Sequences within the C terminus of the metabotropic glutamate receptor 5 (mGluR5) are responsible for inner nuclear membrane localization

Journal of Biological Chemistry

Volumn 292, Issue 9, 2017, Pages 3637-3655

  Sergin, Ismail ^a   Jong, Yuh Jiin I ^a   Harmon, Steven K ^a   Kumar, Vikas ^a   O'Malley, Karen L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY;

BIOLOGICAL FUNCTIONS; C-TERMINAL DOMAINS; EXTRACELLULAR SIGNALS; G-PROTEIN COUPLED RECEPTORS; INNER NUCLEAR MEMBRANES; METABOTROPIC GLUTAMATE RECEPTORS; NUCLEAR LOCALIZATION SIGNAL; SUBCELLULAR COMPARTMENTS;

CELL MEMBRANES;

CALCIUM ION; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN ALPHA SUBUNIT; METABOTROPIC RECEPTOR 5; CALCIUM; CHROMATIN; GLUTAMIC ACID DERIVATIVE; GRM5 PROTEIN, HUMAN; NUCLEAR LOCALIZATION SIGNAL;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL COMPARTMENTALIZATION; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CELL SURFACE; CHROMATIN; CONTROLLED STUDY; CYTOPLASM; EMBRYO; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; NEWBORN; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN TRANSPORT; RAT; SIGNAL TRANSDUCTION; ANIMAL; CELL MEMBRANE; CHEMISTRY; CORPUS STRIATUM; CYTOLOGY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GLYCOSYLATION; GOLGI COMPLEX; METABOLISM; NERVE CELL; NUCLEOCYTOPLASMIC TRANSPORT;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID MOTIFS; ANIMALS; CALCIUM; CELL MEMBRANE; CHROMATIN; CORPUS STRIATUM; CYTOPLASM; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GLUTAMATES; GLYCOSYLATION; GOLGI APPARATUS; HEK293 CELLS; HUMANS; NEURONS; NUCLEAR ENVELOPE; NUCLEAR LOCALIZATION SIGNALS; PROTEIN DOMAINS; RATS; RECEPTOR, METABOTROPIC GLUTAMATE 5;

EID: 85014696777     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.757724     Document Type: Article

References (77)

