An interaction between α7 nicotinic receptors and a G-protein pathway complex regulates neurite growth in neural cells

Journal of Cell Science

Volumn 125, Issue 22, 2012, Pages 5502-5513

  Nordman, Jacob C ^a   Kabbani, Nadine ^a  

^a GEORGE MASON UNIVERSITY   (United States)

Author keywords

Axon growth; Bungarotoxin; Cytoskeleton; GAP 43; Gprin; Growth cone; Neurite; Nicotine; Proteomics

Indexed keywords

BUNGAROTOXIN RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; NEUROMODULIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN CELL; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL GROWTH; CELL STRUCTURE; CELL SURFACE; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NERVE CELL; NERVE FIBER; NEURITE; NONHUMAN; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RAT; SIGNAL TRANSDUCTION;

ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; AXONS; BUNGAROTOXINS; CALMODULIN; CELL DIFFERENTIATION; CELL MEMBRANE; CEREBRAL CORTEX; GAP-43 PROTEIN; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; GTP-BINDING PROTEINS; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; NEURITES; NICOTINE; PC12 CELLS; PHOSPHORYLATION; PROTEIN BINDING; RATS; RECEPTORS, NICOTINIC; SIGNAL TRANSDUCTION;

EID: 84873561278     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.110379     Document Type: Article

References (87)

