DDIT4/REDD1/RTP801 is a novel negative regulator of schwann cell myelination

Journal of Neuroscience

Volumn 33, Issue 38, 2013, Pages 15295-15305

  Noseda, Roberta ^a,b   Belin, Sophie ^a,g   Piguet, Francoise ^a   Vaccari, Ilaria ^a   Scarlino, Stefania ^a   Brambilla, Paola ^c   Boneschi, Filippo Martinelli ^c   Feltri, Maria Laura ^d   Wrabetz, Lawrence ^d   Quattrini, Angelo ^c   Feinstein, Elena ^e   Huganir, Richard L ^f   Bolino, Alessandra ^a  

^a DULBECCO TELETHON INSTITUTE   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c SAN RAFFAELE HOSPITAL   (Italy)

^d UNIVERSITY AT BUFFALO   (United States)

^e QBI Enterprises Ltd   (Israel)

^f JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY AT BUFFALO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN; PROTEIN DDIT4; PROTEIN KINASE B; PROTEIN REDD1; PROTEIN RTP801; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; GENE EXPRESSION PROFILING; IMMUNOHISTOCHEMISTRY; MICROARRAY ANALYSIS; MOUSE; MYELINATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCHWANN CELL; UPREGULATION; WESTERN BLOTTING;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; COCULTURE TECHNIQUES; EMBRYO, MAMMALIAN; GANGLIA, SPINAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; MYELIN BASIC PROTEIN; MYELIN P0 PROTEIN; MYELIN SHEATH; NERVE TISSUE PROTEINS; NEUROFILAMENT PROTEINS; NEURONS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RNA, MESSENGER; RNA, SMALL INTERFERING; SCHWANN CELLS; SCIATIC NERVE; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC;

EID: 84884175477     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2408-13.2013     Document Type: Article

References (43)

