Patient-derived xenograft models of ALK+ ALCL reveal preclinical promise for therapy with brigatinib

. 2023 Sep ; 202 (5) : 985-994. [epub] 20230625

Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid37357529

Anaplastic large-cell lymphoma (ALCL) is a T-cell malignancy predominantly driven by the oncogenic anaplastic lymphoma kinase (ALK), accounting for approximately 15% of all paediatric non-Hodgkin lymphoma. Patients with central nervous system (CNS) relapse are particularly difficult to treat with a 3-year overall survival of 49% and a median survival of 23.5 months. The second-generation ALK inhibitor brigatinib shows superior penetration of the blood-brain barrier unlike the first-generation drug crizotinib and has shown promising results in ALK+ non-small-cell lung cancer. However, the benefits of brigatinib in treating aggressive paediatric ALK+ ALCL are largely unknown. We established a patient-derived xenograft (PDX) resource from ALK+ ALCL patients at or before CNS relapse serving as models to facilitate the development of future therapies. We show in vivo that brigatinib is effective in inducing the remission of PDX models of crizotinib-resistant (ALK C1156Y, TP53 loss) ALCL and furthermore that it is superior to crizotinib as a second-line approach to the treatment of a standard chemotherapy relapsed/refractory ALCL PDX pointing to brigatinib as a future therapeutic option.

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Alessandri AJ, Pritchard SL, Schultz KR, Massing BG. A population‐based study of pediatric anaplastic large cell lymphoma. Cancer. 2002;94:1830–5. PubMed

Morris SW, Kirstein MN, Valentine MB, Dittmer KG, Shapiro DN, Saltman DL, et al. Fusion of a kinase gene, ALK, to a nucleolar protein gene, NPM, in non‐Hodgkin's lymphoma. Science. 1994;263:1281–4. PubMed

Brugières L, Le Deley M‐C, Rosolen A, Williams D, Horibe K, Wrobel G, et al. Impact of the methotrexate administration dose on the need for intrathecal treatment in children and adolescents with anaplastic large‐cell lymphoma: results of a randomized trial of the EICNHL group. J Clin Oncol. 2009;27:897–903. PubMed

Mussolin L, Le Deley M‐C, Carraro E, Damm‐Welk C, Attarbaschi A, Williams D, et al. Prognostic factors in childhood anaplastic large cell lymphoma: long term results of the international ALCL99 trial. Cancers (Basel). 2020;12:2747. PubMed PMC

Lowe EJ, Reilly AF, Lim MS, Gross TG, Saguilig L, Barkauskas DA, et al. Crizotinib in combination with chemotherapy for pediatric patients with ALK+ anaplastic large‐cell lymphoma: the results of Children's oncology group trial ANHL12P1. J Clin Oncol. 2022;41:2043–53. PubMed PMC

Brugières L, Quartier P, Le Deley MC, Pacquement H, Perel Y, Bergeron C, et al. Relapses of childhood anaplastic large‐cell lymphoma: treatment results in a series of 41 children—a report from the French Society of Pediatric Oncology. Ann Oncol. 2000;11:53–8. PubMed

Mori T, Takimoto T, Katano N, Kikuchi A, Tabuchi K, Kobayashi R, et al. Recurrent childhood anaplastic large cell lymphoma: a retrospective analysis of registered cases in Japan. Br J Haematol. 2006;132:594–7. PubMed

Knörr F, Brugières L, Pillon M, Zimmermann M, Ruf S, Attarbaschi A, et al. Stem cell transplantation and vinblastine monotherapy for relapsed pediatric anaplastic large cell lymphoma: results of the international, prospective ALCL‐relapse trial. J Clin Oncol. 2020;38:3999–4009. PubMed

Aparicio T, Cozic N, de la Fouchardière C, Meriaux E, Plaza J, Mineur L, et al. The activity of crizotinib in chemo‐refractory MET‐amplified esophageal and gastric adenocarcinomas: results from the AcSé‐crizotinib program. Target Oncol. 2021;16:381–8. PubMed PMC

Balis FM, Thompson PA, Mosse YP, Blaney SM, Minard CG, Weigel BJ, et al. First‐dose and steady‐state pharmacokinetics of orally administered crizotinib in children with solid tumors: a report on ADVL0912 from the Children's Oncology Group Phase 1/Pilot Consortium. Cancer Chemother Pharmacol. 2017;79:181–7. PubMed PMC

Mosse YP, Voss SD, Lim MS, Rolland D, Minard CG, Fox E, et al. Targeting ALK with crizotinib in pediatric anaplastic large cell lymphoma and inflammatory myofibroblastic tumor: a Children's Oncology Group Study. J Clin Oncol. 2017;35:3215–21. PubMed PMC