1. Albuquerque, E. X., Pereira, E. F., Alkondon, M. and Rogers, S. W. (2009). Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol. Rev. 89, 73-120.
2. Alkondon, M., Pereira, E. F., Potter, M. C., Kauffman, F. C., Schwarcz, R. and Albuquerque, E. X. (2007). Strain-specific nicotinic modulation of glutamatergic transmission in the CA1 field of the rat hippocampus: August Copenhagen Irish versus Sprague-Dawley. J. Neurophysiol. 97, 1163-1170.
3. Aramakis, V. B. and Metherate, R. (1998). Nicotine selectively enhances NMDA receptor-mediated synaptic transmission during postnatal development in sensory neocortex. J. Neurosci. 18, 8485-8495.
4. Berg, D. K. and Conroy, W. G. (2002). Nicotinic α7 receptors: synaptic options and downstream signaling in neurons. J. Neurobiol. 53, 512-523.
5. Berg, D. K., Conroy, W. G., Liu, Z. and Zago, W. M. (2006). Nicotinic signal transduction machinery. J. Mol. Neurosci. 30, 149-152.
6. i/o signaling pathways. Front. Biosci. 13, 4544-4557.
7. Chan, J. and Quik, M. (1993). A role for the nicotinic a-bungarotoxin receptor in neurite outgrowth in PC12 cells. Neuroscience 56, 441-451.
8. Changeux, J. P. (2010). Nicotine addiction and nicotinic receptors: lessons from genetically modified mice. Nat. Rev. Neurosci. 11, 389-401.
9. Chen, L. T., Gilman, A. G. and Kozasa, T. (1999). A candidate target for G protein action in brain. J. Biol. Chem. 274, 26931-26938.
10. Connolly, J. L., Greene, L. A., Viscarello, R. R. and Riley, W. D. (1979). Rapid, sequential changes in surface morphology of PC12 pheochromocytoma cells in response to nerve growth factor. J. Cell Biol. 82, 820-827.
11. Coronas, V., Durand, M., Chabot, J. G., Jourdan, F. and Quirion, R. (2000). Acetylcholine induces neuritic outgrowth in rat primary olfactory bulb cultures. Neuroscience 98, 213-219.
12. Corriveau, R. A., Romano, S. J., Conroy, W. G., Oliva, L. and Berg, D. K. (1995). Expression of neuronal acetylcholine receptor genes in vertebrate skeletal muscle during development. J. Neurosci. 15, 1372-1383.
13. Csillik, B., Mihaly, A. and Knyihar-Csillik, E. (2004). Cytochemical correlates of the sleep-wake interface: concerted expression of brain-derived nitric oxide synthase (bNOS) and the nicotinic acetylcholine receptor (nAChR) in a columnoid organization of the primate prefrontal cortex. Ann. Anat. 186, 217-221.
14. D'Alcantara, P., Schiffrann, S. N. and Swillens, S. (2003). Bidirectional synaptic plasticity as a consequence of interdependent calcium controlled phosphorylation and dephosphorylation pathways. Eur. J. Neurosci. 17, 2521-2528.
15. Dani, J. A. and Bertrand, D. (2007). Nicotinic acetylcholine receptors and nicotinic cholinergic mechanisms of the central nervous system. Annu. Rev. Pharmacol. Toxicol. 47, 699-729.
16. Danthi, S. and Boyd, R. T. (2006). Cell specificity of a rat neuronal nicotinic acetylcholine receptor α7 subunit gene promoter. Neurosci. Lett. 400, 63-68.
17. 2+/calmodulin-dependent kinase pathway. J. Neurosci. 15, 7966-7978.
18. de Lucas-Cerrillo, A. M., Maldifassi, M. C., Arnalich, F., Renart, J., Atienza, G., Serantes, R., Cruces, J., Sánchez-Pacheco, A., Andrès-Mateos, E. and Montiel, C. (2011). Function of partially duplicated human α7 nicotinic receptor subunit CHRFAM7A gene: potential implications for the cholinergic anti-inflammatory response. J. Biol. Chem. 286, 594-606.
19. Denny, J. B. (2006). Molecular mechanisms, biological actions, and neuropharmacology of the growth-associated protein GAP-43. Curr. Neuropharmacol. 4, 293-304.
20. Di Giovanni, S., De Biase, A., Yakovlev, A., Finn, T., Beers, J., Hoffman, E. P. and Faden, A. I. (2005). In vivo and in vitro characterization of novel neuronal plasticity factors identified following spinal cord injury. J. Biol. Chem. 280, 2084-2091.
21. Drubin, D.G., Feinstein, S. C., Shooter, E. M. andKirschner, M. W. (1985). Nerve growth factor-induced neurite outgrowth in PC12 cells involves the coordinate induction of microtubule assembly and assembly-promoting factors. J. Cell Biol. 101, 1799-1807.
22. Duffy, A. M., Fitzgerald, M. L., Chan, J., Robinson, D. C., Milner, T. A., Mackie, K. and Pickel, V. M. (2011). Acetylcholine α7 nicotinic and dopamine D2 receptors are targeted to many of the same postsynaptic dendrites and astrocytes in the rodent prefrontal cortex. Synapse 65, 1350-1367.