1. Abraham RT (2005) TOR signaling: an odyssey from cellular stress to the cell growth machinery. Curr Biol 15:R139-R141. CrossRef Medline
2. Bolino A, Muglia M, Conforti FL, LeGuern E, Salih MA, Georgiou DM, Christodoulou K, Hausmanowa-Petrusewicz I, Mandich P, Schenone A, Gambardella A, Bono F, Quattrone A, Devoto M, Monaco AP (2000) Charcot-Marie-Tooth type 4B is caused by mutations in the gene encoding myotubularin-related protein-2. Nat Genet 25:17-19. CrossRef Medline
3. Bolino A, Bolis A, Previtali SC, Dina G, Bussini S, Dati G, Amadio S, Del Carro U, Mruk DD, Feltri ML, Cheng CY, Quattrini A, Wrabetz L (2004) Disruption of Mtmr2 produces CMT4B1-like neuropathy with myelin outfolding and impaired spermatogenesis. J Cell Biol 167:711-721. CrossRef Medline
4. Bolis A, Coviello S, Bussini S, Dina G, Pardini C, Previtali SC, Malaguti M, Morana P, Del Carro U, Feltri ML, Quattrini A, Wrabetz L, Bolino A (2005) Loss of Mtmr2 phosphatase in Schwann cells but not in motor neurons causes Charcot-Marie-Tooth type 4B1 neuropathy with myelin outfoldings. J Neurosci 25:8567-8577. CrossRef Medline
5. Bolis A, Coviello S, Visigalli I, Taveggia C, Bachi A, Chishti AH, Hanada T, Quattrini A, Previtali SC, Biffi A, Bolino A (2009) Dlg1, Sec8, and Mtmr2 regulate membrane homeostasis in Schwann cell myelination. J Neurosci 29:8858-8870. CrossRef Medline
6. Brafman A, Mett I, Shafir M, Gottlieb H, Damari G, Gozlan-Kelner S, Vishnevskia-Dai V, Skaliter R, Einat P, Faerman A, Feinstein E, Shoshani T (2004) Inhibition of oxygen-induced retinopathy in RTP801- deficient mice. Invest Ophthalmol Vis Sci 45:3796-3805. CrossRef Medline
7. Cam H, Houghton PJ (2011) Regulation of mammalian target of rapamycin complex 1 (mTORC1) by hypoxia: causes and consequences. Target Oncol 6:95-102. CrossRef Medline
8. Cotter L, Ozcelik M, Jacob C, Pereira JA, Locher V, Baumann R, Relvas JB, Suter U, Tricaud N (2010) Dlg1-PTEN interaction regulates myelin thickness to prevent damaging peripheral nerve overmyelination. Science 328:1415-1418. CrossRef Medline
9. DeYoung MP, Horak P, Sofer A, Sgroi D, Ellisen LW (2008) Hypoxia regulates TSC1/2-mTOR signaling and tumor suppression through REDD1- mediated 14-3-3 shuttling. Genes Dev 22:239-251. CrossRef Medline
10. Ellisen LW (2005) Growth control under stress: mTOR regulation through the REDD1-TSC pathway. Cell Cycle 4:1500-1502. CrossRef Medline
11. Feltri ML, D'Antonio M, Quattrini A, Numerato R, Arona M, Previtali S, Chiu SY, Messing A, Wrabetz L (1999) A novel P0 glycoprotein transgene activates expression of lacZ in myelin-forming Schwann cells. Eur J Neurosci 11:1577-1586. CrossRef Medline
12. Goebbels S, Oltrogge JH, Kemper R, Heilmann I, Bormuth I, Wolfer S, Wichert SP, Mobius W, Liu X, Lappe-Siefke C, Rossner MJ, Groszer M, Suter U, Frahm J, Boretius S, Nave KA (2010) Elevated phosphatidylinositol 3,4,5-trisphosphate in glia triggers cell-autonomous membrane wrapping and myelination. J Neurosci 30:8953-8964. CrossRef Medline
13. Goebbels S, Oltrogge JH, Wolfer S, Wieser GL, Nientiedt T, Pieper A, Ruhwedel T, Groszer M, Sereda MW, Nave KA (2012) Genetic disruption of Pten in a novel mouse model of tomaculous neuropathy. EMBOMol Med 4:486-499. CrossRef Medline
14. Guertin DA, Sabatini DM (2007) Defining the role of mTOR in cancer. Cancer Cell 12:9-22. CrossRef Medline
15. Harrington EP, Zhao C, Fancy SP, Kaing S, Franklin RJ, Rowitch DH (2010) Oligodendrocyte PTEN is required for myelin and axonal integrity, not remyelination. Ann Neurol 68:703-716. CrossRef Medline
16. Harrington LS, Findlay GM, Lamb RF (2005) Restraining PI3K: mTOR signalling goes back to the membrane. Trends Biochem Sci 30:35-42. CrossRef Medline
17. Hatanaka M, Shimba S, Sakaue M, Kondo Y, Kagechika H, Kokame K, Miyata T, Hara S (2009) Hypoxia-inducible factor-3alpha functions as an accelerator of 3T3-L1 adipose differentiation. Biol Pharm Bull 32:1166-1172. CrossRef Medline
18. Horn M, Baumann R, Pereira JA, Sidiropoulos PN, Somandin C, Welzl H, Stendel C, Luhmann T, Wessig C, Toyka KV, Relvas JB, Senderek J, Suter U (2012) Myelin is dependent on the Charcot-Marie-Tooth Type 4H disease culprit protein FRABIN/FGD4 in Schwann cells. Brain 135:3567-3583. CrossRef Medline
19. Macklin WB (2010) The myelin brake: when enough is enough. Sci Signal 3:pe32. CrossRef Medline
20. Maiese K, Chong ZZ, Shang YC, Wang S (2013) mTOR: on target for novel therapeutic strategies in the nervous system. Trends Mol Med 19:51-60. CrossRef Medline
21. Malagelada C, Lopez-Toledano MA, Willett RT, Jin ZH, Shelanski ML, Greene LA (2011) RTP801/REDD1 regulates the timing of cortical neurogenesis and neuron migration. J Neurosci 31:3186-3196. CrossRef Medline
