Direct association of the reticulon protein RTN1A with the ryanodine receptor 2 in neurons

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 6, 2013, Pages 1421-1433

  Kaya, Levent ^a   Meissner, Barbara ^a   Riedl, Maria Christine ^b   Muik, Martin ^b   Schwarzer, Christoph ^a   Ferraguti, Francesco ^a   Sarg, Bettina ^a   Lindner, Herbert ^a   Schweigreiter, Rüdiger ^a   Knaus, Hans Günther ^a   Romanin, Christoph ^b   Bandtlow, Christine E ^a  

^a INNSBRUCK MEDICAL UNIVERSITY   (Austria)

^b JOHANNES KEPLER UNIVERSITY LINZ   (Austria)

Author keywords

Brain; Calcium homeostasis; Protein protein interaction; Reticulon

Indexed keywords

PROTEIN; RTN1A PROTEIN; RYANODINE RECEPTOR 2; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; HIPPOCAMPUS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MASS SPECTROMETRY; MOUSE; NERVE CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PURKINJE CELL;

ANIMALS; BINDING SITES; BLOTTING, WESTERN; CALCIUM; CELLS, CULTURED; CYTOSOL; HIPPOCAMPUS; HUMANS; IMMUNOENZYME TECHNIQUES; IMMUNOPRECIPITATION; MALE; MICE; NERVE TISSUE PROTEINS; NEURONS; PROTEIN BINDING; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT FUSION PROTEINS; RYANODINE; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; TANDEM MASS SPECTROMETRY;

MAMMALIA;

EID: 84875768299     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.02.012     Document Type: Article

References (68)

