1du3 › Citations

Crystal structure of TRAIL-DR5 complex identifies a critical role of the unique frame insertion in conferring recognition specificity.

Cha SS, Sung BJ, Kim YA, Song YL, Kim HJ, Kim S, Lee MS, Oh BH
J Biol Chem 275 31171-7 (2000)
Cited: 83 times
EuropePMC logo PMID: 10893238

Abstract

TRAIL is a cytokine that induces apoptosis in a wide variety of tumor cells but rarely in normal cells. It contains an extraordinarily elongated loop because of an unique insertion of 12-16 amino acids compared with the other members of tumor necrosis factor family. Biological implication of the frame insertion has not been clarified. We have determined the crystal structure of TRAIL in a complex with the extracellular domain of death receptor DR5 at 2.2 A resolution. The structure reveals extensive contacts between the elongated loop and DR5 in an interaction mode that would not be allowed without the frame insertion. These interactions are missing in the structures of the complex determined by others recently. This observation, along with structure-inspired deletion analysis, identifies the critical role of the frame insertion as a molecular strategy conferring specificity upon the recognition of cognate receptors. The structure also suggests that a built-in flexibility of the tumor necrosis factor receptor family members is likely to play a general and important role in the binding and recognition of tumor necrosis factor family members.

Reviews - 1du3 mentioned but not cited (1)

  1. On the TRAIL of Better Therapies: Understanding TNFRSF Structure-Function. Vanamee ÉS, Faustman DL. Cells 9 E764 (2020)

Articles - 1du3 mentioned but not cited (15)

  1. The structure of the trimer of human 4-1BB ligand is unique among members of the tumor necrosis factor superfamily. Won EY, Cha K, Byun JS, Kim DU, Shin S, Ahn B, Kim YH, Rice AJ, Walz T, Kwon BS, Cho HS. J. Biol. Chem. 285 9202-9210 (2010)
  2. Enriching the human apoptosis pathway by predicting the structures of protein-protein complexes. Acuner Ozbabacan SE, Keskin O, Nussinov R, Gursoy A. J. Struct. Biol. 179 338-346 (2012)
  3. Integrating structure to protein-protein interaction networks that drive metastasis to brain and lung in breast cancer. Engin HB, Guney E, Keskin O, Oliva B, Gursoy A. PLoS One 8 e81035 (2013)
  4. Structure of human cytomegalovirus UL141 binding to TRAIL-R2 reveals novel, non-canonical death receptor interactions. Nemčovičová I, Benedict CA, Zajonc DM. PLoS Pathog. 9 e1003224 (2013)
  5. Modeling the assembly order of multimeric heteroprotein complexes. Peterson LX, Togawa Y, Esquivel-Rodriguez J, Terashi G, Christoffer C, Roy A, Shin WH, Kihara D. PLoS Comput Biol 14 e1005937 (2018)
  6. Cavities in protein-DNA and protein-RNA interfaces. Sonavane S, Chakrabarti P. Nucleic Acids Res. 37 4613-4620 (2009)
  7. Highly precise protein-protein interaction prediction based on consensus between template-based and de novo docking methods. Ohue M, Matsuzaki Y, Shimoda T, Ishida T, Akiyama Y. BMC Proc 7 S6 (2013)
  8. Exploring potential mechanisms of Suhexiang Pill against COVID-19 based on network pharmacology and molecular docking. Li J, Huang Z, Lu S, Luo H, Tan Y, Ye P, Liu X, Wu Z, Wu C, Stalin A, Wang H, Liu Y, Shen L, Fan X, Zhang B, Yi J, Yao L, Xu Y, Wu J, Duan X. Medicine (Baltimore) 100 e27112 (2021)
  9. The structure of the death receptor 4-TNF-related apoptosis-inducing ligand (DR4-TRAIL) complex. Ramamurthy V, Yamniuk AP, Lawrence EJ, Yong W, Schneeweis LA, Cheng L, Murdock M, Corbett MJ, Doyle ML, Sheriff S. Acta Crystallogr F Struct Biol Commun 71 1273-1281 (2015)
  10. Soluble Fas ligand drives autoantibody-induced arthritis by binding to DR5/TRAIL-R2. Jeong D, Kim HS, Kim HY, Kang MJ, Jung H, Oh Y, Kim D, Koh J, Cho SY, Jeon YK, Lee EB, Lee SH, Shin EC, Kim HM, Yi EC, Chung DH. Elife 10 e48840 (2021)
  11. research-article Heparan sulfate promotes TRAIL-induced tumor cell apoptosis. Luo Y, Hao H, Wang Z, Ong C, Dutcher R, Xu Y, Liu J, Pedersen LC, Xu D. bioRxiv 2023.07.26.550758 (2023)
  12. High-Throughput Metabolomics Integrated Network Pharmacology Reveals the Underlying Mechanism of Paeoniae Radix Alba Treating Rheumatoid Arthritis. Liu L, Li T, Dong H, Wang X. Molecules 27 7014 (2022)
  13. In Silico, In Vitro, and In Vivo Evaluation of Caffeine-Coated Nanoparticles as a Promising Therapeutic Avenue for AML through NF-Kappa B and TRAIL Pathways Modulation. Siddique MH, Bukhari S, Khan IU, Essa A, Ali Z, Sabir U, Ayoub O, Saadia H, Yaseen M, Sultan A, Murtaza I, Kerr PG, Bhat MA, Anees M. Pharmaceuticals (Basel) 16 1742 (2023)
  14. Morniga-G, a T/Tn-Specific Lectin, Induces Leukemic Cell Death via Caspase and DR5 Receptor-Dependent Pathways. Poiroux G, Barre A, Simplicien M, Pelofy S, Segui B, Van Damme EJM, Rougé P, Benoist H. Int J Mol Sci 20 (2019)
  15. Synthesis, Physicochemical Characterization, Biological Evaluation, In Silico and Molecular Docking Studies of Pd(II) Complexes with P, S-Donor Ligands. Khan H, Sirajuddin M, Badshah A, Ahmad S, Bilal M, Salman SM, Butler IS, Wani TA, Zargar S. Pharmaceuticals (Basel) 16 806 (2023)


