Brain-Derived Neurotrophic Factor-Tyrosine Kinase B Pathway Mediates NMDA Receptor NR2B Subunit Phosphorylation in the Supraoptic Nuclei Following Progressive Dehydration

Journal of Neuroendocrinology

Volumn 23, Issue 10, 2011, Pages 894-905

  Carreno F R ^a   Walch, J D ^a,b   Dutta, M ^a   Nedungadi, T P ^a   Cunningham, J T ^a  

^a UNIVERSITY OF NORTH TEXAS HEALTH SCIENCE CENTER   (United States)

^b UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

Brain derived neurotrophic factor; NMDA receptor; Osmotic pressure; Vasopressin

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; RECEPTOR SUBUNIT; VASOPRESSIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BRAIN; CONTROLLED STUDY; DEHYDRATION; IMMUNOHISTOCHEMISTRY; LASER MICRODISSECTION; MALE; NERVE CELL; NONHUMAN; OSMOTIC PRESSURE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RAT; REHYDRATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUPRAOPTIC NUCLEUS; WATER DEPRIVATION;

ANIMALS; BASE SEQUENCE; BLOTTING, WESTERN; BRAIN-DERIVED NEUROTROPHIC FACTOR; DEHYDRATION; DNA PRIMERS; IMMUNOHISTOCHEMISTRY; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; RATS, SPRAGUE-DAWLEY; RECEPTORS, N-METHYL-D-ASPARTATE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SUPRAOPTIC NUCLEUS;

EID: 80053147165     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2011.02209.x     Document Type: Article

References (70)