23. Esdar, C., Oehrlein, S. A., Reinhardt, S., Maelicke, A. and Herget, T. (1999). The protein kinase C (PKC) substrate GAP-43 is already expressed in neural precursor cells, colocalizes with PKCη and binds calmodulin. Eur. J. Neurosci. 11, 503-516.
24. Flavell, S. W. and Greenberg, M. E. (2008). Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu. Rev. Neurosci. 31, 563-590.
25. Gamby, C., Waage, M. C., Allen, R. G. and Baizer, L. (1996). Analysis of the role of calmodulin binding and sequestration in neuromodulin (GAP-43) function. J. Biol. Chem. 271, 26698-26705.
26. Ge, X., Qiu, Y., Loh, H. H. and Law, P. Y. (2009). GRIN1 regulates m-opioid receptor activities by tethering the receptor and G protein in the lipid raft. J. Biol. Chem. 284, 36521-36534.
27. Grabe, H. J., Schwahn, C., Mahler, J., Schulz, A., Spitzer, C., Fenske, K., Appel, K., Barnow, S., Nauck, M., Schomerus, G. et al. (2012a). Moderation of adult depression by the serotonin transporter promoter variant (5-HTTLPR), childhood abuse and adult traumatic events in a general population sample. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 159B, 298-309.
28. Grabe, H. J., Schwahn, C., Mahler, J., Appel, K., Schulz, A., Spitzer, C., Fenske, K., Barnow, S., Freyberger, H. J., Teumer, A. et al. (2012b). Genetic epistasis between the brain-derived neurotrophic factor Val66Met polymorphism and the 5-HTT promoter polymorphism moderates the susceptibility to depressive disorders after childhood abuse. Prog. Neuropsychopharmacol. Biol. Psychiatry 36, 264-270.
29. Gutièrrez, G., Mendoza, C., Zapata, E., Montiel, A., Reyes, E., Montañ o, L. F. and Löpez-Marure, R. (2007). Dehydroepiandrosterone inhibits the TNF-alpha-induced inflammatory response in human umbilical vein endothelial cells. Atherosclerosis 190, 90-99.
30. Hannan, M. A., Kabbani, N., Paspalas, C. D. and Levenson, R. (2008). Interaction with dopamine D2 receptor enhances expression of transient receptor potential channel 1 at the cell surface. Biochim. Biophys. Acta 1778, 974-982.
31. Henley, J. R., Huang, K. H., Wang, D. and Poo, M. M. (2004). Calcium mediates bidirectional growth cone turning induced by myelin-associated glycoprotein. Neuron 44, 909-916.
32. Hieber, V., Agranoff, B. W. and Goldman, D. (1992). Target-dependent regulation of retinal nicotinic acetylcholine receptor and tubulin RNAs during optic nerve regeneration in goldfish. J. Neurochem. 58, 1009-1015.
33. Hilmas, C., Pereira, E. F., Alkondon, M., Rassoulpour, A., Schwarcz, R. and Albuquerque, E. X. (2001). The brain metabolite kynurenic acid inhibits α7 nicotinic receptor activity and increases non-α7 nicotinic receptor expression: physiopathological implications. J. Neurosci. 21, 7463-7473.
34. Hruska, M. and Nishi, R. (2007). Cell-autonomous inhibition of α7-containing nicotinic acetylcholine receptors prevents death of parasympathetic neurons during development. J. Neurosci. 27, 11501-11509.
35. 1-42-induced neurite outgrowth reduction in rat primary cortical neurons: neuroprotective effects of α7 neuronal nicotinic acetylcholine receptor ligands. Brain Res. 1151, 227-235.
36. Jian, X., Hidaka, H. and Schmidt, J. T. (1994). Kinase requirement for retinal growth cone motility. J. Neurobiol. 25, 1310-1328.
37. Jouvenceau, A. and Dutar, P. (2006). A role for the protein phosphatase 2B in altered hippocampal synaptic plasticity in the aged rat. J. Physiol. Paris 99, 154-161.
38. Kabbani, N. and Levenson, R. (2007). A proteomic approach to receptor signaling: molecular mechanisms and therapeutic implications derived from discovery of the dopamine D2 receptor signalplex. Eur. J. Pharmacol. 572, 83-93.
39. Kabbani, N., Woll, M. P., Levenson, R., Lindstrom, J. M. and Changeux, J.-P. (2007). Intracellular complexes of the β2 subunit of the nicotinic acetylcholine receptor in brain identified by proteomics. Proc. Natl. Acad. Sci. USA 104, 20570-20575.
40. Kaiser, P., Akerboom, T., Molnar, P. and Reinauer, H. (2008). Modified HPLCelectrospray ionization/mass spectrometry method for HbA1c based on IFCC reference measurement procedure. Clin. Chem. 54, 1018-1022.
