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PMID: 25326666 Published · ppublish English Journal Article

A highly potent and selective Vps34 inhibitor alters vesicle trafficking and autophagy.

Nature chemical biology ·Vol. 10 ·No. 12 ·2014-12-00 ·Pages 1013-9

Ronan B, Flamand O, Vescovi L, Dureuil C, Durand L, Fassy F, Bachelot MF, Lamberton A, Mathieu M, Bertrand T, Marquette JP, El-Ahmad Y, Filoche-Romme B, Schio L, Garcia-Echeverria C, Goulaouic H, Pasquier B

Abstract

Vps34 is a phosphoinositide 3-kinase (PI3K) class III isoform that has attracted major attention over the recent years because of its role in autophagy. Herein we describe the biological characterization of SAR405, which is a low-molecular-mass kinase inhibitor of Vps34 (KD 1.5 nM). This compound has an exquisite protein and lipid kinase selectivity profile that is explained by its unique binding mode and molecular interactions within the ATP binding cleft of human Vps34. To the best of our knowledge, this is the first potent and specific Vps34 inhibitor described so far. Our results demonstrate that inhibition of Vps34 kinase activity by SAR405 affects both late endosome-lysosome compartments and prevents autophagy. Moreover, we show that the concomitant inhibition of Vps34 and mTOR, with SAR405 and the US Food and Drug Administration-approved mTOR inhibitor everolimus, results in synergistic antiproliferative activity in renal tumor cell lines, indicating a potential clinical application in cancer.

