Structural basis and targeting of the interaction between fibroblast growth factor-inducible 14 and tumor necrosis factor-like weak inducer of apoptosis

Journal of Biological Chemistry

Volumn 288, Issue 45, 2013, Pages 32261-32276

  Dhruv, Harshil ^a   Loftus, Joseph C ^b   Narang, Pooja ^b   Petit, Joachim L ^b   Fameree, Maureen ^a   Burton, Julien ^a   Tchegho, Giresse ^a   Chow, Donald ^a   Yin, Holly ^a   Al Abed, Yousef ^c   Berens, Michael E ^a   Tran, Nhan L ^a   Meurice, Nathalie ^b  

^a TRANSLATIONAL GENOMICS RESEARCH INSTITUTE   (United States)

^b MAYO CLINIC   (United States)

^c FEINSTEIN INSTITUTE FOR MEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE-RICH DOMAINS; EXPERIMENTAL VALIDATIONS; LIGAND-RECEPTOR INTERACTIONS; SITE DIRECTED MUTAGENESIS; SMALL MOLECULE INHIBITOR; STRUCTURAL ELEMENTS; THERAPEUTIC INTERVENTION; THERAPEUTIC TARGETS;

AMINO ACIDS; CELL DEATH; DIGITAL LIBRARIES; DISEASES; MOLECULES;

CELL SIGNALING;

FIBROBLAST GROWTH FACTOR 14; FIBROBLAST GROWTH FACTOR INDUCIBLE 14; I KAPPA B; LUCIFERASE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR LIKE WEAK INDUCER OF APOPTOSIS; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CELL INVASION; CELL MIGRATION; CELL SURVIVAL; CONTROLLED STUDY; HUMAN; HUMAN CELL; MOLECULAR DOCKING; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; PROTEIN TARGETING; SIGNAL TRANSDUCTION; STRUCTURAL HOMOLOGY; STRUCTURE ANALYSIS;

CANCER; CELL SIGNALING; CELL SURFACE RECEPTOR; DOCKING; DRUG DEVELOPMENT; DRUG DISCOVERY; DRUG SCREENING; PROTEIN-PROTEIN INTERACTIONS;

AMINO ACID SUBSTITUTION; CELL LINE, TUMOR; HEK293 CELLS; HUMANS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; MUTATION, MISSENSE; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASMS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTORS;

EID: 84887496644     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.493536     Document Type: Article

References (50)

