Role of the Sigma-1 receptor in Amyotrophic Lateral Sclerosis (ALS)

Journal of Pharmacological Sciences

Volumn 127, Issue 1, 2015, Pages 10-16

  Mavlyutov, Timur A ^a   Guo, Lian Wang ^a   Epstein, Miles L ^a   Ruoho, Arnold E ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

ALS; C terminals; Motoneurons; Sigma 1 receptor

Indexed keywords

COPPER ZINC SUPEROXIDE DISMUTASE; EPIDERMAL GROWTH FACTOR RECEPTOR; INDOLE(ETHYL)AMINE N METHYLTRANSFERASE; METHYLTRANSFERASE; MUSCARINIC M2 RECEPTOR; MUTANT PROTEIN; N,N DIMETHYLTRYPTAMINE; NEU DIFFERENTIATION FACTOR; SIGMA 1 OPIATE RECEPTOR; THIOETHER METHYLTRANSFERASE; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; SIGMA OPIATE RECEPTOR; SIGMA-1 RECEPTOR;

AMYOTROPHIC LATERAL SCLEROSIS; CARBOXY TERMINAL SEQUENCE; CELLULAR DISTRIBUTION; DISEASE ASSOCIATION; DISEASE EXACERBATION; ENDOPLASMIC RETICULUM STRESS; GENE MUTATION; HUMAN; KNOCKOUT MOUSE; LONGEVITY; MOLECULAR BIOLOGY; MOTONEURON; NERVE EXCITABILITY; NERVE POTENTIAL; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; RECEPTOR BINDING; REVIEW; S1R GENE; SIGNAL TRANSDUCTION; WILD TYPE; ACTION POTENTIAL; ANIMAL; GENETICS; PATHOPHYSIOLOGY; PHYSIOLOGY; ULTRASTRUCTURE;

ACTION POTENTIALS; AMYOTROPHIC LATERAL SCLEROSIS; ANIMALS; HUMANS; MICE, KNOCKOUT; MOTOR NEURONS; RECEPTORS, SIGMA;

EID: 84924056576     PISSN: 13478613     EISSN: 13478648     Source Type: Journal    
DOI: 10.1016/j.jphs.2014.12.013     Document Type: Review

References (88)

