Proteolipid protein is required for transport of sirtuin 2 into CNS myelin

Journal of Neuroscience

Volumn 27, Issue 29, 2007, Pages 7717-7730

  Werner, Hauke B ^a   Kuhlmann, Katja ^a,c   Shen, Siming ^b   Uecker, Marina ^a,c   Schardt, Anke ^a   Dimova, Kalina ^a   Orfaniotou, Foteini ^a   Dhaunchak, Ajit ^a   Brinkmann, Bastian G ^a   Möbius, Wiebke ^a   Guarente, Lenny ^d   Casaccia Bonnefil, Patrizia ^b   Jahn, Olaf ^a,c   Nave, Klaus Armin ^a,c  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c Deutsche Forschungsgemeinschaft   (Germany)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Acetylation; Cytoskeleton; Hereditary spastic paraplegia; Metabolism; Myelin; NAD+ NADH; Neurodegeneration; Oligodendrocyte; Pelizaeus Merzbacher disease

Indexed keywords

MYELIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; PROTEOLIPID PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SEPTIN; SIRTUIN; SIRTUIN 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL MONITORING; CELL LINEAGE; CELL METABOLISM; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DISEASE MODEL; DOWN REGULATION; GEL ELECTROPHORESIS; GENETIC TRANSCRIPTION; GLIA; IMMUNOELECTRON MICROSCOPY; MASS SPECTROMETRY; MOLECULAR DYNAMICS; MYELIN SHEATH; NERVE FIBER; NERVE FIBER DEGENERATION; NEUROPROTECTION; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN TRANSPORT; PROTEOMICS; PURIFICATION; RAT; SPASTIC PARAPLEGIA;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MYELIN PROTEOLIPID PROTEIN; MYELIN SHEATH; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; PROTEIN TRANSPORT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIRTUINS;

EID: 34447638901     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1254-07.2007     Document Type: Article

References (78)