22. Michailov GV, Sereda MW, Brinkmann BG, Fischer TM, Haug B, Birchmeier C, Role L, Lai C, Schwab MH, Nave KA (2004) Axonal neuregulin-1 regulates myelin sheath thickness. Science 304:700-703. CrossRef Medline
23. Nave KA (2010) Myelination and support of axonal integrity by glia. Nature 468:244-252. CrossRef Medline
24. Nave KA, Salzer JL (2006) Axonal regulation of myelination by neuregulin 1. Curr Opin Neurobiol 16:492-500. CrossRef Medline
25. Pareyson D, Marchesi C (2009) Diagnosis, natural history, and management of Charcot-Marie-Tooth disease. Lancet Neurol 8:654-667. CrossRef Medline
26. Pereira JA, Lebrun-Julien F, Suter U (2012) Molecular mechanisms regulating myelination in the peripheral nervous system. Trends Neurosci 35:123-134. CrossRef Medline
27. Pirooznia M, Nagarajan V, Deng Y (2007) GeneVenn-A web application for comparing gene lists using Venn diagrams. Bioinformation 1:420-422. CrossRef Medline
28. Polak P, Hall MN (2009) mTORand the control of whole body metabolism. Curr Opin Cell Biol 21:209-218. CrossRef Medline
29. Roberts SA, Lloyd AC (2012) Aspects of cell growth control illustrated by the Schwann cell. Curr Opin Cell Biol 24:852-857. CrossRef Medline
30. Sarbassov DD, Ali SM, Sabatini DM (2005) Growing roles for the mTOR pathway. Curr Opin Cell Biol 17:596-603. CrossRef Medline
31. Schwarzer R, Tondera D, Arnold W, Giese K, Klippel A, Kaufmann J (2005) REDD1 integrates hypoxia-mediated survival signaling downstream of phosphatidylinositol 3-kinase. Oncogene 24:1138-1149. CrossRef Medline
32. Sheng M, Sala C (2001) PDZ domains and the organization of supramolecular complexes. Annu Rev Neurosci 24:1-29. CrossRef Medline
33. Sherman DL, Krols M, Wu LM, Grove M, Nave KA, Gangloff YG, Brophy PJ (2012) Arrest of myelination and reduced axon growth when Schwann cells lack mTOR. J Neurosci 32:1817-1825. CrossRef Medline
34. Shoshani T, Faerman A, Mett I, Zelin E, Tenne T, Gorodin S, Moshel Y, Elbaz S, Budanov A, Chajut A, Kalinski H, Kamer I, Rozen A, Mor O, Keshet E, Leshkowitz D, Einat P, Skaliter R, Feinstein E (2002) Identification of a novel hypoxia-inducible factor 1-responsive gene, RTP801, involved in apoptosis. Mol Cell Biol 22:2283-2293. CrossRef Medline
35. Sofer A, Lei K, Johannessen CM, Ellisen LW (2005) Regulation of mTOR and cell growth in response to energy stress by REDD1. Mol Cell Biol 25:5834-5845. CrossRef Medline
36. Stendel C, Roos A, Deconinck T, Pereira J, Castagner F, Niemann A, Kirschner J, Korinthenberg R, Ketelsen UP, Battaloglu E, Parman Y, Nicholson G, Ouvrier R, Seeger J, De Jonghe P, Weis J, Kruttgen A, Rudnik- Schoneborn S, Bergmann C, Suter U, et al. (2007) Peripheral nerve demyelination caused by a mutant Rho GTPase guanine nucleotide exchange factor, frabin/FGD4. Am J Hum Genet 81:158-164. CrossRef Medline
37. Tanaka T, Wiesener M, Bernhardt W, Eckardt KU, Warnecke C (2009) The human HIF (hypoxia-inducible factor)-3alpha gene is a HIF-1 target gene and may modulate hypoxic gene induction. Biochem J 424:143-151. CrossRef Medline
38. Taveggia C, Zanazzi G, Petrylak A, Yano H, Rosenbluth J, Einheber S, Xu X, Esper RM, Loeb JA, Shrager P, Chao MV, Falls DL, Role L, Salzer JL (2005) Neuregulin-1 type III determines the ensheathment fate of axons. Neuron 47:681-694. CrossRef Medline
39. Triolo D, Dina G, Taveggia C, Vaccari I, Porrello E, Rivellini C, Domi T, La Marca R, Cerri F, Bolino A, Quattrini A, Previtali SC (2012) Vimentin regulates peripheral nerve myelination. Development 139:1359-1367. CrossRef Medline
40. Wrabetz L, Feltri ML, Quattrini A, Imperiale D, Previtali S, D'Antonio M, Martini R, Yin X, Trapp BD, Zhou L, Chiu SY, Messing A (2000) P(0) glycoprotein overexpression causes congenital hypomyelination of peripheral nerves. J Cell Biol 148:1021-1034. CrossRef Medline
41. Yoshida T, Mett I, Bhunia AK, Bowman J, Perez M, Zhang L, Gandjeva A, Zhen L, Chukwueke U, Mao T, Richter A, Brown E, Ashush H, Notkin N, Gelfand A, Thimmulappa RK, Rangasamy T, Sussan T, Cosgrove G, Mouded M, et al. (2010) Rtp801, a suppressor of mTOR signaling, is an essential mediator of cigarette smoke-induced pulmonary injury and emphysema. Nat Med 16:767-773. CrossRef Medline
42. Zhou W, Zhang L, Guoxiang X, Mojsilovic-Petrovic J, Takamaya K, Sattler R, Huganir R, Kalb R (2008) GluR1 controls dendrite growth through its binding partner, SAP97. J Neurosci 28:10220-10233. CrossRef Medline
43. Zolov SN, Bridges D, Zhang Y, Lee WW, Riehle E, Verma R, Lenk GM, Converso-Baran K, Weide T, Albin RL, Saltiel AR, Meisler MH, Russell MW, Weisman LS (2012) In vivo, Pikfyve generates PI(3,5)P2, which serves as both a signaling lipid and the major precursor for PI5P. Proc Natl Acad Sci U S A 109:17472-17477. CrossRef Medline