1. Yang Y.S., Strittmatter S.M. The reticulons: a family of proteins with diverse functions. Genome Biol. 2007, 8:234.
2. Oertle T., Schwab M.E. Nogo and its partners. Trends Cell Biol. 2003, 13(4):187-194.
3. Park S.H., Blackstone C. Further assembly required: construction and dynamics of the endoplasmic reticulum network. EMBO Rep. 2010, 11(7):515-521.
4. Liu Y., Vidensky S., Ruggiero A.M., Maier S., Sitte H.H., Rothstein J.D. Reticulon RTN2B regulates trafficking and function of neuronal glutamate transporter EAAC1. J. Biol. Chem. 2008, 283(10):6561-6571.
5. Steiner P., Kulangara K., Sarria J.C.F., Glauser L., Regazzi R., Hirling H. Reticulon 1-C/neuroendocrine-specific protein-C interacts with SNARE proteins. J. Neurochem. 2004, 89(3):569-580.
6. Montenegro G., Rebelo A.P., Connell J., Allison R., Babalini C., Aloia M.D., Montieri P., Schüle R., Ishiura H., Price J., Strickland A., Gonzalez M.A., Baumbach-Reardon L., Deconinck T., Huang J., Bernardi G., Vance J.M., Rogers M.T., Tsuji S., De Jonghe P., Pericak-Vance M.A., Schöls L., Orlacchio A., Reid E., Züchner S. Mutations in the ER-shaping protein reticulon 2 cause the axon-degenerative disorder hereditary spastic paraplegia type 12. J. Clin. Invest. 2012, 122:538-544.
7. He W., Lu Y., Qahwash I., Hu X.-Y., Chang A., Yan R. Reticulon family members modulate BACE1 activity and amyloid-beta peptide generation. Nat. Med. 2004, 10(9):959-965.
8. Tagami S., Eguchi Y., Kinoshita M., Takeda M., Tsujimoto Y. A novel protein, RTN-XS, interacts with both Bcl-XL and Bcl-2 on endoplasmic reticulum and reduces their anti-apoptotic activity. Oncogene 2000, 19(50):5736-5746.
9. Di Sano F., Fazi B., Citro G., Lovat P.E., Cesareni G., Piacentini M. Glucosylceramide synthase and its functional interaction with RTN-1C regulate chemotherapeutic-induced apoptosis in neuroepithelioma cells. Cancer Res. 2003, 63(14):3860-3865.
10. Schwab M.E. Functions of Nogo proteins and their receptors in the nervous system. Nat. Rev. Neurosci. 2010, 11(12):799-811.
11. van de Velde H.J., Roebroek A.J., van Leeuwen F.W., Van de Ven W.J. Molecular analysis of expression in rat brain of NSP-A, a novel neuroendocrine-specific protein of the endoplasmic reticulum. Brain Res. Mol. Brain Res. 1994, 23(1-2):81-92.
12. van de Velde H.J., Roebroek A.J., Senden N.H., Ramaekers F.C., Van de Ven W.J. NSP-encoded reticulons, neuroendocrine proteins of a novel gene family associated with membranes of the endoplasmic reticulum. J. Cell Sci. 1994, 107:2403-2416.
13. Mannan A.U., Boehm J., Sauter S.M., Rauber A., Byrne P.C., Neesen J., Engel W. Spastin, the most commonly mutated protein in hereditary spastic paraplegia interacts with Reticulon 1 an endoplasmic reticulum protein. Neurogenetics 2006, 7(2):93-103.
14. Zhao X., Jäntti J. Functional characterization of the trans-membrane domain interactions of the Sec61 protein translocation complex beta-subunit. BMC Cell Biol. 2009, 10:76.
15. Iwahashi J., Hamada N. Human reticulon 1-A and 1-B interact with a medium chain of the AP-2 adaptor complex. Cell. Mol. Biol. 2003, 49(6):467-471.
16. Giannini G., Conti A., Mammarella S., Scrobogna M., Sorrentino V. The ryanodine receptor/calcium channel genes are widely and differentially expressed in murine brain and peripheral tissues. J. Cell Biol. 1995, 128(5):893-904.
17. 2+ release. J. Neurophysiol. 2004, 92:135-143.
18. Sorrentino V., Rizzuto R. Molecular genetics of Ca(2+) stores and intracellular Ca(2+) signalling. Trends Pharmacol. Sci. 2001, 22(9):459-464.
19. Liu X., Betzenhauser M.J., Reiken S., Meli A.C., Xie W., Chen B.X., Arancio O., Marks A.R. Role of leaky neuronal ryanodine receptors in stress-induced cognitive dysfunction. Cell 2012, 150(5):1055-1067.
20. Zhao M., Li P., Li X., Zhang L., Winkfein R.J., Chen S.R. Molecular identification of the ryanodine receptor pore-forming segment. J. Biol. Chem. 1999, 274(37):25971-25974.
21. Nakai J., Ogura T., Protasi F., Franzini-Armstrong C., Allen P.D., Beam K.G. Functional nonequality of the cardiac and skeletal ryanodine receptors. Proc. Natl. Acad. Sci. U. S. A. 1997, 94(3):1019-1022.