1. Almqvist P, Carlsson SR, Hardy JA, Winblad B (1986) Regional and subcellular distribution of Thy-1 in human brain assayed by a solid-phase radioimmunoassay. J Neurochem 46:681-685.
2. Anekonda TS, Reddy PH (2006) Neuronal protection by sirtuins in Alzheimer's disease. J Neurochem 96:305-313.
3. Araki T, Sasaki Y, Milbrandt J (2004) Increased nuclear NAD biosynthesis and SIRT1 activation prevent axonal degeneration. Science 305:1010-1013.
4. Barbarese E, Koppel DE, Deutscher MP, Smith CL, Ainger K, Morgan F, Carson JH (1995) Protein translation components are colocalized in granules in oligodendrocytes. J Cell Sci 108:2781-2790.
5. Benjamins JA, Morell P (1978) Proteins of myelin and their metabolism. Neurochem Res 3:137-174.
6. Bifulco M, Laezza C, Stingo S, Wolff J (2002) 2′,3′-Cyclic nucleotide 3′-phosphodiesterase: a membrane-bound, microtubule-associated protein and membrane anchor for tubulin. Proc Natl Acad Sci USA 99:1807-1812.
7. Bizzozero OA, Bixler HA, Davis JD, Espinosa A, Messier AM (2001) Chemical deacylation reduces the adhesive properties of proteolipid protein and leads to decompaction of the myelin sheath. J Neurochem 76:1129-1141.
8. Bjartmar C, Yin X, Trapp BD (1999) Axonal pathology in myelin disorders. J Neurocytol 28:383-395.
9. Blander G, Guarente L (2004) The Sir2 family of protein deacetylases. Annu Rev Biochem 73:417-435.
10. Boggs JM (2006) Myelin basic protein: a multifunctional protein. Cell Mol Life Sci 63:1945-1961.
11. Bronstein JM, Tiwari-Woodruff S, Buznikov AG, Stevens DB (2000) Involvement of OSP/claudin-11 in oligodendrocyte membrane interactions: role in biology and disease. J Neurosci Res 59:706-711.
12. Cerdan S, Rodrigues TB, Sierra A, Benito M, Fonseca LL, Fonseca CP, Garcia-Martin ML (2006) The redox switch/redox coupling hypothesis. Neurochem Int 48:523-530.
13. Chamrad D, Meyer HE (2005) Valid data from large-scale proteomics studies. Nat Methods 2:647-648.
14. Cunliffe VT, Casaccia-Bonnefil P (2006) Histone deacetylase 1 is essential for oligodendrocyte specification in the zebrafish CNS. Mech Dev 123:24-30.
15. Denu JM (2005) The Sir 2 family of protein deacetylases. Curr Opin Chem Biol 9:431-440.
16. Edgar JM, McLaughlin M, Yool D, Zhang SC, Fowler JH, Montague P, Barrie JA, McCulloch MC, Duncan ID, Garbern J, Nave KA, Griffiths IR (2004) Oligodendroglial modulation of fast axonal transport in a mouse model of hereditary spastic paraplegia. J Cell Biol 166:121-131.
17. Falk J, Bonnon C, Girault JA, Faivre-Sarrailh C (2002) F3/contactin, a neuronal cell adhesion molecule implicated in axogenesis and myelination. Biol Cell 94:327-334.
18. Garbern JY, Cambi F, Tang XM, Sima AA, Vallat JM, Bosch EP, Lewis R, Shy M, Sohi J, Kraft G, Chen KL, Joshi I, Leonard DG, Johnson W, Raskind W, Dlouhy SR, Pratt V, Hodes ME, Bird T, Kamholz J (1997) Proteolipid protein is necessary in peripheral as well as central myelin. Neuron 19:205-218.
19. Griffiths I, Klugmann M, Anderson T, Thomson C, Vouyiouklis D, Nave KA (1998a) Current concepts of PLP and its role in the nervous system. Microsc Res Tech 41:344-358.
20. Griffiths I, Klugmann M, Anderson T, Yool D, Thomson C, Schwab MH, Schneider A, Zimmermann F, McCulloch M, Nadon N, Nave KA (1998b) Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280:1610-1613.
21. Haigis MC, Mostoslavsky R, Haigis KM, Fahie K, Christodoulou DC, Murphy AJ, Valenzuela DM, Yancopoulos GD, Karow M, Blander G, Wolberger C, Prolla TA, Weindruch R, Alt FW, Guarente L (2006) SIRT4 inhibits glutamate dehydrogenase and opposes the effects of calorie restriction in pancreatic beta cells. Cell 126:941-954.
22. Hartinger J, Stenius K, Hogemann D, Jahn R (1996) 16-BAC/SDS-PAGE: a two-dimensional gel electrophoresis system suitable for the separation of integral membrane proteins. Anal Biochem 240:126-133.
23. Helling S, Schmitt E, Joppich C, Schulenborg T, Mullner S, Felske-Muller S, Wiebringhaus T, Becker G, Linsenmann G, Sitek B, Lutter P, Meyer HE, Marcus K (2006) 2-D differential membrane proteome analysis of scarce protein samples. Proteomics 6:4506-4513.
24. Huang JK, Phillips GR, Roth AD, Pedraza L, Shan W, Belkaid W, Mi S, Fex-Svenningsen A, Florens L, Yates III JR, Colman DR (2005) Glial membranes at the node of Ranvier prevent neurite outgrowth. Science 310:1813-1817.
25. Imai S, Armstrong CM, Kaeberlein M, Guarente L (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403:795-800.