Reviews citing this publication (18)

  1. Promoting apoptosis as a strategy for cancer drug discovery. Fesik SW. Nat. Rev. Cancer 5 876-885 (2005)
  2. The molecular architecture of the TNF superfamily. Bodmer JL, Schneider P, Tschopp J. Trends Biochem. Sci. 27 19-26 (2002)
  3. Following a TRAIL: update on a ligand and its five receptors. Kimberley FC, Screaton GR. Cell Res. 14 359-372 (2004)
  4. Three is better than one: pre-ligand receptor assembly in the regulation of TNF receptor signaling. Chan FK. Cytokine 37 101-107 (2007)
  5. Death to the bad guys: targeting cancer via Apo2L/TRAIL. Bouralexis S, Findlay DM, Evdokiou A. Apoptosis 10 35-51 (2005)
  6. Tumor necrosis factor family ligand-receptor binding. Zhang G. Curr. Opin. Struct. Biol. 14 154-160 (2004)
  7. Receptors for myelin inhibitors: Structures and therapeutic opportunities. Cao Z, Gao Y, Deng K, Williams G, Doherty P, Walsh FS. Mol. Cell. Neurosci. 43 1-14 (2010)
  8. Principles of antibody-mediated TNF receptor activation. Wajant H. Cell Death Differ. 22 1727-1741 (2015)
  9. Survey of the year 2000 commercial optical biosensor literature. Rich RL, Myszka DG. J. Mol. Recognit. 14 273-294 (2001)
  10. Death receptors and caspases: role in lymphocyte proliferation, cell death, and autoimmunity. Adam-Klages S, Adam D, Janssen O, Kabelitz D. Immunol. Res. 33 149-166 (2005)
  11. The TNF receptor superfamily: role in immune inflammation and bone formation. Cheng X, Kinosaki M, Murali R, Greene MI. Immunol. Res. 27 287-294 (2003)
  12. Structural principles of tumor necrosis factor superfamily signaling. Vanamee ÉS, Faustman DL. Sci Signal 11 (2018)
  13. The role of tumor necrosis factor receptor superfamily members in mammalian brain development, function and homeostasis. Twohig JP, Cuff SM, Yong AA, Wang EC. Rev Neurosci 22 509-533 (2011)
  14. Multifunctional role of Fas-associated death domain protein in apoptosis. Kim KS. J. Biochem. Mol. Biol. 35 1-6 (2002)
  15. TNF superfamily protein-protein interactions: feasibility of small- molecule modulation. Song Y, Buchwald P. Curr Drug Targets 16 393-408 (2015)
  16. Molecular Mode of Action of TRAIL Receptor Agonists-Common Principles and Their Translational Exploitation. Wajant H. Cancers (Basel) 11 (2019)
  17. Piecing it together: Unraveling the elusive structure-function relationship in single-pass membrane receptors. Valley CC, Lewis AK, Sachs JN. Biochim Biophys Acta Biomembr 1859 1398-1416 (2017)
  18. [Clinical applications of TRAIL in cancers. The prostate cancer example] Hesry V, Guillaudeux T, Patard JJ. Pathol. Biol. 51 123-128 (2003)

