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2.8 A resolution crystal structure of human TRAIL, a cytokine with selective antitumor activity.

Cha SS, Kim MS, Choi YH, Sung BJ, Shin NK, Shin HC, Sung YC, Oh BH
Immunity 11 253-61 (1999)
Cited: 93 times
EuropePMC logo PMID: 10485660

Abstract

TRAIL is a newly identified cytokine belonging to the large tumor necrosis factor (TNF) family. TRAIL is a novel molecule inducing apoptosis in a wide variety of tumor cells but not in normal cells. To help in elucidating its biological roles and designing mutants with improved therapeutic potential, we have determined the crystal structure of human TRAIL. The structure reveals that a unique frame insertion of 12-16 amino acids adopts a salient loop structure penetrating into the receptor-binding site. The loop drastically alters the common receptor-binding surface of the TNF family most likely for the specific recognition of cognate partners. A structure-based mutagenesis study demonstrates a critical role of the insertion loop in the cytotoxic activity of TRAIL.

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  2. Structure of the Chlamydia trachomatis immunodominant antigen Pgp3. Galaleldeen A, Taylor AB, Chen D, Schuermann JP, Holloway SP, Hou S, Gong S, Zhong G, Hart PJ. J Biol Chem 288 22068-22079 (2013)
  3. Mechanistic basis for functional promiscuity in the TNF and TNF receptor superfamilies: structure of the LIGHT:DcR3 assembly. Liu W, Zhan C, Cheng H, Kumar PR, Bonanno JB, Nathenson SG, Almo SC. Structure 22 1252-1262 (2014)
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Reviews citing this publication (27)

  1. TNF alpha and the TNF receptor superfamily: structure-function relationship(s). Idriss HT, Naismith JH. Microsc Res Tech 50 184-195 (2000)
  2. New insights into apoptosis signaling by Apo2L/TRAIL. Gonzalvez F, Ashkenazi A. Oncogene 29 4752-4765 (2010)
  3. Onto better TRAILs for cancer treatment. de Miguel D, Lemke J, Anel A, Walczak H, Martinez-Lostao L. Cell Death Differ 23 733-747 (2016)
  4. Ligands working as receptors: reverse signaling by members of the TNF superfamily enhance the plasticity of the immune system. Eissner G, Kolch W, Scheurich P. Cytokine Growth Factor Rev 15 353-366 (2004)
  5. Structural principles of tumor necrosis factor superfamily signaling. Vanamee ÉS, Faustman DL. Sci Signal 11 eaao4910 (2018)
  6. TNF-related apoptosis-inducing ligand (TRAIL): a new path to anti-cancer therapies. Holoch PA, Griffith TS. Eur J Pharmacol 625 63-72 (2009)
  7. Principles of antibody-mediated TNF receptor activation. Wajant H. Cell Death Differ 22 1727-1741 (2015)
  8. Molecular mechanisms of death-receptor-mediated apoptosis. Sartorius U, Schmitz I, Krammer PH. Chembiochem 2 20-29 (2001)
  9. TRAILing death in cancer. Mellier G, Huang S, Shenoy K, Pervaiz S. Mol Aspects Med 31 93-112 (2010)
  10. Regulation of the human TRAIL gene. Allen JE, El-Deiry WS. Cancer Biol Ther 13 1143-1151 (2012)
  11. TRAIL gene therapy: from preclinical development to clinical application. Griffith TS, Stokes B, Kucaba TA, Earel JK, VanOosten RL, Brincks EL, Norian LA. Curr Gene Ther 9 9-19 (2009)
  12. Role of pancreatic β-cell death and inflammation in diabetes. Quan W, Jo EK, Lee MS. Diabetes Obes Metab 15 Suppl 3 141-151 (2013)
  13. Tumor necrosis factor family ligand-receptor binding. Zhang G. Curr Opin Struct Biol 14 154-160 (2004)
