The MT2 receptor stimulates axonogenesis and enhances synaptic transmission by activating Akt signaling

Cell Death and Differentiation

Volumn 22, Issue 4, 2015, Pages 583-596

  Liu, D ^a,b   Wei, N ^a,b   Man, H Y ^c   Lu, Y ^a,b   Zhu, L Q ^a,b   Wang, J Z ^a,b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^c USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; GLYCOGEN SYNTHASE KINASE 3; HORMONE RECEPTOR BLOCKING AGENT; MELATONIN 2 RECEPTOR; PROTEIN KINASE B; SHORT HAIRPIN RNA; 4-PHENYL-2-PROPIONAMIDOTETRALINE; GLYCOGEN SYNTHASE KINASE 3 BETA; MELATONIN; MELATONIN 1 RECEPTOR; SMALL INTERFERING RNA; TETRALIN DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DENDRITE; ELECTROPORATION; EMBRYO; ENZYME ACTIVATION; ENZYME BINDING; HORMONE RECEPTOR INTERACTION; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER; NERVE FIBER GROWTH; NERVE GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN MOTIF; RAT; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL CULTURE; CYTOLOGY; DRUG EFFECTS; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GENETICS; HEK293 CELL LINE; IN VITRO STUDY; METABOLISM; NERVE CELL;

ANIMALS; AXONS; CELLS, CULTURED; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GLYCOGEN SYNTHASE KINASE 3; HEK293 CELLS; HUMANS; IN VITRO TECHNIQUES; MELATONIN; MICE; MICE, KNOCKOUT; NEURONS; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RECEPTOR, MELATONIN, MT1; RECEPTOR, MELATONIN, MT2; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; TETRAHYDRONAPHTHALENES;

EID: 84925482594     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2014.195     Document Type: Article

References (61)

