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Solution structure and heparin interaction of human hepatoma-derived growth factor.

Sue SC, Chen JY, Lee SC, Wu WG, Huang TH
J Mol Biol 343 1365-77 (2004)
Cited: 32 times
EuropePMC logo PMID: 15491618

Abstract

Hepatoma-derived growth factor (HDGF)-related proteins (HRPs) comprise a new protein family that has been implicated in nephrogenesis, tumorigenesis, vascular development, cell proliferation, and transcriptional activation. All HRPs share a conserved N-terminal homologous to the amino terminus of HDGF (HATH) domain, but vary significantly in the C-terminal region. Here, we show that in solution the N and C termini of human HDGF form two structurally independent domains. The 100 amino acid residue N-terminal HATH domain is well-structured while the 140 amino acid residue C-terminal domain is disordered. We determined the solution structure of the HATH domain by NMR. The core structure of the HATH domain is a five-stranded beta-barrel followed by two alpha-helices, similar to those of PWWP domains of known structures. Surface plasmon resonance results showed that the HATH domain is primarily responsible for heparin binding. On the basis of the chemical shift perturbation induced by binding of heparin-derived hexasaccharide, we identified a prominent, highly positively charged region as the putative heparin-binding site. Sequence comparison and structure prediction suggest that all HRPs are likely to adapt a similar modular structure.

Reviews - 1ri0 mentioned but not cited (1)

  1. PWWP domains and their modes of sensing DNA and histone methylated lysines. Rona GB, Eleutherio ECA, Pinheiro AS. Biophys Rev 8 63-74 (2016)

Articles - 1ri0 mentioned but not cited (1)

  1. Domain swapping and SMYD1 interactions with the PWWP domain of human hepatoma-derived growth factor. Chen LY, Huang YC, Huang ST, Hsieh YC, Guan HH, Chen NC, Chuankhayan P, Yoshimura M, Tai MH, Chen CJ. Sci Rep 8 287 (2018)


Reviews citing this publication (4)

  1. Structure and function of the nucleosome-binding PWWP domain. Qin S, Min J. Trends Biochem Sci 39 536-547 (2014)
  2. Survey of the year 2004 commercial optical biosensor literature. Rich RL, Myszka DG. J Mol Recognit 18 431-478 (2005)
  3. HDGF: a novel jack-of-all-trades in cancer. Bao C, Wang J, Ma W, Wang X, Cheng Y. Future Oncol 10 2675-2685 (2014)
  4. Catching Nucleosome by Its Decorated Tails Determines Its Functional States. Sehrawat P, Shobhawat R, Kumar A. Front Genet 13 903923 (2022)

Articles citing this publication (26)