  14. The TRAIL to viral pathogenesis: the good, the bad and the ugly. Cummins N, Badley A. Curr Mol Med 9 495-505 (2009)
  15. Resistance to TRAIL and how to surmount it. Maksimovic-Ivanic D, Stosic-Grujicic S, Nicoletti F, Mijatovic S. Immunol Res 52 157-168 (2012)
  16. The role of neutrophils and TNF-related apoptosis-inducing ligand (TRAIL) in bacillus Calmette-Guérin (BCG) immunotherapy for urothelial carcinoma of the bladder. Rosevear HM, Lightfoot AJ, O'Donnell MA, Griffith TS. Cancer Metastasis Rev 28 345-353 (2009)
  17. Importance of TRAIL Molecular Anatomy in Receptor Oligomerization and Signaling. Implications for Cancer Therapy. Naval J, de Miguel D, Gallego-Lleyda A, Anel A, Martinez-Lostao L. Cancers (Basel) 11 E444 (2019)
  18. Harnessing TRAIL-induced cell death for cancer therapy: a long walk with thrilling discoveries. Montinaro A, Walczak H. Cell Death Differ 30 237-249 (2023)
  19. Cell surface receptors. Deller MC, Yvonne Jones E. Curr Opin Struct Biol 10 213-219 (2000)
  20. Should We Keep Walking along the Trail for Pancreatic Cancer Treatment? Revisiting TNF-Related Apoptosis-Inducing Ligand for Anticancer Therapy. Kretz AL, von Karstedt S, Hillenbrand A, Henne-Bruns D, Knippschild U, Trauzold A, Lemke J. Cancers (Basel) 10 E77 (2018)
  21. Death ligands and granulysin: mechanisms of tumor cell death induction and therapeutic opportunities. Martinez-Lostao L, de Miguel D, Al-Wasaby S, Gallego-Lleyda A, Anel A. Immunotherapy 7 883-882 (2015)
  22. Overview of protein structural and functional folds. Sun PD, Foster CE, Boyington JC. Curr Protoc Protein Sci Chapter 17 Unit 17.1 (2004)
  23. Death receptor ligands in tumors. Cappello P, Novelli F, Forni G, Giovarelli M. J Immunother 25 1-15 (2002)
  24. TNF superfamily protein-protein interactions: feasibility of small- molecule modulation. Song Y, Buchwald P. Curr Drug Targets 16 393-408 (2015)
  25. Functional roles in cell signaling of adaptor protein TRADD from a structural perspective. Li Z, Yuan W, Lin Z. Comput Struct Biotechnol J 18 2867-2876 (2020)
  26. The tumour necrosis factor receptor family: life or death choices. Jones EY. Curr Opin Struct Biol 10 644-648 (2000)
  27. TRAIL-Sensitizing Effects of Flavonoids in Cancer. Luiz-Ferreira A, Pacifico T, Cruz ÁC, Laudisi F, Monteleone G, Stolfi C. Int J Mol Sci 24 16596 (2023)

Articles citing this publication (61)

  1. Triggering cell death: the crystal structure of Apo2L/TRAIL in a complex with death receptor 5. Hymowitz SG, Christinger HW, Fuh G, Ultsch M, O'Connell M, Kelley RF, Ashkenazi A, de Vos AM. Mol Cell 4 563-571 (1999)
  2. Modulation of T-cell-mediated immunity in tumor and graft-versus-host disease models through the LIGHT co-stimulatory pathway. Tamada K, Shimozaki K, Chapoval AI, Zhu G, Sica G, Flies D, Boone T, Hsu H, Fu YX, Nagata S, Ni J, Chen L. Nat Med 6 283-289 (2000)
  3. The methionine-aromatic motif plays a unique role in stabilizing protein structure. Valley CC, Cembran A, Perlmutter JD, Lewis AK, Labello NP, Gao J, Sachs JN. J Biol Chem 287 34979-34991 (2012)
  4. Crystal structure of sTALL-1 reveals a virus-like assembly of TNF family ligands. Liu Y, Xu L, Opalka N, Kappler J, Shu HB, Zhang G. Cell 108 383-394 (2002)
  5. 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)
  6. Structural and functional analysis of the interaction between the agonistic monoclonal antibody Apomab and the proapoptotic receptor DR5. Adams C, Totpal K, Lawrence D, Marsters S, Pitti R, Yee S, Ross S, Deforge L, Koeppen H, Sagolla M, Compaan D, Lowman H, Hymowitz S, Ashkenazi A. Cell Death Differ 15 751-761 (2008)