Mossé YP, Lim MS, Voss SD, Wilner K, Ruffner K, Laliberte J, et al. Safety and activity of crizotinib for paediatric patients with refractory solid tumours or anaplastic large‐cell lymphoma: a Children's Oncology Group Phase 1 Consortium Study. Lancet Oncol. 2013;14:472–80. PubMed PMC

Knörr F, Schellekens KPJ, Schoot RA, Landman‐Parker J, Teltschik H‐M, Förster J, et al. Combination therapy with crizotinib and vinblastine for relapsed or refractory pediatric ALK‐positive anaplastic large cell lymphoma. Haematologica. 2022;108:1442–6. 10.3324/haematol.2022.281896 PubMed DOI PMC

Gambacorti Passerini C, Farina F, Stasia A, Redaelli S, Ceccon M, Mologni L, et al. Crizotinib in advanced, chemoresistant anaplastic lymphoma kinase‐positive lymphoma patients. J Natl Cancer Inst. 2014;106:djt378. PubMed

Brugières L, Houot R, Cozic N, De La Fouchardière C, Morschhauser F, Brice P, et al. Crizotinib in advanced ALK+ anaplastic large cell lymphoma in children and adults: results of the Acs© phase II trial. Blood. 2017;130:2831.

Del Baldo G, Abbas R, Woessmann W, Horibe K, Pillon M, Burke A, et al. Neuro‐meningeal relapse in anaplastic large‐cell lymphoma: incidence, risk factors and prognosis—a report from the European intergroup for childhood non‐Hodgkin lymphoma. Br J Haematol. 2021;192:1039–48. PubMed

Gettinger SN, Huber RM, Kim D‐W, Bazhenova L, Hansen KH, Tiseo M, et al. Long‐term efficacy and safety of brigatinib in crizotinib‐refractory ALK+ NSCLC: final results of the phase 1/2 and randomized phase 2 (ALTA) trials. JTO Clin Res Rep. 2022;3:100385. PubMed PMC

Pfeifer W, Levi E, Petrogiannis‐Haliotis T, Lehmann L, Wang Z, Kadin ME. A murine xenograft model for human CD30+ anaplastic large cell lymphoma. Successful growth inhibition with an anti‐CD30 antibody (HeFi‐1). Am J Pathol. 1999;155:1353–9. PubMed PMC

Ng SY, Yoshida N, Christie AL, Ghandi M, Dharia NV, Dempster J, et al. Targetable vulnerabilities in T‐ and NK‐cell lymphomas identified through preclinical models. Nat Commun. 2018;9:2024. PubMed PMC

Mölder F, Jablonski KP, Letcher B, Hall MB, Tomkins‐Tinch CH, Sochat V, et al. Sustainable data analysis with snakemake. F1000Res. 2021;10:33. 10.12688/f1000research.29032.1 PubMed DOI PMC

DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, Hartl C, et al. A framework for variation discovery and genotyping using next‐generation DNA sequencing data. Nat Genet. 2011;43:491–8. PubMed PMC

Rigaud C, Abbou S, Minard‐Colin V, Geoerger B, Scoazec JY, Vassal G, et al. Efficacy of nivolumab in a patient with systemic refractory ALK+ anaplastic large cell lymphoma. Pediatr Blood Cancer. 2018;65:65. 10.1002/pbc.26902 PubMed DOI

Berlanga P, Pierron G, Lacroix L, Chicard M, Adam de Beaumais T, Marchais A, et al. The European MAPPYACTS trial: precision Medicine program in pediatric and adolescent patients with recurrent malignancies. Cancer Discov. 2022;12:1266–81. PubMed PMC

Krumbholz M, Woessmann W, Zierk J, Seniuk D, Ceppi P, Zimmermann M, et al. Characterization and diagnostic application of genomic NPM‐ALK fusion sequences in anaplastic large‐cell lymphoma. Oncotarget. 2018;9:26543–55. PubMed PMC

Chiarle R, Simmons WJ, Cai H, Dhall G, Zamo A, Raz R, et al. Stat3 is required for ALK‐mediated lymphomagenesis and provides a possible therapeutic target. Nat Med. 2005;11:623–9. PubMed

Choi YL, Soda M, Yamashita Y, Ueno T, Takashima J, Nakajima T, et al. EML4‐ALK mutations in lung cancer that confer resistance to ALK inhibitors. N Engl J Med. 2010;363:1734–9. PubMed

Rotow J, Bivona TG. Understanding and targeting resistance mechanisms in NSCLC. Nat Rev Cancer. 2017;17:637–58. PubMed

Monti P, Campomenosi P, Ciribilli Y, Iannone R, Inga A, Abbondandolo A, et al. Tumour P53 mutations exhibit promoter selective dominance over wild type P53. Oncogene. 2002;21:1641–8. PubMed

Malcikova J, Smardova J, Rocnova L, Tichy B, Kuglik P, Vranova V, et al. Monoallelic and biallelic inactivation of TP53 gene in chronic lymphocytic leukemia: selection, impact on survival, and response to DNA damage. Blood. 2009;114:5307–14. PubMed

