Cdc-like/dual-specificity tyrosine phosphorylation-regulated kinases inhibitor leucettine l41 induces mtor-dependent autophagy: Implication for alzheimer's disease

Molecular Pharmacology

Volumn 85, Issue 3, 2014, Pages 441-450

  Fant, Xavier ^a   Durieu, Emilie ^a   Chicanne, Gaëtan ^b   Payrastre, Bernard ^b   Sbrissa, Diego ^c   Shisheva, Assia ^c   Limanton, Emmanuelle ^d   Carreaux, Francois ^d   Bazureau, Jean Pierre ^d   Meijer, Laurent ^e  

^a CNRS   (France)

^b University Hospital of Toulouse   (France)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITÉ DE RENNES 1   (France)

^e ManRos Therapeutics   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALZHEIMER DISEASE; ANIMALS; AUTOPHAGY; CELL LINE; CELL LINE, TUMOR; DIOXOLES; ENZYME INHIBITORS; HUMANS; IMIDAZOLES; MICE; MICROTUBULE-ASSOCIATED PROTEINS; OSTEOSARCOMA; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; TOR SERINE-THREONINE KINASES; TYROSINE;

EID: 84894090606     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.090837     Document Type: Article

References (60)

1. Allende-Vega N, Dayal S, Agarwala U, Sparks A, Bourdon JC, and Saville MK (2013) p53 is activated in response to disruption of the pre-mRNA splicing machinery. Oncogene 32:1-14.
2. Bettayeb K, Oumata N, Echalier A, Ferandin Y, Endicott JA, Galons H, and Meijer L (2008) CR8, a potent and selective, roscovitine-derived inhibitor of cyclindependent kinases. Oncogene 27:5797-5807.
3. Biamonti G and Caceres JF (2009) Cellular stress and RNA splicing. Trends Biochem Sci 34:146-153.
4. Blencowe BJ (2006) Alternative splicing: New insights from global analyses. Cell 126: 37-47.
5. Boland B, Kumar A, Lee S, Platt FM, Wegiel J, Yu WH, and Nixon RA (2008) Autophagy induction and autophagosome clearance in neurons: Relationship to autophagic pathology in Alzheimer's disease. J Neurosci 28:6926-6937.
6. Bonnal S, Vigevani L, and Valcárcel J (2012) The spliceosome as a target of novel antitumour drugs. Nat Rev Drug Discov 11:847-859.
7. Caccamo A, Majumder S, Richardson A, Strong R, and Oddo S (2010) Molecular interplay between mammalian target of rapamycin (mTOR), amyloid-beta, and Tau: Effects on cognitive impairments. J Biol Chem 285:13107-13120.
8. Chan EY, Kir S, and Tooze SA (2007) siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J Biol Chem 282:25464-25474.
9. Chicanne G, Severin S, Boscheron C, Terrisse AD, Gratacap MP, Gaits-Iacovoni F, Tronchère H, and Payrastre B (2012) A novel mass assay to quantify the bioactive lipid PtdIns3P in various biological samples. Biochem J 447:17-23.
10. Congdon EE, Wu JW, Myeku N, Figueroa YH, Herman M, Marinec PS, Gestwicki JE, Dickey CA, Yu WH, and Duff KE (2012) Methylthioninium chloride (methylene blue) induces autophagy and attenuates tauopathy in vitro and in vivo. Autophagy 8:609-622.
11. Debdab M, Carreaux F, Renault S, Soundararajan M, Fedorov O, Filippakopoulos P, Lozach O, Babault L, Tahtouh T, and Baratte B et al. (2011) Leucettines, a class of potent inhibitors of cdc2-like kinases and dual specificity, tyrosine phosphorylation regulated kinases derived from the marine sponge leucettamine B: Modulation of alternative pre-RNA splicing. J Med Chem 54:4172-4186.
12. Deegan S, Saveljeva S, Gorman AM, and Samali A (2013) Stress-induced selfcannibalism: On the regulation of autophagy by endoplasmic reticulum stress. Cell Mol Life Sci 70:2425-2441.
13. de Graaf K, Hekerman P, Spelten O, Herrmann A, Packman LC, Büssow K, Müller-Newen G, and BeckerW(2004) Characterization of cyclin L2, a novel cyclin with an arginine/serine-rich domain: Phosphorylation by DYRK1A and colocalization with splicing factors. J Biol Chem 279:4612-4624.
14. Dehay B, Bové J, Rodríguez-Muela N, Perier C, Recasens A, Boya P, and Vila M (2010) Pathogenic lysosomal depletion in Parkinson's disease. J Neurosci 30: 12535-12544.
15. de Lartigue J, Polson H, Feldman M, Shokat K, Tooze SA, Urbé S, and Clague MJ (2009) PIKfyve regulation of endosome-linked pathways. Traffic 10:883-893.