41. Kano, Y., Hiragami, F., Kawamura, K., Kimata, Y., Nakagiri, S., Poffenberger, C. K., Akiyama, J., Okishima, K., Koike, Y. and Gomita, Y. (2002). Immunosuppressant FK506 induces sustained activation of MAP kinase and promotes neurite outgrowth in PC12 mutant cells incapable of differentiating. Cell Struct. Funct. 27, 393-398.
42. Lauder, J. M. and Schambra, U. B. (1999). Morphogenetic roles of acetylcholine. Environ. Health Perspect. 107 Suppl. 1, 65-69.
43. Lee, G., Newman, S. T., Gard, D. L., Band, H. and Panchamoorthy, G. (1998). Tau interacts with src-family non-receptor tyrosine kinases. J. Cell Sci. 111, 3167-3177.
44. Leu, B., Koch, E. and Schmidt, J. T. (2010). GAP43 phosphorylation is critical for growth and branching of retinotectal arbors in zebrafish. Dev. Neurobiol. 70, 897-911.
45. Lin, R., Karpa, K., Kabbani, N., Goldman-Rakic, P. and Levenson, R. (2001). Dopamine D2 and D3 receptors are linked to the actin cytoskeleton via interaction with filamin A. Proc. Natl. Acad. Sci. USA 98, 5258-5263.
46. Lin, H., Vicini, S., Hsu, F. C., Doshi, S., Takano, H., Coulter, D. A. and Lynch, D. R. (2010). Axonal α7 nicotinic ACh receptors modulate presynaptic NMDA receptor expression and structural plasticity of glutamatergic presynaptic boutons. Proc. Natl. Acad. Sci. USA 107, 16661-16666.
47. Lindstrom, J., Schoepfer, R., Conroy, W. G. and Whiting, P. (1990). Structural and functional heterogeneity of nicotinic receptors. Ciba Found. Symp. 152, 23-42, discussion 43-52.
48. Liu, Q. and Berg, D. K. (1999). Actin filaments and the opposing actions of CaM kinase II and calcineurin in regulating α7-containing nicotinic receptors on chick ciliary ganglion neurons. J. Neurosci. 19, 10280-10288.
49. Liu, Y. C. and Storm, D. R. (1989). Dephosphorylation of neuromodulin by calcineurin. J. Biol. Chem. 264, 12800-12804.
50. Lopes, C., Pereira, E. F., Wu, H. Q., Purushottamachar, P., Njar, V., Schwarcz, R. and Albuquerque, E. X. (2007). Competitive antagonism between the nicotinic allosteric potentiating ligand galantamine and kynurenic acid at α7* nicotinic receptors. J. Pharmacol. Exp. Ther. 322, 48-58.
51. Lowery, L. A. and Van Vactor, D. (2009). The trip of the tip: understanding the growth cone machinery. Nat. Rev. Mol. Cell Biol. 10, 332-343.
52. Madsen, J. R., MacDonald, P., Irwin, N., Goldberg, D. E., Yao, G. L., Meiri, K. F., Rimm, I. J., Stieg, P. E. and Benowitz, L. I. (1998). Tacrolimus (FK506) increases neuronal expression of GAP-43 and improves functional recovery after spinal cord injury in rats. Exp. Neurol. 154, 673-683.
53. Masuho, I., Mototani, Y., Sahara, Y., Asami, J., Nakamura, S., Kozasa, T. and Inoue, T. (2008). Dynamic expression patterns of G protein-regulated inducer of neurite outgrowth 1 (GRIN1) and its colocalization with Gao implicate significant roles of Gao-GRIN1 signaling in nervous system. Dev. Dyn. 237, 2415-2429.
54. Mattson, M. P. (2008). Glutamate and neurotrophic factors in neuronal plasticity and disease. Ann. N. Y. Acad. Sci. 1144, 97-112.
55. Mortimer, D., Fothergill, T., Pujic, Z., Richards, L. J. and Goodhill, G. J. (2008). Growth cone chemotaxis. Trends Neurosci. 31, 90-98.
56. Myatt, D. R. and Nasuto, S. J. (2008). Improved automatic midline tracing of neurites with Neuromantic. BMC Neurosci. 9 Suppl. 1, P81.
57. Nakata, H. and Kozasa, T. (2005). Functional characterization of Gao signaling through G protein-regulated inducer of neurite outgrowth 1. Mol. Pharmacol. 67, 695-702.
58. Owen, A. and Bird, M. (1995). Acetylcholine as a regulator of neurite outgrowth and motility in cultured embryonic mouse spinal cord. Neuroreport 6, 2269-2272.
59. Pankratov, Y., Lalo, U., Krishtal, O. and Verkhratsky, A. (2002). Ionotropic P2X purinoreceptors mediate synaptic transmission in rat pyramidal neurones of layer II/ III of somato-sensory cortex. J. Physiol. 542, 529-536.
60. Paulo, J. A., Brucker, W. J. and Hawrot, E. (2009). Proteomic analysis of an α7 nicotinic acetylcholine receptor interactome. J. Proteome Res. 8, 1849-1858.
61. Pereira, E. F., Hilmas, C., Santos, M. D., Alkondon, M., Maelicke, A. and Albuquerque, E. X. (2002). Unconventional ligands and modulators of nicotinic receptors. J. Neurobiol. 53, 479-500.
62. Perry, D. C., Mao, D., Gold, A. B., McIntosh, J. M., Pezzullo, J. C. and Kellar, K. J. (2007). Chronic nicotine differentially regulates α6- and β3-containing nicotinic cholinergic receptors in rat brain. J. Pharmacol. Exp. Ther. 322, 306-315.
