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The structural basis for membrane binding and pore formation by lymphocyte perforin.

Law RH, Lukoyanova N, Voskoboinik I, Caradoc-Davies TT, Baran K, Dunstone MA, D'Angelo ME, Orlova EV, Coulibaly F, Verschoor S, Browne KA, Ciccone A, Kuiper MJ, Bird PI, Trapani JA, Saibil HR, Whisstock JC
Nature 468 447-51 (2010)
Cited: 242 times
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Abstract

Natural killer cells and cytotoxic T lymphocytes accomplish the critically important function of killing virus-infected and neoplastic cells. They do this by releasing the pore-forming protein perforin and granzyme proteases from cytoplasmic granules into the cleft formed between the abutting killer and target cell membranes. Perforin, a 67-kilodalton multidomain protein, oligomerizes to form pores that deliver the pro-apoptopic granzymes into the cytosol of the target cell. The importance of perforin is highlighted by the fatal consequences of congenital perforin deficiency, with more than 50 different perforin mutations linked to familial haemophagocytic lymphohistiocytosis (type 2 FHL). Here we elucidate the mechanism of perforin pore formation by determining the X-ray crystal structure of monomeric murine perforin, together with a cryo-electron microscopy reconstruction of the entire perforin pore. Perforin is a thin 'key-shaped' molecule, comprising an amino-terminal membrane attack complex perforin-like (MACPF)/cholesterol dependent cytolysin (CDC) domain followed by an epidermal growth factor (EGF) domain that, together with the extreme carboxy-terminal sequence, forms a central shelf-like structure. A C-terminal C2 domain mediates initial, Ca(2+)-dependent membrane binding. Most unexpectedly, however, electron microscopy reveals that the orientation of the perforin MACPF domain in the pore is inside-out relative to the subunit arrangement in CDCs. These data reveal remarkable flexibility in the mechanism of action of the conserved MACPF/CDC fold and provide new insights into how related immune defence molecules such as complement proteins assemble into pores.

Reviews - 3nsj mentioned but not cited (7)

  1. Hotze EM, Tweten RK. Biochim Biophys Acta 1818 1028-1038 (2012)
  2. Dunstone MA, Tweten RK. Curr Opin Struct Biol 22 342-349 (2012)
  3. Ni T, Gilbert RJC. Philos Trans R Soc Lond B Biol Sci 372 20160212 (2017)
  4. Bayly-Jones C, Pang SS, Spicer BA, Whisstock JC, Dunstone MA. Front Immunol 11 581906 (2020)
  5. Benton JT, Bayly-Jones C. Biochem Soc Trans 49 2749-2765 (2021)
  6. Guerra AJ, Carruthers VB. Toxins (Basel) 9 E265 (2017)
  7. Stadermann A, Haar M, Riecke A, Mayer T, Neumann C, Bauer A, Schulz A, Nagarathinam K, Gebauer N, B枚hm S, Gro脽 M, Grunert M, M眉ller M, Witte H. Int J Mol Sci 25 2762 (2024)

Articles - 3nsj mentioned but not cited (14)

  1. Ruan J, Xia S, Liu X, Lieberman J, Wu H. Nature 557 62-67 (2018)
  2. Wirth CC, Glushakova S, Scheuermayer M, Repnik U, Garg S, Schaack D, Kachman MM, Wei脽bach T, Zimmerberg J, Dandekar T, Griffiths G, Chitnis CE, Singh S, Fischer R, Pradel G. Cell Microbiol 16 709-733 (2014)
  3. Lovelace LL, Cooper CL, Sodetz JM, Lebioda L. J Biol Chem 286 17585-17592 (2011)
  4. Ni T, Jiao F, Yu X, Aden S, Ginger L, Williams SI, Bai F, Pra啪谩k V, Karia D, Stansfeld P, Zhang P, Munson G, Anderluh G, Scheuring S, Gilbert RJC. Sci Adv 6 eaax8286 (2020)
  5. D'Angelo ME, Dunstone MA, Whisstock JC, Trapani JA, Bird PI. BMC Evol Biol 12 59 (2012)
  6. Ni T, Harlos K, Gilbert R. Open Biol 6 160053 (2016)
  7. House IG, House CM, Brennan AJ, Gilan O, Dawson MA, Whisstock JC, Law RH, Trapani JA, Voskoboinik I. EMBO Rep 18 1775-1785 (2017)