MeSH Terms
Adenosine Triphosphate/chemistry,metabolism Antineoplastic Agents/chemical synthesis,pharmacology Autophagy/drug effects,genetics Catalytic Domain Cell Line, Tumor Cell Proliferation/drug effects Class III Phosphatidylinositol 3-Kinases/antagonists & inhibitors,chemistry,genetics Drug Synergism Endosomes/drug effects,metabolism Everolimus Gene Expression Humans Kidney/enzymology,pathology Kinetics Lysosomes/drug effects,metabolism Molecular Docking Simulation Protein Kinase Inhibitors/chemical synthesis,pharmacology Pyridines/chemical synthesis,pharmacology Pyrimidinones/chemical synthesis,pharmacology Recombinant Proteins/chemistry,genetics Signal Transduction Sirolimus/analogs & derivatives,chemical synthesis,pharmacology TOR Serine-Threonine Kinases/antagonists & inhibitors,chemistry,genetics
Chemicals
Antineoplastic Agents Protein Kinase Inhibitors Pyridines Pyrimidinones Recombinant Proteins SAR405 Adenosine Triphosphate Everolimus MTOR protein, human Class III Phosphatidylinositol 3-Kinases TOR Serine-Threonine Kinases Sirolimus
Authors & Affiliations
17 authors, click to expand affiliations / ORCID
Ronan Baptiste
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Flamand Odile
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Vescovi Lionel
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Dureuil Christine
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Durand Laurence
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Fassy Florence
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Bachelot Marie-France
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Lamberton Annabelle
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Mathieu Magali
Structure, Design and Informatics, Sanofi, Vitry Sur Seine, France..
Bertrand Thomas
Structure, Design and Informatics, Sanofi, Vitry Sur Seine, France..
Marquette Jean-Pierre
Structure, Design and Informatics, Sanofi, Vitry Sur Seine, France..
El-Ahmad Youssef
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Filoche-Romme Bruno
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Schio Laurent
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Garcia-Echeverria Carlos
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Goulaouic Hélène
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
Pasquier Benoit
Oncology Drug Discovery, Sanofi, Vitry Sur Seine, France.
References (53)
53 references, click to expand
  1. p62/SQSTM1/A170: physiology and pathology.
    Pharmacol Res. 2012 Dec;66(6):457-62 PMID: 22841931
  2. Loss of Tsc1/Tsc2 activates mTOR and disrupts PI3K-Akt signaling through downregulation of PDGFR.
    J Clin Invest. 2003 Oct;112(8):1223-33 PMID: 14561707
  3. Cellular functions of phosphatidylinositol 3-phosphate and FYVE domain proteins.
    Biochem J. 2001 Apr 15;355(Pt 2):249-58 PMID: 11284710
  4. Methods in mammalian autophagy research.
    Cell. 2010 Feb 5;140(3):313-26 PMID: 20144757
  5. Features and development of Coot.
    Acta Crystallogr D Biol Crystallogr. 2010 Apr;66(Pt 4):486-501 PMID: 20383002
  6. Regulation of membrane traffic by phosphoinositide 3-kinases.
    J Cell Sci. 2006 Feb 15;119(Pt 4):605-14 PMID: 16467569
  7. Autophagy in human health and disease.
    N Engl J Med. 2013 Feb 14;368(7):651-62 PMID: 23406030
  8. Cathepsin D: a cellular roadmap.
    Biochem Biophys Res Commun. 2008 Nov 7;376(1):5-9 PMID: 18762174
  9. Deletion of PIK3C3/Vps34 in sensory neurons causes rapid neurodegeneration by disrupting the endosomal but not the autophagic pathway.
    Proc Natl Acad Sci U S A. 2010 May 18;107(20):9424-9 PMID: 20439739
  10. Myotubularin phosphoinositide phosphatases: cellular functions and disease pathophysiology.
    Trends Mol Med. 2012 Jun;18(6):317-27 PMID: 22578719
  11. mTOR signaling in growth control and disease.
    Cell. 2012 Apr 13;149(2):274-93 PMID: 22500797
  12. Allosteric and ATP-competitive kinase inhibitors of mTOR for cancer treatment.
    Bioorg Med Chem Lett. 2010 Aug 1;20(15):4308-12 PMID: 20561789
  13. Surface comparison of active and inactive protein kinases identifies a conserved activation mechanism.
    Proc Natl Acad Sci U S A. 2006 Nov 21;103(47):17783-8 PMID: 17095602
  14. Identifying Small Molecules which Inhibit Autophagy: a Phenotypic Screen Using Image-Based High-Content Cell Analysis.
    Curr Chem Genom Transl Med. 2014 Feb 07;8(Suppl 1):3-15 PMID: 24596680
  15. Design and analysis of drug combination experiments.
    Biom J. 2005 Jun;47(3):299-308 PMID: 16053254
  16. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids.
    Nucleic Acids Res. 2007 Jul;35(Web Server issue):W375-83 PMID: 17452350
  17. Characterization of VPS34, a gene required for vacuolar protein sorting and vacuole segregation in Saccharomyces cerevisiae.
    Mol Cell Biol. 1990 Dec;10(12):6742-54 PMID: 2247081
  18. The emerging mechanisms of isoform-specific PI3K signalling.
    Nat Rev Mol Cell Biol. 2010 May;11(5):329-41 PMID: 20379207
  19. Guidelines for the use and interpretation of assays for monitoring autophagy.
    Autophagy. 2012 Apr;8(4):445-544 PMID: 22966490
  20. Discovery and optimization of new benzimidazole- and benzoxazole-pyrimidone selective PI3Kβ inhibitors for the treatment of phosphatase and TENsin homologue (PTEN)-deficient cancers.