1. Polleux F, Ince-Dunn G, Ghosh A. Transcriptional regulation of vertebrate axon guidance and synapse formation. Nat Rev Neurosci 2007; 8: 331-340.
2. Bradke F, Dotti CG. The role of local actin instability in axon formation. Science 1999; 283: 1931-1934.
3. Schwamborn JC, Muller M, Becker AH, Puschel AW. Ubiquitination of the GTPase Rap1B by the ubiquitin ligase Smurf2 is required for the establishment of neuronal polarity. EMBO J 2007; 26: 1410-1422.
4. Song AH, Wang D, Chen G, Li Y, Luo J, Duan S et al. A selective filter for cytoplasmic transport at the axon initial segment. Cell 2009; 136: 1148-1160.
5. Ozdinler PH, Macklis JD. IGF-I specifically enhances axon outgrowth of corticospinal motor neurons. Nat Neurosci 2006; 9: 1371-1381.
6. Dalva MB, Takasu MA, Lin MZ, Shamah SM, Hu L, Gale NW et al. EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 2000; 103: 945-956.
7. Pandi-Perumal SR, Trakht I, Srinivasan V, Spence DW, Maestroni GJ, Zisapel N et al. Physiological effects of melatonin: role of melatonin receptors and signal transduction pathways. Prog Neurobiol 2008; 85: 335-353.
8. Ochoa-Sanchez R, Comai S, Lacoste B, Bambico FR, Dominguez-Lopez S, Spadoni G et al. Promotion of non-rapid eye movement sleep and activation of reticular thalamic neurons by a novel MT2 melatonin receptor ligand. J Neurosci 2011; 31: 18439-18452.
9. Comai S, Ochoa-Sanchez R, Gobbi G. Sleep-wake characterization of double MT(1)/MT(2) receptor knockout mice and comparison with MT(1) and MT(2) receptor knockout mice. Behav Brain Res 2013; 243: 231-238.
10. Dubocovich ML, Masana MI, Iacob S, Sauri DM. Melatonin receptor antagonists that differentiate between the human Mel1a and Mel1b recombinant subtypes are used to assess the pharmacological profile of the rabbit retina ML1 presynaptic heteroreceptor. Naunyn-Schmiedeberg's Arch Pharmacol 1997; 355: 365-375.
11. Lankford KL, DeMello FG, Klein WL. D1-type dopamine receptors inhibit growth cone motility in cultured retina neurons: evidence that neurotransmitters act as morphogenic growth regulators in the developing central nervous system. Proc Natl Acad Sci USA 1988; 85: 4567-4571.
12. Larson J, Jessen RE, Uz T, Arslan AD, Kurtuncu M, Imbesi M et al. Impaired hippocampal long-term potentiation in melatonin MT2 receptor-deficient mice. Neurosci Lett 2006; 393: 23-26.
13. Wan Q, Man HY, Liu F, Braunton J, Niznik HB, Pang SF et al. Differential modulation of GABAA receptor function by Mel1a and Mel1b receptors. Nat Neurosci 1999; 2: 401-403.
14. Savaskan E, Ayoub MA, Ravid R, Angeloni D, Fraschini F, Meier F et al. Reduced hippocampal MT2 melatonin receptor expression in Alzheimer's disease. J Pineal Res 2005; 38: 10-16.
15. Comai S, Gobbi G. Unveiling the role of melatonin MT2 receptors in sleep, anxiety and other neuropsychiatric diseases: a novel target in psychopharmacology. J Psychiatry Neurosci 2014; 39: 6-21.
16. Ochoa-Sanchez R, Rainer Q, Comai S, Spadoni G, Bedini A, Rivara S et al. Anxiolytic effects of the melatonin MT(2) receptor partial agonist UCM765: comparison with melatonin and diazepam. Prog Neuropsychopharmacol Biol Psychiatry 2012; 39: 318-325.
17. Gumuslu E, Mutlu O, Sunnetci D, Ulak G, Celikyurt IK, Cine N et al. The antidepressant agomelatine improves memory deterioration and upregulates CREB and BDNF gene expression levels in unpredictable chronic mild stress (UCMS)-exposed mice. Drug Target Insights 2014; 8: 11-21.
18. Kaech S, Banker G. Culturing hippocampal neurons. Nat Protoc 2006; 1: 2406-2415.
19. Dotti CG, Sullivan CA, Banker GA. The establishment of polarity by hippocampal neurons in culture. J Neurosci 1988; 8: 1454-1468.
20. Barnes AP, Polleux F. Establishment of axon-dendrite polarity in developing neurons. Annu Rev Neurosci 2009; 32: 347-381.
21. Dotti CG, Banker GA. Experimentally induced alteration in the polarity of developing neurons. Nature 1987; 330: 254-256.
22. Jepsen K, Hermanson O, Onami TM, Gleiberman AS, Lunyak V, McEvilly RJ et al. Combinatorial roles of the nuclear receptor corepressor in transcription and development. Cell 2000; 102: 753-763.
23. Shelly M, Cancedda L, Heilshorn S, Sumbre G, Poo MM. LKB1/STRAD promotes axon initiation during neuronal polarization. Cell 2007; 129: 565-577.
24. Hatanaka Y, Murakami F. In vitro analysis of the origin, migratory behavior, and maturation of cortical pyramidal cells. J Comp Neurol 2002; 454: 1-14.
25. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 2004; 7: 136-144.
26. Craig AM, Graf ER, Linhoff MW. How to build a central synapse: clues from cell culture. Trends Neurosci 2006; 29: 8-20.
27. Ryan TA, Reuter H, Wendland B, Schweizer FE, Tsien RW, Smith SJ. The kinetics of synaptic vesicle recycling measured at single presynaptic boutons. Neuron 1993; 11: 713-724.
28. Matteoli M, Takei K, Perin MS, Sudhof TC, De Camilli P. Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons. J Cell Biol 1992; 117: 849-861.
29. Zhu LQ, Liu D, Hu J, Cheng J, Wang SH, Wang Q et al. GSK-3 beta inhibits presynaptic vesicle exocytosis by phosphorylating P/Q-type calcium channel and interrupting SNARE complex formation. J Neurosci 2010; 30: 3624-3633.
30. Yoshimura T, Kawano Y, Arimura N, Kawabata S, Kikuchi A, Kaibuchi K. GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 2005; 120: 137-149.