  8. Yagi H, Conroy PJ, Leung EW, Law RH, Trapani JA, Voskoboinik I, Whisstock JC, Norton RS. J Biol Chem 290 25213-25226 (2015)
  9. An O, Gursoy A, Gurgey A, Keskin O. Protein Sci 22 823-839 (2013)
  10. Zaitseva J, Vaknin D, Krebs C, Doroghazi J, Milam SL, Balasubramanian D, Duck NB, Freigang J. Proc Natl Acad Sci U S A 116 2897-2906 (2019)
  11. Evans JC, Johnstone BA, Lawrence SL, Morton CJ, Christie MP, Parker MW, Tweten RK. mBio 11 e02351-20 (2020)
  12. Ivanova ME, Lukoyanova N, Malhotra S, Topf M, Trapani JA, Voskoboinik I, Saibil HR. Sci Adv 8 eabk3147 (2022)
  13. Brennan AJ, Law RHP, Conroy PJ, Noori T, Lukoyanova N, Saibil H, Yagita H, Ciccone A, Verschoor S, Whisstock JC, Trapani JA, Voskoboinik I. Cell Death Differ 25 1517-1529 (2018)
  14. Bryant P, No茅 F. Nat Commun 15 7328 (2024)


Reviews citing this publication (72)

  1. Voskoboinik I, Whisstock JC, Trapani JA. Nat Rev Immunol 15 388-400 (2015)
  2. Dal Peraro M, van der Goot FG. Nat Rev Microbiol 14 77-92 (2016)
  3. Prager I, Watzl C. J Leukoc Biol 105 1319-1329 (2019)
  4. Cooper ST, McNeil PL. Physiol Rev 95 1205-1240 (2015)
  5. Luzio JP, Hackmann Y, Dieckmann NM, Griffiths GM. Cold Spring Harb Perspect Biol 6 a016840 (2014)
  6. Risma K, Jordan MB. Curr Opin Pediatr 24 9-15 (2012)
  7. Wen C, Seeger RC, Fabbri M, Wang L, Wayne AS, Jong AY. J Extracell Vesicles 6 1400370 (2017)
  8. Gilbert RJ, Dalla Serra M, Froelich CJ, Wallace MI, Anderluh G. Trends Biochem Sci 39 510-516 (2014)
  9. Zhang J, Yang Y, He W, Sun L. Cell Mol Life Sci 73 2153-2163 (2016)
  10. Osi艅ska I, Popko K, Demkow U. Cent Eur J Immunol 39 109-115 (2014)
  11. Lieberman J, Wu H, Kagan JC. Sci Immunol 4 eaav1447 (2019)
  12. Bayly-Jones C, Bubeck D, Dunstone MA. Philos Trans R Soc Lond B Biol Sci 372 20160221 (2017)
  13. Ammendolia DA, Bement WM, Brumell JH. BMC Biol 19 71 (2021)
  14. Liu X, Lieberman J. Annu Rev Immunol 38 455-485 (2020)
  15. Tweten RK, Hotze EM, Wade KR. Annu Rev Microbiol 69 323-340 (2015)
  16. Susanto O, Trapani JA, Brasacchio D. Tissue Antigens 80 477-487 (2012)
  17. Schmidt S, Zimmermann SY, Tramsen L, Koehl U, Lehrnbecher T. Clin Vaccine Immunol 20 452-458 (2013)
  18. Gilbert RJ, Mikelj M, Dalla Serra M, Froelich CJ, Anderluh G. Cell Mol Life Sci 70 2083-2098 (2013)
  19. Schmidt S, Tramsen L, Lehrnbecher T. Front Immunol 8 1623 (2017)
  20. McCormack R, Podack ER. J Leukoc Biol 98 761-768 (2015)
  21. Voskoboinik I, Trapani JA. Front Immunol 4 441 (2013)
  22. Qin Y, Zhang L, Xu Z, Zhang J, Jiang YY, Cao Y, Yan T. Virulence 7 512-526 (2016)
  23. Fert-Bober J, Darrah E, Andrade F. Immunol Rev 294 133-147 (2020)
  24. McCormack R, de Armas L, Shiratsuchi M, Podack ER. Immunol Res 57 268-278 (2013)
  25. Lukoyanova N, Hoogenboom BW, Saibil HR. J Cell Sci 129 2125-2133 (2016)
  26. Hay ZLZ, Slansky JE. Int J Mol Sci 23 1833 (2022)
  27. Podobnik M, Anderluh G. Semin Cell Dev Biol 72 133-141 (2017)
  28. Galea CA, Nguyen HM, George Chandy K, Smith BJ, Norton RS. Cell Mol Life Sci 71 1191-1210 (2014)
  29. Wood SM, Ljunggren HG, Bryceson YT. Cell Mol Life Sci 68 3479-3493 (2011)
  30. Tuomela K, Ambrose AR, Davis DM. Front Immunol 13 867098 (2022)
  31. Su SC, Chung WH. Toxins (Basel) 6 194-210 (2014)
  32. Nestorovich EM, Bezrukov SM. Chem Rev 112 6388-6430 (2012)
  33. Spicer BA, Conroy PJ, Law RHP, Voskoboinik I, Whisstock JC. Semin Cell Dev Biol 72 117-123 (2017)
  34. Podack ER, Munson GP. Front Immunol 7 464 (2016)
  35. Lange S. Front Neurol 7 22 (2016)
  36. Bolivar-Wagers S, Larson JH, Jin S, Blazar BR. Front Immunol 13 864748 (2022)
  37. Martinvalet D. Oxid Med Cell Longev 2019 9165214 (2019)
  38. Schmidt S, Ullrich E, Bochennek K, Zimmermann SY, Lehrnbecher T. Expert Rev Hematol 9 1119-1127 (2016)