1. Leibrock J, Lottspeich F, Hohn A, Hofer M, Hengerer B, Masiakowski P, Thoenen H, Barde YA. Molecular cloning and expression of brain-derived neurotrophic factor. Nature 1989; 341: 149-152.
2. Lu B. BDNF and activity-dependent synaptic modulation. Learn Mem 2003; 10: 86-98.
3. Bramham CR, Messaoudi E. BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis. Prog Neurobiol 2005; 76: 99-125.
4. Soule J, Messaoudi E, Bramham CR. Brain-derived neurotrophic factor and control of synaptic consolidation in the adult brain. Biochem Soc Trans 2006; 34: 600-604.
5. Numakawa T, Suzuki S, Kumamaru E, Adachi N, Richards M, Kunugi H. BDNF function and intracellular signaling in neurons. Histol Histopathol 2010; 25: 237-258.
6. Brunig I, Penschuck S, Berninger B, Benson J, Fritschy JM. BDNF reduces miniature inhibitory postsynaptic currents by rapid downregulation of GABA(A) receptor surface expression. Eur J Neurosci 2001; 13: 1320-1328.
7. Hewitt SA, Bains JS. Brain-derived neurotrophic factor silences GABA synapses onto hypothalamic neuroendocrine cells through a postsynaptic dynamin-mediated mechanism. J Neurophysiol 2006; 95: 2193-2198.
8. Jovanovic JN, Thomas P, Kittler JT, Smart TG, Moss SJ. Brain-derived neurotrophic factor modulates fast synaptic inhibition by regulating GABA(A) receptor phosphorylation, activity, and cell-surface stability. J Neurosci 2004; 24: 522-530.
9. Caldeira MV, Melo CV, Pereira DB, Carvalho RF, Carvalho AL, Duarte CB. BDNF regulates the expression and traffic of NMDA receptors in cultured hippocampal neurons. Mol Cell Neurosci 2007; 35: 208-219.
10. Carvalho AL, Caldeira MV, Santos SD, Duarte CB. Role of the brain-derived neurotrophic factor at glutamatergic synapses. Br J Pharmacol 2008; 153(Suppl 1): S310-S324.
11. Klau M, Hartmann M, Erdmann KS, Heumann R, Lessmann V. Reduced number of functional glutamatergic synapses in hippocampal neurons overexpressing full-length TrkB receptors. J Neurosci Res 2001; 66: 327-336.
12. Marmigere F, Rage F, Tapia-Arancibia L, Arancibia S. Expression of mRNAs encoding BDNF and its receptor in adult rat hypothalamus. Neuroreport 1998; 9: 1159-1163.
13. Yan Q, Radeke MJ, Matheson CR, Talvenheimo J, Welcher AA, Feinstein SC. Immunocytochemical localization of TrkB in the central nervous system of the adult rat. J Comp Neurol 1997; 378: 135-157.
14. Ohbuchi T, Yokoyama T, Saito T, Hashimoto H, Suzuki H, Otsubo H, Fujihara H, Suzuki H, Ueta Y. Brain-derived neurotrophic factor inhibits spontaneous inhibitory postsynaptic currents in the rat supraoptic nucleus. Brain Res 2009; 1258: 34-42.
15. Armstrong WE. Morphological and electrophysiological classification of hypothalamic supraoptic neurons. Prog Neurobiol 1995; 47: 291-339.
16. Hatton GI. Oxytocin and vasopressin neurones: vive la difference!. J Physiol 1997; 500: 284.
17. McKinley MJ, Mathai ML, McAllen RM, McClear RC, Miselis RR, Pennington GL, Vivas L, Wade JD, Oldfield BJ. Vasopressin secretion: osmotic and hormonal regulation by the lamina terminalis. J Neuroendocrinol 2004; 16: 340-347.
18. Bourque CW. Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci 2008; 9: 519-531.
19. Leng G, Brown CH, Bull PM, Brown D, Scullion S, Currie J, Blackburn-Munro RE, Feng J, Onaka T, Verbalis JG, Russell JA, Ludwig M. Responses of magnocellular neurons to osmotic stimulation involves coactivation of excitatory and inhibitory input: an experimental and theoretical analysis. J Neurosci 2001; 21: 6967-6977.
20. Verbalis JG. How does the brain sense osmolality? J Am Soc Nephrol 2007; 18: 3056-3059.
21. Mason WT. Supraoptic neurones of rat hypothalamus are osmosensitive. Nature 1980; 287: 154-157.
22. Aliaga E, Arancibia S, Givalois L, Tapia-Arancibia L. Osmotic stress increases brain-derived neurotrophic factor messenger RNA expression in the hypothalamic supraoptic nucleus with differential regulation of its transcripts. Relation to arginine-vasopressin content. Neuroscience 2002; 112: 841-850.
23. Arancibia S, Lecomte A, Silhol M, Aliaga E, Tapia-Arancibia L. In vivo brain-derived neurotrophic factor release and tyrosine kinase B receptor expression in the supraoptic nucleus after osmotic stress stimulus in rats. Neuroscience 2007; 146: 864-873.
