Novel insights into the mechanism of action of lenalidomide

OncoImmunology

Volumn 3, Issue 2, 2014, Pages

  Semeraro, Michaela ^a,b   Galluzzi, Lorenzo ^a,c,d  

^a INSTITUT GUSTAVE ROUSSY   (France)

^b INSERM   (France)

^c CENTRE DE RECHERCHE DES CORDELIERS   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

Author keywords

Apoptosis; Cereblon; IKZF1; IKZF3; IMiD; Thalidomide

Indexed keywords

CEREBLON; DEXAMETHASONE; IKAROS TRANSCRIPTION FACTOR; LENALIDOMIDE; POMALIDOMIDE; THALIDOMIDE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ANTINEOPLASTIC ACTIVITY; CANCER CELL; CELL PROLIFERATION; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG SAFETY; DRUG TARGETING; EDITORIAL; EMBRYOTOXICITY; FOOD AND DRUG ADMINISTRATION; HUMAN; MULTIPLE MYELOMA; NONHUMAN; TERATOGENICITY;

EID: 84899051541     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/onci.28386     Document Type: Editorial

References (33)

1. Dimopoulos M, Spencer A, Attal M, Prince HM, Harousseau JL, Dmoszynska A, San Miguel J, Hellmann A, Facon T, Foà R, et al.; Multiple Myeloma (010) Study Investigators. Lenalidomide plus dexamethasone for relapsed or refractory multiple myeloma. N Engl J Med 2007; 357:2123-32; PMID:18032762; http://dx.doi.org/10.1056/NEJMoa070594.
2. Weber DM, Chen C, Niesvizky R, Wang M, Belch A, Stadtmauer EA, Siegel D, Borrello I, Rajkumar SV, Chanan-Khan AA, et al.; Multiple Myeloma (009) Study Investigators. Lenalidomide plus dexamethasone for relapsed multiple myeloma in North America. N Engl J Med 2007; 357:2133-42; PMID:18032763; http://dx.doi.org/10.1056/NEJMoa070596.
3. Qian J, Yi Q. DKK1 as a novel target for myeloma immunotherapy. Oncoimmunology 2012; 1:756-8; PMID:22934273; http://dx.doi.org/10.4161/onci.19655.
4. List A, Dewald G, Bennett J, Giagounidis A, Raza A, Feldman E, Powell B, Greenberg P, Thomas D, Stone R, et al.; Myelodysplastic Syndrome-003 Study Investigators. Lenalidomide in the myelodysplastic syndrome with chromosome 5q deletion. N Engl J Med 2006; 355:1456-65; PMID:17021321; http://dx.doi.org/10.1056/NEJMoa061292.
5. List A, Kurtin S, Roe DJ, Buresh A, Mahadevan D, Fuchs D, Rimsza L, Heaton R, Knight R, Zeldis JB. Efficacy of lenalidomide in myelodysplastic syndromes. N Engl J Med 2005; 352:549-57; PMID:15703420; http://dx.doi.org/10.1056/NEJMoa041668.
6. Mailloux AW, Epling-Burnette PK. Effector memory regulatory T-cell expansion marks a pivotal point of immune escape in myelodysplastic syndromes. Oncoimmunology 2013; 2:e22654; PMID:23524348; http://dx.doi.org/10.4161/onci.22654.
7. Curran WJ. The thalidomide tragedy in Germany: the end of a historic medicolegal trial. N Engl J Med 1971; 284:481-2; PMID:5100423; http://dx.doi. org/10.1056/NEJM197103042840906.
8. Bwire R, Freeman J, Houn F. Managing the teratogenic risk of thalidomide and lenalidomide: an industry perspective. Expert Opin Drug Saf 2011; 10:3-8; PMID:21121869; http://dx.doi.org/10.1517/14740338.2011.527331.
9. Christian MS, Laskin OL, Sharper V, Hoberman A, Stirling DI, Latriano L. Evaluation of the developmental toxicity of lenalidomide in rabbits. Birth Defects Res B Dev Reprod Toxicol 2007; 80:188-207; PMID:17570132; http://dx.doi. org/10.1002/bdrb.20115.