  39. Sonnen AF, Henneke P. Clin Dev Immunol 2013 608456 (2013)
  40. Deng J, Zhou M, Liao T, Kuang W, Xia H, Yin Z, Tan Q, Li Y, Song S, Zhou E, Jin Y. Front Cell Dev Biol 10 818453 (2022)
  41. Ghosh A, Holland AM, van den Brink MR. Immunol Rev 257 226-236 (2014)
  42. Wade KR, Tweten RK. Curr Opin Microbiol 26 48-52 (2015)
  43. Krawczyk PA, Laub M, Kozik P. Front Immunol 11 601405 (2020)
  44. Kulma M, Anderluh G. Cell Mol Life Sci 78 6229-6249 (2021)
  45. de Saint Basile G, Sepulveda FE, Maschalidi S, Fischer A. F1000Res 4 930 (2015)
  46. Patarroyo ME, Alba MP, Rojas-Luna R, Bermudez A, Aza-Conde J. Immunotherapy 9 131-155 (2017)
  47. Shrestha AC, Wijesundara DK, Masavuli MG, Mekonnen ZA, Gowans EJ, Grubor-Bauk B. Vaccines (Basel) 7 E38 (2019)
  48. Johnson TK, Henstridge MA, Warr CG. Semin Cell Dev Biol 72 163-170 (2017)
  49. Berkowicz SR, Giousoh A, Bird PI. Semin Cell Dev Biol 72 171-181 (2017)
  50. Lea SM, Johnson S. Immunobiology 217 1117-1121 (2012)
  51. Willenbring RC, Johnson AJ. Int J Mol Sci 18 E1608 (2017)
  52. Pattu V, Halimani M, Ming M, Schirra C, Hahn U, Bzeih H, Chang HF, Weins L, Krause E, Rettig J. Front Immunol 4 411 (2013)
  53. Schmidt S, Condorelli A, Koltze A, Lehrnbecher T. J Fungi (Basel) 3 E25 (2017)
  54. Kozlov AV, Grillari J. Front Med (Lausanne) 9 806462 (2022)
  55. Boyd CM, Bubeck D. Curr Opin Struct Biol 52 41-49 (2018)
  56. Li J, Liu Y, Yuan Y, Huang B. Front Med 15 43-52 (2021)
  57. Merselis LC, Rivas ZP, Munson GP. Front Immunol 12 597951 (2021)
  58. Nozaki K, Miao EA. Trends Cell Biol 33 803-815 (2023)
  59. Rivera-de-Torre E, Palacios-Ortega J, Slotte JP, Gavilanes JG, Mart铆nez-Del-Pozo 脕, Garc铆a-Linares S. Int J Mol Sci 21 E8915 (2020)
  60. Sassmannshausen J, Pradel G, Bennink S. Front Cell Infect Microbiol 10 578883 (2020)
  61. Quentin D, Raunser S. J Mol Med (Berl) 96 483-493 (2018)
  62. Ockfen E, Filali L, Pereira Fernandes D, Hoffmann C, Thomas C. Front Immunol 14 1276602 (2023)
  63. Hsu CH, Lee KJ, Chiu YH, Huang KC, Wang GS, Chen LP, Liao KW, Lin CS. Cells 11 1492 (2022)
  64. Scott H, Huang W, Bann JG, Taylor DJ. Protein Sci 27 1544-1556 (2018)
  65. Keb G, Fields KA. Front Immunol 11 1490 (2020)
  66. Spicer JA, Huttunen KM, Jose J, Dimitrov I, Akhlaghi H, Sutton VR, Voskoboinik I, Trapani J. J Med Chem 65 14305-14325 (2022)
  67. Kamiya M, Kimura N, Umezawa N, Hasegawa H, Yasuda S. Front Immunol 14 1191815 (2023)
  68. Karageorgos S, Platt AS, Bassiri H. Adv Exp Med Biol 1448 75-101 (2024)
  69. Cigalotto L, Martinvalet D. Front Immunol 15 1371743 (2024)
  70. Bickel JK, Voisin TB, Tate EW, Bubeck D. Subcell Biochem 96 273-295 (2021)
  71. Co毛non L, Geindreau M, Ghiringhelli F, Villalba M, Bruchard M. Cell Death Dis 15 614 (2024)
  72. Guan X, Guo H, Guo Y, Han Q, Li Z, Zhang C. Biomolecules 14 910 (2024)

Articles citing this publication (149)

  1. Liu X, Zhang Z, Ruan J, Pan Y, Magupalli VG, Wu H, Lieberman J. Nature 535 153-158 (2016)
  2. Prager I, Liesche C, van Ooijen H, Urlaub D, Verron Q, Sandstr枚m N, Fasbender F, Claus M, Eils R, Beaudouin J, 脰nfelt B, Watzl C. J Exp Med 216 2113-2127 (2019)
  3. Samson AL, Zhang Y, Geoghegan ND, Gavin XJ, Davies KA, Mlodzianoski MJ, Whitehead LW, Frank D, Garnish SE, Fitzgibbon C, Hempel A, Young SN, Jacobsen AV, Cawthorne W, Petrie EJ, Faux MC, Shield-Artin K, Lalaoui N, Hildebrand JM, Silke J, Rogers KL, Lessene G, Hawkins ED, Murphy JM. Nat Commun 11 3151 (2020)
  4. Lopez JA, Susanto O, Jenkins MR, Lukoyanova N, Sutton VR, Law RH, Johnston A, Bird CH, Bird PI, Whisstock JC, Trapani JA, Saibil HR, Voskoboinik I. Blood 121 2659-2668 (2013)
