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The crystal structure of a proliferation-inducing ligand, APRIL.

Wallweber HJ, Compaan DM, Starovasnik MA, Hymowitz SG
J Mol Biol 343 283-90 (2004)
Related entries: 1u5y, 1u5z

Cited: 34 times
EuropePMC logo PMID: 15451660

Abstract

A proliferation-inducing ligand (APRIL) is a TNF-like cytokine that stimulates tumor cell growth. Within the TNF ligand superfamily, APRIL is most similar to B-cell activation factor (BAFF) with which it shares 30% sequence identity. APRIL binds the receptors B-cell maturation antigen (BCMA) and TACI with high affinity; both of these receptors have also been shown to bind BAFF, although BCMA has significantly higher affinity for APRIL than BAFF. Determination of the crystal structure of APRIL from three crystallization conditions at resolutions of 1.8-2.4A over a pH range from 5.0 to 8.5 reveals a compact trimeric ligand with a backbone fold very similar to that of BAFF (1.1A RMSD over 122 structurally equivalent Calpha atoms), with the exception of differences in the AA' and DE loop regions. Whereas BAFF has been shown to form 20-trimer assemblies under certain conditions, the molecular determinants required for BAFF-like assemblies are absent in the APRIL structure. No crystal packing suggestive of the formation of higher-order assemblies is seen in any of the crystal forms nor does the structure vary significantly between pH 5.0 and 8.5. Modeling of the APRIL-BCMA complex shows the resulting interface is in agreement with mutagenesis data.

Reviews citing this publication (14)

  1. The BAFF/APRIL system in SLE pathogenesis. Vincent FB, Morand EF, Schneider P, Mackay F. Nat Rev Rheumatol 10 365-373 (2014)
  2. An APRIL to remember: novel TNF ligands as therapeutic targets. Dillon SR, Gross JA, Ansell SM, Novak AJ. Nat Rev Drug Discov 5 235-246 (2006)
  3. Targeting B Cell Maturation Antigen (BCMA) in Multiple Myeloma: Potential Uses of BCMA-Based Immunotherapy. Cho SF, Anderson KC, Tai YT. Front Immunol 9 1821 (2018)
  4. Structural principles of tumor necrosis factor superfamily signaling. Vanamee ÉS, Faustman DL. Sci Signal 11 eaao4910 (2018)
  5. Targeting BAFF and APRIL in systemic lupus erythematosus and other antibody-associated diseases. Samy E, Wax S, Huard B, Hess H, Schneider P. Int Rev Immunol 36 3-19 (2017)
  6. Principles of antibody-mediated TNF receptor activation. Wajant H. Cell Death Differ 22 1727-1741 (2015)
  7. Role of BAFF and APRIL in human B-cell chronic lymphocytic leukaemia. Haiat S, Billard C, Quiney C, Ajchenbaum-Cymbalista F, Kolb JP. Immunology 118 281-292 (2006)
  8. The BLyS family: toward a molecular understanding of B cell homeostasis. Treml JF, Hao Y, Stadanlick JE, Cancro MP. Cell Biochem Biophys 53 1-16 (2009)
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  10. BAFF, APRIL, TWE-PRIL: who's who? Daridon C, Youinou P, Pers JO. Autoimmun Rev 7 267-271 (2008)
  11. Promising Antigens for the New Frontier of Targeted Immunotherapy in Multiple Myeloma. Cho SF, Xing L, Anderson KC, Tai YT. Cancers (Basel) 13 6136 (2021)
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  13. The BAFF-APRIL System in Cancer. Ullah MA, Mackay F. Cancers (Basel) 15 1791 (2023)
  14. A PRoliferation-Inducing Ligand (APRIL) in the Pathogenesis of Immunoglobulin A Nephropathy: A Review of the Evidence. Mathur M, Chan TM, Oh KH, Kooienga L, Zhuo M, Pinto CS, Chacko B. J Clin Med 12 6927 (2023)

Articles citing this publication (20)

