The myelin membrane-associated enzyme 2′,3′-cyclic nucleotide 3′-phosphodiesterase: on a highway to structure and function

Neuroscience Bulletin

Volumn 30, Issue 6, 2014, Pages 956-966

  Raasakka, Arne ^a   Kursula, Petri ^a,b  

^a UNIVERSITY OF OULU   (Finland)

^b UNIVERSITY OF HAMBURG   (Germany)

Author keywords

2 ,3 cyclic nucleotide 3 phosphodiesterase; calmodulin; central nervous system; cytoskeleton; myelin proteins; RNA

Indexed keywords

2',3' CYCLIC NUCLEOTIDE 3' PHOSPHODIESTERASE;

CLINICAL RESEARCH; GLIA; HEALTH; HUMAN; MITOCHONDRIAL MEMBRANE; MYELIN SHEATH; NONHUMAN; OBSERVATIONAL STUDY; PHYSIOLOGICAL PROCESS; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; BRAIN; CYTOSKELETON; METABOLISM; SPINAL CORD;

2',3'-CYCLIC NUCLEOTIDE 3'-PHOSPHODIESTERASE; BRAIN; CYTOSKELETON; HUMANS; MYELIN SHEATH; SPINAL CORD;

EID: 84914675705     PISSN: 16737067     EISSN: 19958218     Source Type: Journal    
DOI: 10.1007/s12264-013-1437-5     Document Type: Review

References (90)