Prokoph N, Probst NA, Lee LC, Monahan JM, Matthews JD, Liang H‐C, et al. IL10RA modulates crizotinib sensitivity in NPM1‐ALK+ anaplastic large cell lymphoma. Blood. 2020;136:1657–69. PubMed PMC

Larose H, Prokoph N, Matthews JD, Schlederer M, Högler S, Alsulami AF, et al. Whole exome sequencing reveals NOTCH1 mutations in anaplastic large cell lymphoma and points to NOTCH both as a key pathway and a potential therapeutic target. Haematologica. 2021;106:1693–704. PubMed PMC

Crescenzo R, Abate F, Lasorsa E, Tabbo' F, Gaudiano M, Chiesa N, et al. Convergent mutations and kinase fusions lead to oncogenic STAT3 activation in anaplastic large cell lymphoma. Cancer Cell. 2015;27:516–32. PubMed PMC

Lobello C, Tichy B, Bystry V, Radova L, Filip D, Mraz M, et al. STAT3 and TP53 mutations associate with poor prognosis in anaplastic large cell lymphoma. Leukemia. 2021;35:1500–5. PubMed PMC

Piao J, Sakurai N, Iwamoto S, Nishioka J, Nakatani K, Komada Y, et al. Functional studies of a novel germline P53 splicing mutation identified in a patient with Li‐Fraumeni‐like syndrome. Mol Carcinog. 2013;52:770–6. PubMed

Costa DB, Kobayashi S, Pandya SS, Yeo W‐L, Shen Z, Tan W, et al. CSF concentration of the anaplastic lymphoma kinase inhibitor crizotinib. J Clin Oncol Off J Am Soc Clin Oncol. 2011;29:e443–5. PubMed

Peters S, Camidge DR, Shaw AT, Gadgeel S, Ahn JS, Kim D‐W, et al. Alectinib versus crizotinib in untreated ALK‐positive non‐small‐cell lung cancer. New Engl J Med. 2017;377:829–38. PubMed

Hida T, Nokihara H, Kondo M, Kim YH, Azuma K, Seto T, et al. Alectinib versus crizotinib in patients with ALK‐positive non‐small‐cell lung cancer (J‐ALEX): an open‐label, randomised phase 3 trial. Lancet (London, England). 2017;390:29–39. PubMed

Shaw AT, Felip E, Bauer TM, Besse B, Navarro A, Postel‐Vinay S, et al. Lorlatinib in non‐small‐cell lung cancer with ALK or ROS1 rearrangement: an international, multicentre, open‐label, single‐arm first‐in‐man phase 1 trial. Lancet Oncol. 2017;18:1590–9. PubMed PMC

Kim D‐W, Tiseo M, Ahn M‐J, Reckamp KL, Hansen KH, Kim S‐W, et al. Brigatinib in patients with Crizotinib‐refractory anaplastic lymphoma kinase‐positive non‐small‐cell lung cancer: a randomized, multicenter phase II trial. J Clin Oncol. 2017;35:2490–8. PubMed

Rigaud C, Abbou S, Ducassou S, Simonin M, Mouel LL, Pereira V, et al. Profound and sustained response with next‐generation ALK inhibitors in patients with relapsed or progressive ALK‐positive anaplastic large cell lymphoma with central nervous system involvement. Haematologica. 2022;107:2255–60. PubMed PMC

Wada DA, Law ME, Hsi ED, DiCaudo DJ, Ma L, Lim MS, et al. Specificity of IRF4 translocations for primary cutaneous anaplastic large cell lymphoma: a multicenter study of 204 skin biopsies. Mod Pathol. 2011;24:596–605. PubMed PMC

Kim DH, Li S, Garces S, Xu J. Large B‐cell lymphoma with IRF4 rearrangement and follicular pattern: a differential diagnosis of follicular lymphoma. Hum Pathol Rep. 2022;27:300602.

Weilemann A, Grau M, Erdmann T, Merkel O, Sobhiafshar U, Anagnostopoulos I, et al. Essential role of IRF4 and MYC signaling for survival of anaplastic large cell lymphoma. Blood. 2015;125:124–32. PubMed

Bandini C, Pupuleku A, Spaccarotella E, Pellegrino E, Wang R, Vitale N, et al. IRF4 mediates the oncogenic effects of STAT3 in anaplastic large cell lymphomas. Cancer. 2018;10:21. PubMed PMC

Youssif C, Goldenbogen J, Hamoudi R, Carreras J, Viskaduraki M, Cui Y, et al. Genomic profiling of pediatric ALK‐positive anaplastic large cell lymphoma: a Children's Cancer and Leukaemia Group Study. Genes Chromosomes Cancer. 2009;48:1018–26. PubMed

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