  1. Identification of proteoglycans as the APRIL-specific binding partners. Ingold K, Zumsteg A, Tardivel A, Huard B, Steiner QG, Cachero TG, Qiang F, Gorelik L, Kalled SL, Acha-Orbea H, Rennert PD, Tschopp J, Schneider P. J Exp Med 201 1375-1383 (2005)
  2. Heparan sulfate proteoglycan binding promotes APRIL-induced tumor cell proliferation. Hendriks J, Planelles L, de Jong-Odding J, Hardenberg G, Pals ST, Hahne M, Spaargaren M, Medema JP. Cell Death Differ 12 637-648 (2005)
  3. Transmembrane activator and calcium-modulating cyclophilin ligand interactor mutations in common variable immunodeficiency: clinical and immunologic outcomes in heterozygotes. Zhang L, Radigan L, Salzer U, Behrens TW, Grimbacher B, Diaz G, Bussel J, Cunningham-Rundles C. J Allergy Clin Immunol 120 1178-1185 (2007)
  4. The crystal structure of the costimulatory OX40-OX40L complex. Compaan DM, Hymowitz SG. Structure 14 1321-1330 (2006)
  5. Rational design of a trimeric APRIL-based CAR-binding domain enables efficient targeting of multiple myeloma. Schmidts A, Ormhøj M, Choi BD, Taylor AO, Bouffard AA, Scarfò I, Larson RC, Frigault MJ, Gallagher K, Castano AP, Riley LS, Cabral ML, Boroughs AC, Velasco Cárdenas RM, Schamel W, Zhou J, Mackay S, Tai YT, Anderson KC, Maus MV. Blood Adv 3 3248-3260 (2019)
  6. The proteoglycan (heparan sulfate proteoglycan) binding domain of APRIL serves as a platform for ligand multimerization and cross-linking. Kimberley FC, van Bostelen L, Cameron K, Hardenberg G, Marquart JA, Hahne M, Medema JP. FASEB J 23 1584-1595 (2009)
  7. Role of B cells in common variable immune deficiency. Ahn S, Cunningham-Rundles C. Expert Rev Clin Immunol 5 557-564 (2009)
  8. Two related ligands of the TNF family, BAFF and APRIL, in rabbit: molecular cloning, 3D modeling, and tissue distribution. Guan ZB, Shui Y, Zhang SQ. Cytokine 39 192-200 (2007)
  9. APRIL mediates peritoneal B-1 cell homeostasis. Sindhava VJ, Scholz JL, Stohl W, Cancro MP. Immunol Lett 160 120-127 (2014)
  10. The construction and characterization of a bifunctional EGFP/sAPRIL fusion protein. Guan Z, Yao W, Ye J, Dan W, Shen J, Zhang S. Appl Microbiol Biotechnol 73 1114-1122 (2007)
  11. Roles for BLyS family members in meeting the distinct homeostatic demands of innate and adaptive B cells. Sindhava VJ, Scholz JL, Cancro MP. Front Immunol 4 37 (2013)
  12. Structures of mouse and human GITR-GITRL complexes reveal unique TNF superfamily interactions. Wang F, Chau B, West SM, Kimberlin CR, Cao F, Schwarz F, Aguilar B, Han M, Morishige W, Bee C, Dollinger G, Rajpal A, Strop P. Nat Commun 12 1378 (2021)
  13. 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)
  14. Reduced APRIL expression induces cellular senescence via a HSPG-dependent pathway. Ding W, Ju S, Jiang S, Zhu L, Wang Y, Wang H. Pathol Oncol Res 15 693-701 (2009)
  15. Improved secretion of human Fas ligand extracellular domain by N-terminal part truncation in Pichia pastoris and preparation of the N-linked carbohydrate chain trimmed derivative. Muraki M. Protein Expr Purif 60 205-213 (2008)
  16. Multiple novel classes of APRIL-specific receptor-blocking peptides isolated by phage display. Gordon NC, Lien S, Johnson J, Wallweber HJ, Tran T, Currell B, Mathieu M, Quan C, Starovasnik MA, Hymowitz SG, Kelley RF. J Mol Biol 396 166-177 (2010)
  17. Structural prediction of antibody-APRIL complexes by computational docking constrained by antigen saturation mutagenesis library data. Wollacott AM, Robinson LN, Ramakrishnan B, Tissire H, Viswanathan K, Shriver Z, Babcock GJ. J Mol Recognit 32 e2778 (2019)
  18. 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)
  19. [Targeting BCMA in multiple myeloma using chimeric antigen receptor-engineered T cells]. Zhong MJ, Xu YX, Xing HY, Tang KJ, Tian Z, Rao Q, Wang M, Wang JX. Zhonghua Xue Ye Xue Za Zhi 40 804-811 (2019)
  20. Development of a Bispecific IgG1 Antibody Targeting BCMA and PDL1. Cattaneo I, Choblet S, Valgardsdottir R, Roth M, Massafra A, Beeg M, Gobbi M, Duonor-Cerutti M, Golay J. Antibodies (Basel) 13 15 (2024)


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