1. Hartline DK. What is myelin? Neuron Glia Biol 2008, 4: 153–163.
2. Aggarwal S, Yurlova L, Simons M. Central nervous system myelin: Structure, synthesis and assembly. Trends Cell Biol 2011, 21: 585–593.
3. Aggarwal S, Yurlova L, Snaidero N, Reetz C, Frey S, Zimmermann J, et al. A size barrier limits protein diffusion at the cell surface to generate lipid-rich myelin-membrane sheets. Dev Cell 2011, 21: 445–456.
4. de Monasterio-Schrader P, Jahn O, Tenzer S, Wichert SP, Patzig J, Werner HB. Systematic approaches to central nervous system myelin. Cell Mol Life Sci 2012, 69: 2879–2894.
5. Kursula P. Structural properties of proteins specific to the myelin sheath. Amino Acids 2008, 34: 175–185.
6. Quarles R. Myelin sheaths: Glycoproteins involved in their formation, maintenance and degeneration. Cell Mol Life Sci 2002, 59: 1851–1871.
7. Mirshafiey A, Kianiaslani M. Autoantigens and autoantibodies in multiple sclerosis. Iran J Allergy Asthma Immunol 2013, 12: 292–303.
8. Li J, Parker B, Martyn C, Natarajan C, Guo J. The PMP22 gene and its related diseases. Mol Neurobiol 2013, 47: 673–698.
9. Yamamoto T, Shimojima K. Pelizaeus-Merzbacher disease as a chromosomal disorder. Congenit Anom (Kyoto) 2013, 53: 3–8.
10. Hobson GM, Garbern JY. Pelizaeus-Merzbacher disease, Pelizaeus-Merzbacher-like disease 1, and related hypomyelinating disorders. Semin Neurol 2012, 32: 62–67.
11. Rösener M, Muraro PA, Riethmüller A, Kalbus M, Sappler G, Thompson RJ, et al. 2′,3′-cyclic nucleotide 3′-phosphodiesterase: A novel candidate autoantigen in demyelinating diseases. J Neuroimmunol 1997, 75: 28–34.
12. Drummond GI, Iyer NT, Keith J. Hydrolysis of ribonucleoside 2′,3′-cyclic phosphates by a diesterase from brain. J Biol Chem 1962, 237: 3535–3539
13. Drummond GI, Perrott-Yee S. Enzymatic hydrolysis of adenosine 3′,5′-phosphoric acid. J Biol Chem 1961, 236: 1126–1129.
14. Trapp BD, Bernier L, Andrews SB, Colman DR. Cellular and subcellular distribution of 2′,3′-cyclic nucleotide 3′-phosphodiesterase and its mRNA in the rat central nervous system. J Neurochem 1988, 51: 859–868.
15. Radtke C, Sasaki M, Lankford KL, Gallo V, Kocsis JD. CNPase expression in olfactory ensheathing cells. J Biomed Biotechnol 2011, 2011: 608496.
16. Monoh K, Kurihara T, Takahashi Y, Ichikawa T, Kumanishi T, Hayashi S, et al. Structure, expression and chromosomal localization of the gene encoding human 2′,3′-cyclicnucleotide 3′-phosphodiesterase. Gene 1993, 129: 297–301.
17. Kurihara T, Monoh K, Sakimura K, Takahashi Y. Alternative splicing of mouse-brain 2′,3′-cyclic-nucleotide 3′-phosphodiesterase messenger-RNA. Biochem Biophys Res Commun 1990, 170: 1074–1081.
18. Kurihara T, Tohyama Y, Yamamoto J, Kanamatsu T, Watanabe R, Kitajima S. Origin of brain 2′,3′-cyclic-nucleotide 3′-phosphodiesterase doublet. Neurosci Lett 1992, 138: 49–52.
19. Douglas AJ, Fox MF, Abbott CM, Hinks LJ, Sharpe G, Povey S, et al. Structure and chromosomal localization of the human 2′,3′-cyclic nucleotide 3′-phosphodiesterase gene. Ann Hum Genet 1992, 56: 243–254.
20. O’Neill R, Minuk J, Cox M, Braun P, Gravel M. CNP2 mRNA directs synthesis of both CNP1 and CNP2 polypeptides. J Neurosci Res 1997, 50: 248–257.
21. Gravel M, Gao E, Hervouet-Zeiber C, Parsons V, Braun P. Transcriptional regulation of 2′,3′-cyclic nucleotide 3′-phosphodiesterase gene expression by cyclic AMP in C6 cells. J Neurochem 2000, 75: 1940–1950.
