PM060184, a new tubulin binding agent with potent antitumor activity including P-glycoprotein over-expressing tumors

Biochemical Pharmacology

Volumn 88, Issue 3, 2014, Pages 291-302

  Martínez Díez, Marta ^a   Guillén Navarro, María José ^a   Pera, Benet ^b,d   Bouchet, Benjamin Pierre ^c,e   Martínez Leal, Juan Fernando ^a   Barasoain, Isabel ^b   Cuevas, Carmen ^a   Andreu, Jose M ^b   García Fernández, Luis Francisco ^a   Díaz, J Fernando ^b   Avilés, Pablo ^a   Galmarini, Carlos M ^a  

^a PHARMAMAR S A   (Spain)

^b CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^c CENTRE LÉON BÉRARD   (France)

^d MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^e ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

Antimitotic agents; Cancer therapy; Microtubules; P glycoprotein; Polymerization inhibitors; Tubulin modulators

Indexed keywords

ANTINEOPLASTIC AGENT; MULTIDRUG RESISTANCE PROTEIN; PM 060184; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; BINDING AFFINITY; CANCER INHIBITION; CELL CULTURE; CELL CYCLE; CELL GROWTH; CELL MIGRATION; CHROMOSOME; CONTROLLED STUDY; DRUG POTENCY; DRUG STRUCTURE; FEMALE; FLOW CYTOMETRY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOFLUORESCENCE; METAPHASE; MICROTUBULE; MICROTUBULE ASSEMBLY; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROMETAPHASE; PROTEIN EXPRESSION; TUMOR REGRESSION; WOUND HEALING;

ANTIMITOTIC AGENTS; CANCER THERAPY; MICROTUBULES; P-GLYCOPROTEIN; POLYMERIZATION INHIBITORS; TUBULIN MODULATORS;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL MOVEMENT; CENTROSOME; FEMALE; INTERPHASE; MICE, NUDE; MICROTUBULES; P-GLYCOPROTEIN; POLYKETIDES; PROMETAPHASE; PYRONES; SPINDLE APPARATUS; TUBULIN MODULATORS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84897111969     PISSN: 00062952     EISSN: 18732968     Source Type: Journal    
DOI: 10.1016/j.bcp.2014.01.026     Document Type: Article

References (50)