  5. Romero V, Fert-Bober J, Nigrovic PA, Darrah E, Haque UJ, Lee DM, van Eyk J, Rosen A, Andrade F. Sci Transl Med 5 209ra150 (2013)
  6. Serna M, Giles JL, Morgan BP, Bubeck D. Nat Commun 7 10587 (2016)
  7. Krzewski K, Coligan JE. Front Immunol 3 335 (2012)
  8. Poon IKh, Baxter AA, Lay FT, Mills GD, Adda CG, Payne JA, Phan TK, Ryan GF, White JA, Veneer PK, van der Weerden NL, Anderson MA, Kvansakul M, Hulett MD. Elife 3 e01808 (2014)
  9. Hadders MA, Bubeck D, Roversi P, Hakobyan S, Forneris F, Morgan BP, Pangburn MK, Llorca O, Lea SM, Gros P. Cell Rep 1 200-207 (2012)
  10. Wu CH, Li J, Li L, Sun J, Fabbri M, Wayne AS, Seeger RC, Jong AY. J Extracell Vesicles 8 1588538 (2019)
  11. Schulert GS, Zhang M, Fall N, Husami A, Kissell D, Hanosh A, Zhang K, Davis K, Jentzen JM, Napolitano L, Siddiqui J, Smith LB, Harms PW, Grom AA, Cron RQ. J Infect Dis 213 1180-1188 (2016)
  12. Cohnen A, Chiang SC, Stojanovic A, Schmidt H, Claus M, Saftig P, Jan脽en O, Cerwenka A, Bryceson YT, Watzl C. Blood 122 1411-1418 (2013)
  13. Lukoyanova N, Kondos SC, Farabella I, Law RH, Reboul CF, Caradoc-Davies TT, Spicer BA, Kleifeld O, Traore DA, Ekkel SM, Voskoboinik I, Trapani JA, Hatfaludi T, Oliver K, Hotze EM, Tweten RK, Whisstock JC, Topf M, Saibil HR, Dunstone MA. PLoS Biol 13 e1002049 (2015)
  14. B谩lint 艩, M眉ller S, Fischer R, Kessler BM, Harkiolaki M, Valitutti S, Dustin ML. Science 368 897-901 (2020)
  15. Dudkina NV, Spicer BA, Reboul CF, Conroy PJ, Lukoyanova N, Elmlund H, Law RH, Ekkel SM, Kondos SC, Goode RJ, Ramm G, Whisstock JC, Saibil HR, Dunstone MA. Nat Commun 7 10588 (2016)
  16. Bertrand F, M眉ller S, Roh KH, Laurent C, Dupr茅 L, Valitutti S. Proc Natl Acad Sci U S A 110 6073-6078 (2013)
  17. K枚ster S, van Pee K, Hudel M, Leustik M, Rhinow D, K眉hlbrandt W, Chakraborty T, Yildiz 脰. Nat Commun 5 3690 (2014)
  18. Bavdek A, Kostanj拧ek R, Antonini V, Lakey JH, Dalla Serra M, Gilbert RJ, Anderluh G. FEBS J 279 126-141 (2012)
  19. Garg S, Agarwal S, Kumar S, Yazdani SS, Chitnis CE, Singh S. Nat Commun 4 1736 (2013)
  20. Rodriguez L, Gonzalez-Guzman M, Diaz M, Rodrigues A, Izquierdo-Garcia AC, Peirats-Llobet M, Fernandez MA, Antoni R, Fernandez D, Marquez JA, Mulet JM, Albert A, Albert A, Rodriguez PL. Plant Cell 26 4802-4820 (2014)
  21. Lu CC, Wu TS, Hsu YJ, Chang CJ, Lin CS, Chia JH, Wu TL, Huang TT, Martel J, Ojcius DM, Young JD, Lai HC. J Leukoc Biol 96 1119-1129 (2014)
  22. Rakowska PD, Jiang H, Ray S, Pyne A, Lamarre B, Carr M, Judge PJ, Ravi J, Gerling UI, Koksch B, Martyna GJ, Hoogenboom BW, Watts A, Crain J, Grovenor CR, Ryadnov MG. Proc Natl Acad Sci U S A 110 8918-8923 (2013)
  23. Pereiro P, Balseiro P, Romero A, Dios S, Forn-Cuni G, Fuste B, Planas JV, Beltran S, Novoa B, Figueras A. PLoS One 7 e35369 (2012)
  24. Dowd KJ, Farrand AJ, Tweten RK. PLoS Pathog 8 e1002787 (2012)
  25. McCormack R, de Armas LR, Shiratsuchi M, Ramos JE, Podack ER. J Innate Immun 5 185-194 (2013)
  26. Aleshin AE, Schraufstatter IU, Stec B, Bankston LA, Liddington RC, DiScipio RG. J Biol Chem 287 10210-10222 (2012)
  27. Sharp TH, Koster AJ, Gros P. Cell Rep 15 1-8 (2016)
  28. Brennan AJ, Chia J, Browne KA, Ciccone A, Ellis S, Lopez JA, Susanto O, Verschoor S, Yagita H, Whisstock JC, Trapani JA, Voskoboinik I. Immunity 34 879-892 (2011)
  29. Laurent C, M眉ller S, Do C, Al-Saati T, Allart S, Larocca LM, Hohaus S, Duchez S, Quillet-Mary A, Laurent G, Brousset P, Valitutti S. Blood 118 5371-5379 (2011)
  30. Ota K, Leonardi A, Mikelj M, Sko膷aj M, Wohlschlager T, K眉nzler M, Aebi M, Narat M, Kri啪aj I, Anderluh G, Sep膷i膰 K, Ma膷ek P. Biochimie 95 1855-1864 (2013)