22. Lee J, O’Neill R, Park M, Gravel M, Braun P. Mitochondrial localization of CNP2 is regulated by phosphorylation of the N-terminal targeting signal by PKC: Implications of a mitochondrial function for CNP2 in glial and non-glial cells. Mol Cell Neurosci 2006, 31: 446–462.
23. Gravel M, DeAngelis D, Braun PE. Molecular-cloning and characterization of rat-brain 2′,3′-cyclic nucleotide 3′-phosphodiesterase isoform-2. J Neurosci Res 1994, 38: 243–247.
24. Toyama BH, Savas JN, Park SK, Harris MS, Ingolia NT, Yates JR 3rd, et al. Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 2013, 154: 971–982.
25. Stingo S, Masullo M, Polverini E, Laezza C, Ruggiero I, Arcone R, et al. The N-terminal domain of 2′,3′-cyclic nucleotide 3′-phosphodiesterase harbors a GTP/ATP binding site. Chem Biol Drug Des 2007, 70: 502–510.
26. Kursula P. The current status of structural studies on proteins of the myelin sheath (review). Int J Mol Med 2001, 8: 475–479.
27. Myllykoski M, Baumgärtel P, Kursula P. Conformations of peptides derived from myelin-specific proteins in membranemimetic conditions probed by synchrotron radiation CD spectroscopy. Amino Acids 2012, 42: 1467–1474.
28. Lee J, Gravel M, Gao E, O’Neill R, Braun P. Identification of essential residues in 2′,3′-cyclic nucleotide 3′-phosphodiesterase — chemical modification and site-directed mutagenesis to investigate the role of cysteine and histidine residues in enzymatic activity. J Biol Chem 2001, 276: 14804–14813.
29. Kozlov G, Lee J, Elias D, Gravel M, Gutierrez P, Ekiel I, et al. Structural evidence that brain cyclic nucleotide phosphodiesterase is a member of the 2H phosphodiesterase superfamily. J Biol Chem 2003, 278: 46021–46028.
30. Myllykoski M, Raasakka A, Lehtimäki M, Han H, Kursula I, Kursula P. Crystallographic analysis of the reaction cycle of 2′,3′-cyclic nucleotide 3′-phosphodiesterase, a unique member of the 2H phosphoesterase family. J Mol Biol 2013, 425: 4307–432
31. Verrier JD, Jackson TC, Bansal R, Kochanek PM, Puccio AM, Okonkwo DO, et al. The brain in vivo expresses the 2′,3′-cAMP-adenosine pathway. J Neurochem 2012, 122: 115–125.
32. Verrier J, Jackson T, Bansal R, Kochanek PM, Jackson E. Oligodendrocyte 2′,3′-cyclic nucleotide 3′-phosphodiesterase participates in localized adenosine production: Possible role in traumatic brain injury. J Neurotrauma 2012, 29: A168–A169.
33. Lappe-Siefke C, Goebbels S, Gravel M, Nicksch E, Lee J, Braun PE, et al. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat Genet 2003, 33: 366–374.
34. Gravel M, Peterson J, Yong VW, Kottis V, Trapp B, Braun PE. Overexpression of 2′,3′-cyclic nucleotide 3′-phosphodiesterase in transgenic mice alters oligodendrocyte development and produces aberrant myelination. Mol Cell Neurosci 1996, 7: 453–466.
35. Yin X, Peterson J, Gravel M, Braun P, Trapp B. CNP overexpression induces aberrant oligodendrocyte membranes and inhibits MBP accumulation and myelin compaction. J Neurosci Res 1997, 50: 238–247.
36. Hinman JD, Chen C, Oh S, Hollander W, Abraham CR. Age-dependent accumulation of ubiquitinated 2′,3′-cyclic nucleotide 3′-phosphodiesterase in myelin lipid rafts. Glia 2008, 56: 118–133.
37. Lee J, Gravel M, Zhang R, Thibault P, Braun P. Process outgrowth in oligodendrocytes is mediated by CNP, a novel microtubule assembly myelin protein. J Cell Biol 2005, 170: 661–673.
38. Walsh MJ, Murray JM. Dual implication of 2′,3′-cyclic nucleotide 3′ phosphodiesterase as major autoantigen and C3 complement-binding protein in the the pathogenesis of multiple sclerosis. J Clin Invest 1998, 101: 1923–1931.
