Expression and distribution of TRPV2 in rat brain

Experimental Neurology

Volumn 237, Issue 1, 2012, Pages 223-237

  Nedungadi, Thekkethil Prashant ^a,b   Dutta, Mayurika ^a,b   Bathina, Chandra Sekhar ^a,b   Caterina, Michael J ^a,b   Cunningham, J Thomas ^a,b  

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

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Brainstem; Hypothalamus; Nucleus of the solitary tract; Supraoptic nucleus; Vasopressin

Indexed keywords

DOPAMINE BETA MONOOXYGENASE; VANILLOID RECEPTOR 2;

ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CINGULATE GYRUS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; HYPOTHALAMIC PARAVENTRICULAR NUCLEUS; HYPOTHALAMUS; IMMUNOREACTIVITY; LASER CAPTURE MICRODISSECTION; MALE; NEUROANATOMY; NONHUMAN; ORGANUM VASCULOSUM OF THE LAMINA TERMINALIS; OSMOREGULATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SOMATOSENSORY SYSTEM; SUPRAOPTIC NUCLEUS;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; BODY FLUIDS; BRAIN CHEMISTRY; CALCIUM CHANNELS; HOMEOSTASIS; HYPOTHALAMUS; MALE; MICE; MICE, KNOCKOUT; NERVE NET; RATS; RHOMBENCEPHALON; SUPRAOPTIC NUCLEUS; TRPV CATION CHANNELS;

EID: 84864037037     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.06.017     Document Type: Article

References (74)