1. V. Rodionov, E. Nadezhdina, and G. Borisy Centrosomal control of microtubule dynamics Proc Natl Acad Sci U S A 96 1999 115 120 (Pubitemid 29036062)
2. R.L. Margolis, and L. Wilson Microtubule treadmilling: what goes around comes around Bioessays 20 1998 830 836 (Pubitemid 28486019)
3. M.A. Jordan, K. Wendell, S. Gardiner, W.B. Derry, H. Copp, and L. Wilson Mitotic block induced in HeLa cells by low concentrations of paclitaxel (Taxol) results in abnormal mitotic exit and apoptotic cell death Cancer Res 56 1996 816 825 (Pubitemid 26055472)
4. E. Komlodi-Pasztor, D. Sackett, J. Wilkerson, and T. Fojo Mitosis is not a key target of microtubule agents in patient tumors Nat Rev Clin Oncol 8 2011 244 250
5. M.A. Jordan, and K. Kamath How do microtubule-targeted drugs work? An overview Curr Cancer Drug Targets 7 2007 730 742
6. A.D. Rudner, and A.W. Murray The spindle assembly checkpoint Curr Opin Cell Biol 8 1996 773 780 (Pubitemid 26399936)
7. A. Younes, A.K. Gopal, S.E. Smith, S.M. Ansell, J.D. Rosenblatt, and K.J. Savage et al. Results of a pivotal phase II study of brentuximab vedotin for patients with relapsed or refractory Hodgkin's lymphoma J Clin Oncol 30 2012 2183 2189
8. B. Pro, R. Advani, P. Brice, N.L. Bartlett, J.D. Rosenblatt, and T. Illidge et al. Brentuximab vedotin (SGN-35) in patients with relapsed or refractory systemic anaplastic large-cell lymphoma: results of a phase II study J Clin Oncol 30 2012 2190 2196
9. B.A. Teicher, and J.H. Doroshow The promise of antibody-drug conjugates N Engl J Med 367 2012 1847 1848
10. S. Verma, D. Miles, L. Gianni, I.E. Krop, M. Welslau, and J. Baselga et al. Trastuzumab emtansine for HER2-positive advanced breast cancer N Engl J Med 367 2012 1783 1791
11. U. Swami, I. Chaudhary, M.H. Ghalib, and S. Goel Eribulin - a review of preclinical and clinical studies Crit Rev Oncol Hematol 81 2012 163 184
12. B.P. Bouchet, and C.M. Galmarini Cabazitaxel, a new taxane with favorable properties Drugs Today (Barc) 46 2010 735 742
13. R.H. Alvarez, V. Valero, and G.N. Hortobagyi Ixabepilone for the treatment of breast cancer Ann Med 43 2011 477 486
14. M.J. Martín, L. Coello, R. Fernández, F. Reyes, A. Rodríguez, and C. Murcia et al. Isolation and first total synthesis of PM050489 and PM060184, two new marine anticancer compounds J Am Chem Soc 135 2013 10164 10171
15. B. Pera, I. Barasoain, A. Pantazopoulou, A. Canales, R. Matesanz, and J. Rodriguez-Salarichs et al. New interfacial microtubule inhibitors of marine origin, PM050489/PM060184, with potent antitumor activity and a distinct mechanism ACS Chem Biol 2013 10.1021/cb400461j (in press)
16. M. Hidalgo, A. Tolcher, A. Cubillo, D. Rasco, V. Boni, and A. Patnaik et al. Phase I, open-label, dose-escalating clinical and pharmacokinetic study of the novel antimicrotubulin agent PM060184 administered over 10 minutes on day 1 and 8 every three weeks to patients with advanced malignant solid tumors Eur J Cancer 49 2013 A888
17. J.P. Delord, E. Elez, C. Gomez Roca, C. Coronado, N. Lignon, and L. Martinez de Arenzana et al. First-in-man phase I, open-label, dose-escalating clinical and pharmacokinetic study of the novel antimicrotubulin agent PM060184 administered over 10 minutes on days 1, 8, and 15 every four weeks to patients with advanced malignant solid tumours Eur J Cancer 49 2013 A889
18. J.F. Leal, M. Martinez-Diez, V. Garcia-Hernandez, V. Moneo, A. Domingo, and J.A. Bueren-Calabuig et al. PM01183, a new DNA minor groove covalent binder with potent in vitro and in vivo anti-tumour activity Br J Pharmacol 161 2010 1099 1110
19. J.F. Leal, V. Garcia-Hernandez, V. Moneo, A. Domingo, J.A. Bueren-Calabuig, and A. Negri et al. Molecular pharmacology and antitumor activity of Zalypsis in several human cancer cell lines Biochem Pharmacol 78 2009 162 170
20. R.J. Kowalski, P. Giannakakou, S.P. Gunasekera, R.E. Longley, B.W. Day, and E. Hamel The microtubule-stabilizing agent discodermolide competitively inhibits the binding of paclitaxel (Taxol) to tubulin polymers, enhances tubulin nucleation reactions more potently than paclitaxel, and inhibits the growth of paclitaxel-resistant cells Mol Pharmacol 52 1997 613 622 (Pubitemid 27443983)
21. R. Matesanz, I. Barasoain, C.G. Yang, L. Wang, X. Li, and C. de Ines et al. Optimization of taxane binding to microtubules: binding affinity dissection and incremental construction of a high-affinity analog of paclitaxel Chem Biol 15 2008 573 585 (Pubitemid 351815058)
22. E. Calvo, I. Barasoain, R. Matesanz, B. Pera, E. Camafeita, and O. Pineda et al. Cyclostreptin derivatives specifically target cellular tubulin and further map the paclitaxel site Biochemistry 51 2012 329 341
23. R.M. Buey, I. Barasoain, E. Jackson, A. Meyer, P. Giannakakou, and I. Paterson et al. Microtubule interactions with chemically diverse stabilizing agents: thermodynamics of binding to the paclitaxel site predicts cytotoxicity Chem Biol 12 2005 1269 1279 (Pubitemid 41779467)
24. B.P. Bouchet, A. Puisieux, and C.M. Galmarini BetaIII-tubulin is required for interphase microtubule dynamics in untransformed human mammary epithelial cells Eur J Cell Biol 90 2011 872 878