  31. McCormack RM, de Armas LR, Shiratsuchi M, Fiorentino DG, Olsson ML, Lichtenheld MG, Morales A, Lyapichev K, Gonzalez LE, Strbo N, Sukumar N, Stojadinovic O, Plano GV, Munson GP, Tomic-Canic M, Kirsner RS, Russell DG, Podack ER. Elife 4 e06508 (2015)
  32. Leung C, Hodel AW, Brennan AJ, Lukoyanova N, Tran S, House CM, Kondos SC, Whisstock JC, Dunstone MA, Trapani JA, Voskoboinik I, Saibil HR, Hoogenboom BW. Nat Nanotechnol 12 467-473 (2017)
  33. Metkar SS, Marchioretto M, Antonini V, Lunelli L, Wang B, Gilbert RJ, Anderluh G, Roth R, Pooga M, Pardo J, Heuser JE, Serra MD, Froelich CJ. Cell Death Differ 22 74-85 (2015)
  34. Degen M, Santos JC, Pluhackova K, Cebrero G, Ramos S, Jankevicius G, Hartenian E, Guillerm U, Mari SA, Kohl B, M眉ller DJ, Schanda P, Maier T, Perez C, Sieben C, Broz P, Hiller S. Nature 618 1065-1071 (2023)
  35. Rudd-Schmidt JA, Hodel AW, Noori T, Lopez JA, Cho HJ, Verschoor S, Ciccone A, Trapani JA, Hoogenboom BW, Voskoboinik I. Nat Commun 10 5396 (2019)
  36. Wickham SE, Hotze EM, Farrand AJ, Polekhina G, Nero TL, Tomlinson S, Parker MW, Tweten RK. J Biol Chem 286 20952-20962 (2011)
  37. Johnson S, Brooks NJ, Smith RA, Lea SM, Bubeck D. Cell Rep 3 1369-1377 (2013)
  38. Parsons ES, Stanley GJ, Pyne ALB, Hodel AW, Nievergelt AP, Menny A, Yon AR, Rowley A, Richter RP, Fantner GE, Bubeck D, Hoogenboom BW. Nat Commun 10 2066 (2019)
  39. Pang SS, Bayly-Jones C, Radjainia M, Spicer BA, Law RHP, Hodel AW, Parsons ES, Ekkel SM, Conroy PJ, Ramm G, Venugopal H, Bird PI, Hoogenboom BW, Voskoboinik I, Gambin Y, Sierecki E, Dunstone MA, Whisstock JC. Nat Commun 10 4288 (2019)
  40. Hotze EM, Wilson-Kubalek E, Farrand AJ, Bentsen L, Parker MW, Johnson AE, Tweten RK. J Biol Chem 287 24534-24543 (2012)
  41. Thompson JR, Cronin B, Bayley H, Wallace MI. Biophys J 101 2679-2683 (2011)
  42. Roiko MS, Carruthers VB. J Biol Chem 288 8712-8725 (2013)
  43. Khazen R, M眉ller S, Gaudenzio N, Espinosa E, Puissegur MP, Valitutti S. Nat Commun 7 10823 (2016)
  44. Brenu EW, Hardcastle SL, Atkinson GM, van Driel ML, Kreijkamp-Kaspers S, Ashton KJ, Staines DR, Marshall-Gradisnik SM. Auto Immun Highlights 4 69-80 (2013)
  45. Metkar SS, Wang B, Catalan E, Anderluh G, Gilbert RJ, Pardo J, Froelich CJ. PLoS One 6 e24286 (2011)
  46. Huang CY, Araujo K, S谩nchez JN, Kund G, Trumble J, Roper C, Godfrey KE, Jin H. Proc Natl Acad Sci U S A 118 e2019628118 (2021)
  47. Fields KA, McCormack R, de Armas LR, Podack ER. Infect Immun 81 3045-3054 (2013)
  48. Jones RB, Mueller S, Kumari S, Vrbanac V, Genel S, Tager AM, Allen TM, Walker BD, Irvine DJ. Biomaterials 117 44-53 (2017)
  49. Spicer BA, Law RHP, Caradoc-Davies TT, Ekkel SM, Bayly-Jones C, Pang SS, Conroy PJ, Ramm G, Radjainia M, Venugopal H, Whisstock JC, Dunstone MA. Nat Commun 9 3266 (2018)
  50. Johnson TK, Crossman T, Foote KA, Henstridge MA, Saligari MJ, Forbes Beadle L, Herr A, Whisstock JC, Warr CG. Proc Natl Acad Sci U S A 110 14688-14692 (2013)
  51. McCormack RM, Lyapichev K, Olsson ML, Podack ER, Munson GP. Elife 4 e06505 (2015)
  52. Chiusolo V, Jacquemin G, Yonca Bassoy E, Vinet L, Liguori L, Walch M, Kozjak-Pavlovic V, Martinvalet D. Cell Death Differ 24 747-758 (2017)
  53. Ellisdon AM, Reboul CF, Panjikar S, Huynh K, Oellig CA, Winter KL, Dunstone MA, Hodgson WC, Seymour J, Dearden PK, Tweten RK, Whisstock JC, McGowan S. Proc Natl Acad Sci U S A 112 15360-15365 (2015)
  54. Garc铆a-Linares S, Castrillo I, Bruix M, Men茅ndez M, Alegre-Cebollada J, Mart铆nez-del-Pozo 脕, Gavilanes JG. Arch Biochem Biophys 532 39-45 (2013)
  55. Zhai Y, Ran W, Su J, Lang T, Meng J, Wang G, Zhang P, Li Y, Li Y. Adv Mater e1802378 (2018)
  56. Tosi T, Estrozi LF, Job V, Guilvout I, Pugsley AP, Schoehn G, Dessen A. Structure 22 1348-1355 (2014)
  57. Wang S, Xia P, Shi L, Fan Z. Cell Death Differ 19 605-615 (2012)