  7. Ligand-receptor binding revealed by the TNF family member TALL-1. Liu Y, Hong X, Kappler J, Jiang L, Zhang R, Xu L, Pan CH, Martin WE, Murphy RC, Shu HB, Dai S, Zhang G. Nature 423 49-56 (2003)
  8. 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)
  9. Interferon-activated neutrophils store a TNF-related apoptosis-inducing ligand (TRAIL/Apo-2 ligand) intracellular pool that is readily mobilizable following exposure to proinflammatory mediators. Cassatella MA, Huber V, Calzetti F, Margotto D, Tamassia N, Peri G, Mantovani A, Rivoltini L, Tecchio C. J Leukoc Biol 79 123-132 (2006)
  10. Liposome-bound APO2L/TRAIL is an effective treatment in a rabbit model of rheumatoid arthritis. Martinez-Lostao L, García-Alvarez F, Basáñez G, Alegre-Aguarón E, Desportes P, Larrad L, Naval J, Martínez-Lorenzo MJ, Anel A. Arthritis Rheum 62 2272-2282 (2010)
  11. Progranulin-derived Atsttrin directly binds to TNFRSF25 (DR3) and inhibits TNF-like ligand 1A (TL1A) activity. Liu C, Li XX, Gao W, Liu W, Liu DS. PLoS One 9 e92743 (2014)
  12. IFN-gamma enhances TRAIL-induced apoptosis through IRF-1. Park SY, Seol JW, Lee YJ, Cho JH, Kang HS, Kim IS, Park SH, Kim TH, Yim JH, Kim M, Billiar TR, Seol DW. Eur J Biochem 271 4222-4228 (2004)
  13. 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)
  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. Regulation of Akt by EGF-R inhibitors, a possible mechanism of EGF-R inhibitor-enhanced TRAIL-induced apoptosis. Park SY, Seol DW. Biochem Biophys Res Commun 295 515-518 (2002)
  16. The secretable form of trimeric TRAIL, a potent inducer of apoptosis. Kim MH, Billiar TR, Seol DW. Biochem Biophys Res Commun 321 930-935 (2004)
  17. Cancer gene therapy using a novel secretable trimeric TRAIL. Kim CY, Jeong M, Mushiake H, Kim BM, Kim WB, Ko JP, Kim MH, Kim M, Kim TH, Robbins PD, Billiar TR, Seol DW. Gene Ther 13 330-338 (2006)
  18. Soluble TRAIL Armed Human MSC As Gene Therapy For Pancreatic Cancer. Spano C, Grisendi G, Golinelli G, Rossignoli F, Prapa M, Bestagno M, Candini O, Petrachi T, Recchia A, Miselli F, Rovesti G, Orsi G, Maiorana A, Manni P, Veronesi E, Piccinno MS, Murgia A, Pinelli M, Horwitz EM, Cascinu S, Conte P, Dominici M. Sci Rep 9 1788 (2019)
  19. The extracellular matrix glycoprotein elastin microfibril interface located protein 2: a dual role in the tumor microenvironment. Mongiat M, Marastoni S, Ligresti G, Lorenzon E, Schiappacassi M, Perris R, Frustaci S, Colombatti A. Neoplasia 12 294-304 (2010)
  20. Structure of CrmE, a virus-encoded tumour necrosis factor receptor. Graham SC, Bahar MW, Abrescia NG, Smith GL, Stuart DI, Grimes JM. J Mol Biol 372 660-671 (2007)
  21. A placental protective role for trophoblast-derived TNF-related apoptosis-inducing ligand (TRAIL). Bai X, Williams JL, Greenwood SL, Baker PN, Aplin JD, Crocker IP. Placenta 30 855-860 (2009)
  22. Activation of human monocyte-derived dendritic cells in vitro by the biological response modifier arabinoxylan rice bran (MGN-3/Biobran). Ghoneum M, Agrawal S. Int J Immunopathol Pharmacol 24 941-948 (2011)
  23. 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)
  24. A hypoxia- and telomerase-responsive oncolytic adenovirus expressing secretable trimeric TRAIL triggers tumour-specific apoptosis and promotes viral dispersion in TRAIL-resistant glioblastoma. Oh E, Hong J, Kwon OJ, Yun CO. Sci Rep 8 1420 (2018)