1. Jong, Y. J., Sergin, I., Purgert, C. A., and O'Malley, K. L. (2014) Locationdependent signaling of the group 1 metabotropic glutamate receptor mGlu5. Mol. Pharmacol. 86, 774-785
2. Branco, A. F., and Allen, B. G. (2015)Gprotein-coupled receptor signaling in cardiac nuclear membranes. J. Cardiovasc. Pharmacol. 65, 101-109
3. Campden, R., Audet, N., and Hébert, T. E. (2015) Nuclear G protein signaling: new tricks for old dogs. J. Cardiovasc. Pharmacol. 65, 110-122
4. Irannejad, R., and von Zastrow, M. (2014) GPCR signaling along the endocytic pathway. Curr. Opin. Cell Biol. 27, 109-116
5. Calebiro, D., Godbole, A., Lyga, S., and Lohse, M. J. (2015) Trafficking and function of GPCRs in the endosomal compartment. Methods Mol. Biol. 1234, 197-211
6. Bénard, G., Massa, F., Puente, N., Lourenço, J., Bellocchio, L., Soria-Gó-mez, E., Matias, I., Delamarre, A., Metna-Laurent, M., Cannich, A., Hebert-Chatelain, E., Mulle, C., Ortega-Gutiérrez, S., Martín-Fontecha, M., Klugmann, M., et al. (2012) Mitochondrial CB(1) receptors regulate neuronal energy metabolism. Nat. Neurosci. 15, 558-564
7. Meads, M. B., and Medveczky, P. G. (2004) Kaposi's sarcoma-associated herpesvirus-encoded viral interleukin-6 is secreted and modified differently than human interleukin-6: evidence for a unique autocrine signaling mechanism. J. Biol. Chem. 279, 51793-51803
8. Rozenfeld, R., and Devi, L. A. (2008) Regulation of CB1 cannabinoid receptor trafficking by the adaptor protein AP-3. FASEB J. 22, 2311-2322
9. Oksche, A., Boese, G., Horstmeyer, A., Furkert, J., Beyermann, M., Bienert, M., and Rosenthal, W. (2000) Late endosomal/lysosomal targeting and lack of recycling of the ligand-occupied endothelin B receptor. Mol. Pharmacol. 57, 1104-1113
10. Calebiro, D., Nikolaev, V. O., Persani, L., and Lohse, M. J. (2010) Signaling by internalized G-protein-coupled receptors. Trends Pharmacol. Sci. 31, 221-228
11. Gobeil, F., Fortier, A., Zhu, T., Bossolasco, M., Leduc, M., Grandbois, M., Heveker, N., Bkaily, G., Chemtob, S., and Barbaz, D. (2006) G-proteincoupled receptors signalling at the cell nucleus: An emerging paradigm. Can. J. Physiol. Pharmacol. 84, 287-297
12. Tadevosyan, A., Vaniotis, G., Allen, B. G., Hébert, T. E., and Nattel, S. (2012) G protein-coupled receptor signalling in the cardiac nuclear membrane: evidence and possible roles in physiological and pathophysiological function. J. Physiol. 590, 1313-1330
13. Lee, D. K., Lança, A. J., Cheng, R., Nguyen, T., Ji, X. D., Gobeil, F., Jr, Chemtob, S., George, S. R., and O'Dowd, B. F. (2004) Agonist-independent nuclear localization of the Apelin, angiotensin AT1, and bradykinin B2 receptors. J. Biol. Chem. 279, 7901-7908
14. Morinelli, T. A., Raymond, J. R., Baldys, A., Yang, Q., Lee, M. H., Luttrell, L., and Ullian, M. E. (2007) Identification of a putative nuclear localization sequence within ANG II AT(1A) receptor associated with nuclear activation. Am. J. Physiol. Cell Physiol. 292, C1398-C1408
15. Wright, C. D., Wu, S. C., Dahl, E. F., Sazama, A. J., and O'Connell, T. D. (2012) Nuclear localization drives 1-adrenergic receptor oligomerization and signaling in cardiac myocytes. Cell. Signal. 24, 794-802
16. Joyal, J. S., Nim, S., Zhu, T., Sitaras, N., Rivera, J. C., Shao, Z., Sapieha, P., Hamel, D., Sanchez, M., Zaniolo, K., St-Louis, M., Ouellette, J., Montoya-Zavala, M., Zabeida, A., Picard, E., et al. (2014) Subcellular localization of coagulation factor II receptor-like 1 in neurons governs angiogenesis. Nat. Med. 20, 1165-1173
17. Boivin, B., Vaniotis, G., Allen, B. G., and Hébert, T. E. (2008) G proteincoupled receptors in and on the cell nucleus: A new signaling paradigm J. Recept. Signal. Transduct. Res. 28, 15-28
18. Barlow, C. A., Laishram, R. S., and Anderson, R. A. (2010) Nuclear phosphoinositides: A signaling enigma wrapped in a compartmental conundrum. Trends Cell Biol. 20, 25-35