16. Duncan PI, Stojdl DF, Marius RM, and Bell JC (1997) In vivo regulation of alternative pre-mRNA splicing by the Clk1 protein kinase. Mol Cell Biol 17:5996-6001.
17. Ertmer A, Huber V, Gilch S, Yoshimori T, Erfle V, Duyster J, Elsässer HP, and Schätzl HM (2007) The anticancer drug imatinib induces cellular autophagy. Leukemia 21:936-942.
18. Faustino NA and Cooper TA (2003) Pre-mRNA splicing and human disease. Genes Dev 17:419-437.
19. Gui JF, Tronchère H, Chandler SD, and Fu XD (1994) Purification and characterization of a kinase specific for the serine-and arginine-rich pre-mRNA splicing factors. Proc Natl Acad Sci USA 91:10824-10828.
20. Hagiwara M (2005) Alternative splicing: A new drug target of the post-genome era. Biochim Biophys Acta 1754:324-331.
21. He C and Klionsky DJ (2009) Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43:67-93.
22. Hochfeld WE, Lee S, and Rubinsztein DC (2013) Therapeutic induction of autophagy to modulate neurodegenerative disease progression. Acta Pharmacol Sin 34: 600-604.
23. Høyer-Hansen M and Jäättelä M (2007) AMP-activated protein kinase: A universal regulator of autophagy? Autophagy 3:381-383.
24. Ikonomov OC, Sbrissa D, and Shisheva A (2009) YM201636, an inhibitor of retroviral budding and PIKfyve-catalyzed PtdIns(3,5)P2 synthesis, halts glucose entry by insulin in adipocytes. Biochem Biophys Res Commun 382:566-570.
25. Jefferies HB, Cooke FT, Jat P, Boucheron C, Koizumi T, Hayakawa M, Kaizawa H, Ohishi T, Workman P, and Waterfield MD et al. (2008) A selective PIKfyve inhibitor blocks PtdIns(3,5)P(2) production and disrupts endomembrane transport and retroviral budding. EMBO Rep 9:164-170.
26. Kaida D, Schneider-Poetsch T, and Yoshida M (2012) Splicing in oncogenesis and tumor suppression. Cancer Sci 103:1611-1616.
27. Kimura S, Noda T, and Yoshimori T (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3:452-460.
28. Kuma A, Matsui M, and Mizushima N (2007) LC3, an autophagosome marker, can be incorporated into protein aggregates independent of autophagy: Caution in the interpretation of LC3 localization. Autophagy 3:323-328.
29. Leost M, Schultz C, Link A, Wu YZ, Biernat J, Mandelkow EM, Bibb JA, Snyder GL, Greengard P, and Zaharevitz DW et al. (2000) Paullones are potent inhibitors of glycogen synthase kinase-3beta and cyclin-dependent kinase 5/p25. Eur J Biochem 267:5983-5994.
30. Long JC and Caceres JF (2009) The SR protein family of splicing factors: Master regulators of gene expression. Biochem J 417:15-27.
31. Maiuri MC, Galluzzi L, Morselli E, Kepp O, Malik SA, and Kroemer G (2010) Autophagy regulation by p53. Curr Opin Cell Biol 22:181-185.
32. Majumder S, Richardson A, Strong R, and Oddo S (2011) Inducing autophagy by rapamycin before, but not after, the formation of plaques and tangles ameliorates cognitive deficits. PLoS ONE 6:e25416.
33. Marcel V, Khoury MP, Fernandes K, Diot A, Lane DP, and Bourdon JC (2013) Detecting p53 isoforms at protein level. Methods Mol Biol 962:15-29.
34. Margariti A, Li H, Chen T, Martin D, Vizcay-Barrena G, Alam S, Karamariti E, Xiao Q, Zampetaki A, and Zhang Z et al. (2013) XBP1 mRNA splicing triggers an autophagic response in endothelial cells through BECLIN-1 transcriptional activation. J Biol Chem 288:859-872.
35. Mariño G, Madeo F, and Kroemer G (2011) Autophagy for tissue homeostasis and neuroprotection. Curr Opin Cell Biol 23:198-206.
36. Martin S, Harper CB, May LM, Coulson EJ, Meunier FA, and Osborne SL (2013) Inhibition of PIKfyve by YM-201636 dysregulates autophagy and leads to apoptosis-independent neuronal cell death. PLoS ONE 8:e60152.
37. Mettey Y, Gompel M, Thomas V, Garnier M, Leost M, Ceballos-Picot I, Noble M, Endicott J, Vierfond JM, and Meijer L (2003) Aloisines, a new family of CDK/GSK-3 inhibitors. SAR study, crystal structure in complex with CDK2, enzyme selectivity, and cellular effects. J Med Chem 46:222-236.
38. Mills JD and Janitz M (2012) Alternative splicing of mRNA in the molecular pathology of neurodegenerative diseases. Neurobiol Aging 33:1012 e1011-1024.