1. S. Boillee, C. Vande Velde, and D.W. Cleveland ALS: a disease of motor neurons and their nonneuronal neighbors Neuron 52 2006 39 59
2. H. Ilieva, M. Polymenidou, and D.W. Cleveland Non-cell autonomous toxicity in neurodegenerative disorders: ALS and beyond J Cell Biol 187 2009 761 772
3. O. Abel, J.F. Powell, P.M. Andersen, and A. Al-Chalabi ALSoD: a user-friendly online bioinformatics tool for amyotrophic lateral sclerosis genetics Hum Mutat 33 2012 1345 1351
4. A. Al-Saif, F. Al-Mohanna, and S. Bohlega A mutation in sigma-1 receptor causes juvenile amyotrophic lateral sclerosis Ann Neurol 70 2011 913 919
5. B. Marin, I. Kacem, M. Diagana, M. Boulesteix, R. Gouider, and P.M. Preux Juvenile and adult-onset ALS/MND among Africans: incidence, phenotype, survival: a review Amyotroph Lateral Scler 13 2012 276 283
6. B.C. Cheah, S. Vucic, A.V. Krishnan, and M.C. Kiernan Riluzole, neuroprotection and amyotrophic lateral sclerosis Curr Med Chem 17 2010 1942 1959
7. S. Vucic, C.S. Lin, B.C. Cheah, J. Murray, P. Menon, and A.V. Krishnan Riluzole exerts central and peripheral modulating effects in amyotrophic lateral sclerosis Brain 136 2013 1361 1370
8. R.W. Wyckoff, and J.Z. Young The motorneuron surface Proc R Soc Lond, B, Biol Sci 144 1956 440 450
9. S. Conradi Ultrastructure and distribution of neuronal and glial elements on the motoneuron surface in the lumbosacral spinal cord of the adult cat Acta Physiol Scand Suppl 332 1969 5 48
10. G.B. Miles, R. Hartley, A.J. Todd, and R.M. Brownstone Spinal cholinergic interneurons regulate the excitability of motoneurons during locomotion Proc Natl Acad Sci U S A 104 2007 2448 2453
11. A.H. Pullen, and D. Athanasiou Increase in presynaptic territory of C-terminals on lumbar motoneurons of G93A SOD1 mice during disease progression Eur J Neurosci 29 2009 551 561
12. L.R. Herron, and G.B. Miles Gender-specific perturbations in modulatory inputs to motoneurons in a mouse model of amyotrophic lateral sclerosis Neuroscience 226 2012 313 323
13. M. Nagao, H. Misawa, S. Kato, and S. Hirai Loss of cholinergic synapses on the spinal motor neurons of amyotrophic lateral sclerosis J Neuropathol Exp Neurol 57 1998 329 333
14. C. Casas, M. Herrando-Grabulosa, R. Manzano, R. Mancuso, R. Osta, and X. Navarro Early presymptomatic cholinergic dysfunction in a murine model of amyotrophic lateral sclerosis Brain Behav 3 2013 145 158
15. A.S. Deardorff, S.H. Romer, P.M. Sonner, and R.E. Fyffe Swimming against the tide: investigations of the C-bouton synapse Front Neural Circuits 8 2014 106
16. T.P. Su, T. Hayashi, T. Maurice, S. Buch, and A.E. Ruoho The sigma-1 receptor chaperone as an inter-organelle signaling modulator Trends Pharmacol Sci 31 2010 557 566
17. T. Maurice, and T.P. Su The pharmacology of sigma-1 receptors Pharmacol Ther 124 2009 195 206
18. J. Mei, and G.W. Pasternak Molecular cloning and pharmacological characterization of the rat sigma1 receptor Biochem Pharmacol 62 2001 349 355
19. V. Sabino, P. Cottone, S.L. Parylak, L. Steardo, and E.P. Zorrilla Sigma-1 receptor knockout mice display a depressive-like phenotype Behav Brain Res 198 2009 472 476
20. V. Villard, J. Espallergues, E. Keller, A. Vamvakides, and T. Maurice Anti-amnesic and neuroprotective potentials of the mixed muscarinic receptor/sigma 1 (sigma1) ligand ANAVEX2-73, a novel aminotetrahydrofuran derivative J Psychopharmacol 25 2011 1101 1117