  58. Liu Y, Zhang T, Zhou Y, Li J, Liang X, Zhou N, Lv J, Xie J, Cheng F, Fang Y, Gao Y, Wang N, Huang B. Cell Mol Immunol 16 611-620 (2019)
  59. Huttunen KM, Huttunen J, Aufderhaar I, Gynther M, Denny WA, Spicer JA. Int J Pharm 498 205-216 (2016)
  60. Tesi B, Chiang SC, El-Ghoneimy D, Hussein AA, Langenski枚ld C, Wali R, Fadoo Z, Silva JP, Lecumberri R, Unal S, Nordenskj枚ld M, Bryceson YT, Henter JI, Meeths M. Pediatr Blood Cancer 62 2094-2100 (2015)
  61. Gargett T, Grubor-Bauk B, Garrod TJ, Yu W, Miller D, Major L, Wesselingh S, Suhrbier A, Gowans EJ. Immunol Cell Biol 92 359-367 (2014)
  62. Grubor-Bauk B, Yu W, Wijesundara D, Wijesundara D, Gummow J, Garrod T, Brennan AJ, Voskoboinik I, Gowans EJ. Gene Ther 23 26-37 (2016)
  63. Gao M, Wang K, Yang M, Meng F, Lu R, Zhuang H, Cheng G, Wang X. Front Immunol 9 1403 (2018)
  64. Petris G, Casini A, Sasset L, Cesaratto F, Bestagno M, Cereseto A, Burrone OR. J Biol Chem 289 1-12 (2014)
  65. Stewart SE, Kondos SC, Matthews AY, D'Angelo ME, Dunstone MA, Whisstock JC, Trapani JA, Bird PI. J Biol Chem 289 9172-9181 (2014)
  66. Pyne A, Pfeil MP, Bennett I, Ravi J, Iavicoli P, Lamarre B, Roethke A, Ray S, Jiang H, Bella A, Reisinger B, Yin D, Little B, Mu帽oz-Garc铆a JC, Cerasoli E, Judge PJ, Faruqui N, Calzolai L, Henrion A, Martyna GJ, Grovenor CRM, Crain J, Hoogenboom BW, Watts A, Ryadnov MG. Chem Sci 8 1105-1115 (2017)
  67. Moreno-Hagelsieb G, Vitug B, Medrano-Soto A, Saier MH. J Mol Microbiol Biotechnol 27 252-267 (2017)
  68. Janiszewski T, Ko艂t S, Kaiserman D, Snipas SJ, Li S, Kulbacka J, Saczko J, Bovenschen N, Salvesen G, Dr膮g M, Bird PI, Kasperkiewicz P. J Biol Chem 295 9567-9582 (2020)
  69. Mouchacca P, Schmitt-Verhulst AM, Boyer C. PLoS One 8 e67239 (2013)
  70. Praper T, Sonnen AF, Kladnik A, Andrighetti AO, Viero G, Morris KJ, Volpi E, Lunelli L, Dalla Serra M, Froelich CJ, Gilbert RJ, Anderluh G. Proc Natl Acad Sci U S A 108 21016-21021 (2011)
  71. Li Y, Orange JS. PLoS Biol 19 e3001328 (2021)
  72. Sampson K, Zaitseva J, Stauffer M, Vande Berg B, Guo R, Tomso D, McNulty B, Desai N, Balasubramanian D. J Invertebr Pathol 142 34-43 (2017)
  73. Bai F, McCormack RM, Hower S, Plano GV, Lichtenheld MG, Munson GP. J Immunol 201 2710-2720 (2018)
  74. Trapani JA. Cell Death Differ 19 21-27 (2012)
  75. Henstridge MA, Johnson TK, Warr CG, Whisstock JC. Nat Commun 5 3419 (2014)
  76. Chia J, Thia K, Brennan AJ, Little M, Williams B, Lopez JA, Trapani JA, Voskoboinik I. Blood 119 1713-1716 (2012)
  77. Lu CC, Hsu YJ, Chang CJ, Lin CS, Martel J, Ojcius DM, Ko YF, Lai HC, Young JD. Innate Immun 22 522-533 (2016)
  78. Duggal NA, Upton J, Phillips AC, Hampson P, Lord JM. Age (Dordr) 37 9748 (2015)
  79. Chang CJ, Chen YY, Lu CC, Lin CS, Martel J, Tsai SH, Ko YF, Huang TT, Ojcius DM, Young JD, Lai HC. Innate Immun 20 301-311 (2014)
  80. Traore DA, Brennan AJ, Law RH, Dogovski C, Perugini MA, Lukoyanova N, Leung EW, Norton RS, Lopez JA, Browne KA, Yagita H, Lloyd GJ, Ciccone A, Verschoor S, Trapani JA, Whisstock JC, Voskoboinik I. Biochem J 456 323-335 (2013)
  81. Menny A, Lukassen MV, Couves EC, Franc V, Heck AJR, Bubeck D. Nat Commun 12 6086 (2021)
  82. Ko艂t S, Janiszewski T, Kaiserman D, Modrzycka S, Snipas SJ, Salvesen G, Dra G M, Bird PI, Kasperkiewicz P. J Med Chem 63 3359-3369 (2020)
  83. Spicer JA, Lena G, Lyons DM, Huttunen KM, Miller CK, O'Connor PD, Bull M, Helsby N, Jamieson SM, Denny WA, Ciccone A, Browne KA, Lopez JA, Rudd-Schmidt J, Voskoboinik I, Trapani JA. J Med Chem 56 9542-9555 (2013)
  84. Chaudhry MS, Gilmour KC, House IG, Layton M, Panoskaltsis N, Sohal M, Trapani JA, Voskoboinik I. Oncoimmunology 5 e1179415 (2016)