39. Mizushima N and Levine B (2010) Autophagy in mammalian development and differentiation. Nat Cell Biol 12:823-830.
40. Muraki M, Ohkawara B, Hosoya T, Onogi H, Koizumi J, Koizumi T, Sumi K, Yomoda J, Murray MV, and Kimura H et al. (2004) Manipulation of alternative splicing by a newly developed inhibitor of Clks. J Biol Chem 279:24246-24254.
41. Quidville V, Alsafadi S, Goubar A, Commo F, Scott V, Pioche-Durieu C, Girault I, Baconnais S, Le Cam E, and Lazar V et al. (2013) Targeting the deregulated spliceosome core machinery in cancer cells triggers mTOR blockade and autophagy. Cancer Res 73:2247-2258.
42. Romeo V (2012) Myotonic Dystrophy Type 1 or Steinert's disease. Adv Exp Med Biol 724:239-257.
43. Sarkar S, Floto RA, Berger Z, Imarisio S, Cordenier A, Pasco M, Cook LJ, and Rubinsztein DC (2005) Lithium induces autophagy by inhibiting inositol monophosphatase. J Cell Biol 170:1101-1111.
44. Sbrissa D, Ikonomov OC, and Shisheva A (1999) PIKfyve, a mammalian ortholog of yeast Fab1p lipid kinase, synthesizes 5-phosphoinositides. Effect of insulin. J Biol Chem 274:21589-21597.
45. Sbrissa D, Ikonomov OC, Deeb R, and Shisheva A (2002) Phosphatidylinositol 5-phosphate biosynthesis is linked to PIKfyve and is involved in osmotic response pathway in mammalian cells. J Biol Chem 277:47276-47284.
46. Sbrissa D, Ikonomov OC, Filios C, Delvecchio K, and Shisheva A (2012) Functional dissociation between PIKfyve-synthesized PtdIns5P and PtdIns(3,5)P2 by means of the PIKfyve inhibitor YM201636. Am J Physiol Cell Physiol 303:C436-C446.
47. Schaeffer V and Goedert M (2012) Stimulation of autophagy is neuroprotective in a mouse model of human tauopathy. Autophagy 8:1686-1687.
48. Shisheva A (2012) PIKfyve and its Lipid products in health and in sickness. Curr Top Microbiol Immunol 362:127-162.
49. Shisheva A (2013) PtdIns5P: News and views of its appearance, disappearance and deeds. Arch Biochem Biophys 538:171-180.
50. Singh RK and Cooper TA (2012) Pre-mRNA splicing in disease and therapeutics. Trends Mol Med 18:472-482.
51. Smith B, Medda F, Gokhale V, Dunckley T, and Hulme C (2012) Recent advances in the design, synthesis, and biological evaluation of selective DYRK1A inhibitors: A new avenue for a disease modifying treatment of Alzheimer's? ACS Chem Neurosci 3:857-872.
52. Spilman P, Podlutskaya N, Hart MJ, Debnath J, Gorostiza O, Bredesen D, Richardson A, Strong R, and Galvan V (2010) Inhibition of mTOR by rapamycin abolishes cognitive deficits and reduces amyloid-beta levels in a mouse model of Alzheimer's disease. PLoS ONE 5:e9979.
53. Steele JW and Gandy S (2013) Latrepirdine (Dimebon®), a potential Alzheimer therapeutic, regulates autophagy and neuropathology in an Alzheimer mouse model. Autophagy 9:617-618.
54. Tahtouh T, Elkins JM, Filippakopoulos P, Soundararajan M, Burgy G, Durieu E, Cochet C, Schmid RS, Lo DC, and Delhommel F et al. (2012) Selectivity, cocrystal structures, and neuroprotective properties of leucettines, a family of protein kinase inhibitors derived from the marine sponge alkaloid leucettamine B. J Med Chem 55:9312-9330.
55. Tchevkina E and Komelkov A (2012) Protein phosphorylation as a key mechanism of mTORC1/2 signaling pathways, in Protein Phosphorylation in Human Health (Huang C ed) InTech, Rijeka, Croatia.
56. Tian Y, Bustos V, Flajolet M, and Greengard P (2011) A small-molecule enhancer of autophagy decreases levels of Abeta and APP-CTF via Atg5-dependent autophagy pathway. FASEB J 25:1934-1942.
57. Vila M, Bové J, Dehay B, Rodríguez-Muela N, and Boya P (2011) Lysosomal membrane permeabilization in Parkinson disease. Autophagy 7:98-100.
58. Wullschleger S, Loewith R, and Hall MN (2006) TOR signaling in growth and metabolism. Cell 124:471-484.
59. Yang Z and Klionsky DJ (2010) Eaten alive: A history of macroautophagy. Nat Cell Biol 12:814-822.
60. Yomoda J, Muraki M, Kataoka N, Hosoya T, Suzuki M, Hagiwara M, and Kimura H (2008) Combination of Clk family kinase and SRp75 modulates alternative splicing of Adenovirus E1A. Genes Cells 13:233-244.