21. V. Francardo, F. Bez, T. Wieloch, H. Nissbrandt, K. Ruscher, and M.A. Cenci Pharmacological stimulation of sigma-1 receptors has neurorestorative effects in experimental parkinsonism Brain 137 2014 1998 2014
22. A. Hyrskyluoto, I. Pulli, K. Tornqvist, T.H. Ho, L. Korhonen, and D. Lindholm Sigma-1 receptor agonist PRE084 is protective against mutant huntingtin-induced cell degeneration: involvement of calpastatin and the NF-kappaB pathway Cell Death Dis 4 2013 e646
23. H. Ishiguro, T. Ohtsuki, M. Toru, M. Itokawa, J. Aoki, and H. Shibuya Association between polymorphisms in the type 1 sigma receptor gene and schizophrenia Neurosci Lett 257 1998 45 48
24. C.T. Ajmo Jr., D.O. Vernon, L. Collier, K.R. Pennypacker, and J. Cuevas Sigma receptor activation reduces infarct size at 24 hours after permanent middle cerebral artery occlusion in rats Curr Neurovasc Res 3 2006 89 98
25. T.A. Mavlyutov, R.W. Nickells, and L.W. Guo Accelerated retinal ganglion cell death in mice deficient in the Sigma-1 receptor Mol Vis 17 2011 1034 1043
26. K. Aamodt, A. Abrahantes Quintana, D. Adamova, A.M. Adare, M.M. Aggarwal, and G. Aglieri Rinella Centrality dependence of the charged-particle multiplicity density at midrapidity in Pb-Pb collisions at sqrt[s(NN)] = 2.76 TeV Phys Rev Lett 106 2011 032301
27. A.L. Gundlach, B.L. Largent, and S.H. Snyder Autoradiographic localization of sigma receptor binding sites in guinea pig and rat central nervous system with (+)3H-3-(3-hydroxyphenyl)-N-(1-propyl)piperidine J Neurosci 6 1986 1757 1770
28. T.A. Mavlyutov, M.L. Epstein, K.A. Andersen, L. Ziskind-Conhaim, and A.E. Ruoho The sigma-1 receptor is enriched in postsynaptic sites of C-terminals in mouse motoneurons. An anatomical and behavioral study Neuroscience 167 2010 247 255
29. F. Langa, X. Codony, V. Tovar, A. Lavado, E. Gimenez, and P. Cozar Generation and phenotypic analysis of sigma receptor type I (sigma 1) knockout mice Eur J Neurosci 18 2003 2188 2196
30. T.A. Mavlyutov, M.L. Epstein, Y.I. Verbny, M.S. Huerta, I. Zaitoun, and L. Ziskind-Conhaim Lack of Sigma-1 receptor exacerbates ALS progression in mice Neuroscience 240 2013 129 134
31. M. Peviani, E. Salvaneschi, L. Bontempi, A. Petese, A. Manzo, and D. Rossi Neuroprotective effects of the Sigma-1 receptor (S1R) agonist PRE-084, in a mouse model of motor neuron disease not linked to SOD1 mutation Neurobiol Dis 62 2014 218 232
32. R. Mancuso, S. Olivan, A. Rando, C. Casas, R. Osta, and X. Navarro Sigma-1R agonist improves motor function and motoneuron survival in ALS mice Neurother: J Am Soc Exp Neurother 9 2012 814 826
33. Y. Ono, H. Tanaka, M. Takata, Y. Nagahara, Y. Noda, and K. Tsuruma SA4503, a sigma-1 receptor agonist, suppresses motor neuron damage in in vitro and in vivo amyotrophic lateral sclerosis models Neurosci Lett 559 2014 174 178
34. W.R. Martin, C.G. Eades, J.A. Thompson, R.E. Huppler, and P.E. Gilbert The effects of morphine- and nalorphine- like drugs in the nondependent and morphine-dependent chronic spinal dog J Pharmacol Exp Ther 197 3 1976 Jun 517 532
35. R. Quirion, W.D. Bowen, Y. Itzhak, J.L. Junien, J.M. Musacchio, and R.B. Rothman A proposal for the classification of sigma binding sites Trends Pharmacol Sci 13 1992 85 86