26. Inoue K (2005) PLP1-related inherited dysmyelinating disorders: Pelizaeus-Merzbacher disease and spastic paraplegia type 2. Neurogenetics 6:1-16.
27. Jahn O, Hesse D, Reinelt M, Kratzin HD (2006) Technical innovations for the automated identification of gel-separated proteins by MALDI-TOF mass spectrometry. Anal Bioanal Chem 386:92-103.
28. Johns TG, Bernard CC (1999) The structure and function of myelin oligodendrocyte glycoprotein. J Neurochem 72:1-9.
29. Jung M, Sommer I, Schachner M, Nave KA (1996) Monoclonal antibody O10 defines a conformationally sensitive cell-surface epitope of proteolipid protein (PLP): evidence that PLP misfolding underlies dysmyelination in mutant mice. J Neurosci 16:7920-7929.
30. Karp NA, Griffin JL, Lilley KS (2005) Application of partial least squares discriminant analysis to two-dimensional difference gel studies in expression proteomics. Proteomics 5:81-90.
31. Kinoshita M (2006) Diversity of septin scaffolds. Curr Opin Cell Biol 18:54-60.
32. Klein C, Kramer EM, Cardine AM, Schraven B, Brandt R, Trotter J (2002) Process outgrowth of oligodendrocytes is promoted by interaction of fyn kinase with the cytoskeletal protein tau. J Neurosci 22:698-707.
33. Klugmann M, Schwab MH, Puhlhofer A, Schneider A, Zimmermann F, Griffiths IR, Nave KA (1997) Assembly of CNS myelin in the absence of proteolipid protein. Neuron 18:59-70.
34. Knapp PE, Itkis OS, Mata M (2000) Neuronal interaction determines the expression of the alpha-2 isoform of Na, K-ATPase in oligodendrocytes. Brain Res Dev Brain Res 125:89-97.
35. Kramer EM, Klein C, Koch T, Boytinck M, Trotter J (1999) Compartmentation of Fyn kinase with glycosylphosphatidylinositol-anchored molecules in oligodendrocytes facilitates kinase activation during myelination. J Biol Chem 274:29042-29049.
36. Kramer EM, Schardt A, Nave KA (2001) Membrane traffic in myelinating oligodendrocytes. Microsc Res Tech 52:656-671.
37. Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, Braun PE, Griffiths IR, Nave KA (2003) Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 33:366-374.
38. Lee AG (2001) Myelin: delivery by raft. Curr Biol 11:R60-R62.
39. Lee J, Gravel M, Zhang R, Thibault P, Braun PE (2005) Process outgrowth in oligodendrocytes is mediated by CNP, a novel microtubule assembly myelin protein. J Cell Biol 170:661-673.
40. Li W, Zhang B, Tang J, Cao Q, Wu Y, Wu C, Guo J, Ling EA, Liang F (2007) Sirtuin 2, a mammalian homolog of yeast silent information regulator-2 longevity regulator, is an oligodendroglial protein that decelerates cell differentiation through deacetylating α-tubulin. J Neurosci 27:2606-2616.
41. Liang X, Draghi NA, Resh MD (2004) Signaling from integrins to Fyn to Rho family GTPases regulates morphologic differentiation of oligodendrocytes. J Neurosci 24:7140-7149.
42. Linnington C, Webb M, Woodhams PL (1984) A novel myelin-associated glycoprotein defined by a mouse monoclonal antibody. J Neuroimmunol 6:387-396.
43. Liou W, Geuze HJ, Slot JW (1996) Improving structural integrity of cryosections for immunogold labeling. Histochem Cell Biol 106:41-58.
44. MacCoss MJ, McDonald WH, Saraf A, Sadygov R, Clark JM, Tasto JJ, Gould KL, Wolters D, Washburn M, Weiss A, Clark JI, Yates III JR, (2002) Shotgun identification of protein modifications from protein complexes and lens tissue. Proc Natl Acad Sci USA 99:7900-7905.
45. Madison DL, Krueger WH, Cheng D, Trapp BD, Pfeiffer SE (1999) SNARE complex proteins, including the cognate pair VAMP-2 and syntaxin-4, are expressed in cultured oligodendrocytes. J Neurochem 72:988-998.
46. Marin-Husstege M, Muggironi M, Liu A, Casaccia-Bonnefil P (2002) Histone deacetylase activity is necessary for oligodendrocyte lineage progression. J Neurosci 22:10333-10345.
47. McCarthy KD, de Vellis J (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol 85:890-902.
48. Montague P, McCallion AS, Davies RW, Griffiths IR (2006) Myelin-associated oligodendrocytic basic protein: a family of abundant CNS myelin proteins in search of a function. Dev Neurosci 28:479-487.
49. Nave KA, Lai C, Bloom FE, Milner RJ (1987) Splice site selection in the proteolipid protein (PLP) gene transcript and primary structure of the DM-20 protein of central nervous system myelin. Proc Natl Acad Sci USA 84:5665-5669.