1. Wiley, S. R., and Winkles, J. A. (2003) TWEAK, a member of the TNF superfamily, is a multifunctional cytokine that binds the TweakR/Fn14 receptor. Cytokine Growth Factor Rev. 14, 241-249
2. Chicheportiche, Y., Bourdon, P. R., Xu, H., Hsu, Y. M., Scott, H., Hession, C., Garcia, I., and Browning, J. L. (1997) TWEAK, a new secreted ligand in the tumor necrosis factor family that weakly induces apoptosis. J. Biol. Chem. 272, 32401-32410
3. Feng, S. L., Guo, Y., Factor, V. M., Thorgeirsson, S. S., Bell, D. W., Testa, J. R., Peifley, K. A., and Winkles, J. A. (2000) The Fn14 immediate-early response gene is induced during liver regeneration and highly expressed in both human and murine hepatocellular carcinomas. Am. J. Pathol. 156, 1253-1261
4. Kölzsch, J. (1990) Clinical aspects and therapy of frequent viral diseases of the skin. Z. Arztl. Fortbild. 84, 1199-1202
5. Kolfschoten, G. M., Pradet-Balade, B., Hahne, M., and Medema, J. P. (2003) TWE-PRIL; a fusion protein of TWEAK and APRIL. Biochem. Pharmacol. 66, 1427-1432
6. Brown, S. A., Ghosh, A., and Winkles, J. A. (2010) Full-length, membraneanchored TWEAK can function as a juxtacrine signaling molecule and activate the NF-κB pathway. J. Biol. Chem. 285, 17432-17441
7. Meighan-Mantha, R. L., Hsu, D. K., Guo, Y., Brown, S. A., Feng, S. L., Peifley, K. A., Alberts, G. F., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Richards, C. M., and Winkles, J. A. (1999) The mitogen-inducible Fn14 gene encodes a type I transmembrane protein that modulates fibroblast adhesion and migration. J. Biol. Chem. 274, 33166-33176
8. Harada, N., Nakayama, M., Nakano, H., Fukuchi, Y., Yagita, H., and Okumura, K. (2002) Pro-inflammatory effect of TWEAK/Fn14 interaction on human umbilical vein endothelial cells. Biochem. Biophys. Res. Commun. 299, 488-493
9. Polek, T. C., Talpaz, M., Darnay, B. G., and Spivak-Kroizman, T. (2003) TWEAK mediates signal transduction and differentiation of RAW264.7 cells in the absence of Fn14/TweakR. Evidence for a second TWEAK receptor. J. Biol. Chem. 278, 32317-32323
10. Brown, S. A., Hanscom, H. N., Vu, H., Brew, S. A., and Winkles, J. A. (2006) TWEAK binding to the Fn14 cysteine-rich domain depends on charged residues located in both the A1 and D2 modules. Biochem. J. 397, 297-304
11. Burkly, L. C., Michaelson, J. S., and Zheng, T. S. (2011) TWEAK/Fn14 pathway: an immunological switch for shaping tissue responses. Immunol. Rev. 244, 99-114
12. Han, H., Bearss, D. J., Browne, L. W., Calaluce, R., Nagle, R. B., and Von Hoff, D. D. (2002) Identification of differentially expressed genes in pancreatic cancer cells using cDNA microarray. Cancer Res. 62, 2890-2896
13. Tran, N. L., McDonough, W. S., Donohue, P. J., Winkles, J. A., Berens, T. J., Ross, K. R., Hoelzinger, D. B., Beaudry, C., Coons, S. W., and Berens, M. E. (2003) The human Fn14 receptor gene is up-regulated in migrating glioma cells in vitro and overexpressed in advanced glial tumors. Am. J. Pathol. 162, 1313-1321
14. Watts, G. S., Tran, N. L., Berens, M. E., Bhattacharyya, A. K., Nelson, M. A., Montgomery, E. A., and Sampliner, R. E. (2007) Identification of Fn14/TWEAK receptor as a potential therapeutic target in esophageal adenocarcinoma. Int. J. Cancer 121, 2132-2139
15. Willis, A. L., Tran, N. L., Chatigny, J. M., Charlton, N., Vu, H., Brown, S. A., Black, M. A., McDonough, W. S., Fortin, S. P., Niska, J. R., Winkles, J. A., and Cunliffe, H. E. (2008) The fibroblast growth factor-inducible 14 receptor is highly expressed in HER2-positive breast tumors and regulates breast cancer cell invasive capacity. Mol. Cancer Res. 6, 725-734
16. Whitsett, T. G., Cheng, E., Inge, L., Asrani, K., Jameson, N. M., Hostetter, G., Weiss, G. J., Kingsley, C. B., Loftus, J. C., Bremner, R., Tran, N. L., and Winkles, J. A. (2012) Elevated expression of Fn14 in non-small cell lung cancer correlates with activated EGFR and promotes tumor cell migration and invasion. Am. J. Pathol. 181, 111-120