36. S.B. Hellewell, A. Bruce, G. Feinstein, J. Orringer, W. Williams, and W.D. Bowen Rat liver and kidney contain high densities of sigma 1 and sigma 2 receptors: characterization by ligand binding and photoaffinity labeling Eur J Pharmacol 268 1994 9 18
37. T. Hayashi, and T.P. Su Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival Cell 131 2007 596 610
38. K.A. Gromek, F.P. Suchy, H.R. Meddaugh, R.L. Wrobel, L.M. LaPointe, and U.B. Chu The oligomeric states of the purified Sigma-1 receptor are stabilized by ligands J Biol Chem 289 2014 20333 20344
39. T. Mavlyutov, U. Chu, J. Yag, B.G. Fox, K. Gromek, and J. Primm Oligomerization of the sigma-1 receptor Neurosci Soc Abstr 2013
40. Z. Wu, and W.D. Bowen Role of sigma-1 receptor C-terminal segment in inositol 1,4,5-trisphosphate receptor activation: constitutive enhancement of calcium signaling in MCF-7 tumor cells J Biol Chem 283 2008 28198 28215
41. D. Balasuriya, A.P. Stewart, D. Crottes, F. Borgese, O. Soriani, and J.M. Edwardson The sigma-1 receptor binds to the Nav1.5 voltage-gated Na+ channel with 4-fold symmetry J Biol Chem 287 2012 37021 37029
42. D. Balasuriya, A.P. Stewart, and J.M. Edwardson The sigma-1 receptor interacts directly with GluN1 but not GluN2A in the GluN1/GluN2A NMDA receptor J Neurosci 33 2013 18219 18224
43. S.M. Carnally, M. Johannessen, R.M. Henderson, M.B. Jackson, and J.M. Edwardson Demonstration of a direct interaction between sigma-1 receptors and acid-sensing ion channels Biophys J 98 2010 1182 1191
44. D. Balasuriya, L. D'Sa, R. Talker, E. Dupuis, F. Maurin, and P. Martin A direct interaction between the sigma-1 receptor and the hERG voltage-gated K+ channel revealed by atomic force microscopy and homogeneous time-resolved fluorescence (HTRF(R)) J Biological Chem 289 2014 32353 32363
45. M.J. Robson, B. Noorbakhsh, M.J. Seminerio, and R.R. Matsumoto Sigma-1 receptors: potential targets for the treatment of substance abuse Curr Pharm Des 18 2012 902 919
46. F. Berardi, C. Abate, S. Ferorelli, N.A. Colabufo, and R. Perrone 1-Cyclohexylpiperazine and 3,3-dimethylpiperidine derivatives as sigma-1 (sigma1) and sigma-2 (sigma2) receptor ligands: a review Cent Nerv Syst Agents Med Chem 9 2009 205 219
47. S. Ramachandran, U.B. Chu, T.A. Mavlyutov, A. Pal, S. Pyne, and A.E. Ruoho The sigma1 receptor interacts with N-alkyl amines and endogenous sphingolipids Eur J Pharmacol 609 2009 19 26
48. T.P. Su, E.D. London, and J.H. Jaffe Steroid binding at sigma receptors suggests a link between endocrine, nervous, and immune systems Science 240 1988 219 221
49. D. Fontanilla, M. Johannessen, A.R. Hajipour, N.V. Cozzi, M.B. Jackson, and A.E. Ruoho The hallucinogen N,N-dimethyltryptamine (DMT) is an endogenous sigma-1 receptor regulator Science 323 2009 934 937
50. S. Kourrich, T.P. Su, M. Fujimoto, and A. Bonci The sigma-1 receptor: roles in neuronal plasticity and disease Trends Neurosci 35 2012 762 771
51. F.J. Kim, I. Kovalyshyn, M. Burgman, C. Neilan, C.C. Chien, and G.W. Pasternak Sigma 1 receptor modulation of G-protein-coupled receptor signaling: potentiation of opioid transduction independent from receptor binding Mol Pharmacol 77 2010 695 703
52. G. Navarro, E. Moreno, M. Aymerich, D. Marcellino, P.J. McCormick, and J. Mallol Direct involvement of sigma-1 receptors in the dopamine D1 receptor-mediated effects of cocaine Proc Natl Acad Sci U S A 107 2010 18676 18681