22. Oertle T., van der Haar M.E., Bandtlow C.E., Robeva A., Burfeind P., Buss A., Huber A.B., Simonen M., Schnell L., Brösamle C., Kaupmann K., Vallon R., Schwab M.E. Nogo-A inhibits neurite outgrowth and cell spreading with three discrete regions. J. Neurosci. 2003, 23(13):5393-5406.
23. Blum H., Beier H., Gross H.J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis 1987, 8(2):93-99.
24. Shevchenko A., Wilm M., Vorm O., Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68(5):850-858.
25. Arnitz R., Sarg B., Ott H.W., Neher A., Lindner H., Nagl M. Protein sites of attack of N-chlorotaurine in Escherichia coli. Proteomics 2006, 6:865-869.
26. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 1987, 7(8):2745-2752.
27. Schindl R., Kahr H., Graz I., Groschner K., Romanin C. Store depletion-activated CaT1 currents in rat basophilic leukemia mast cells are inhibited by 2-aminoethoxydiphenyl borate. Evidence for a regulatory component that controls activation of both CaT1 and CRAC (Ca(2+) release-activated Ca(2+) channel) channels. J. Biol. Chem. 2002, 277:26950-26958.
28. Jiang D., Wang R., Xiao B., Kong H., Hunt D.J., Choi P., Zhang L., Chen S.R. Enhanced store overload-induced Ca2+ release and channel sensitivity to luminal Ca2+ activation are common defects of RyR2 mutations linked to ventricular tachycardia and sudden death. Circ. Res. 2005, 97:1173-1181.
29. + channels in rat brain. J. Neurosci. 2002, 22(22):9698-9707.
30. West D.J., Smith E.C., Williams A.J. A novel and rapid approach to isolating functional ryanodine receptors. Biochem. Biophys. Res. Commun. 2002, 294(2):402-407.
31. Zissimopoulos S., West D.J., Williams A.J., Lai F.A. Ryanodine receptor interaction with the SNARE-associated protein snapin. J. Cell Sci. 2006, 119:2386-2397.
32. (2+)-release channel isoform in mammalian brain. Biochem. J. 1992, 288:553-564.
33. Ouyang Y., Deerinck T.J., Walton P.D., Airey J.A., Sutko J.L., Ellisman M.H. Distribution of ryanodine receptors in the chicken central nervous system. Brain Res. 1993, 620(2):269-280.
34. Dent M.A., Raisman G., Lai F.A. Expression of type 1 inositol 1,4,5-trisphosphate receptor during axogenesis and synaptic contact in the central and peripheral nervous system of developing rat. Development 1996, 122:1029-1039.
35. Nakagawa T., Okano H., Furuichi T., Aruga J., Mikoshiba K. The subtypes of the mouse inositol 1,4,5-trisphosphate receptor are expressed in a tissue-specific and developmentally specific manner. Proc. Natl. Acad. Sci. U. S. A. 1991, 88:6244-6248.
36. Dodd D.A., Niederoest B., Bloechlinger S., Dupuis L., Loeffler J.P., Schwab M.E. Nogo-A, -B, and -C are found on the cell surface and interact together in many different cell types. J. Biol. Chem. 2005, 280(13):12494-12502.
37. Shibata Y., Voss C., Rist J.M., Hu J., Rapoport T.A., Prinz W.A., Voeltz G.K. The reticulon and DP1/Yop1p proteins form immobile oligomers in the tubular endoplasmic reticulum. J. Biol. Chem. 2008, 283(27):18892-18904.
38. Zurek N., Sparks L., Voeltz G. Reticulon short hairpin transmembrane domains are used to shape ER tubules. Traffic 2011, 3:28-41.
39. 2+ release channel. J. Biol. Chem. 1993, 268(26):19785-19790.
40. 2+ signaling by axonal ryanodine receptors at the hippocampal mossy fiber synapse. Proc. Natl. Acad. Sci. U. S. A. 2008, 105(33):11998-12003.
41. 2+ and redox modification of ryanodine receptor channels from rat brain cortex. J. Neurosci. 2008, 28(38):9463-9472.
42. 2+-release channel complex of skeletal muscle sarcoplasmic reticulum: evidence for a cooperatively coupled, negatively charged homotetramer. J. Biol. Chem. 1989, 264(28):16776-16785.
43. Padua R.A., Wan W.H., Nagy J.I., Geiger J.D. [3H]ryanodine binding sites in rat brain demonstrated by membrane binding and autoradiography. Brain Res. 1991, 542(1):135-140.
44. Padua R.A., Nagy J.I., Geiger J.D. Subcellular localization of ryanodine receptors in rat brain. Eur. J. Pharmacol. 1996, 298(2):185-189.
45. Zimanyi I., Pessah I.N. Pharmacological characterization of the specific binding of [3H]ryanodine to rat brain microsomal membranes. Brain Res. 1991, 561(2):181-191.
46. 2+ dependences of [3H]ryanodine binding to α- and β-ryanodine receptors purified from bullfrog skeletal muscle in an isotonic medium. FEBS Lett. 1996, 380(3):267-271.