Articles citing this publication (49)

  1. Preligand assembly domain-mediated ligand-independent association between TRAIL receptor 4 (TR4) and TR2 regulates TRAIL-induced apoptosis. Clancy L, Mruk K, Archer K, Woelfel M, Mongkolsapaya J, Screaton G, Lenardo MJ, Chan FK. Proc. Natl. Acad. Sci. U.S.A. 102 18099-18104 (2005)
  2. Crystal structure of the TRANCE/RANKL cytokine reveals determinants of receptor-ligand specificity. Lam J, Nelson CA, Ross FP, Teitelbaum SL, Fremont DH. J. Clin. Invest. 108 971-979 (2001)
  3. Designed tumor necrosis factor-related apoptosis-inducing ligand variants initiating apoptosis exclusively via the DR5 receptor. van der Sloot AM, Tur V, Szegezdi E, Mullally MM, Cool RH, Samali A, Serrano L, Quax WJ. Proc. Natl. Acad. Sci. U.S.A. 103 8634-8639 (2006)
  4. Crystal structure of extracellular human BAFF, a TNF family member that stimulates B lymphocytes. Karpusas M, Cachero TG, Qian F, Boriack-Sjodin A, Mullen C, Strauch K, Hsu YM, Kalled SL. J. Mol. Biol. 315 1145-1154 (2002)
  5. Early diversification of the TNF superfamily in teleosts: genomic characterization and expression analysis. Glenney GW, Wiens GD. J Immunol 178 7955-7973 (2007)
  6. The crystal structures of EDA-A1 and EDA-A2: splice variants with distinct receptor specificity. Hymowitz SG, Compaan DM, Yan M, Wallweber HJ, Dixit VM, Starovasnik MA, de Vos AM. Structure 11 1513-1520 (2003)
  7. RNA aptamers selected against the receptor activator of NF-kappaB acquire general affinity to proteins of the tumor necrosis factor receptor family. Mori T, Oguro A, Ohtsu T, Nakamura Y. Nucleic Acids Res. 32 6120-6128 (2004)
  8. Resistance of mitochondrial DNA-deficient cells to TRAIL: role of Bax in TRAIL-induced apoptosis. Kim JY, Kim YH, Chang I, Kim S, Pak YK, Oh BH, Yagita H, Jung YK, Oh YJ, Lee MS. Oncogene 21 3139-3148 (2002)
  9. Crystal structure of human RANKL complexed with its decoy receptor osteoprotegerin. Luan X, Lu Q, Jiang Y, Zhang S, Wang Q, Yuan H, Zhao W, Wang J, Wang X. J Immunol 189 245-252 (2012)
  10. Disabling of receptor activator of nuclear factor-kappaB (RANK) receptor complex by novel osteoprotegerin-like peptidomimetics restores bone loss in vivo. Cheng X, Kinosaki M, Takami M, Choi Y, Zhang H, Murali R. J. Biol. Chem. 279 8269-8277 (2004)
  11. Targeting TNFR2 with antagonistic antibodies inhibits proliferation of ovarian cancer cells and tumor-associated Tregs. Torrey H, Butterworth J, Mera T, Okubo Y, Wang L, Baum D, Defusco A, Plager S, Warden S, Huang D, Vanamee E, Foster R, Faustman DL. Sci Signal 10 (2017)
  12. Structure-based development of a receptor activator of nuclear factor-kappaB ligand (RANKL) inhibitor peptide and molecular basis for osteopetrosis. Ta HM, Nguyen GT, Jin HM, Choi J, Park H, Kim N, Hwang HY, Kim KK. Proc. Natl. Acad. Sci. U.S.A. 107 20281-20286 (2010)