50. North BJ, Marshall BL, Borra MT, Denu JM, Verdin E (2003) The human Sir2 ortholog, SIRT2, is an NAD+-dependent tubulin deacetylase. Mol Cell 11:437-444.
51. Norton WT, Poduslo SE (1973) Myelination in rat brain: method of myelin isolation. J Neurochem 21:749-757.
52. Polevoda B, Sherman F (2002) The diversity of acetylated proteins. Genome Biol 3:0006.
53. Popko B (2003) Myelin: not just a conduit for conduction. Nat Genet 33:327-328.
54. Rabilloud T (1996) Solubilization of proteins for electrophoretic analyses. Electrophoresis 17:813-829.
55. Rasband MN, Tayler J, Kaga Y, Yang Y, Lappe-Siefke C, Nave KA, Bansal R (2005) CNP is required for maintenance of axon-glia interactions at nodes of Ranvier in the CNS. Glia 50:86-90.
56. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208-212.
57. Rosenbluth J, Nave KA, Mierzwa A, Schiff R (2006) Subtle myelin defects in PLP-null mice. Glia 54:172-182.
58. Roth AD, Ivanova A, Colman DR (2006) New observations on the compact myelin proteome. Neuron Glia Biol 2:15-21.
59. Roth J, Bendayan M, Orci L (1978) Ultrastructural localization of intracellular antigens by the use of protein A-gold complex. J Histochem Cytochem 26:1074-1081.
60. Saher G, Brugger B, Lappe-Siefke C, Mobius W, Tozawa R, Wehr MC, Wieland F, Ishibashi S, Nave KA (2005) High cholesterol level is essential for myelin membrane growth. Nat Neurosci 8:468-475.
61. Schachner M, Bartsch U (2000) Multiple functions of the myelin-associated glycoprotein MAG (siglec-4a) in formation and maintenance of myelin. Glia 29:154-165.
62. Scherer SS, Xu T, Crino P, Arroyo EJ, Gutmann DH (2001) Ezrin, radixin, and moesin are components of Schwann cell microvilli. J Neurosci Res 65:150-164.
63. Shen S, Li J, Casaccia-Bonnefil P (2005) Histone modifications affect timing of oligodendrocyte progenitor differentiation in the developing rat brain. J Cell Biol 169:577-589.
64. Shimazu T, Horinouchi S, Yoshida M (2007) Multiple histone deacetylases and the CREB-binding protein regulate pre-mRNA 3′-end processing. J Biol Chem 282:4470-4478.
65. Slot JW, Geuze HJ (1985) A new method of preparing gold probes for multiple-labeling cytochemistry. Eur J Cell Biol 38:87-93.
66. Smith R, Kavanagh E, Morrison HG, Gould RM (2001) Messenger RNAs located in spiny dogfish oligodendrocyte processes. Biol Bull 201:255-256.
67. Southwood CM, Peppi M, Dryden S, Tainsky MA, Gow A (2007) Microtubule deacetylases, SirT2 and HDAC6, in the nervous system. Neurochem Res 32:187-195.
68. Tait S, Gunn-Moore F, Collinson JM, Huang J, Lubetzki C, Pedraza L, Sherman DL, Colman DR, Brophy PJ (2000) An oligodendrocyte cell adhesion molecule at the site of assembly of the paranodal axo-glial junction. J Cell Biol 150:657-666.
69. Tanny JC, Dowd GJ, Huang J, Hilz H, Moazed D (1999) An enzymatic activity in the yeast Sir2 protein that is essential for gene silencing. Cell 99:735-745.
70. Taylor CM, Marta CB, Claycomb RJ, Han DK, Rasband MN, Coetzee T, Pfeiffer SE (2004) Proteomic mapping provides powerful insights into functional myelin biology. Proc Natl Acad Sci USA 101:4643-4648.
71. Trajkovic K, Dhaunchak AS, Goncalves JT, Wenzel D, Schneider A, Bunt G, Nave KA, Simons M (2006) Neuron to glia signaling triggers myelin membrane exocytosis from endosomal storage sites. J Cell Biol 172:937-948.
72. Unlu M, Morgan ME, Minden JS (1997) Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18:2071-2077.
73. Vanrobaeys F, Van Coster R, Dhondt G, Devreese B, Van Beeumen J (2005) Profiling of myelin proteins by 2D-gel electrophoresis and multidimensional liquid chromatography coupled to MALDI TOF-TOF mass spectrometry. J Proteome Res 4:2283-2293.
74. Voelter-Mahlknecht S, Ho AD, Mahlknecht U (2005) FISH-mapping and genomic organization of the NAD-dependent histone deacetylase gene, Sirtuin 2 (Sirt2). Int J Oncol 27:1187-1196.
75. Werner H, Jung M, Klugmann M, Sereda M, Griffiths IR, Nave KA (1998) Mouse models of myelin diseases. Brain Pathol 8:771-793.
76. Wessel D, Flugge UI (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem 138:141-143.
77. Yang YH, Chen YH, Zhang CY, Nimmakayalu MA, Ward DC, Weissman S (2000) Cloning and characterization of two mouse genes with homology to the yeast Sir2 gene. Genomics 69:355-369.
78. Yin X, Baek RC, Kirschner DA, Peterson A, Fujii Y, Nave KA, Macklin WB, Trapp BD (2006) Evolution of a neuroprotective function of central nervous system myelin. J Cell Biol 172:469-478.