  85. Huysmans GHM, Guilvout I, Pugsley AP. J Biol Chem 288 30700-30707 (2013)
  86. Mishra RR, Chaudhary JK, Bajaj GD, Rath PC. PLoS One 6 e28433 (2011)
  87. Pang Y, Gou M, Yang K, Lu J, Han Y, Teng H, Li C, Wang H, Liu C, Zhang K, Yang Y, Li Q. Cell Commun Signal 17 54 (2019)
  88. Miller CK, Huttunen KM, Denny WA, Jaiswal JK, Ciccone A, Browne KA, Trapani JA, Spicer JA. Bioorg Med Chem Lett 26 355-360 (2016)
  89. Couves EC, Gardner S, Voisin TB, Bickel JK, Stansfeld PJ, Tate EW, Bubeck D. Nat Commun 14 890 (2023)
  90. Liesche C, Sauer P, Prager I, Urlaub D, Claus M, Eils R, Beaudouin J, Watzl C. Front Immunol 9 1840 (2018)
  91. Mishra RR, Chaudhary JK, Rath PC. Mol Biol Rep 39 7389-7402 (2012)
  92. Woodsworth DJ, Dunsing V, Coombs D. Biophys J 109 477-488 (2015)
  93. Yu L, Liu D, Chen S, Dai Y, Guo W, Zhang X, Wang L, Ma S, Xiao M, Qi H, Xiao S, Chen Q. Int J Mol Sci 21 E5736 (2020)
  94. Gratzinger D, Jaffe ES, Chadburn A, Chan JK, de Jong D, Goodlad JR, Said J, Natkunam Y. Am J Clin Pathol 147 204-216 (2017)
  95. Varela M, Forn-Cun铆 G, Dios S, Figueras A, Novoa B. J Innate Immun 8 43-56 (2016)
  96. Woodsworth DJ, Dreolini L, Abraham L, Holt RA. Mol Ther Methods Clin Dev 7 132-145 (2017)
  97. Burns JR, Morton CJ, Parker MW, Tweten RK. mBio 10 e01017-19 (2019)
  98. Yang NJ, Liu DV, Sklaviadis D, Gui DY, Vander Heiden MG, Wittrup KD. Mol Pharm 12 1992-2000 (2015)
  99. Spicer JA, Miller CK, O'Connor PD, Jose J, Huttunen KM, Jaiswal JK, Denny WA, Akhlaghi H, Browne KA, Trapani JA. Bioorg Med Chem Lett 27 1050-1054 (2017)
  100. Editorial Beebe SJ. Int J Nanomedicine 8 3401-3404 (2013)
  101. Maurer J, Hupp S, Pillich H, Mitchell TJ, Chakraborty T, Iliev AI. Sci Rep 8 15846 (2018)
  102. Wu F, Feng B, Ren Y, Wu D, Chen Y, Huang S, Chen S, Xu A. Cell Discov 3 17033 (2017)
  103. Forbes-Beadle L, Crossman T, Johnson TK, Burke R, Warr CG, Whisstock JC. Genetics 204 675-681 (2016)
  104. Willenbring RC, Ikeda Y, Pease LR, Johnson AJ. Mol Genet Genomic Med 6 44-55 (2018)
  105. Vuong NL, Cheung KW, Periaswamy B, Vi TT, Duyen HTL, Leong YS, Binte Hamis ZN, Gregorova M, Ooi EE, Sessions O, Rivino L, Yacoub S. J Infect Dis 226 1338-1347 (2022)
  106. Jiao F, Dehez F, Ni T, Yu X, Dittman JS, Gilbert R, Chipot C, Scheuring S. Nat Commun 13 5039 (2022)
  107. Wade KR, Lawrence SL, Farrand AJ, Hotze EM, Kuiper MJ, Gorman MA, Christie MP, Panjikar S, Morton CJ, Parker MW, Tweten RK. mBio 10 e00538-19 (2019)
  108. Filali L, Puissegur MP, Cortacero K, Cussat-Blanc S, Khazen R, Van Acker N, Frenois FX, Abreu A, Lamant L, Meyer N, Vergier B, M眉ller S, McKenzie B, Valitutti S. Sci Adv 8 eabk3234 (2022)
  109. Holmes DR, Bredow M, Thor K, Pascetta SA, Sementchoukova I, Siegel KR, Zipfel C, Monaghan J. Genetics 217 iyab022 (2021)
  110. Romero CA, S谩nchez IP, Gutierrez-Hincapi茅 S, 脕lvarez-脕lvarez JA, Perea帽ez JA, Ochoa R, Muskus-L贸pez CE, Eraso RG, Echeverry C, Arango C, Restrepo JL, Trujillo-Vargas CM. J Clin Immunol 35 501-511 (2015)
  111. Giousoh A, Vaz R, Bryson-Richardson RJ, Whisstock JC, Verkade H, Bird PI. Gene Expr Patterns 18 37-43 (2015)
  112. Hodel AW, Rudd-Schmidt JA, Trapani JA, Voskoboinik I, Hoogenboom BW. Faraday Discuss 232 236-255 (2021)
  113. Li T, Wang L, Zhang Y, Guo X, Chen X, Zhang F, Yang G, Wen W, Li H. BMC Vet Res 14 299 (2018)
  114. Wang Y, Zhang M, Wang C, Ye B, Hua Z. Fish Shellfish Immunol 35 1993-2000 (2013)
  115. Sevim H, Kocaefe Y脟, Onur MA, U莽kan-脟etinkaya D, G眉rp谋nar 脰A. Stem Cell Res Ther 9 198 (2018)
  116. Marsh RA, Filipovich AH. Ann N Y Acad Sci 1238 106-121 (2011)
  117. Guerra AJ, Zhang O, Zhang O, Bahr CME, Huynh MH, DelProposto J, Brown WC, Wawrzak Z, Koropatkin NM, Carruthers VB. PLoS Pathog 14 e1007476 (2018)