  13. Activation of the proapoptotic death receptor DR5 by oligomeric peptide and antibody agonists. Li B, Russell SJ, Compaan DM, Totpal K, Marsters SA, Ashkenazi A, Cochran AG, Hymowitz SG, Sidhu SS. J. Mol. Biol. 361 522-536 (2006)
  14. Homomeric and heteromeric interactions of the extracellular domains of death receptors and death decoy receptors. Lee HW, Lee SH, Lee HW, Ryu YW, Kwon MH, Kim YS. Biochem. Biophys. Res. Commun. 330 1205-1212 (2005)
  15. Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) induces death receptor 5 networks that are highly organized. Valley CC, Lewis AK, Mudaliar DJ, Perlmutter JD, Braun AR, Karim CB, Thomas DD, Brody JR, Sachs JN. J. Biol. Chem. 287 21265-21278 (2012)
  16. Engineering a leucine zipper-TRAIL homotrimer with improved cytotoxicity in tumor cells. Rozanov DV, Savinov AY, Golubkov VS, Rozanova OL, Postnova TI, Sergienko EA, Vasile S, Aleshin AE, Rega MF, Pellecchia M, Strongin AY. Mol. Cancer Ther. 8 1515-1525 (2009)
  17. TRAIL receptor signaling and therapeutic option in bone tumors: the trap of the bone microenvironment. Picarda G, Trichet V, Téletchéa S, Heymann D, Rédini F. Am J Cancer Res 2 45-64 (2012)
  18. Molecular identification of an MHC-independent ligand recognized by a human {alpha}/{beta} T-cell receptor. Hanada K, Wang QJ, Inozume T, Yang JC. Blood 117 4816-4825 (2011)
  19. Synthetic constrained peptide selectively binds and antagonizes death receptor 5. Vrielink J, Heins MS, Setroikromo R, Szegezdi E, Mullally MM, Samali A, Quax WJ. FEBS J. 277 1653-1665 (2010)
  20. The conformation of the extracellular binding domain of Death Receptor 5 in the presence and absence of the activating ligand TRAIL: a molecular dynamics study. Wassenaar TA, Quax WJ, Mark AE. Proteins 70 333-343 (2008)
  21. A genetically encoded multifunctional TRAIL trimer facilitates cell-specific targeting and tumor cell killing. Spitzer D, McDunn JE, Plambeck-Suess S, Goedegebuure PS, Hotchkiss RS, Hawkins WG. Mol. Cancer Ther. 9 2142-2151 (2010)
  22. The crystal structure of death receptor 6 (DR6): a potential receptor of the amyloid precursor protein (APP). Kuester M, Kemmerzehl S, Dahms SO, Roeser D, Than ME. J. Mol. Biol. 409 189-201 (2011)
  23. Association of human tumor necrosis factor-related apoptosis inducing ligand with membrane upon acidification. Nam GH, Choi KY. Eur. J. Biochem. 269 5280-5287 (2002)
  24. Insertion of foreign T cell epitopes in human tumor necrosis factor alpha with minimal effect on protein structure and biological activity. Nielsen FS, Sauer J, Bäcklund J, Voldborg B, Gregorius K, Mouritsen S, Bratt T. J. Biol. Chem. 279 33593-33600 (2004)
  25. Unraveling the binding mechanism of trivalent tumor necrosis factor ligands and their receptors. Reis CR, van Assen AH, Quax WJ, Cool RH. Mol. Cell Proteomics 10 M110.002808 (2011)