19. Purgert, C. A., Izumi, Y., Jong, Y. J., Kumar, V., Zorumski, C. F., and O'Malley, K. L. (2014) Intracellular mGluR5 can mediate synaptic plasticity in the hippocampus. J. Neurosci. 34, 4589-4598
20. Zuleger, N., Kerr, A. R., and Schirmer, E. C. (2012) Many mechanisms, one entrance: membrane protein translocation into the nucleus. Cell. Mol. Life Sci. 69, 2205-2216
21. Katta, S. S., Smoyer, C. J., and Jaspersen, S. L. (2014) Destination: inner nuclear membrane. Trends Cell Biol. 24, 221-229
22. Lusk, C. P., Blobel, G., and King, M. C. (2007) Highway to the inner nuclear membrane: rules for the road. Nat. Rev. Mol. Cell Biol. 8, 414-420
23. Hinshaw, J. E., Carragher, B. O., and Milligan, R. A. (1992) Architecture and design of the nuclear pore complex. Cell 69, 1133-1141
24. Zuleger, N., Korfali, N., and Schirmer, E. C. (2008) Inner nuclear membrane protein transport is mediated by multiple mechanisms. Biochem. Soc. Trans. 36, 1373-1377
25. Reichelt, R., Holzenburg, A., Buhle, E. L., Jr, Jarnik, M., Engel, A., and Aebi, U. (1990) Correlation between structure and mass distribution of the nuclear pore complex and of distinct pore complex components. J. Cell Biol. 110, 883-894
26. Holzenburg, A., Wilson, F. H., Finbow, M. E., and Ford, R. C. (1992) Structural investigations of membrane proteins: the versatility of electron microscopy. Biochem. Soc. Trans. 20, 591-597
27. Soullam, B., and Worman, H. J. (1995) Signals and structural features involved in integral membrane protein targeting to the inner nuclear membrane. J. Cell Biol. 130, 15-27
28. Zuleger, N., Kelly, D. A., Richardson, A. C., Kerr, A. R., Goldberg, M. W., Goryachev, A. B., and Schirmer, E. C. (2011) System analysis shows distinct mechanisms and common principles of nuclear envelope protein dynamics. J. Cell Biol. 193, 109-123
29. Hubert, G. W., Paquet, M., and Smith, Y. (2001) Differential subcellular localization of mGluR1a and mGluR5 in the rat and monkey substantia nigra. J. Neurosci. 21, 1838-1847
30. O'Malley, K. L., Jong, Y. J., Gonchar, Y., Burkhalter, A., and Romano, C. (2003) Activation of metabotropic glutamate receptor mGlu5 on nuclear membranes mediates intranuclear Ca2 changes in heterologous cell types and neurons. J. Biol. Chem. 278, 28210-28219
31. Jong, Y. J., Kumar, V., Kingston, A. E., Romano, C., and O'Malley, K. L. (2005) Functional metabotropic glutamate receptors on nuclei from brain and primary cultured striatal neurons. Role of transporters in delivering ligand. J. Biol. Chem. 280, 30469-30480
32. Hermans, E., and Challiss, R. A. (2001) Structural, signalling and regulatory properties of the group I metabotropic glutamate receptors: prototypic family C G-protein-coupled receptors. Biochem. J. 359, 465-484
33. Vincent, K., Cornea, V. M., Jong, Y. J., Laferrière, A., Kumar, N., Mickeviciute, A., Fung, J. S., Bandegi, P., Ribeiro-da-Silva, A., O'Malley, K. L., Coderre T. J. (2016) Intracellular mGluR5 plays a critical role in neuropathic pain. Nat. Commun. 7, 10604
34. Kumar, V., Jong, Y. J., and O'Malley, K. L. (2008) Activated nuclear metabotropic glutamate receptor mGlu5 couples to nuclear Gq/11 proteins to generate inositol 1,4,5-trisphosphate-mediated nuclear Ca2 release. J. Biol. Chem. 283, 14072-14083
35. Kumar, V., Fahey, P. G., Jong, Y. J., Ramanan, N., and O'Malley, K. L. (2012) Activation of intracellular metabotropic glutamate receptor 5 in striatal neurons leads to up-regulation of genes associated with sustained synaptic transmission including Arc/Arg3.1 protein. J. Biol. Chem. 287, 5412-5425
36. Jong, Y. J., Kumar, V., and O'Malley, K. L. (2009) Intracellular metabotropic glutamate receptor 5 (mGluR5) activates signaling cascades distinct from cell surface counterparts. J. Biol. Chem. 284, 35827-35838
37. Walther, C., and Ferguson, S. S. (2013) Arrestins: role in the desensitization, sequestration, and vesicular trafficking of G protein-coupled receptors. Prog. Mol. Biol. Transl. Sci. 118, 93-113