17. Tran, N. L., McDonough, W. S., Savitch, B. A., Fortin, S. P., Winkles, J. A., Symons, M., Nakada, M., Cunliffe, H. E., Hostetter, G., Hoelzinger, D. B., Rennert, J. L., Michaelson, J. S., Burkly, L. C., Lipinski, C. A., Loftus, J. C., Mariani, L., and Berens, M. E. (2006) Increased fibroblast growth factorinducible 14 expression levels promote glioma cell invasion via Rac1 and nuclear factor-κB and correlate with poor patient outcome. Cancer Res. 66, 9535-9542
18. Burkly, L. C., Michaelson, J. S., Hahm, K., Jakubowski, A., and Zheng, T. S. (2007) TWEAKing tissue remodeling by a multifunctional cytokine: role of TWEAK/Fn14 pathway in health and disease. Cytokine 40, 1-16
19. Winkles, J. A. (2008) The TWEAK-Fn14 cytokine-receptor axis: discovery, biology and therapeutic targeting. Nat. Rev. Drug Discov. 7, 411-425
20. Jain, M., Jakubowski, A., Cui, L., Shi, J., Su, L., Bauer, M., Guan, J., Lim, C. C., Naito, Y., Thompson, J. S., Sam, F., Ambrose, C., Parr, M., Crowell, T., Lincecum, J. M., Wang, M. Z., Hsu, Y. M., Zheng, T. S., Michaelson, J. S., Liao, R., and Burkly, L. C. (2009) A novel role for tumor necrosis factor-like weak inducer of apoptosis (TWEAK) in the development of cardiac dysfunction and failure. Circulation 119, 2058-2068
21. Yoriki, R., Akashi, S., Sho, M., Nomi, T., Yamato, I., Hotta, K., Takayama, T., Matsumoto, S., Wakatsuki, K., Migita, K., Yagita, H., and Nakajima, Y. (2011) Therapeutic potential of the TWEAK/Fn14 pathway in intractable gastrointestinal cancer. Exp. Ther. Med. 2, 103-108
22. Zheng, T. S., and Burkly, L. C. (2008) No end in site: TWEAK/Fn14 activation and autoimmunity associated-end-organ pathologies. J. Leukocyte Biol. 84, 338-347
23. Bhatnagar, S., and Kumar, A. (2012) The TWEAK-Fn14 system: breaking the silence of cytokine-induced skeletal muscle wasting. Curr. Mol. Med. 12, 3-13
24. Campbell, S., Burkly, L. C., Gao, H. X., Berman, J. W., Su, L., Browning, B., Zheng, T., Schiffer, L., Michaelson, J. S., and Putterman, C. (2006) Proinflammatory effects of TWEAK/Fn14 interactions in glomerular mesangial cells. J. Immunol. 176, 1889-1898
25. Bhattacharjee, M., Raju, R., Radhakrishnan, A., Nanjappa, V., Muthusamy, B., Singh, K., Kuppusamy, D., Lingala, B. T., Pan, A., Mathur, P. P., Harsha, H. C., Prasad, T. S., Atkins, G. J., Pandey, A., and Chatterjee, A. (2012) A bioinformatics resource for TWEAK-Fn14 signaling pathway. J. Signal Transduct. 2012:376470
26. Tansey, M. G., and Szymkowski, D. E. (2009) The TNF superfamily in 2009: new pathways, new indications, and new drugs. Drug Discov. Today 14, 1082-1088
27. He, M. M., Smith, A. S., Oslob, J. D., Flanagan, W. M., Braisted, A. C., Whitty, A., Cancilla, M. T., Wang, J., Lugovskoy, A. A., Yoburn, J. C., Fung, A. D., Farrington, G., Eldredge, J. K., Day, E. S., Cruz, L. A., Cachero, T. G., Miller, S. K., Friedman, J. E., Choong, I. C., and Cunningham, B. C. (2005) Small-molecule inhibition of TNF-α. Science 310, 1022-1025
28. Silvian, L. F., Friedman, J. E., Strauch, K., Cachero, T. G., Day, E. S., Qian, F., Cunningham, B., Fung, A., Sun, L., Shipps, G. W., Su, L., Zheng, Z., Kumaravel, G., and Whitty, A. (2011) Small molecule inhibition of the TNF family cytokine CD40 ligand through a subunit fracture mechanism. ACS Chem. Biol. 6, 636-647
29. Benicchi, T., Iozzi, S., Svahn, A., Axelsson, H., Mori, E., Bernocco, S., Cappelli, F., Caramelli, C., Fanti, P., Genesio, E., Maccari, L., Markova, N., Micco, I., Porcari, V., Schultz, J., and Fecke, W. (2012) A homogeneous HTRF assay for the identification of inhibitors of the TWEAK-Fn14 protein interaction. J. Biomol. Screen. 17, 933-945
30. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N., and Bourne, P. E. (2000) The Protein Data Bank. Nucleic Acids Res. 28, 235-242
31. Molecular Operating Environment (2010) Molecular Operating Environment, Version 2010.10, Chemical Computing Group Inc., Montreal, Quebec, Canada
32. Abagyan, R., Totrov, M., and Kuznetsov, D. (1994) ICM-A new method for protein modeling and design: Applications to docking and structure prediction from the distorted native conformation. J. Comput. Chem. 15, 488-506
33. Nemethy, G., Gibson, K. D., Palmer, K. A., Yoon, C. N., Paterlini, G., Zagari, A., Rumsey, S., and Scheraga, H. A. (1992) Energy parameters in polypeptides. 10. Improved geometrical parameters and nonbonded interactions for use in the ECEPP/3 algorithm, with application to prolinecontaining peptides. J. Phys. Chem. 96, 6472-6484