  1. Menin critically links MLL proteins with LEDGF on cancer-associated target genes. Yokoyama A, Cleary ML. Cancer Cell 14 36-46 (2008)
  2. Solution structure of the HIV-1 integrase-binding domain in LEDGF/p75. Cherepanov P, Sun ZY, Rahman S, Maertens G, Wagner G, Engelman A. Nat Struct Mol Biol 12 526-532 (2005)
  3. Modular organization of SARS coronavirus nucleocapsid protein. Chang CK, Sue SC, Yu TH, Hsieh CM, Tsai CK, Chiang YC, Lee SJ, Hsiao HH, Wu WJ, Chang WL, Lin CH, Huang TH. J Biomed Sci 13 59-72 (2006)
  4. Identification and characterization of the chromatin-binding domains of the HIV-1 integrase interactor LEDGF/p75. Llano M, Vanegas M, Hutchins N, Thompson D, Delgado S, Poeschla EM. J Mol Biol 360 760-773 (2006)
  5. Regulation of Set9-mediated H4K20 methylation by a PWWP domain protein. Wang Y, Reddy B, Thompson J, Wang H, Noma K, Yates JR, Jia S. Mol Cell 33 428-437 (2009)
  6. Structure shows that a glycosaminoglycan and protein recognition site in factor H is perturbed by age-related macular degeneration-linked single nucleotide polymorphism. Herbert AP, Deakin JA, Schmidt CQ, Blaum BS, Egan C, Ferreira VP, Pangburn MK, Lyon M, Uhrín D, Barlow PN. J Biol Chem 282 18960-18968 (2007)
  7. High resolution structure of the HDGF PWWP domain: a potential DNA binding domain. Lukasik SM, Cierpicki T, Borloz M, Grembecka J, Everett A, Bushweller JH. Protein Sci 15 314-323 (2006)
  8. The dimer interface of the SARS coronavirus nucleocapsid protein adapts a porcine respiratory and reproductive syndrome virus-like structure. Chang CK, Sue SC, Yu TH, Hsieh CM, Tsai CK, Chiang YC, Lee SJ, Hsiao HH, Wu WJ, Chang CF, Huang TH. FEBS Lett 579 5663-5668 (2005)
  9. Downregulation of hepatoma-derived growth factor activates the Bad-mediated apoptotic pathway in human cancer cells. Tsang TY, Tang WY, Tsang WP, Co NN, Kong SK, Kwok TT. Apoptosis 13 1135-1147 (2008)
  10. PWWP module of human hepatoma-derived growth factor forms a domain-swapped dimer with much higher affinity for heparin. Sue SC, Lee WT, Tien SC, Lee SC, Yu JG, Wu WJ, Wu WG, Huang TH. J Mol Biol 367 456-472 (2007)
  11. Solution structure of the Arabidopsis thaliana telomeric repeat-binding protein DNA binding domain: a new fold with an additional C-terminal helix. Sue SC, Hsiao HH, Chung BC, Cheng YH, Hsueh KL, Chen CM, Ho CH, Huang TH. J Mol Biol 356 72-85 (2006)
  12. Expression of hepatoma-derived growth factor family members in the adult central nervous system. El-Tahir HM, Dietz F, Dringen R, Schwabe K, Strenge K, Kelm S, Abouzied MM, Gieselmann V, Franken S. BMC Neurosci 7 6 (2006)
  13. Interactome study suggests multiple cellular functions of hepatoma-derived growth factor (HDGF). Zhao J, Yu H, Lin L, Tu J, Cai L, Chen Y, Zhong F, Lin C, He F, Yang P. J Proteomics 75 588-602 (2011)
  14. Hepatoma-derived growth factor-related protein-3 interacts with microtubules and promotes neurite outgrowth in mouse cortical neurons. El-Tahir HM, Abouzied MM, Gallitzendoerfer R, Gieselmann V, Franken S. J Biol Chem 284 11637-11651 (2009)
  15. TOX4 and NOVA1 proteins are partners of the LEDGF PWWP domain and affect HIV-1 replication. Morchikh M, Naughtin M, Di Nunzio F, Xavier J, Charneau P, Jacob Y, Lavigne M. PLoS One 8 e81217 (2013)
  16. SUMOylation of the hepatoma-derived growth factor negatively influences its binding to chromatin. Thakar K, Niedenthal R, Okaz E, Franken S, Jakobs A, Gupta S, Kelm S, Dietz F. FEBS J 275 1411-1426 (2008)
  17. Secretion of hepatoma-derived growth factor is regulated by N-terminal processing. Thakar K, Kröcher T, Savant S, Gollnast D, Kelm S, Dietz F. Biol Chem 391 1401-1410 (2010)
  18. The nature of the conserved basic amino acid sequences found among 437 heparin binding proteins determined by network analysis. Rudd TR, Preston MD, Yates EA. Mol Biosyst 13 852-865 (2017)
  19. Hepatoma-derived growth factor and nucleolin exist in the same ribonucleoprotein complex. Bremer S, Klein K, Sedlmaier A, Abouzied M, Gieselmann V, Franken S. BMC Biochem 14 2 (2013)
  20. Hepatoma-derived growth factor-related protein-3: a new neurotrophic and neurite outgrowth-promoting factor for cortical neurons. Abouzied MM, El-Tahir HM, Gieselmann V, Franken S. J Neurosci Res 88 3610-3620 (2010)
  21. Interaction of HRP-2 isoforms with HDGF: chromatin binding of a specific heteromer. Thakar K, Votteler I, Kelkar D, Shidore T, Gupta S, Kelm S, Dietz F. FEBS J 279 737-751 (2012)
  22. Significance of heparin binding to basic residues in homologous to the amino terminus of hepatoma-derived growth factor and related proteins. Chen FF, Lin WH, Lin SC, Kuo JH, Chu HY, Huang WC, Chuang YJ, Lee SC, Sue SC. Glycobiology 22 649-661 (2012)
  23. NMR characterization of the electrostatic interaction of the basic residues in HDGF and FGF2 during heparin binding. Chiu LY, Hung KW, Tjong SC, Chiang YW, Sue SC. Biochim Biophys Acta 1844 1851-1859 (2014)
  24. The HRP3 PWWP domain recognizes the minor groove of double-stranded DNA and recruits HRP3 to chromatin. Tian W, Yan P, Xu N, Chakravorty A, Liefke R, Xi Q, Wang Z. Nucleic Acids Res 47 5436-5448 (2019)
  25. Conservation of the glycoprotein B homologs of the Kaposi׳s sarcoma-associated herpesvirus (KSHV/HHV8) and old world primate rhadinoviruses of chimpanzees and macaques. Bruce AG, Horst JA, Rose TM. Virology 494 29-46 (2016)
  26. Proteomics-based screening of the endothelial heparan sulfate interactome reveals that C-type lectin 14a (CLEC14A) is a heparin-binding protein. Sandoval DR, Gomez Toledo A, Painter CD, Tota EM, Sheikh MO, West AMV, Frank MM, Wells L, Xu D, Bicknell R, Corbett KD, Esko JD. J Biol Chem 295 2804-2821 (2020)


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