39. Muraro PA, Kalbus M, Afshar G, McFarland HF, Martin R. T cell response to 2′,3′-cyclic nucleotide 3′-phosphodiesterase (CNPase) in multiple sclerosis patients. J Neuroimmunol 2002, 130: 233–242.
40. Lovato L, Cianti R, Gini B, Marconi S, Bianchi L, Armini A, et al. Transketolase and 2′,3′-cyclic-nucleotide 3′-phosphodiesterase type I isoforms are specifically recognized by IgG autoantibodies in multiple sclerosis patients. Mol Cell Proteomics 2008, 7: 2337–2349.
41. Vlkolinsky R, Cairns N, Fountoulakis M, Lubec G. Decreased brain levels of 2′,3′-cyclic nucleotide-3′-phosphodiesterase in Down syndrome and Alzheimer’s disease. Neurobiol Aging 2001, 22: 547–553.
42. Hagemeyer N, Goebbels S, Papiol S, Kästner A, Hofer S, Begemann M, et al. A myelin gene causative of a catatonia-depression syndrome upon aging. EMBO Mol Med 2012, 4: 528–539.
43. Peirce TR, Bray NJ, Williams NM, Haroutunian V, Buxbaum J, Buckland P, et al. Convergent functional genomics, association and linkage analysis suggests 2′,3′-cyclic nucleotide 3′-phosphodiesterase (CNP) as a potential susceptibility gene for schizophrenia. Am J Med Genet, B Neuropsychiatr Genet 2004, 130B: 81.
44. Peirce TR, Bray NJ, Williams NM, Norton N, Moskvina V, Preece A, et al. Convergent evidence for 2′,3′-cyclic nucleotide 3′-phosphodiesterase as a possible susceptibility gene for schizophrenia. Arch Gen Psychiatry 2006, 63: 18–24.
45. Georgieva L, Moskvina V, Peirce T, Norton N, Bray NJ, Jones L, et al. Convergent evidence that oligodendrocyte lineage transcription factor 2 (OLIG2) and interacting genes influence susceptibility to schizophrenia. Proc Natl Acad Sci U S A 2006, 103: 12469–12474.
46. Dracheva S, Davis K, Chin B, Woo D, Schmeidler J, Haroutunian V. Myelin-associated mRNA and protein expression deficits in the anterior cingulate cortex and hippocampus in elderly schizophrenia patients. Neurobiol Dis 2006, 21: 531–540.
47. Barley K, Dracheva S, Byne W. Subcortical oligodendrocyte- and astrocyte-associated gene expression in subjects with schizophrenia, major depression and bipolar disorder. Schizophr Res 2009, 112: 54–64.
48. Usui H, Takahashi N, Saito S, Ishihara R, Aoyama N, Ikeda M, et al. The 2′,3′-cyclic nucleotide 3′-phosphodiesterase and oligodendrocyte lineage transcription factor 2 genes do not appear to be associated with schizophrenia in the Japanese population. Schizophr Res 2006, 88: 245–250.
49. Donohoe G, Morris D, Allot E, Clarke S, Quinn E, Robertson I, et al. Olig-2 and CNP are associated with schizophrenia risk and variance in general cognition and memory function in an Irish sample. Biol Psychiatry 2007, 61(8): 189S.
50. Le-Niculescu H, Balaraman Y, Patel S, Tan J, Sidhu K, Jerome RE, et al. Towards understanding the schizophrenia code: An expanded convergent functional genomics approach. Am J Med Genet B Neuropsychiatr Genet 2007, 144B: 129–158.
51. Tang F, Qu M, Wang L, Ruan Y, Lu T, Zhang H, et al. Casecontrol association study of the 2′,3′-cyclic nucleotide 3′-phosphodiesterase (CNP) gene and schizophrenia in the Han Chinese population. Neurosci Lett 2007, 416: 113–116.
52. Voineskos AN, de Luca V, Bulgin NL, van Adrichem Q, Shaikh S, Lang DJ, et al. A family-based association study of the myelin-associated glycoprotein and 2′,3′-cyclic nucleotide 3′-phosphodiesterase genes with schizophrenia. Psychiatr Genet 2008, 18: 143–146.