53. T. Hayashi, Z. Justinova, E. Hayashi, G. Cormaci, T. Mori, and S.Y. Tsai Regulation of sigma-1 receptors and endoplasmic reticulum chaperones in the brain of methamphetamine self-administering rats J Pharmacol Exp Ther 332 2010 1054 1063
54. A. Pal, D. Fontanilla, A. Gopalakrishnan, Y.K. Chae, J.L. Markley, and A.E. Ruoho The sigma-1 receptor protects against cellular oxidative stress and activates antioxidant response elements Eur J Pharmacol 682 2012 12 20
55. C.M. Cendan, J.M. Pujalte, E. Portillo-Salido, L. Montoliu, and J.M. Baeyens Formalin-induced pain is reduced in sigma(1) receptor knockout mice Eur J Pharmacol 511 2005 73 74
56. D. Crottes, H. Guizouarn, P. Martin, F. Borgese, and O. Soriani The sigma-1 receptor: a regulator of cancer cell electrical plasticity? Front Physiol 4 2013 175
57. P.J. Lupardus, R.A. Wilke, E. Aydar, C.P. Palmer, Y. Chen, and A.E. Ruoho Membrane-delimited coupling between sigma receptors and K+ channels in rat neurohypophysial terminals requires neither G-protein nor ATP J Physiol 526 2000 527 539
58. B.M. Gardner, D. Pincus, K. Gotthardt, C.M. Gallagher, and P. Walter Endoplasmic reticulum stress sensing in the unfolded protein response Cold Spring Harb Perspect Biol 5 2013 a013169
59. T. Omi, H. Tanimukai, D. Kanayama, Y. Sakagami, S. Tagami, and M. Okochi Fluvoxamine alleviates ER stress via induction of Sigma-1 receptor Cell Death Dis 5 2014 e1332
60. T. Mori, T. Hayashi, E. Hayashi, and T.P. Su Sigma-1 receptor chaperone at the ER-mitochondrion interface mediates the mitochondrion-ER-nucleus signaling for cellular survival PLoS One 8 2013 e76941
61. C.D. Ferris, D.J. Hirsch, B.P. Brooks, and S.H. Snyder Sigma receptors: from molecule to man J Neurochem 57 1991 729 737
62. T.P. Su Sigma receptors. Putative links between nervous, endocrine and immune systems Eur J Biochem 200 1991 633 642
63. H. Tagashira, Y. Shinoda, N. Shioda, and K. Fukunaga Methyl pyruvate rescues mitochondrial damage caused by SIGMAR1 mutation related to amyotrophic lateral sclerosis Biochim Biophys Acta 1840 2014 3320 3334
64. A.A. Luty, J.B. Kwok, C. Dobson-Stone, C.T. Loy, K.G. Coupland, and H. Karlstrom Sigma nonopioid intracellular receptor 1 mutations cause frontotemporal lobar degeneration-motor neuron disease Ann Neurol 68 2010 639 649
65. M. Henkart, D.M. Landis, and T.S. Reese Similarity of junctions between plasma membranes and endoplasmic reticulum in muscle and neurons J Cell Biol 70 1976 338 347
66. M. Henkart Identification and function of intracellular calcium stores in axons and cell bodies of neurons Fed Proc 39 1980 2783 2789
67. S. Fujimoto, K. Yamamoto, K. Kuba, K. Morita, and E. Kato Calcium localization in the sympathetic ganglion of the bullfrog and effects of caffeine Brain Res 202 1980 21 32
68. A.S. Deardorff, S.H. Romer, Z. Deng, K.L. Bullinger, P. Nardelli, and T.C. Cope Expression of postsynaptic Ca2+-activated K+ (SK) channels at C-bouton synapses in mammalian lumbar -motoneurons J Physiol 591 2013 875 897
69. S. Kourrich, T. Hayashi, J.Y. Chuang, S.Y. Tsai, T.P. Su, and A. Bonci Dynamic interaction between sigma-1 receptor and Kv1.2 shapes neuronal and behavioral responses to cocaine Cell 152 2013 236 247
70. E. Aydar, C.P. Palmer, V.A. Klyachko, and M.B. Jackson The sigma receptor as a ligand-regulated auxiliary potassium channel subunit Neuron 34 2002 399 410