31. Chi XX, Schmutzler BS, Brittain JM, Wang Y, Hingtgen CM, Nicol GD et al. Regulation of N-type voltage-gated calcium channels (Cav2.2) and transmitter release by collapsin response mediator protein-2 (CRMP-2) in sensory neurons. J Cell Sci 2009; 122: 4351-4362.
32. Peineau S, Bradley C, Taghibiglou C, Doherty A, Bortolotto ZA, Wang YT et al. The role of GSK-3 in synaptic plasticity. Br J Pharmacol 2008; 153: S428-S437.
33. Jiang H, Guo W, Liang X, Rao Y. Both the establishment and the maintenance of neuronal polarity require active mechanisms: critical roles of GSK-3beta and its upstream regulators. Cell 2005; 120: 123-135.
34. Cole AR, Knebel A, Morrice NA, Robertson LA, Irving AJ, Connolly CN et al. GSK-3 phosphorylation of the Alzheimer epitope within collapsin response mediator proteins regulates axon elongation in primary neurons. J Biol Chem 2004; 279: 50176-50180.
35. Shi SH, Jan LY, Jan YN. Hippocampal neuronal polarity specified by spatially localized mPar3/mPar6 and PI 3-kinase activity. Cell 2003; 112: 63-75.
36. Bockaert J, Roussignol G, Becamel C, Gavarini S, Joubert L, Dumuis A et al. GPCR-interacting proteins (GIPs): nature and functions. Biochem Soc Trans 2004; 32: 851-855.
37. Brydon L, Petit L, Delagrange P, Strosberg AD, Jockers R. Functional expression of MT2 (Mel1b) melatonin receptors in human PAZ6 adipocytes. Endocrinology 2001; 142: 4264-4271.
38. Shelly M, Lim BK, Cancedda L, Heilshorn SC, Gao H, Poo MM. Local and long-range reciprocal regulation of cAMP and cGMP in axon/dendrite formation. Science 2010; 327: 547-552.
39. Beaulieu JM, Sotnikova TD, Marion S, Lefkowitz RJ, Gainetdinov RR, Caron MG. An Akt/ beta-arrestin 2/PP2A signaling complex mediates dopaminergic neurotransmission and behavior. Cell 2005; 122: 261-273.
40. Du K, Tsichlis PN. Regulation of the Akt kinase by interacting proteins. Oncogene 2005; 24: 7401-7409.
41. Reddy PH. Abnormal tau, mitochondrial dysfunction, impaired axonal transport of mitochondria, and synaptic deprivation in Alzheimer's disease. Brain Res 2011; 1415: 136-148.
42. Rossi F, Gianola S, Corvetti L. Regulation of intrinsic neuronal properties for axon growth and regeneration. Prog Neurobiol 2007; 81: 1-28.
43. Deumens R, Koopmans GC, Joosten EA. Regeneration of descending axon tracts after spinal cord injury. Prog Neurobiol 2005; 77: 57-89.
44. Zhu LQ, Zheng HY, Peng CX, Liu D, Li HL, Wang Q et al. Protein phosphatase 2A facilitates axonogenesis by dephosphorylating CRMP2. J Neurosci 2010; 30: 3839-3848.
45. Peng CX, Hu J, Liu D, Hong XP, Wu YY, Zhu LQ et al. Disease-modified glycogen synthase kinase-3beta intervention by melatonin arrests the pathology and memory deficits in an Alzheimer's animal model. Neurobiol Aging 2013; 34: 1555-1563.
46. Bahna SG, Sathiyapalan A, Foster JA, Niles LP. Regional upregulation of hippocampal melatonin MT2 receptors by valproic acid: therapeutic implications for Alzheimer's disease. Neurosci Lett 2014; 576: 84-87.
47. Iuvone PM, Gan J. Functional interaction of melatonin receptors and D1 dopamine receptors in cultured chick retinal neurons. J Neurosci 1995; 15: 2179-2185.
48. Witt-Enderby PA, Bennett J, Jarzynka MJ, Firestine S, Melan MA. Melatonin receptors and their regulation: biochemical and structural mechanisms. Life Sci 2003; 72: 2183-2198.
49. Catala MD, Quay WB, Timiras PS. Effects of thyroid hormone on light/dark melatonin synthesis and release by young and maturing rat pineal glands in vitro. Int J Dev Neurosci 1988; 6: 285-288.
50. Drijfhout WJ, Grol CJ, Westerink BH. Parasympathetic inhibition of pineal indole metabolism by prejunctional modulation of noradrenaline release. Eur J Pharmacol 1996; 308: 117-124.
51. Yamada H, Yatsushiro S, Ishio S, Hayashi M, Nishi T, Yamamoto A et al. Metabotropic glutamate receptors negatively regulate melatonin synthesis in rat pinealocytes. J Neurosci 1998; 18: 2056-2062.
52. Foldes A, Maxwell CA, Rintoul AJ, Edols RW. Sheep pineal beta-adrenoceptor function-interaction with gamma-aminobutyric acid. Neuroendocrinology 1984; 38: 206-211.
53. Simonneaux V, Ribelayga C. Generation of the melatonin endocrine message in mammals: a review of the complex regulation of melatonin synthesis by norepinephrine, peptides, and other pineal transmitters. Pharmacol Rev 2003; 55: 325-395.
54. Liu F, Day M, Muniz LC, Bitran D, Arias R, Revilla-Sanchez R et al. Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci 2008; 11: 334-343.
55. Bernal J. Thyroid hormone receptors in brain development and function. Nat Clin Pract Endocrinol Metab 2007; 3: 249-259.
56. McCarthy MM. Estradiol and the developing brain. Physiol Rev 2008; 88: 91-124.
57. Spencer GE, Klumperman J, Syed NI. Neurotransmitters and neurodevelopment. Role of dopamine in neurite outgrowth, target selection and specific synapse formation. Perspect Dev Neurobiol 1998; 5: 451-467.
58. Ruthel G, Hollenbeck PJ. Growth cones are not required for initial establishment of polarity or differential axon branch growth in cultured hippocampal neurons. J Neurosci 2000; 20: 2266-2274.
59. Jensen EC. Quantitative analysis of histological staining and fluorescence using ImageJ. Anat Rec 2013; 296: 378-381.
60. Takeuchi A, O'Leary DD. Radial migration of superficial layer cortical neurons controlled by novel Ig cell adhesion molecule MDGA1. J Neurosci 2006; 26: 4460-4464.
61. Tabata H, Nakajima K. Efficient in utero gene transfer system to the developing mouse brain using electroporation: visualization of neuronal migration in the developing cortex. Neuroscience 2001; 103: 865-872.