    J Med Chem. 2012 May 24;55(10):4788-805 PMID: 22524426
  21. Autophagy fights disease through cellular self-digestion.
    Nature. 2008 Feb 28;451(7182):1069-75 PMID: 18305538
  22. A genome-wide siRNA screen reveals multiple mTORC1 independent signaling pathways regulating autophagy under normal nutritional conditions.
    Dev Cell. 2010 Jun 15;18(6):1041-52 PMID: 20627085
  23. The class III kinase Vps34 promotes T lymphocyte survival through regulating IL-7Rα surface expression.
    J Immunol. 2011 Nov 15;187(10):5051-61 PMID: 22021616
  24. Optimization of potent and selective dual mTORC1 and mTORC2 inhibitors: the discovery of AZD8055 and AZD2014.
    Bioorg Med Chem Lett. 2013 Mar 1;23(5):1212-6 PMID: 23375793
  25. Mammalian phosphoinositide kinases and phosphatases.
    Prog Lipid Res. 2009 Nov;48(6):307-43 PMID: 19580826
  26. Imidazo[4,5-c]quinolines as inhibitors of the PI3K/PKB-pathway.
    Bioorg Med Chem Lett. 2008 Feb 1;18(3):1027-30 PMID: 18248814
  27. The mammalian class 3 PI3K (PIK3C3) is required for early embryogenesis and cell proliferation.
    PLoS One. 2011 Jan 20;6(1):e16358 PMID: 21283715
  28. Impaired autophagy, defective T cell homeostasis, and a wasting syndrome in mice with a T cell-specific deletion of Vps34.
    J Immunol. 2013 May 15;190(10):5086-101 PMID: 23596309
  29. Rapamycin passes the torch: a new generation of mTOR inhibitors.
    Nat Rev Drug Discov. 2011 Oct 31;10(11):868-80 PMID: 22037041
  30. Phospholipase D and mTORC1: nutrients are what bring them together.
    Sci Signal. 2012 Mar 27;5(217):pe13 PMID: 22457329
  31. The role of PI3P phosphatases in the regulation of autophagy.
    FEBS Lett. 2010 Apr 2;584(7):1313-8 PMID: 20188094
  32. The Beclin 1-VPS34 complex--at the crossroads of autophagy and beyond.
    Trends Cell Biol. 2010 Jun;20(6):355-62 PMID: 20356743
  33. Mechanistic similarities in docking of the FYVE and PX domains to phosphatidylinositol 3-phosphate containing membranes.
    Prog Lipid Res. 2007 Nov;46(6):315-27 PMID: 17707914
  34. The mRNA surveillance protein hSMG-1 functions in genotoxic stress response pathways in mammalian cells.
    Mol Cell. 2004 Jun 4;14(5):585-98 PMID: 15175154
  35. Localization of phosphatidylinositol 3-phosphate in yeast and mammalian cells.
    EMBO J. 2000 Sep 1;19(17):4577-88 PMID: 10970851
  36. Data processing and analysis with the autoPROC toolbox.
    Acta Crystallogr D Biol Crystallogr. 2011 Apr;67(Pt 4):293-302 PMID: 21460447
  37. The role of lipids in the control of autophagy.
    Curr Biol. 2013 Jan 7;23(1):R33-45 PMID: 23305670
  38. How good are my data and what is the resolution?
    Acta Crystallogr D Biol Crystallogr. 2013 Jul;69(Pt 7):1204-14 PMID: 23793146
  39. In situ kinase profiling reveals functionally relevant properties of native kinases.
    Chem Biol. 2011 Jun 24;18(6):699-710 PMID: 21700206
  40. Autophagy modulation as a potential therapeutic target for diverse diseases.
    Nat Rev Drug Discov. 2012 Sep;11(9):709-30 PMID: 22935804
  41. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy.
    Cell. 2013 Jan 17;152(1-2):290-303 PMID: 23332761
  42. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase.
    Nat Cell Biol. 2013 Jul;15(7):741-50 PMID: 23685627
  43. The p110 delta structure: mechanisms for selectivity and potency of new PI(3)K inhibitors.
    Nat Chem Biol. 2010 Feb;6(2):117-24 PMID: 20081827
  44. Time-resolved ultrastructural detection of phosphatidylinositol 3-phosphate.
    J Histochem Cytochem. 2010 Nov;58(11):1025-32 PMID: 20713985
  45. Deconvoluting the context-dependent role for autophagy in cancer.
    Nat Rev Cancer. 2012 Apr 26;12(6):401-10 PMID: 22534666
  46. Canonical and non-canonical autophagy: variations on a common theme of self-eating?
    Nat Rev Mol Cell Biol. 2011 Dec 14;13(1):7-12 PMID: 22166994
  47. Emerging regulation and functions of autophagy.
    Nat Cell Biol. 2013 Jul;15(7):713-20 PMID: 23817233
  48. Canonical autophagy dependent on the class III phosphoinositide-3 kinase Vps34 is required for naive T-cell homeostasis.
    Proc Natl Acad Sci U S A. 2012 May 29;109(22):8670-5 PMID: 22592798
  49. Shaping development of autophagy inhibitors with the structure of the lipid kinase Vps34.
    Science. 2010 Mar 26;327(5973):1638-42 PMID: 20339072
  50. The autophagosome: origins unknown, biogenesis complex.
    Nat Rev Mol Cell Biol. 2013 Dec;14(12):759-74 PMID: 24201109
  51. The regulation and function of Class III PI3Ks: novel roles for Vps34.
    Biochem J. 2008 Feb 15;410(1):1-17 PMID: 18215151
  52. Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function.
    Proc Natl Acad Sci U S A. 2012 Feb 7;109(6):2003-8 PMID: 22308354
  53. Gene silencing reveals a specific function of hVps34 phosphatidylinositol 3-kinase in late versus early endosomes.
    J Cell Sci. 2006 Apr 1;119(Pt 7):1219-32 PMID: 16522686
Article Info
Journal
Nature chemical biology
Abbr.
Nat Chem Biol
ISSN
1552-4469
Published
2014-12-00
Epub
2014-00-19
Pages
1013-9
Language
English
Region
United States
NLM ID
101231976
Subset
IM
Databases
PDB
Analysis Services
Analysis Services

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