24. Lessmann V. Neurotrophin-dependent modulation of glutamatergic synaptic transmission in the mammalian CNS. Gen Pharmacol 1998; 31: 667-674.
25. Crozier RA, Bi C, Han YR, Plummer MR. BDNF modulation of NMDA receptors is activity dependent. J Neurophysiol 2008; 100: 3264-3274.
26. Boudaba C, Linn DM, Halmos KC, Tasker JG. Increased tonic activation of presynaptic metabotropic glutamate receptors in the rat supraoptic nucleus following chronic dehydration. J Physiol 2003; 551: 815-823.
27. Curras-Collazo MC, Dao J. Osmotic activation of the hypothalamo-neurohypophysial system reversibly downregulates the NMDA receptor subunit, NR2B, in the supraoptic nucleus of the hypothalamus. Brain Res Mol Brain Res 1999; 70: 187-196.
28. Pak CW, Curras-Collazo MC. Expression and plasticity of glutamate receptors in the supraoptic nucleus of the hypothalamus. Microsc Res Tech 2002; 56: 92-100.
29. Kuczewski N, Porcher C, Lessmann V, Medina I, Gaiarsa JL. Activity-dependent dendritic release of BDNF and biological consequences. Mol Neurobiol 2009; 39: 37-49.
30. Nagappan G, Lu B. Activity-dependent modulation of the BDNF receptor TrkB: mechanisms and implications. Trends Neurosci 2005; 28: 464-471.
31. Dunn FL, Brennan TJ, Nelson AE, Robertson GL. The role of blood osmolality and volume in regulating vasopressin secretion in the rat. J Clin Invest 1973; 52: 3212-3219.
32. Gottlieb HB, Ji LL, Jones H, Penny ML, Fleming T, Cunningham JT. Differential effects of water and saline intake on water deprivation-induced c-Fos staining in the rat. Am J Physiol Regul Integr Comp Physiol 2006; 290: R1251-R1261.
33. Jiang B, Akaneya Y, Ohshima M, Ichisaka S, Hata Y, Tsumoto T. Brain-derived neurotrophic factor induces long-lasting potentiation of synaptic transmission in visual cortex in vivo in young rats, but not in the adult. Eur J Neurosci 2001; 14: 1219-1228.
34. Liang FQ, Allen G, Earnest D. Role of brain-derived neurotrophic factor in the circadian regulation of the suprachiasmatic pacemaker by light. J Neurosci 2000; 20: 2978-2987.
35. Rattiner LM, Davis M, French CT, Ressler KJ. Brain-derived neurotrophic factor and tyrosine kinase receptor B involvement in amygdala-dependent fear conditioning. J Neurosci 2004; 24: 4796-4806.
36. Wang C, Bomberg E, Levine A, Billington C, Kotz CM. Brain-derived neurotrophic factor in the ventromedial nucleus of the hypothalamus reduces energy intake. Am J Physiol Regul Integr Comp Physiol 2007; 293: R1037-R1045.
37. Carreno FR, Ji LL, Cunningham JT. Altered central TRPV4 expression and lipid raft association related to inappropriate vasopressin secretion in cirrhotic rats. Am J Physiol Regul Integr Comp Physiol 2009; 296: R454-R466.
38. Shahar T, House SB, Gainer H. Neural activity protects hypothalamic magnocellular neurons against axotomy-induced programmed cell death. J Neurosci 2004; 24: 6553-6562.
39. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, Inc., 1998.
40. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976; 72: 248-254.
41. Mizuno M, Yamada K, Olariu A, Nawa H, Nabeshima T. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J Neurosci 2000; 20: 7116-7121.
42. Briski KP, Nedungadi TP, Koshy Cherian A. Effects of hypoglycaemia on neurotransmitter and hormone receptor gene expression in laser-dissected arcuate neuropeptide Y/agouti-related peptide neurones. J Neuroendocrinol 2010; 22: 599-607.
43. Koyama Y, Baba A, Matsuda T. Endothelins stimulate the expression of neurotrophin-3 in rat brain and rat cultured astrocytes. Neuroscience 2005; 136: 425-433.
44. Zeeni N, Chaumontet C, Moyse E, Fromentin G, Tardivel C, Tome D, Jean A, Darcel N. A positive change in energy balance modulates TrkB expression in the hypothalamus and nodose ganglia of rats. Brain Res 2009; 1289: 49-55.
45. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method. Methods 2001; 25: 402-408.
46. Ji LL, Gottlieb HB, Penny ML, Fleming T, Toney GM, Cunningham JT. Differential effects of water deprivation and rehydration on Fos and FosB/DeltaFosB staining in the rat brainstem. Exp Neurol 2007; 203: 445-456.
47. Huang EJ, Reichardt LF. Trk receptors: roles in neuronal signal transduction. Annu Rev Biochem 2003; 72: 609-642.