34. Watts, K. S., Dalal, P., Murphy, R. B., Sherman, W., Friesner, R. A., and Shelley, J. C. (2010) ConfGen: a conformational search method for efficient generation of bioactive conformers. J. Chem. Inf. Model. 50, 534-546
35. Dixon, S. L., Smondyrev, A. M., and Rao, S. N. (2006) PHASE: a novel approach to pharmacophore modeling and 3D database searching. Chem. Biol. Drug Des. 67, 370-372
36. Friesner, R. A., Banks, J. L., Murphy, R. B., Halgren, T. A., Klicic, J. J., Mainz, D. T., Repasky, M. P., Knoll, E. H., Shelley, M., Perry, J. K., Shaw, D. E., Francis, P., and Shenkin, P. S. (2004) Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J. Med. Chem. 47, 1739-1749
37. Ramachandran, N., Hainsworth, E., Bhullar, B., Eisenstein, S., Rosen, B., Lau, A. Y., Walter, J. C., and LaBaer, J. (2004) Self-assembling protein microarrays. Science 305, 86-90
38. Frostell-Karlsson, A., Remaeus, A., Roos, H., Andersson, K., Borg, P., Hämäläinen, M., and Karlsson, R. (2000) Biosensor analysis of the interaction between immobilized human serum albumin and drug compounds for prediction of human serum albumin binding levels. J. Med. Chem. 43, 1986-1992
39. Lamszus, K., Schmidt, N. O., Jin, L., Laterra, J., Zagzag, D., Way, D., Witte, M., Weinand, M., Goldberg, I. D., Westphal, M., and Rosen, E. M. (1998) Scatter factor promotes motility of human glioma and neuromicrovascular endothelial cells. Int. J. Cancer 75, 19-28
40. Brockmann, M. A., Ulbricht, U., Gruner, K., Fillbrandt, R., Westphal, M., and Lamszus, K. (2003) Glioblastoma and cerebral microvascular endothelial cell migration in response to tumor-associated growth factors. Neurosurgery 52, 1391-1399
41. He, F., Dang, W., Saito, K., Watanabe, S., Kobayashi, N., Güntert, P., Kigawa, T., Tanaka, A., Muto, Y., and Yokoyama, S. (2009) Solution structure of the cysteine-rich domain in Fn14, a member of the tumor necrosis factor receptor superfamily. Protein Sci. 18, 650-656
42. Banner, D. W., D'Arcy, A., Janes, W., Gentz, R., Schoenfeld, H. J., Broger, C., Loetscher, H., and Lesslauer, W. (1993) Crystal structure of the soluble human 55 kDTNFreceptor-humanTNFβ complex: implications forTNF receptor activation. Cell 73, 431-445
43. Chothia, C., and Lesk, A. M. (1986) The relation between the divergence of sequence and structure in proteins. EMBO J. 5, 823-826
44. Hymowitz, S. G., Patel, D. R., Wallweber, H. J., Runyon, S., Yan, M., Yin, J., Shriver, S. K., Gordon, N. C., Pan, B., Skelton, N. J., Kelley, R. F., and Starovasnik, M. A. (2005) Structures of APRIL-receptor complexes: like BCMA, TACI employs only a single cysteine-rich domain for high affinity ligand binding. J. Biol. Chem. 280, 7218-7227
45. Bogan, A. A., and Thorn, K. S. (1998) Anatomy of hot spots in protein interfaces. J. Mol. Biol. 280, 1-9
46. Meireles, L. M., Dömling, A. S., and Camacho, C. J. (2010) ANCHOR: a web server and database for analysis of protein-protein interaction binding pockets for drug discovery. Nucleic Acids Res. 38, W407-W411
47. Schneider, P., Schwenzer, R., Haas, E., Mühlenbeck, F., Schubert, G., Scheurich, P., Tschopp, J., and Wajant, H. (1999) TWEAK can induce cell death via endogenous TNF and TNF receptor 1. Eur. J. Immunol. 29, 1785-1792
48. Tran, N. L., McDonough, W. S., Savitch, B. A., Sawyer, T. F., Winkles, J. A., and Berens, M. E. (2005) The tumor necrosis factor-like weak inducer of apoptosis (TWEAK)-fibroblast growth factor-inducible 14 (Fn14) signaling system regulates glioma cell survival via NFκB pathway activation and BCL-XL/BCL-W expression. J. Biol. Chem. 280, 3483-3492
49. Pellegrini, M., Willen, L., Perroud, M., Krushinskie, D., Strauch, K., Cuervo, H., Day, E. S., Schneider, P., and Zheng, T. S. (2013) Structure of the extracellular domains of human and Xenopus Fn14: implications in the evolution of TWEAK and Fn14 interactions. FEBS J. 280, 1818-1829
50. Lammens, A., Baehner, M., Kohnert, U., Niewoehner, J., von Proff, L., Schraeml, M., Lammens, K., and Hopfner, K. P. (2013) Crystal structure of human TWEAK in complex with the Fab fragment of a neutralizing antibody reveals insights into receptor binding. PLoS One 8, e62697