38. Magalhaes, A. C., Dunn, H., and Ferguson, S. S. (2012) Regulation ofGPCR activity, trafficking and localization by GPCR-interacting proteins. Br. J. Pharmacol. 165, 1717-1736
39. Dunn, H. A., and Ferguson, S. S. (2015) PDZ protein regulation of GPCR trafficking and signaling pathways. Mol. Pharmacol. 88, 624-639
40. Dores, M. R., and Trejo, J. (2014) Atypical regulation ofGprotein-coupled receptor intracellular trafficking by ubiquitination. Curr. Opin. Cell Biol. 27, 44-50
41. Shirvani, H., Gätà, G., and Marullo, S. (2012) Regulated GPCR trafficking to the plasma membrane: general issues and the CCR5 chemokine receptor example. Subcell. Biochem. 63, 97-111
42. Margeta-Mitrovic, M., Jan, Y. N., and Jan, L. Y. (2000) A trafficking checkpoint controls GABA(B) receptor heterodimerization. Neuron 27, 97-106
43. White, J. H., Wise, A., Main, M. J., Green, A., Fraser, N. J., Disney, G. H., Barnes, A. A., Emson, P., Foord, S. M., and Marshall, F. H. (1998) Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature 396, 679-682
44. Lester, H. A., Miwa, J. M., and Srinivasan, R. (2012) Psychiatric drugs bind to classical targets within early exocytotic pathways: therapeutic effects. Biol. Psychiatry 72, 907-915
45. Francesconi, A., and Duvoisin, R. M. (1998) Role of the second and third intracellular loops of metabotropic glutamate receptors in mediating dual signal transduction activation. J. Biol. Chem. 273, 5615-5624
46. Kniazeff, J., Bessis, A. S., Maurel, D., Ansanay, H., Prézeau, L., and Pin, J. P. (2004) Closed state of both binding domains of homodimeric mGlu receptors is required for full activity. Nat. Struct. Mol. Biol. 11, 706-713
47. Gomes, D. A., Rodrigues, M. A., Leite, M. F., Gomez, M. V., Varnai, P., Balla, T., Bennett, A. M., and Nathanson, M. H. (2008) c-Met must translocate to the nucleus to initiate calcium signals. J. Biol. Chem. 283, 4344-4351
48. Gerasimenko, O. V., Gerasimenko, J. V., Tepikin, A. V., and Petersen, O. H. (1995) ATP-dependent accumulation and inositol trisphosphate-or cyclic ADP-ribose-mediated release of Ca2 from the nuclear envelope. Cell 80, 439-444
49. Bhave, G., Nadin, B. M., Brasier, D. J., Glauner, K. S., Shah, R. D., Heinemann, S. F., Karim, F., and Gereau, R. W., 4th (2003) Membrane topology of a metabotropic glutamate receptor. J. Biol. Chem. 278, 30294-30301
50. Poon, I. K., and Jans, D. A. (2005) Regulation of nuclear transport: central role in development and transformation Traffic 6, 173-186
51. Goldfarb, D. S., Corbett, A. H., Mason, D. A., Harreman, M. T., and Adam, S. A. (2004) Importin : A multipurpose nuclear-transport receptor. Trends Cell Biol. 14, 505-514
52. Sekine-Aizawa, Y., and Huganir, R. L. (2004) Imaging of receptor trafficking by using -bungarotoxin-binding-site-tagged receptors. Proc. Natl. Acad. Sci. U.S.A. 101, 17114-17119
53. Trivedi, R. R., and Bhattacharyya, S. (2012) Constitutive internalization and recycling of metabotropic glutamate receptor 5 (mGluR5). Biochem. Biophys. Res. Commun. 427, 185-190
54. Ulbert, S., Platani, M., Boue, S., and Mattaj, I. W. (2006) Direct membrane protein-DNA interactions required early in nuclear envelope assembly. J. Cell Biol. 173, 469-476
55. Batzer, M. A., and Deininger, P. L. (2002) Alu repeats and human genomic diversity. Nat. Rev. Genet. 3, 370-379
56. Marfori, M., Mynott, A., Ellis, J. J., Mehdi, A. M., Saunders, N. F., Curmi, P. M., Forwood, J. K., Bodén, M., and Kobe, B. (2011) Molecular basis for specificity of nuclear import and prediction of nuclear localization. Biochim. Biophys. Acta 1813, 1562-1577
57. Fourgeaud, L., Bessis, A. S., Rossignol, F., Pin, J. P., Olivo-Marin, J. C., and Hémar, A. (2003) The metabotropic glutamate receptor mGluR5 is endocytosed by a clathrin-independent pathway. J. Biol. Chem. 278, 12222-12230
58. Francesconi, A., Kumari, R., and Zukin, R. S. (2009) Regulation of group I metabotropic glutamate receptor trafficking and signaling by the caveolar/lipid raft pathway. J. Neurosci. 29, 3590-3602