63. Petros, T. J., Rebsam, A. and Mason, C. A. (2008). Retinal axon growth at the optic chiasm: to cross or not to cross. Annu. Rev. Neurosci. 31, 295-315.
64. Rashid, T., Banerjee, M. and Nikolic, M. (2001). Phosphorylation of Pak1 by the p35/ Cdk5 kinase affects neuronal morphology. J. Biol. Chem. 276, 49043-49052.
65. Romano, S. J., Corriveau, R. A., Schwarz, R. I. and Berg, D. K. (1997). Expression of the nicotinic receptor α7 gene in tendon and periosteum during early development. J. Neurochem. 68, 640-648.
66. Rü diger, T. and Bolz, J. (2008). Acetylcholine influences growth cone motility and morphology of developing thalamic axons. Cell Adh. Migr. 2, 30-37.
67. Sarma, T., Voyno-Yasenetskaya, T., Hope, T. J. and Rasenick, M. M. (2003). Heterotrimeric G-proteins associate with microtubules during differentiation in PC12 pheochromocytoma cells. FASEB J. 17, 848-859.
68. Skene, J. H. (1989). Axonal growth-associated proteins. Annu. Rev. Neurosci. 12, 127-156.
69. Skene, J. H. (1990). GAP-43 as a 'calmodulin sponge' and some implications for calcium signalling in axon terminals. Neurosci. Res. 13 Suppl, S112-S125.
70. Slemmon, J. R., Morgan, J. I., Fullerton, S. M., Danho, W., Hilbush, B. S. and Wengenack, T. M. (1996). Camstatins are peptide antagonists of calmodulin based upon a conserved structural motif in PEP-19, neurogranin, and neuromodulin. J. Biol. Chem. 271, 15911-15917.
71. Spitzer, N. C. (2012). Activity-dependent neurotransmitter respecification. Nat. Rev. Neurosci. 13, 94-106.
72. Spitzer, T. L., Rojas, A., Zelenko, Z., Aghajanova, L., Erikson, D. W., Barragan, F., Meyer, M., Tamaresis, J. S., Hamilton, A. E., Irwin, J. C. et al. (2012). Perivascular human endometrial mesenchymal stem cells express pathways relevant to self-renewal, lineage specification, and functional phenotype. Biol. Reprod. 86, 58.
73. Stefan, M. I., Edelstein, S. J. and Le Novére, N. (2008). An allosteric model of calmodulin explains differential activation of PP2B and CaMKII. Proc. Natl. Acad. Sci. USA 105, 10768-10773.
74. Stiess, M. and Bradke, F. (2011). Neuronal polarization: the cytoskeleton leads the way. Dev. Neurobiol. 71, 430-444.
75. Stone, T. W. and Darlington, L. G. (2002). Endogenous kynurenines as targets for drug discovery and development. Nat. Rev. Drug Discov. 1, 609-620.
76. Strittmatter, S. M., Valenzuela, D., Vartanian, T., Sudo, Y., Zuber, M. X. and Fishman, M. C. (1991). Growth cone transduction: Go and GAP-43. J. Cell Sci. 15 Suppl, 27-33.
77. Strittmatter, S. M., Fishman, M. C. and Zhu, X. P. (1994a). Activated mutants of the a subunit of Go promote an increased number of neurites per cell. J. Neurosci. 14, 2327-2338.
78. Strittmatter, S. M., Igarashi, M. and Fishman, M. C. (1994b). GAP-43 amino terminal peptides modulate growth cone morphology and neurite outgrowth. J. Neurosci. 14, 5503-5513.
79. Swarzenski, B. C., O'Malley, K. L. and Todd, R. D. (1996). PTX-sensitive regulation of neurite outgrowth by the dopamine D3 receptor. Neuroreport 7, 573-576.
80. 2+/calmodulin-dependent protein kinase IV-mediated LIM kinase activation is critical for calcium signal-induced neurite outgrowth. J. Biol. Chem. 284, 28554-28562.
81. Vallejo, Y. F., Buisson, B., Bertrand, D. and Green, W. N. (2005). Chronic nicotine exposure upregulates nicotinic receptors by a novel mechanism. J. Neurosci. 25, 5563- 5572.
82. van Kesteren, R. E. and Spencer, G. E. (2003). The role of neurotransmitters in neurite outgrowth and synapse formation. Rev. Neurosci. 14, 217-231.
83. 2+-dependent growth cone guidance. Neuron 43, 835-846.
84. Yamatani, H., Kawasaki, T., Mita, S., Inagaki, N. and Hirata, T. (2010). Proteomics analysis of the temporal changes in axonal proteins during maturation. Dev. Neurobiol. 70, 523-537.
85. Yang, H., Wan, L., Song, F., Wang, M. and Huang, Y. (2009). Palmitoylation modification of Gao depresses its susceptibility to GAP-43 activation. Int. J. Biochem. Cell Biol. 41, 1495-1501.
86. Zheng, J. Q., Felder, M., Connor, J. A. and Poo, M. M. (1994). Turning of nerve growth cones induced by neurotransmitters. Nature 368, 140-144.
87. Zhou, F. Q.,Waterman-Storer, C.M. andCohan, C. S. (2002). Focal loss of actin bundles causes microtubule redistribution and growth cone turning. J. Cell Biol. 157, 839-849.