  26. Inducing rigid local structure around the zinc-binding region by hydrophobic interactions enhances the homotrimerization and apoptotic activity of zinc-free TRAIL. Lee HW, Kim TI, Chan KH, Kwon MH, Kim JS, Jin M, Kim YS. Biochem. Biophys. Res. Commun. 362 766-772 (2007)
  27. Purification and crystallization of recombinant human TNF-like ligand TL1A. Jin T, Kim S, Guo F, Howard A, Zhang YZ. Cytokine 40 115-122 (2007)
  28. TRAIL-R2 Superoligomerization Induced by Human Monoclonal Agonistic Antibody KMTR2. Tamada T, Shinmi D, Ikeda M, Yonezawa Y, Kataoka S, Kuroki R, Mori E, Motoki K. Sci Rep 5 17936 (2015)
  29. TRAIL-R4-beta: a new splice variant of TRAIL-receptor 4 lacking the cysteine rich domain 1. Krieg A, Schulte am Esch J, Ramp U, Hosch SB, Knoefel WT, Gabbert HE, Mahotka C. Biochem. Biophys. Res. Commun. 349 115-121 (2006)
  30. Targeting a novel N-terminal epitope of death receptor 5 triggers tumor cell death. Zhang P, Zheng Y, Shi J, Zhang Y, Liu S, Liu Y, Zheng D. J. Biol. Chem. 285 8953-8966 (2010)
  31. RGD-avidin-biotin pretargeting to alpha v beta 3 integrin enhances the proapoptotic activity of TNF alpha related apoptosis inducing ligand (TRAIL). Tarrus M, van der Sloot AM, Temming K, Lacombe M, Opdam F, Quax WJ, Molema G, Poelstra K, Kok RJ. Apoptosis 13 225-235 (2008)
  32. Structural Insight for Roles of DR5 Death Domain Mutations on Oligomerization of DR5 Death Domain-FADD Complex in the Death-Inducing Signaling Complex Formation: A Computational Study. Yang H, Song Y. J Mol Model 22 89 (2016)
  33. Knowledge-based modeling of peptides at protein interfaces: PiPreD. Oliva B, Fernandez-Fuentes N. Bioinformatics 31 1405-1410 (2015)
  34. Structure of the extracellular domains of human and Xenopus Fn14: implications in the evolution of TWEAK and Fn14 interactions. Pellegrini M, Willen L, Perroud M, Krushinskie D, Strauch K, Cuervo H, Day ES, Schneider P, Zheng TS. FEBS J. 280 1818-1829 (2013)
  35. Trimeric coiled-coil domain of human pulmonary surfactant protein D enhances zinc-binding ability and biologic activity of soluble TRAIL. Wu X, Li P, Qian C, Li O, Zhou Y. Mol. Immunol. 46 2381-2388 (2009)
  36. Variants of Osteoprotegerin Lacking TRAIL Binding for Therapeutic Bone Remodeling in Osteolytic Malignancies. Higgs JT, Jarboe JS, Lee JH, Chanda D, Lee CM, Deivanayagam C, Ponnazhagan S. Mol. Cancer Res. 13 819-827 (2015)
  37. A patch of positively charged residues regulates the efficacy of clinical DR5 antibodies in solid tumors. Shivange G, Mondal T, Lyerly E, Bhatnagar S, Landen CN, Reddy S, Kim J, Doan B, Riddle P, Tushir-Singh J. Cell Rep 37 109953 (2021)
  38. Insights into ligand binding by a viral tumor necrosis factor (TNF) decoy receptor yield a selective soluble human type 2 TNF receptor. Pontejo SM, Sanchez C, Ruiz-Argüello B, Alcami A. J. Biol. Chem. 294 5214-5227 (2019)