47. 2+ dependence of RyR channels from rat brain cortex. Am. J. Physiol. Cell Physiol. 2007, 293(1):162-171.
48. Balshaw D.M., Yamaguchi N., Meissner G. Modulation of intracellular calcium-release channels by calmodulin. J. Membr. Biol. 2002, 185(1):1-8.
49. Voeltz G.K., Prinz W., Shibata Y., Rist J.M., Rapoport T.A. A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 2006, 124(3):573-586.
50. Sparkes I., Tolley N., Aller I., Svozil J., Osterrieder A., Botchway S., Mueller C., et al. Five Arabidopsis reticulon isoforms share endoplasmic reticulum location, topology, and membrane-shaping properties. Plant Cell 2010, 22(4):1333-1343.
51. Chelu M.G., Danila C.I., Gilman C.P., Hamilton S.L. Regulation of ryanodine receptors by FK506 binding proteins. Trends Cardiovasc. Med. 2004, 14(6):227-234.
52. Jayaraman T., Brillantes A.M., Timerman A.P., Fleischer S., Erdjument-Bromage H., Tempst P., Marks A.R. FK506 binding protein associated with the calcium release channel (ryanodine receptor). J. Biol. Chem. 1992, 267(14):9474-9477.
53. Timerman A.P., Onoue H., Xin H.B., Barg S., Copello J., Wiederrecht G., Fleischer S. Selective binding of FKBP12.6 by the cardiac ryanodine receptor. J. Biol. Chem. 1996, 271(34):20385-20391.
54. Wehrens X.H.T., Lehnart S.E., Reiken S.R., Deng S.-X., Vest J.A., Cervantes D., Coromilas J., Landry D.W., Marks A.R. Protection from cardiac arrhythmia through ryanodine receptor-stabilizing protein calstabin 2. Science 2004, 304:292-296.
55. GrandPré T., Nakamura F., Vartanian T., Strittmatter S.M. Identification of the Nogo inhibitor of axon regeneration as a Reticulon protein. Nature 2000, 403:439-444.
56. Wang X., Chun S.J., Treloar H., Vartanian T., Greer C.A., Strittmatter S.M. Localization of Nogo-A and Nogo-66 receptor proteins at sites of axon-myelin and synaptic contact. J. Neurosci. 2002, 22(13):5505-5515.
57. Laurén J., Hu F., Chin J., Liao J., Airaksinen M.S., Strittmatter S.M. Characterization of myelin ligand complexes with neuronal Nogo-66 receptor family members. J. Biol. Chem. 2007, 282(8):5715-5725.
58. Furuichi T., Furutama D., Hakamata Y., Nakai J., Takeshima H., Mikoshiba K. Multiple types of ryanodine receptor/Ca2+ release channels are differentially expressed in rabbit brain. J. Neurosci. 1994, 14(8):4794-4805.
59. Usachev Y.M., Thayer S.A. All-or-none Ca2+ release from intracellular stores triggered by Ca2+ influx through voltage-gated Ca2+ channels in rat sensory neurons. J. Neurosci. 1997, 17(19):7404-7414.
60. Gruol D.L., Netzeband J.G., Parsons K.L. Ca2+ signaling pathways linked to glutamate receptor activation in the somatic and dendritic regions of cultured cerebellar purkinje neurons. J. Neurophysiol. 1996, 76(5):3325-3340.
61. Martín E.D., Buño W. Caffeine-mediated presynaptic long-term potentiation in hippocampal CA1 pyramidal neurons. J. Neurophysiol. 2003, 89(6):3029-3038.
62. Sajikumar S., Li Q., Abraham W.C., Xiao Z.C. Priming of short-term potentiation and synaptic tagging/capture mechanisms by ryanodine receptor activation in rat hippocampal CA1. Learn. Mem. 2009, 16(3):178-186.
63. Zhao W., Meiri N., Xu H., Cavallaro S., Quattrone A., Zhang L., Alkon D.L. Spatial learning induced changes in expression of the ryanodine type II receptor in the rat hippocampus. FASEB J. 2000, 14(2):290-300.
64. Kobayashi K., Manabe T., Takahashi T. Calcium-dependent mechanisms involved in presynaptic long-term depression at the hippocampal mossy fibre-CA3 synapse. Eur. J. Neurosci. 1999, 11:1633-1638.
65. Wang Y., Rowan M.J., Anwyl R. Ryanodine produces a low frequency stimulation-induced NMDA receptor-independent long-term potentiation in the rat dentate gyrus in vitro. J. Physiol. 1996, 495:755-767.
66. Reyes M., Stanton P.K. Induction of hippocampal long-term depression requires release of Ca2+ from separate presynaptic and postsynaptic intracellular stores. J. Neurosci. 1996, 16(19):5951-5960.
67. Adasme T., Haeger P., Paula-Lima A.C., Espinoza I., Casas-Alarcón M.M., Carrasco M.A., Hidalgo C. Involvement of ryanodine receptors in neurotrophin-induced hippocampal synaptic plasticity and spatial memory formation. Proc. Natl. Acad. Sci. U. S. A. 2011, 108(7):3029-3034.
68. 2+-dysregulation aging phenotype in hippocampal neurons. J. Neurosci. 2011, 31(5):1693-1703.