53. Voineskos AN, Bulgin N, von Adrichem Q, Wong A, Lang D, Honer W et al. MAG gene but not CNP gene associated with schizophrenia. Biol Psychiatry 2007, 61: S209.
54. Mitkus SN, Hyde TM, Vakkalanka R, Kolachana B, Weinberger DR, Kleinman JE, et al. Expression of oligodendrocyte-associated genes in dorsolateral prefrontal cortex of patients with schizophrenia. Schizophr Res 2008, 98: 129–138.
55. Verrier JD, Exo JL, Jackson TC, Ren J, Gillespie DG, Dubey RK, et al. Expression of the 2′,3′-cAMP-adenosine pathway in astrocytes and microglia. J Neurochem 2011, 118: 979–987.
56. Verrier JD, Jackson TC, Gillespie DG, Janesko-Feldman K, Bansal R, Goebbels S, et al. Role of CNPase in the oligodendrocytic extracellular 2′,3′-cAMP-adenosine pathway. Glia 2013, 61: 1595–1606
57. Jackson EK. The 2′,3′-cAMP-adenosine pathway. A Am J Physiol Renal Physiol 2011, 301: 1160–1167.
58. Thompson JE, Venegas FD, Raines RT. Energetics of catalysis by ribonucleases: Fate of the 2′,3′-cyclic phosphodiester intermediate. Biochemistry 1994, 33: 7408–7414.
59. Azarashvili T, Krestinina O, Galvita A, Grachev D, Baburina Y, Stricker R, et al. Ca2+-dependent permeability transition regulation in rat brain mitochondria by 2′,3′-cyclic nucleotides and 2′,3′-cyclic nucleotide 3′-phosphodiesterase. Am J Physiol Cell Physiol 2009, 296: C1428–C1439.
60. Popow J, Schleiffer A, Martinez J. Diversity and roles of (t) RNA ligases. Cell Mol Life Sci 2012, 69: 2657–2670.
61. Gravel M, Robert F, Kottis V, Gallouzi I, Pelletier J, Braun PE. 2′,3′-cyclic nucleotide 3′-phosphodiesterase: A novel RNA-binding protein that inhibits protein synthesis. J Neurosci Res 2009, 87: 1069–1079.
62. Myllykoski M, Itoh K, Kangas SM, Heape AM, Kang SU, Lubec G, et al. The N-terminal domain of the myelin enzyme 2′,3′-cyclic nucleotide 3′-phosphodiesterase: Direct molecular interaction with the calcium sensor calmodulin. J Neurochem 2012, 123: 515–524.
63. Olafson R, Drummond G, Lee J. Studies on 2′,3′-cyclic nucleotide-3′-phosphohydrolase from brain. Can J Biochem 1969, 47: 961–966.
64. Schwer B, Aronova A, Ramirez A, Braun P, Shuman S. Mammalian 2′,3′ cyclic nucleotide phosphodiesterase (CNP) can function as a tRNA splicing enzyme in vivo. RNA 2008, 14: 204–210.
65. Heaton P, Eckstein F. Diastereomeric specificity of 2′,3′-cyclic nucleotide 3′-phosphodiesterase. Nucleic Acids Res 1996, 24: 850–853.
66. Sakamoto Y, Tanaka N, Ichimiya T, Kurihara T, Nakamura K. Crystal structure of the catalytic fragment of human brain 2′,3′-cyclic-nucleotide 3′-phosphodiesterase. J Mol Biol 2005, 346: 789–800.
67. Myllykoski M, Raasakka A, Han H, Kursula P. Myelin 2′,3′-cyclic nucleotide 3′-phosphodiesterase: Active-site ligand binding and molecular conformation. PLoS One 2012, 7: e32336.
68. Mazumder R, Iyer L, Vasudevan S, Aravind L. Detection of novel members, structure-function analysis and evolutionary classification of the 2H phosphoesterase superfamily. Nucleic Acids Res 2002, 30: 5229–5243.
69. Nasr F, Filipowicz W. Characterization of the saccharomyces cerevisiae cyclic nucleotide phosphodiesterase involved in the metabolism of ADP-ribose 1″,2″-cyclic phosphate. Nucleic Acids Res 2000, 28: 1676–1683.
70. Greer CL, Peebles CL, Gegenheimer P, Abelson J. Mechanism of action of a yeast RNA ligase in tRNA splicing. Cell 1983, 32: 537–546.
71. Xu Q, Teplow D, Lee TD, Abelson J. Domain structure in yeast tRNA ligase. Biochemistry 1990, 29: 6132–6138.