  25. Ala228 variant of trail receptor 1 affecting the ligand binding site is associated with chronic lymphocytic leukemia, mantle cell lymphoma, prostate cancer, head and neck squamous cell carcinoma and bladder cancer. Wolf S, Mertens D, Pscherer A, Schroeter P, Winkler D, Gröne HJ, Hofele C, Hemminki K, Kumar R, Steineck G, Döhner H, Stilgenbauer S, Lichter P. Int J Cancer 118 1831-1835 (2006)
  26. Possible novel therapy for malignant gliomas with secretable trimeric TRAIL. Jeong M, Kwon YS, Park SH, Kim CY, Jeun SS, Song KW, Ko Y, Robbins PD, Billiar TR, Kim BM, Seol DW. PLoS One 4 e4545 (2009)
  27. Functional analysis of tumour necrosis factor-alpha-related apoptosis-inducing ligand (TRAIL): cysteine-230 plays a critical role in the homotrimerization and biological activity of this novel tumoricidal cytokine. Trabzuni D, Famulski KS, Ahmad M. Biochem J 350 Pt 2 505-510 (2000)
  28. In situ facile-forming PEG cross-linked albumin hydrogels loaded with an apoptotic TRAIL protein. Kim I, Choi JS, Lee S, Byeon HJ, Lee ES, Shin BS, Choi HG, Lee KC, Youn YS. J Control Release 214 30-39 (2015)
  29. Interleukin-10 up-regulates tumour-necrosis-factor-alpha-related apoptosis-inducing ligand (TRAIL) gene expression in mammary epithelial cells at the involution stage. Sohn BH, Moon HB, Kim TY, Kang HS, Bae YS, Lee KK, Kim SJ. Biochem J 360 31-38 (2001)
  30. Physapubescin selectively induces apoptosis in VHL-null renal cell carcinoma cells through down-regulation of HIF-2α and inhibits tumor growth. Chen L, Xia G, Qiu F, Wu C, Denmon AP, Zi X. Sci Rep 6 32582 (2016)
  31. DR4 specific TRAIL variants are more efficacious than wild-type TRAIL in pancreatic cancer. Yu R, Albarenque SM, Cool RH, Quax WJ, Mohr A, Zwacka RM. Cancer Biol Ther 15 1658-1666 (2014)
  32. 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)
  33. Human menstrual blood-derived mesenchymal stem cells as a cellular vehicle for malignant glioma gene therapy. Wang XJ, Xiang BY, Ding YH, Chen L, Zou H, Mou XZ, Xiang C. Oncotarget 8 58309-58321 (2017)
  34. An optimized antibody-single-chain TRAIL fusion protein for cancer therapy. Siegemund M, Seifert O, Zarani M, Džinić T, De Leo V, Göttsch D, Münkel S, Hutt M, Pfizenmaier K, Kontermann RE. MAbs 8 879-891 (2016)
  35. Comparative modeling of TNFRSF25 (DR3) predicts receptor destabilization by a mutation linked to rheumatoid arthritis. Borysenko CW, Furey WF, Blair HC. Biochem Biophys Res Commun 328 794-799 (2005)
  36. Saccharomyces cerevisiae, the Baker's Yeast, suppresses the growth of Ehrlich carcinoma-bearing mice. Ghoneum M, Badr El-Din NK, Noaman E, Tolentino L. Cancer Immunol Immunother 57 581-592 (2008)
  37. 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)
  38. Autophagy as a mechanism of Apo2L/TRAIL resistance. Sharma A, Almasan A. Cancer Biol Ther 19 755-762 (2018)
  39. Death Receptors: New Opportunities in Cancer Therapy. Ukrainskaya VM, Stepanov AV, Glagoleva IS, Knorre VD, Belogurov AAJ, Gabibov AG. Acta Naturae 9 55-63 (2017)
  40. The transmembrane domains of TNF-related apoptosis-inducing ligand (TRAIL) receptors 1 and 2 co-regulate apoptotic signaling capacity. Neumann S, Bidon T, Branschädel M, Krippner-Heidenreich A, Scheurich P, Doszczak M. PLoS One 7 e42526 (2012)
  41. Advances in Viral Vector-Based TRAIL Gene Therapy for Cancer. Norian LA, James BR, Griffith TS. Cancers (Basel) 3 603-620 (2011)