25. B.P. Bouchet, J. Bertholon, N. Falette, C. Audoynaud, C. Lamblot, and A. Puisieux et al. Paclitaxel resistance in untransformed human mammary epithelial cells is associated with an aneuploidy-prone phenotype Br J Cancer 97 2007 1218 1224 (Pubitemid 350035797)
26. R.M. Buey, E. Calvo, I. Barasoain, O. Pineda, M.C. Edler, and R. Matesanz et al. Cyclostreptin binds covalently to microtubule pores and lumenal taxoid binding sites Nat Chem Biol 3 2007 117 125 (Pubitemid 46134999)
27. T. Beckers, and S. Mahoobi Natural, semisynthetic and synthetic microtubule inhibitors for cancer therapy Drugs Fut 28 2003 767 785 (Pubitemid 37345316)
28. G. Attard, A. Greystoke, S. Kaye, and J. De Bono Update on tubulin-binding agents Pathol Biol (Paris) 54 2006 72 84
29. D.G. Kingston Tubulin-interactive natural products as anticancer agents J Nat Prod 72 2009 507 515
30. J.A. Smith, L. Wilson, O. Azarenko, X. Zhu, B.M. Lewis, and B.A. Littlefield et al. Eribulin binds at microtubule ends to a single site on tubulin to suppress dynamic instability Biochemistry 49 2010 1331 1337
31. P.H. Alday, and J.J. Correia Macromolecular interaction of halichondrin B analogues eribulin (E7389) and ER-076349 with tubulin by analytical ultracentrifugation Biochemistry 48 2009 7927 7938
32. M.C. Lo, A. Aulabaugh, G. Krishnamurthy, J. Kaplan, A. Zask, and R.P. Smith et al. Probing the interaction of HTI-286 with tubulin using a stilbene analogue J Am Chem Soc 126 2004 9898 9899 (Pubitemid 39079391)
33. M.M. Wagner, D.C. Paul, C. Shih, M.A. Jordan, L. Wilson, and D.C. Williams In vitro pharmacology of cryptophycin 52 (LY355703) in human tumor cell lines Cancer Chemother Pharmacol 43 1999 115 125 (Pubitemid 29045028)
34. M.J. Towle, K.A. Salvato, J. Budrow, B.F. Wels, G. Kuznetsov, and K.K. Aalfs et al. In vitro and in vivo anticancer activities of synthetic macrocyclic ketone analogues of halichondrin B Cancer Res 61 2001 1013 1021 (Pubitemid 32174419)
35. M. Beckwith, W.J. Urba, and D.L. Longo Growth inhibition of human lymphoma cell lines by the marine products, dolastatins 10 and 15 J Natl Cancer Inst 85 1993 483 488 (Pubitemid 23084094)
36. J.F. Diaz, and R.M. Buey Characterizing ligand-microtubule binding by competition methods Methods Mol Med 137 2007 245 260
37. M.A. Jordan, K. Kamath, T. Manna, T. Okouneva, H.P. Miller, and C. Davis et al. The primary antimitotic mechanism of action of the synthetic halichondrin E7389 is suppression of microtubule growth Mol Cancer Ther 4 2005 1086 1095 (Pubitemid 41079102)
38. D. Panda, K. DeLuca, D. Williams, M.A. Jordan, and L. Wilson Antiproliferative mechanism of action of cryptophycin-52: kinetic stabilization of microtubule dynamics by high-affinity binding to microtubule ends Proc Natl Acad Sci U S A 95 1998 9313 9318 (Pubitemid 28506228)
39. J.G. Chen, and S.B. Horwitz Differential mitotic responses to microtubule-stabilizing and -destabilizing drugs Cancer Res 62 2002 1935 1938 (Pubitemid 34408432)
40. M.A. Jordan, D. Thrower, and L. Wilson Effects of vinblastine, podophyllotoxin and nocodazole on mitotic spindles. Implications for the role of microtubule dynamics in mitosis J Cell Sci 102 Pt 3 1992 401 416
41. C. Sellitto, and R. Kuriyama Distribution of pericentriolar material in multipolar spindles induced by colcemid treatment in Chinese hamster ovary cells J Cell Sci 89 Pt 1 1988 57 65 (Pubitemid 18069292)
42. T.J. Mitchison The role of microtubule polarity in the movement of kinesin and kinetochores J Cell Sci Suppl 5 1986 121 128
43. T.J. Mitchison Polewards microtubule flux in the mitotic spindle: evidence from photoactivation of fluorescence J Cell Biol 109 1989 637 652 (Pubitemid 19197026)
44. R.B. Nicklas The forces that move chromosomes in mitosis Annu Rev Biophys Biophys Chem 17 1988 431 449
45. L.E. Klein, B.S. Freeze, A.B. Smith 3rd, and S.B. Horwitz The microtubule stabilizing agent discodermolide is a potent inducer of accelerated cell senescence Cell Cycle 4 2005 501 507 (Pubitemid 41359741)
46. M.V. Blagosklonny, R. Robey, M.S. Sheikh, and T. Fojo Paclitaxel-induced FasL-independent apoptosis and slow (non-apoptotic) cell death Cancer Biol Ther 1 2002 113 117
47. L.E. Broker, C. Huisman, C.G. Ferreira, J.A. Rodriguez, F.A. Kruyt, and G. Giaccone Late activation of apoptotic pathways plays a negligible role in mediating the cytotoxic effects of discodermolide and epothilone B in non-small cell lung cancer cells Cancer Res 62 2002 4081 4088 (Pubitemid 34791078)
48. C. Huisman, C.G. Ferreira, L.E. Broker, J.A. Rodriguez, E.F. Smit, and P.E. Postmus et al. Paclitaxel triggers cell death primarily via caspase-independent routes in the non-small cell lung cancer cell line NCI-H460 Clin Cancer Res 8 2002 596 606 (Pubitemid 34193982)
49. S.K. Chao, S.B. Horwitz, and H.M. McDaid Insights into 4E-BP1 and p53 mediated regulation of accelerated cell senescence Oncotarget 2 2011 89 98
50. S.K. Chao, J. Lin, J. Brouwer-Visser, A.B. Smith 3rd, S.B. Horwitz, and H.M. McDaid Resistance to discodermolide, a microtubule-stabilizing agent and senescence inducer, is 4E-BP1-dependent Proc Natl Acad Sci U S A 108 2011 391 396