71. M. Kinoshita, Y. Matsuoka, T. Suzuki, J. Mirrielees, and J. Yang Sigma-1 receptor alters the kinetics of Kv1.3 voltage gated potassium channels but not the sensitivity to receptor ligands Brain Res 1452 2012 1 9
72. E. Aydar, P. Onganer, R. Perrett, M.B. Djamgoz, and C.P. Palmer The expression and functional characterization of sigma (sigma) 1 receptors in breast cancer cell lines Cancer Lett 242 2006 245 257
73. M. Martina, M.E. Turcotte, S. Halman, and R. Bergeron The sigma-1 receptor modulates NMDA receptor synaptic transmission and plasticity via SK channels in rat hippocampus J Physiol 578 2007 143 157
74. L. Zagoraiou, T. Akay, J.F. Martin, R.M. Brownstone, T.M. Jessell, and G.B. Miles A cluster of cholinergic premotor interneurons modulates mouse locomotor activity Neuron 64 2009 645 662
75. A.S. Deardorff, S.H. Romer, Z. Deng, K.L. Bullinger, P. Nardelli, and T.C. Cope Expression of postsynaptic Ca2+-activated K+ (SK) channels at C-bouton synapses in mammalian lumbar alpha-motoneurons J Physiol 591 2012 875 897
76. D.E. Clapham A STIMulus package puts orai calcium channels to work Cell 136 2009 814 816
77. J. Rosenbluth Subsurface cisterns and their relationship to the neuronal plasma membrane J Cell Biol 13 1962 405 421
78. H. Misonou, D.P. Mohapatra, and J.S. Trimmer Kv2.1: a voltage-gated k+ channel critical to dynamic control of neuronal excitability Neurotoxicology 26 2005 743 752
79. M.A. Schumacher, A.F. Rivard, H.P. Bachinger, and J.P. Adelman Structure of the gating domain of a Ca2+-activated K+ channel complexed with Ca2+/calmodulin Nature 410 2001 1120 1124
80. X. Gallart-Palau, O. Tarabal, A. Casanovas, J. Sabado, F.J. Correa, and M. Hereu Neuregulin-1 is concentrated in the postsynaptic subsurface cistern of C-bouton inputs to alpha-motoneurons and altered during motoneuron diseases Faseb J 28 2014 3618 3632
81. T.A. Mavlyutov, M.L. Epstein, P. Liu, Y.I. Verbny, L. Ziskind-Conhaim, and A.E. Ruoho Development of the sigma-1 receptor in C-terminals of motoneurons and colocalization with the N,N'-dimethyltryptamine forming enzyme, indole-N-methyl transferase Neuroscience 206 2012 60 68
82. T.A. Mavlyutov, U.B. Chu, A. Schulman, E. Baker, R. Raj, and M.L. Epstein Methylation of a thiols and thioethers by human indolethylamine-n-methyl transferase Soc Neurosci Abstr 2014
83. N.M. Mozier, K.P. McConnell, and J.L. Hoffman S-adenosyl-L-methionine:thioether S-methyltransferase, a new enzyme in sulfur and selenium metabolism J Biol Chem 263 1988 4527 4531
84. H. Steinbrenner, and H. Sies Selenium homeostasis and antioxidant selenoproteins in brain: implications for disorders in the central nervous system Arch Biochem Biophys 536 2013 152 157
85. A. Dharmasena Selenium supplementation in thyroid associated ophthalmopathy: an update Int J Ophthalmol 7 2014 365 375
86. S.Y. Tsai, R.K. Rothman, and T.P. Su Insights into the Sigma-1 receptor chaperone's cellular functions: a microarray report Synapse 66 2012 42 51
87. F. Song, P. Chiang, J. Wang, J. Ravits, and J.A. Loeb Aberrant neuregulin 1 signaling in amyotrophic lateral sclerosis J Neuropathol Exp Neurol 71 2012 104 115
88. M. Fujimoto, T. Hayashi, R. Urfer, S. Mita, and T.P. Su Sigma-1 receptor chaperones regulate the secretion of brain-derived neurotrophic factor Synapse 66 2012 630 639