  118. Bull MR, Spicer JA, Huttunen KM, Denny WA, Ciccone A, Browne KA, Trapani JA, Helsby NA. Eur J Drug Metab Pharmacokinet 40 417-425 (2015)
  119. Yang Y, Chen Y, Guo J, Liu H, Ju H. iScience 24 102980 (2021)
  120. Stewart SE, Bird CH, Tabor RF, D'Angelo ME, Piantavigna S, Whisstock JC, Trapani JA, Martin LL, Bird PI. J Biol Chem 290 31101-31112 (2015)
  121. Lo WC, Luther DG. J Fluoresc 24 465-471 (2014)
  122. Weiland MH, Qian Y, Sodetz JM. Mol Immunol 57 310-316 (2014)
  123. Spicer JA, Miller CK, O'Connor PD, Jose J, Huttunen KM, Jaiswal JK, Denny WA, Akhlaghi H, Browne KA, Trapani JA. Eur J Med Chem 137 139-155 (2017)
  124. Naneh O, Zavec AB, Pahovnik D, 沤agar E, Gilbert RJ, Kri啪aj I, Anderluh G. J Immunol Methods 426 19-28 (2015)
  125. Aggio V, Fabbella L, Poletti S, Lorenzi C, Finardi A, Colombo C, Zanardi R, Furlan R, Benedetti F. Sci Rep 13 22209 (2023)
  126. D'Angelo ME, Arjomand A, Trapani JA, Bird PI. Dev Comp Immunol 41 105-109 (2013)
  127. Song F, Cui L, Piao J, Liang H, Si H, Duan Y, Zhai H. Chem Biol Drug Des 90 535-544 (2017)
  128. Yang Y, Wang Y, Chao Z, Yang Y, Fang Y, Liu Y, Ding L, Chen Y, Ju H. Adv Sci (Weinh) 11 e2304971 (2024)
  129. Rudd-Schmidt JA, Laine RF, Noori T, Brennan AJ, Voskoboinik I. Front Immunol 13 931820 (2022)
  130. Zhou Y, Wang D, Zhou L, Zhou N, Wang Z, Chen J, Pang R, Fu H, Huang Q, Dong F, Cheng H, Zhang H, Tang K, Ma J, Lv J, Cheng T, Fiskesund R, Zhang X, Huang B. Nat Commun 15 1405 (2024)
  131. Wang LF, Wang F, Li JT, Wen WH, Zhao J, Jia LT, Meng YL, Cao YX, Yao LB, Chen SY, Xu YM, Yang AG. PLoS One 7 e40639 (2012)
  132. Johns AR, Henstridge MA, Saligari MJ, Moore KA, Whisstock JC, Warr CG, Johnson TK. G3 (Bethesda) 8 761-769 (2018)
  133. Liu W, Liu B, Zhang G, Yao G, Zhang Y, Cen X, He M. Int J Mol Sci 23 13415 (2022)
  134. Mouchacca P, Guyot V, Gr茅goire C, Schmitt-Verhulst AM, Boyer C. Eur J Immunol 42 264-266 (2012)
  135. Wurzer H, Filali L, Thomas C. PLoS Biol 19 e3001339 (2021)
  136. Rosso DA, Rosato M, G贸mez FD, 脕lvarez RS, Shiromizu CM, Keitelman IA, Ibarra C, Amaral MM, Jancic CC. Front Cell Infect Microbiol 11 765941 (2021)
  137. Froelich C, Metkar S. Immunity 34 823-825 (2011)
  138. Horton MK, Shim JE, Wallace A, Graves JS, Aaen G, Greenberg B, Mar S, Wheeler Y, Weinstock-Guttman B, Waldman A, Schreiner T, Rodriguez M, Tillema JM, Chitnis T, Krupp L, Casper TC, Rensel M, Hart J, Quach HL, Quach DL, Schaefer C, Waubant E, Barcellos LF. Mult Scler 29 505-511 (2023)
  139. Du Preez S, Eaton-Fitch N, Smith PK, Marshall-Gradisnik S. Biomolecules 13 1039 (2023)
  140. Neely AE, Mandigo KA, Robinson RL, Ness TL, Weiland MH. Protein Eng Des Sel 30 105-111 (2017)
  141. Wang Y, Yuan X, Wang T, Wei W, Wu S, Hou H. Virulence 15 2342276 (2024)
  142. Moadab F, Wang X, Le E, Gazitt T, Najjar R, Nelson JL, Joshua V, Malmstr枚m V, Elkon K, Gr枚nwall C, Mustelin T. Sci Rep 14 15511 (2024)
  143. Letter Voskoboinik I, Thia K, Trapani JA. Intern Med J 44 826-827 (2014)
  144. Gorodetskiy V, Sidorova Y, Biderman B, Kupryshina N, Ryzhikova N, Sudarikov A. Front Cell Dev Biol 12 1434676 (2024)
  145. Ma S, Guo Y, Liu D, Zhang X, Guo J, Zhang T, Lai L, Li Y, Chen Q, Yu L. Int J Mol Sci 24 13193 (2023)
  146. Len谩rt M, Bober P, Marcin M, Tk谩膷ikov谩 S, Kac铆rov谩 M, Alexovi膷 M, T贸th D, Mad谩rov谩 N, Rado艌ak J, Urdz铆k P, Feda膷ko J, Sabo J. Int J Mol Sci 25 6423 (2024)
  147. Zhang J, Liu J, Chen H, Wu W, Li X, Wu Y, Wang Z, Zhang K, Li Y, Weng Y, Liao H, Gu L. Immunol Res 64 1033-1040 (2016)
  148. Naneh O, Kozorog M, Merzel F, Gilbert R, Anderluh G. Front Immunol 14 1181020 (2023)
  149. News Whisstock JC, Law RHP. Nature 618 912-914 (2023)


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