10. Sharma RA, Steward WP, Daines CA, Knight RD, O'Byrne KJ, Dalgleish AG. Toxicity profile of the immunomodulatory thalidomide analogue, lenalidomide: phase I clinical trial of three dosing schedules in patients with solid malignancies. Eur J Cancer 2006; 42:2318-25; PMID:16899362; http://dx.doi.org/10.1016/j.ejca.2006.05.018.
11. Singhal S, Mehta J, Desikan R, Ayers D, Roberson P, Eddlemon P, Munshi N, Anaissie E, Wilson C, Dhodapkar M, et al. Antitumor activity of thalidomide in refractory multiple myeloma. N Engl J Med 1999; 341:1565-71; PMID:10564685; http://dx.doi.org/10.1056/NEJM199911183412102.
12. Leleu X, Attal M, Arnulf B, Moreau P, Traulle C, Marit G, Mathiot C, Petillon MO, Macro M, Roussel M, et al.; Intergroupe Francophone du Myélome. Pomalidomide plus low-dose dexamethasone is active and well tolerated in bortezomib and lenalidomiderefractory multiple myeloma: Intergroupe Francophone du Myélome 2009-02. Blood 2013; 121:1968-75; PMID:23319574; http://dx.doi. org/10.1182/blood-2012-09-452375.
13. Richardson PG, Siegel D, Baz R, Kelley SL, Munshi NC, Laubach J, Sullivan D, Alsina M, Schlossman R, Ghobrial IM, et al. Phase 1 study of pomalidomide MTD, safety, and efficacy in patients with refractory multiple myeloma who have received lenalidomide and bortezomib. Blood 2013; 121:1961-7; PMID:23243282; http://dx.doi.org/10.1182/blood-2012-08-450742.
14. Mahony C, Erskine L, Niven J, Greig NH, Fig. WD, Vargesson N. Pomalidomide is nonteratogenic in chicken and zebrafish embryos and nonneurotoxic in vitro. Proc Natl Acad Sci U S A 2013; 110:12703-8; PMID:23858438; http://dx.doi.org/10.1073/pnas.1307684110.
15. Davies F, Baz R. Lenalidomide mode of action: linking bench and clinical findings. Blood Rev 2010; 24(Suppl 1):S13-9; PMID:21126632; http://dx.doi. org/10.1016/S0268-960X(10)70004-7.
16. Hsu A, Ritchie DS, Neeson P. Are the immunostimulatory properties of Lenalidomide extinguished by co-administration of Dexamethasone? Oncoimmunology 2012; 1:372-4; PMID:22737619; http://dx.doi.org/10.4161/onci.18963.
17. Martiniani R, Di Loreto V, Di Sano C, Lombardo A, Liberati AM. Biological activity of lenalidomide and its underlying therapeutic effects in multiple myeloma. Adv Hematol 2012; 2012:842945; PMID:22919394; http://dx.doi.org/10.1155/2012/842945.
18. Semeraro M, Vacchelli E, Eggermont A, Galon J, Zitvogel L, Kroemer G, Galluzzi L. Trial Watch: Lenalidomide-based immunochemotherapy. Oncoimmunology 2013; 2:e2OK6494; PMID:24482747; http://dx.doi.org/10.4161/onci.26494.
19. Viel S, Charrier E, Marçais A, Rouzaire P, Bienvenu J, Karlin L, Salles G, Walzer T. Monitoring NK cell activity in patients with hematological malignancies. Oncoimmunology 2013; 2:e26011; PMID:24327939; http://dx.doi.org/10.4161/onci.26011.
20. McDaniel JM, Pinilla-Ibarz J, Epling-Burnette PK. Molecular action of lenalidomide in lymphocytes and hematologic malignancies. Adv Hematol 2012; 2012:513702; PMID:22888354; http://dx.doi. org/10.1155/2012/513702.
21. McMillin DW, Mitsiades CS. High-throughput approaches to discover novel immunomodulatory agents for cancer. Oncoimmunology 2012; 1:1406-8; PMID:23243609; http://dx.doi.org/10.4161/onci.21058.