72. Kozlov G, Denisov AY, Pomerantseva E, Gravel M, Braun PE, Gehring K. Solution structure of the catalytic domain of RICH protein from goldfish. FEBS J 2007, 274: 1600–1609.
73. Koonin EV, Gorbalenya AE. Related domains in yeast tRNA ligase, bacteriophage T4 polynucleotide kinase and RNA ligase, and mammalian myelin 2′,3′-cyclic nucleotide phosphohydrolase revealed by amino acid sequence comparison. FEBS Lett 1990, 268: 231–234.
74. Hanson PI, Whiteheart SW. AAA+ proteins: Have engine, will work. Nat Rev Mol Cell Biol 2005, 6: 519–529.
75. Walker JE, Saraste M, Runswick MJ, Gay NJ. Distantly related sequences in the alpha- and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1982, 1: 945–951.
76. 2+-calmodulin affinity chromatography and tandem mass spectrometry. J Proteome Res 2006, 5: 669–687.
77. Braun PE, Bambrick LL, Edwards AM, Bernier L. 2′,3′-cyclic nucleotide 3′-phosphodiesterase has characteristics of cytoskeletal proteins — a hypothesis for its function. Ann NY Acad Sci 1990, 605: 55–65.
78. Bifulco M, Laezza C, Stingo S, Wolff J. 2′,3′-cyclic nucleotide 3′-phosphodiesterase: A membrane-bound, microtubule-associated protein and membrane anchor for tubulin. Proc Natl Acad Sci U S A 2002, 99: 1807–1812.
79. Wilson SJ, Schoggins JW, Zang T, Kutluay SB, Jouvenet N, Alim MA, et al. Inhibition of HIV-1 particle assembly by 2′,3′-cyclic nucleotide 3′-phosphodiesterase. Cell Host Microbe 2012, 12: 585–597.
80. Ma H, Zhao XL, Wang XY, Xie XW, Han JC, Guan W, et al. 2′,3′-cyclic nucleotide 3′-phosphodiesterases inhibit hepatitis B virus replication. PLoS One 2013, 8: e80769.
81. De Angelis DA, Braun PE. 2′,3′-cyclic nucleotide 3′-phosphodiesterase binds to actin-based cytoskeletal elements in an isoprenylation-independent manner. J Neurochem 1996, 67: 943–951.
82. Carson JH, Barbarese E. Systems analysis of RNA trafficking in neural cells. Biol Cell 2005, 97: 51–62.
83. Zhang Z, Ottens AK, Golden EC, Hayes RL, Wang KKW. Using calmodulin-affinity capture to study the rat brain calmodulin binding proteome and its vulnerability to calpain and caspase proteolysis. Calcium Bind Proteins 2006, 2: 125–134.
84. Esposito C, Scrima M, Carotenuto A, Tedeschi A, Rovero P, D’Errico G, et al. Structures and micelle locations of the nonlipidated and lipidated C-terminal membrane anchor of 2′,3′-cyclic nucleotide-3′-phosphodiesterase. Biochemistry 2008, 47: 308–319.
85. De Angelis DA, Braun PE. Isoprenylation of brain 2′,3′-cyclic nucleotide 3′-phosphodiesterase modulates cell morphology. J Neurosci Res 1994, 39: 386–397.
86. Agrawal HC, Sprinkle TJ, Agrawal D. 2′,3′-cyclic nucleotide-3′-phosphodiesterase in the central-nervous-system is fattyacylated by thioester linkage. J Biol Chem 1990, 265: 11849–11853.
87. De Angelis DA, Braun PE. Binding of 2′,3′-cyclic nucleotide 3′-phosphodiesterase to myelin: An in vitro study. J Neurochem 1996, 66: 2523–2531.
88. Braun PE, De Angelis DA, Shtybel WW, Bernier L. Isoprenoid modification permits 2′,3′-cyclic nucleotide 3′-phosphodiesterase to bind to membranes. J Neurosci Res 1991, 30(3): 540–544.
89. Myllykoski M, Kursula P. Expression, purification, and initial characterization of different domains of recombinant mouse 2′,3′-cyclic nucleotide 3′-phosphodiesterase, an enigmatic enzyme from the myelin sheath. BMC Res Notes 2010, 3: 1–7.
90. Bankston AN, Mandler MD, Feng Y. Oligodendroglia and neurotrophic factors in neurodegeneration. Neurosci Bull 2013, 29: 216–228.