  42. 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)
  43. Both HIV-Infected and Uninfected Cells Express TRAILshort, Which Confers TRAIL Resistance upon Bystander Cells within the Microenvironment. Nie Z, Aboulnasr F, Natesampillai S, Burke SP, Krogman A, Bren GD, Chung TDY, Anderson JR, Smart MK, Katzmann DJ, Rajagopalan G, Cummins NW, Badley AD. J Immunol 200 1110-1123 (2018)
  44. Expression, purification, and in vitro refolding of soluble tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). Lin Z, Lei H, Cao P. Protein Expr Purif 51 276-282 (2007)
  45. 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)
  46. Improvement of expression level and bioactivity of soluble tumor necrosis factor-related apoptosis-inducing ligand (Apo2L/TRAIL) by a novel zinc ion feeding strategy. Sun AY, Shen YL, Yin JC, Zhang H, Tang YN, Wei DZ. Biotechnol Lett 28 1215-1219 (2006)
  47. 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)
  48. 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)
  49. 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)
  50. Enhanced inhibition of tumor growth using TRAIL-overexpressing adipose-derived stem cells in combination with the chemotherapeutic agent CPT-11 in castration-resistant prostate cancer. Kim JH, Oh E, Han YS, Lee SH, Song YS. Prostate Int 9 31-41 (2021)
  51. Hypoxic resistance to articular chondrocyte apoptosis--a possible mechanism of maintaining homeostasis of normal articular cartilage. Seol JW, Lee HB, Lee YJ, Lee YH, Kang HS, Kim IS, Kim NS, Park SY. FEBS J 276 7375-7385 (2009)
  52. Gene therapy in B-NHL cell line using adenovirus-mediated transfer of secretable trimeric TRAIL gene expression driven by CD20 promoter. Yuan XF, Peng HW, Ding YH, Yan CH, Zhang YJ, Yang M, Xiong DS. Exp Hematol 41 221-230 (2013)
  53. Mutational analysis of human tumor necrosis factor-alpha. Shin HC, Cho KH. Biotechnol Lett 27 107-112 (2005)
  54. Crystallization and preliminary X-ray crystallographic study of the extracellular domain of the 4-1BB ligand, a member of the TNF family. Byun JS, Kim DU, Ahn B, Kwon BS, Cho HS. Acta Crystallogr Sect F Struct Biol Cryst Commun 62 23-25 (2006)
  55. 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)
  56. A simplified method for the efficient purification and refolding of recombinant human TRAIL. Zhang Z, Hahn SB, Cao TM, King MR. Biotechnol Prog 36 e3007 (2020)
  57. DR5 Up-Regulation Induced by Dichloroacetate Sensitizes Tumor Cells to Lipid Nanoparticles Decorated with TRAIL. Marco-Brualla J, de Miguel D, Martínez-Lostao L, Anel A. J Clin Med 12 608 (2023)
  58. Improved cytotoxicity of novel TRAIL variants produced as recombinant fusion proteins. Figiel M, Bonarek P, Górecki A, Pawlak SD, Zerek B, Checinska B, Pieczykolan J, Dziedzicka-Wasylewska M. Protein Eng Des Sel 31 37-46 (2018)
  59. Editorial The roadmap of TRAIL apoptotic pathway-targeted cancer therapies: What is next? Bellail AC, Hao C. Expert Rev Anticancer Ther 12 547-549 (2012)
  60. Heparan sulfate promotes TRAIL-induced tumor cell apoptosis. Luo Y, Hao H, Wang Z, Ong CY, Dutcher R, Xu Y, Liu J, Pedersen LC, Xu D. Elife 12 RP90192 (2024)
  61. Human menstrual blood-derived mesenchymal stem cells as a cellular vehicle for malignant glioma gene therapy. Wang XJ, Xiang BY, Ding YH, Chen L, Zou H, Mou XZ, Xiang C. Oncotarget (2017)


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