22. Ito T, Ando H, Suzuki T, Ogura T, Hotta K, Imamura Y, Yamaguchi Y, Handa H. Identification of a primary target of thalidomide teratogenicity. Science 2010; 327:1345-50; PMID:20223979; http://dx.doi. org/10.1126/science.1177319.
23. Ito T, Ando H, Handa H. Teratogenic effects of thalidomide: molecular mechanisms. Cell Mol Life Sci 2011; 68:1569-79; PMID:21207098; http://dx.doi.org/10.1007/s00018-010-0619-9.
24. Lopez-Girona A, Mendy D, Ito T, Miller K, Gandhi AK, Kang J, Karasawa S, Carmel G, Jackson P, Abbasian M, et al. Cereblon is a direct protein target for immunomodulatory and antiproliferative activities of lenalidomide and pomalidomide. Leukemia 2012; 26:2326-35; PMID:22552008; http://dx.doi.org/10.1038/leu.2012.119.
25. Zhu YX, Braggio E, Shi CX, Bruins LA, Schmidt JE, Van Wier S, Chang XB, Bjorklund CC, Fonseca R, Bergsagel PL, et al. Cereblon expression is required for the antimyeloma activity of lenalidomide and pomalidomide. Blood 2011; 118:4771-9; PMID:21860026; http://dx.doi.org/10.1182/blood-2011-05-356063.
26. Krönke J, Udeshi ND, Narla A, Grauman P, Hurst SN, McConkey M, Svinkina T, Heckl D, Comer E, Li X, et al. Lenalidomide causes selective degradation of IKZF1 and IKZF3 in multiple myeloma cells. Science 2014; 343:301-5; PMID:24292625; http://dx.doi.org/10.1126/science.1244851.
27. Lu G, Middleton RE, Sun H, Naniong M, Ott CJ, Mitsiades CS, Wong KK, Bradner JE, Kaelin WG Jr. The myeloma drug lenalidomide promotes the cereblon-dependent destruction of Ikaros proteins. Science 2014; 343:305-9; PMID:24292623; http://dx.doi.org/10.1126/science.1244917.
28. Lopez-Girona A, Heintel D, Zhang LH, Mendy D, Gaidarova S, Brady H, Bartlett JB, Schafer PH, Schreder M, Bolomsky A, et al. Lenalidomide downregulates the cell survival factor, interferon regulatory factor-4, providing a potential mechanistic link for predicting response. Br J Haematol 2011; 154:325-36; PMID:21707574; http://dx.doi. org/10.1111/j.1365-2141.2011.08689.x.
29. Li S, Pal R, Monaghan SA, Schafer P, Ouyang H, Mapara M, Galson DL, Lentzsch S. IMiD immunomodulatory compounds block C/EBPbeta translation through eIF4E down-regulation resulting in inhibition of MM. Blood 2011; 117:5157-65; PMID:21389327; http://dx.doi.org/10.1182/blood-2010-10-314278.
30. Vacchelli E, Eggermont A, Fridman WH, Galon J, Zitvogel L, Kroemer G, Galluzzi L. Trial Watch: Immunostimulatory cytokines. Oncoimmunology 2013; 2:e24850; PMID:24073369; http://dx.doi. org/10.4161/onci.24850.
31. Vacchelli E, Galluzzi L, Eggermont A, Galon J, Tartour E, Zitvogel L, Kroemer G. Trial Watch: Immunostimulatory cytokines. Oncoimmunology 2012; 1:493-506; PMID:22754768; http://dx.doi. org/10.4161/onci.20459.
32. Zitvogel L, Galluzzi L, Smyth MJ, Kroemer G. Mechanism of action of conventional and targeted anticancer therapies: reinstating immunosurveillance. Immunity 2013; 39:74-88; PMID:23890065; http://dx.doi.org/10.1016/j.immuni.2013.06.014.
33. Galluzzi L, Senovilla L, Zitvogel L, Kroemer G. The secret al.y: immunostimulation by anticancer drugs. Nat Rev Drug Discov 2012; 11:215-33; PMID:22301798; http://dx.doi.org/10.1038/nrd3626.