:91-100.