59. Benyair, R., Ogen-Shtern, N., and Lederkremer, G. Z. (2015) Glycan regulation of ER-associated degradation through compartmentalization. Semin. Cell Dev. Biol. 41, 99-109
60. Abe, T., Sugihara, H., Nawa, H., Shigemoto, R., Mizuno, N., and Nakanishi, S. (1992) Molecular characterization of a novel metabotropic glutamate receptor mGluR5 coupled to inositol phosphate/Ca2 signal transduction. J. Biol. Chem. 267, 13361-13368
61. Gruenbaum, Y., Margalit, A., Goldman, R. D., Shumaker, D. K., and Wilson, K. L. (2005) The nuclear lamina comes of age. Nat. Rev. Mol. Cell Biol. 6, 21-31
62. Schirmer, E. C., and Foisner, R. (2007) Proteins that associate with lamins: many faces, many functions. Exp. Cell Res. 313, 2167-2179
63. Holmer, L., and Worman, H. J. (2001) Inner nuclear membrane proteins: functions and targeting. Cell. Mol. Life Sci. 58, 1741-1747
64. Prokocimer, M., Davidovich, M., Nissim-Rafinia, M., Wiesel-Motiuk, N., Bar, D. Z., Barkan, R., Meshorer, E., and Gruenbaum, Y. (2009) Nuclear lamins: key regulators of nuclear structure and activities. J. Cell Mol. Med. 13, 1059-1085
65. Olins, A. L., Rhodes, G., Welch, D. B., Zwerger, M., and Olins, D. E. (2010) lamin B receptor: multi-tasking at the nuclear envelope. Nucleus 1, 53-70
66. Ye, Q., and Worman, H. J. (1994) Primary structure analysis and lamin B and DNA binding of human LBR, an integral protein of the nuclear envelope inner membrane. J. Biol. Chem. 269, 11306-11311
67. Ribeiro, F. M., Paquet, M., Cregan, S. P., and Ferguson, S. S. (2010) Group I metabotropic glutamate receptor signalling and its implication in neurological disease. CNS Neurol. Disord. Drug Targets 9, 574-595
68. Wang, H., Westin, L., Nong, Y., Birnbaum, S., Bendor, J., Brismar, H., Nestler, E., Aperia, A., Flajolet, M., and Greengard, P. (2009) Norbin is an endogenous regulator of metabotropic glutamate receptor 5 signaling. Science 326, 1554-1557
69. Mao, L. M., Liu, X. Y., Zhang, G. C., Chu, X. P., Fibuch, E. E., Wang, L. S., Liu, Z., and Wang, J. Q. (2008) Phosphorylation of group I metabotropic glutamate receptors (mGluR1/5) in vitro and in vivo. Neuropharmacology 55, 403-408
70. Ko, S. J., Isozaki, K., Kim, I., Lee, J. H., Cho, H. J., Sohn, S. Y., Oh, S. R., Park, S., Kim, D. G., Kim, C. H., and Roche, K. W. (2012) PKC phosphorylation regulates mGluR5 trafficking by enhancing binding of Siah-1A. J. Neurosci. 32, 16391-16401
71. Petralia, R. S., Wang, Y. X., Singh, S., Wu, C., Shi, L., Wei, J., and Wenthold, R. J. (1997) A monoclonal antibody shows discrete cellular and subcellular localizations of mGluR1 metabotropic glutamate receptors. J. Chem. Neuroanat. 13, 77-93
72. Hurt, C. M., Ho, V. K., and Angelotti, T. (2013) Systematic and quantitative analysis of G protein-coupled receptor trafficking motifs. Methods Enzymol. 521, 171-187
73. Goodchild, R. E., Buchwalter, A. L., Naismith, T. V., Holbrook, K., Billion, K., Dauer, W. T., Liang, C. C., Dear, M. L., and Hanson, P. I. (2015) Access of torsinA to the inner nuclear membrane is activity dependent and regulated in the endoplasmic reticulum. J. Cell Sci. 128, 2854-2865
74. Snapp, E. L., Altan, N., and Lippincott-Schwartz, J. (2003) Measuring protein mobility by photobleaching GFP chimeras in living cells. Curr. Protoc. Cell Biol. Chapter 21, Unit 21.21
75. Kang, M., Day, C. A., Kenworthy, A. K., and DiBenedetto, E. (2012) Simplified equation to extract diffusion coefficients from confocal FRAP data. Traffic 13, 1589-1600
76. Luján, R., Roberts, J. D., Shigemoto, R., Ohishi, H., and Somogyi, P. (1997) Differential plasma membrane distribution of metabotropic glutamate receptors mGluR1 , mGluR2 and mGluR5, relative to neurotransmitter release sites. J. Chem. Neuroanat. 13, 219-241
77. López-Bendito, G., Shigemoto, R., Fairén, A., and Luján, R. (2002) Differential distribution of group I metabotropic glutamate receptors during rat cortical development. Cereb. Cortex. 12, 625-638