48. Curras MC, Dao J. Developmental plasticity of NR1 and NR2B subunit expression in the supraoptic nucleus of the rat hypothalamus. Brain Res Dev Brain Res 1998; 109: 1-12.
49. Curras-Collazo MC, Chin C, Diaz G, Stivers C, Bozzetti L, Tran LY. Immunolabeling reveals cellular localization of the N-methyl-D-aspartate receptor subunit NR2B in neurosecretory cells but not astrocytes of the rat magnocellular nuclei. J Comp Neurol 2000; 427: 93-108.
50. Eyigor O, Centers A, Jennes L. Distribution of ionotropic glutamate receptor subunit mRNAs in the rat hypothalamus. J Comp Neurol 2001; 434: 101-124.
51. Pereira DB, Chao MV. The tyrosine kinase Fyn determines the localization of TrkB receptors in lipid rafts. J Neurosci 2007; 27: 4859-4869.
52. Blum R, Konnerth A. Neurotrophin-mediated rapid signaling in the central nervous system: mechanisms and functions. Physiology (Bethesda) 2005; 20: 70-78.
53. Reichardt LF. Neurotrophin-regulated signalling pathways. Philos Trans R Soc Lond B Biol Sci 2006; 361: 1545-1564.
54. Narisawa-Saito M, Silva AJ, Yamaguchi T, Hayashi T, Yamamoto T, Nawa H. Growth factor-mediated Fyn signaling regulates alpha-amino-3- hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor expression in rodent neocortical neurons. Proc Natl Acad Sci USA 1999; 96: 2461-2466.
55. Nakazawa T, Komai S, Tezuka T, Hisatsune C, Umemori H, Semba K, Mishina M, Manabe T, Yamamoto T. Characterization of Fyn-mediated tyrosine phosphorylation sites on GluR epsilon 2 (NR2B) subunit of the N-methyl-D-aspartate receptor. J Biol Chem 2001; 276: 693-699.
56. Wang YT, Salter MW. Regulation of NMDA receptors by tyrosine kinases and phosphatases. Nature 1994; 369: 233-235.
57. Alder J, Thakker-Varia S, Crozier RA, Shaheen A, Plummer MR, Black IB. Early presynaptic and late postsynaptic components contribute independently to brain-derived neurotrophic factor-induced synaptic plasticity. J Neurosci 2005; 25: 3080-3085.
58. Meeker RB. Metabotropic and NMDA glutamate receptor interactions with osmotic stimuli in supraoptic neurons. Pharmacol Biochem Behav 2002; 73: 475-484.
59. Al-Ghoul WM, Meeker RB, Greenwood RS. Differential expression of five N-methyl-D-aspartate receptor subunit mRNAs in vasopressin and oxytocin neuroendocrine cells. Brain Res Mol Brain Res 1997; 44: 262-272.
60. Decavel C, Curras MC. Increased expression of the N-methyl-aspartate receptor subunit, NR1, in immunohistochemically identified magnocellular hypothalamic neurons during dehydration. Neuroscience 1997; 78: 191-202.
61. Doherty FC, Sladek CD. NMDA receptor subunit expression in the supraoptic nucleus of adult rats: dominance of NR2B and NR2D. Brain Res 2011; 1388: 89-99.
62. Leng G, Brown CH, Russell JA. Physiological pathways regulating the activity of magnocellular neurosecretory cells. Prog Neurobiol 1999; 57: 625-655.
63. Sladek CD, Fisher KY, Sidorowicz HE, Mathiasen JR. Osmotic stimulation of vasopressin mRNA content in the supraoptic nucleus requires synaptic activation. Am J Physiol 1995; 268: R1034-R1039.
64. Dyball RE, McKenzie DN, Thomas GP. Osmoresponsiveness of the rat supraoptic nucleus in vivo depends on glutamatergic inputs. Neurobiology (Bp) 1995; 3: 351-362.
65. Hu B, Bourque CW. NMDA receptor-mediated rhythmic bursting activity in rat supraoptic nucleus neurones in vitro. J Physiol 1992; 458: 667-687.
66. Yang CR, Senatorov VV, Renaud LP. Organum vasculosum lamina terminalis-evoked postsynaptic responses in rat supraoptic neurones in vitro. J Physiol 1994; 477: 59-74.
67. Panatier A, Gentles SJ, Bourque CW, Oliet SH. Activity-dependent synaptic plasticity in the supraoptic nucleus of the rat hypothalamus. J Physiol 2006; 573: 711-721.
68. Scott V, Brown CH. State-dependent plasticity in vasopressin neurones: dehydration-induced changes in activity patterning. J Neuroendocrinol 2010; 22: 343-354.
69. Iremonger KJ, Benediktsson AM, Bains JS. Glutamatergic synaptic transmission in neuroendocrine cells: basic principles and mechanisms of plasticity. Front Neuroendocrinol 2010; 31: 296-306.
70. Black IB. Trophic regulation of synaptic plasticity. J Neurobiol 1999; 41: 108-118.