The ubiquitin ligase Mdm2 controls oligodendrocyte maturation by intertwining mTOR with G protein-coupled receptor kinase 2 in the regulation of GPR17 receptor desensitization

GLIA

Volumn 63, Issue 12, 2015, Pages 2327-2339

  Fumagalli, Marta ^a   Bonfanti, Elisabetta ^a   Daniele, Simona ^b   Zappelli, Elisa ^b   Lecca, Davide ^a   Martini, Claudia ^b   Trincavelli, Maria L ^b   Abbracchio, Maria P ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b UNIVERSITY OF PISA   (Italy)

Author keywords

GPR17 receptor; Myelination; Nutlin 3; Oligodendrocyte precursor cells; Rapamycin

Indexed keywords

G PROTEIN COUPLED RECEPTOR KINASE 2; GPR17 RECEPTOR; MAMMALIAN TARGET OF RAPAMYCIN; MEMBRANE RECEPTOR; MYELIN PROTEIN; NUTLIN 3; PROTEIN MDM2; PROTEIN P53; RAPAMYCIN; UNCLASSIFIED DRUG; ADRBK1 PROTEIN, MOUSE; ADRBK1 PROTEIN, RAT; CENTRAL NERVOUS SYSTEM AGENTS; G PROTEIN COUPLED RECEPTOR; GPR17 PROTEIN, MOUSE; GPR17 PROTEIN, RAT; IMIDAZOLE DERIVATIVE; MDM2 PROTEIN, MOUSE; MDM2 PROTEIN, RAT; MTOR PROTEIN, MOUSE; MTOR PROTEIN, RAT; NERVE PROTEIN; PIPERAZINE DERIVATIVE; TARGET OF RAPAMYCIN KINASE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; COMPLEX FORMATION; DOWN REGULATION; MYELINATION; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR DOWN REGULATION; TUMOR GROWTH; UBIQUITINATION; ANIMAL; BRAIN CORTEX; C57BL MOUSE; CELL CULTURE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM AGENTS; CEREBRAL CORTEX; G-PROTEIN-COUPLED RECEPTOR KINASE 2; IMIDAZOLES; MICE, INBRED C57BL; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; PIPERAZINES; PROTO-ONCOGENE PROTEINS C-MDM2; RATS, SPRAGUE-DAWLEY; RECEPTORS, G-PROTEIN-COUPLED; SIROLIMUS; TOR SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84943585077     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22896     Document Type: Article

References (32)