  39. Phenylarsine oxide interferes with the death inducing signaling complex and inhibits tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) induced apoptosis. Sun XM, Canda-Sánchez A, Manjeri GR, Cohen GM, Pinkoski MJ. Exp. Cell Res. 315 2453-2462 (2009)
  40. Preparation and characterization of a novel variant of human tumor necrosis factor-related apoptosis-inducing ligand from the rhesus monkey, Macaca mulatta. Jia D, Yang H, Tao Z, Wan L, Cheng J, Lu X. Appl. Microbiol. Biotechnol. 100 3035-3047 (2016)
  41. 1H, 13C, 15N NMR resonance assignments and secondary structure determination of the extra-cellular domain from the human proapoptotic TRAIL-R2 death receptor 5 (DR5-ECD). Baudin A, Guichard A, Collie GW, Rousseau S, Chaignepain S, Hocquellet A, Berbon M, Loquet A, Mackereth C, Guichard G, Odaert B. Biomol NMR Assign 12 309-314 (2018)
  42. Apoptotic Cell Death Induced by ofLBP6A, Lipopolysaccharide Binding Protein Model Peptide, Derived from Paralichthy olivaceus on MKN-28 Cells. Kang CW, Kim NH, Park NG, Kim GD. Drug Dev. Res. 77 94-102 (2016)
  43. Characterizing the regulatory Fas (CD95) epitope critical for agonist antibody targeting and CAR-T bystander function in ovarian cancer. Mondal T, Gaur H, Wamba BEN, Michalak AG, Stout C, Watson MR, Aleixo SL, Singh A, Condello S, Faller R, Leiserowitz GS, Bhatnagar S, Tushir-Singh J. Cell Death Differ 30 2408-2431 (2023)
  44. Crystal structure of the m4-1BB/4-1BBL complex reveals an unusual dimeric ligand that undergoes structural changes upon 4-1BB receptor binding. Bitra A, Doukov T, Destito G, Croft M, Zajonc DM. J. Biol. Chem. 294 1831-1845 (2019)
  45. Crystal structures of the human 4-1BB receptor bound to its ligand 4-1BBL reveal covalent receptor dimerization as a potential signaling amplifier. Bitra A, Doukov T, Croft M, Zajonc DM. J. Biol. Chem. 293 9958-9969 (2018)
  46. Disulfide bond-disrupting agents activate the tumor necrosis family-related apoptosis-inducing ligand/death receptor 5 pathway. Wang M, Law ME, Davis BJ, Yaaghubi E, Ghilardi AF, Ferreira RB, Chiang CW, Guryanova OA, Kopinke D, Heldermon CD, Castellano RK, Law BK. Cell Death Discov 5 153 (2019)
  47. High-resolution crystal structure of arthropod Eiger TNF suggests a mode of receptor engagement and altered surface charge within endosomes. Bertinelli M, Paesen GC, Grimes JM, Renner M. Commun Biol 2 293 (2019)
  48. Identification of New DR5 Agonistic Nanobodies and Generation of Multivalent Nanobody Constructs for Cancer Treatment. Sadeghnezhad G, Romão E, Bernedo-Navarro R, Massa S, Khajeh K, Muyldermans S, Hassania S. Int J Mol Sci 20 (2019)
  49. Structural basis of LaDR5, a novel agonistic anti-death receptor 5 (DR5) monoclonal antibody, to inhibit DR5/TRAIL complex formation. Qiao C, Hu M, Guo L, Lv M, Lin Z, Geng J, Lang X, Li X, Li Y, Ma Y, Feng J, Shen B. BMC Immunol. 13 40 (2012)


Quick links