1. Arva NC, Talbott KE, Okoro DR, Brekman A, Qiu WG, Bargonetti J. 2008. Disruption of the p53-Mdm2 complex by Nutlin-3 reveals different cancer cell phenotypes. Ethn Dis 18: S2-1-8.
2. Ashcroft M, Vousden KH. 1999. Regulation of p53 stability. Oncogene 18:7637-7643.
3. Boda E, Vigano F, Rosa P, Fumagalli M, Labat-Gest V, Tempia F, Abbracchio MP, Dimou L, Buffo A. 2011. The GPR17 receptor in NG2 expressing cells: Focus on in vivo cell maturation and participation in acute trauma and chronic damage. Glia 59:1958-1973.
4. Caccamo A, Majumder S, Richardson A, Strong R, 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.
5. Ceruti S, Vigano F, Boda E, Ferrario S, Magni G, Boccazzi M, Rosa P, Buffo A, Abbracchio MP. 2011. Expression of the new P2Y-like receptor GPR17 during oligodendrocyte precursor cell maturation regulates sensitivity to ATP-induced death. Glia 59:363-378.
6. Chen Y, Wu H, Wang S, Koito H, Li J, Ye F, Hoang J, Escobar SS, Gow A, Arnett HA, et al. 2009. The oligodendrocyte-specific G protein-coupled receptor GPR17 is a cell-intrinsic timer of myelination. Nat Neurosci 12:1398-1406.
7. Ciana P, Fumagalli M, Trincavelli ML, Verderio C, Rosa P, Lecca D, Ferrario S, Parravicini C, Capra V, Gelosa P, Guerrini U, Belcredito S, Cimino M, Sironi L, Tremoli E, Rovati GE, Martini C, Abbracchio MP. 2006. The orphan receptor GPR17 identified as a new dual uracil nucleotides/cysteinyl-leukotrienes receptor. EMBO J 25:4615-4627.
8. Cobelens PM, Kavelaars A, Heijnen CJ, Ribas C, Mayor F Jr, Penela P. 2007. Hydrogen peroxide impairs GRK2 translation via a calpain-dependent and cdk1-mediated pathway. Cell Signal 19:269-277.
9. Coppi E, Maraula G, Fumagalli M, Failli P, Cellai L, Bonfanti E, Mazzoni L, Coppini R, Abbracchio MP, Pedata F, Pugliese AM. 2013. UDP-glucose enhances outward K(+) currents necessary for cell differentiation and stimulates cell migration by activating the GPR17 receptor in oligodendrocyte precursors. Glia 61:1155-1171.
10. Daniele S, Trincavelli ML, Fumagalli M, Zappelli E, Lecca D, Bonfanti E, Campiglia P, Abbracchio MP, Martini C. 2014. Does GRK-beta arrestin machinery work as a "switch on" for GPR17-mediated activation of intracellular signaling pathways? Cell Signal 26:1310-1325.
11. Feng J, Tamaskovic R, Yang Z, Brazil DP, Merlo A, Hess D, Hemmings BA. 2004. Stabilization of Mdm2 via decreased ubiquitination is mediated by protein kinase B/Akt-dependent phosphorylation. J Biol Chem 279:35510-35517.
12. Franklin RJ, Ffrench-Constant C. 2008. Remyelination in the CNS: from biology to therapy. Nat Rev Neurosci 9:839-855.
13. Fratangeli A, Parmigiani E, Fumagalli M, Lecca D, Benfante R, Passafaro M, Buffo A, Abbracchio MP, Rosa P. 2013. The regulated expression, intracellular trafficking and membrane recycling of the P2Y-like receptor GPR17 in Oli-neu oligodendroglial cells. J Biol Chem 288:5241-5256.
14. Freedman DA, Wu L, Levine AJ. 1999. Functions of the MDM2 oncoprotein. Cell Mol Life Sci 55:96-107.
15. Fumagalli M, Daniele S, Lecca D, Lee PR, Parravicini C, Fields RD, Rosa P, Antonucci F, Verderio C, Trincavelli ML, Bramanti P, Martini C, Abbracchio MP. 2011. Phenotypic changes, signaling pathway, and functional correlates of GPR17-expressing neural precursor cells during oligodendrocyte differentiation. J Biol Chem 286:10593-10604.
16. Guardiola-Diaz HM, Ishii A, Bansal R. 2012. Erk1/2 MAPK and mTOR signaling sequentially regulates progression through distinct stages of oligodendrocyte differentiation. Glia 60:476-486.
17. Gurevich EV, Tesmer JJ, Mushegian A, Gurevich VV. 2012. G protein-coupled receptor kinases: More than just kinases and not only for GPCRs. Pharmacol Ther 133:40-69.
18. Hamano K, Iwasaki N, Takeya T, Takita H. 1996. A quantitative analysis of rat central nervous system myelination using the immunohistochemical method for MBP. Brain Res Dev Brain Res 93:18-22.
19. Kuhlmann T, Miron V, Cui Q, Wegner C, Antel J, Bruck W. 2008. Differentiation block of oligodendroglial progenitor cells as a cause for remyelination failure in chronic multiple sclerosis. Brain 131:1749-1758.
20. Lecca D, Trincavelli ML, Gelosa P, Sironi L, Ciana P, Fumagalli M, Villa G, Verderio C, Grumelli C, Guerrini U, Tremoli E, Rosa P, Cuboni S, Martini C, Buffo A, Cimino M, Abbracchio MP. 2008. The recently identified P2Y-like receptor GPR17 is a sensor of brain damage and a new target for brain repair. PLoS One 3:e3579.
21. Lombardi MS, Kavelaars A, Schedlowski M, Bijlsma JW, Okihara KL, Van de Pol M, Ochsmann S, Pawlak C, Schmidt RE, Heijnen CJ. 1999. Decreased expression and activity of G-protein-coupled receptor kinases in peripheral blood mononuclear cells of patients with rheumatoid arthritis. FASEB J 13:715-725.
22. Mayo LD, Donner DB. 2001. A phosphatidylinositol 3-kinase/Akt pathway promotes translocation of Mdm2 from the cytoplasm to the nucleus. Proc Natl Acad Sci USA 98:11598-11603.
23. Narayanan SP, Flores AI, Wang F, Macklin WB. 2009. Akt signals through the mammalian target of rapamycin pathway to regulate CNS myelination. J Neurosci 29:6860-6870.
24. Salcedo A, Mayor F Jr, Penela P. 2006. Mdm2 is involved in the ubiquitination and degradation of G-protein-coupled receptor kinase 2. EMBO J 25:4752-4762.
25. Taranto E, Xue JR, Lacey D, Hutchinson P, Smith M, Morand EF, Leech M. 2005. Detection of the p53 regulator murine double-minute protein 2 in rheumatoid arthritis. J Rheumatol 32:424-429.
26. Thut CJ, Goodrich JA, Tjian R. 1997. Repression of p53-mediated transcription by MDM2: A dual mechanism. Genes Dev 11:1974-1986.
27. Tyler WA, Gangoli N, Gokina P, Kim HA, Covey M, Levison SW, Wood TL. 2009. Activation of the mammalian target of rapamycin (mTOR) is essential for oligodendrocyte differentiation. J Neurosci 29:6367-6378.
28. Tyler WA, Jain MR, Cifelli SE, Li Q, Ku L, Feng Y, Li H, Wood TL. 2011. Proteomic identification of novel targets regulated by the mammalian target of rapamycin pathway during oligodendrocyte differentiation. Glia 59:1754-1769.
29. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z, Kong N, Kammlott U, Lukacs C, Klein C, Fotouhi N, Liu EA. 2004. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303:844-848.
30. Vroon A, Kavelaars A, Limmroth V, Lombardi MS, Goebel MU, Van Dam AM, Caron MG, Schedlowski M, Heijnen CJ. 2005. G protein-coupled receptor kinase 2 in multiple sclerosis and experimental autoimmune encephalomyelitis. J Immunol 174:4400-4406.
31. Zappelli E, Daniele S, Abbracchio MP, Martini C, Trincavelli ML. 2014. A rapid and efficient immunoenzymatic assay to detect receptor protein interactions: G protein-coupled receptors. Int J Mol Sci 15:6252-6264.
32. Zhao Y, Aguilar A, Bernard D, Wang S. 2015. Small-molecule inhibitors of the MDM2-p53 protein-protein interaction (MDM2 inhibitors) in clinical trials for cancer treatment. J Med Chem 58:1038-1052.