1. Andersson B. Thirst-and brain control of water balance. Am. Sci. 1971, 59:408-415.
2. Beech D.J., Muraki K., Flemming R. Non-selective cationic channels of smooth muscle and the mammalian homologues of Drosophila TRP. J. Physiol. 2004, 559:685-706.
3. Berglöf E., Small B.J., Bickford P.C., Strömberg I. Beneficial effects of antioxidant-enriched diet for tyrosine hydroxylase-positive neurons in ventral mesencephalic tissue in oculo grafts. J. Comp. Neurol. 2009, 515:72-82.
4. Bourque C.W., Ciura S., Trudel E., Stachniak T.J., Sharif-Naeini R. Neurophysiological characterization of mammalian osmosensitive neurones. Exp. Physiol. 2007, 92:499-505.
5. Briski K.P., Nedungadi T.P., 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.
6. Buggy J., Hoffman W.E., Phillips M.I., Fisher A.E., Johnson A.K. Osmosensitivity of rat third ventricle and interactions with angiotensin. Am. J. Physiol. 1979, 236:R75-R82.
7. Carreno F.R., Ji L.L., Cunningham J.T. 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.
8. Carreno F.R., Walch J.D., Dutta M., Nedungadi T.P., Cunningham J.T. BDNF-TrkB pathway mediates NMDA receptor NR2B subunit phosphorylation in the supraoptic nuclei following progressive dehydration. J. Neuroendocrinol. 2011, 23:894-905.
9. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389:816-824.
10. Caterina M.J., Rosen T.A., Tominaga M., Brake A.J., Julius D. A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 1999, 398:436-441.
11. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., Koltzenburg M., Basbaum A.I., Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 2000, 288:306-313.
12. Chakfe Y., Bourque C.W. Peptidergic excitation of supraoptic nucleus neurons: involvement of stretch-inactivated cation channels. Exp. Neurol. 2001, 171:210-218.
13. Christensen A.P., Corey D.P. TRP channels in mechanosensation: direct or indirect activation?. Nat. Rev. Neurosci. 2007, 8:510-521.
14. Chu C.P., Kannan H., Qiu D.L. Effect of hypertonic saline on rat hypothalamic paraventricular nucleus parvocellular neurons in vitro. Neurosci. Lett. 2010, 482:142-145.
15. Ciura S., Bourque C.W. Transient receptor potential vanilloid 1 is required for intrinsic osmoreception in organum vasculosum lamina terminalis neurons and for normal thirst responses to systemic hyperosmolality. J. Neurosci. 2006, 26:9069-9075.
16. Colbert H.A., Smith T.L., Bargmann C.I. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J. Neurosci. 1997, 17:8259-8269.
17. Corey D.P. New TRP channels in hearing and mechanosensation. Neuron 2003, 39:585-588.
18. Curtis K.S., Huang W., Sved A.F., Verbalis J.G., Stricker E.M. Impaired osmoregulatory responses in rats with area postrema lesions. Am. J. Physiol. 1999, 277:R209-R219.
19. Davis J.B., Gray J., Gunthorpe M.J., Hatcher J.P., Davey P.T., Overend P., Harries M.H., Latcham J., Clapham C., Atkinson K., Hughes S.A., Rance K., Grau E., Harper A.J., Pugh P.L., Rogers D.C., Bingham S., Randall A., Sheardown S.A. Vanilloid receptor-1 is essential for inflammatory thermal hyperalgesia. Nature 2000, 405:183-187.
20. Drouyer E., LeSauter J., Hernandez A.L., Silver R. Specializations of gastrin-releasing peptide cells of the mouse suprachiasmatic nucleus. J. Comp. Neurol. 2010, 518:1249-1263.
21. Everitt B.J., Meister B., Hokfelt T., Melander T., Terenius L., Rokaeus A., Theodorsson-Norheim E., Dockray G., Edwardson J., Cuello C., et al. The hypothalamic arcuate nucleus-median eminence complex: immunohistochemistry of transmitters, peptides and DARPP-32 with special reference to coexistence in dopamine neurons. Brain Res. 1986, 396:97-155.
22. Flores C.M., Price T.J., Patwardhan A., Akopian A.N., Hargreaves K.M. Modulation of trigeminal sensory neuron activity by the dual cannabinoid-vanilloid agonists anandamide, N-arachidonoyl-dopamine and arachidonyl-2-chloroethylamide. Br. J. Pharmacol. 2004, 141:1118-1130.
23. Guler A.D., Lee H., Iida T., Shimizu I., Tominaga M., Caterina M. Heat-evoked activation of the ion channel, TRPV4. J. Neurosci. 2002, 22:6408-6414.
24. Guyenet P.G. The sympathetic control of blood pressure. Nat. Rev. Neurosci. 2006, 7:335-346.
25. Hisanaga E., Nagasawa M., Ueki K., Kulkarni R.N., Mori M., Kojima I. Regulation of calcium-permeable TRPV2 channel by insulin in pancreatic beta-cells. Diabetes 2009, 58:174-184.
26. Ichikawa H., Sugimoto T. VR1-immunoreactive primary sensory neurons in the rat trigeminal ganglion. Brain Res. 2001, 890:184-188.
27. Jeske N.A., Patwardhan A.M., Gamper N., Price T.J., Akopian A.N., Hargreaves K.M. Cannabinoid WIN 55,212-2 regulates TRPV1 phosphorylation in sensory neurons. J. Biol. Chem. 2006, 281:32879-32890.
28. Kalia M. Brain stem localization of vagal preganglionic neurons. J. Auton. Nerv. Syst. 1981, 3:451-481.
29. Kanzaki M., Zhang Y.Q., Mashima H., Li L., Shibata H., Kojima I. Translocation of a calcium-permeable cation channel induced by insulin-like growth factor-I. Nat. Cell Biol. 1999, 1:165-170.
30. Knot H.J., Nelson M.T. Regulation of membrane potential and diameter by voltage-dependent K+ channels in rabbit myogenic cerebral arteries. Am. J. Physiol. 1995, 269:H348-H355.
31. Lewinter R.D., Skinner K., Julius D., Basbaum A.I. Immunoreactive TRPV-2 (VRL-1), a capsaicin receptor homolog, in the spinal cord of the rat. J. Comp. Neurol. 2004, 470:400-408.
32. Lewinter R.D., Scherrer G., Basbaum A.I. Dense transient receptor potential cation channel, vanilloid family, type 2 (TRPV2) immunoreactivity defines a subset of motoneurons in the dorsal lateral nucleus of the spinal cord, the nucleus ambiguus and the trigeminal motor nucleus in rat. Neuroscience 2008, 151:164-173.
33. Liapi A., Wood J.N. Extensive co-localization and heteromultimer formation of the vanilloid receptor-like protein TRPV2 and the capsaicin receptor TRPV1 in the adult rat cerebral cortex. Eur. J. Neurosci. 2005, 22:825-834.
34. Liedtke W. Transient receptor potential vanilloid channels functioning in transduction of osmotic stimuli. J. Endocrinol. 2006, 191:515-523.
35. Liedtke W., Friedman J.M. Abnormal osmotic regulation in trpv4-/- mice. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:13698-13703.
36. Liedtke W., Choe Y., Marti-Renom M.A., Bell A.M., Denis C.S., Sali A., Hudspeth A.J., Friedman J.M., Heller S. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 2000, 103:525-535.
37. Lin S.Y., Corey D.P. TRP channels in mechanosensation. Curr. Opin. Neurobiol. 2005, 15:350-357.
38. Link T.M., Park U., Vonakis B.M., Raben D.M., Soloski M.J., Caterina M.J. TRPV2 has a pivotal role in macrophage particle binding and phagocytosis. Nat. Immunol. 2010, 11:232-239.
39. Mason W.T. Supraoptic neurones of rat hypothalamus are osmosensitive. Nature 1980, 287:154-157.
40. McAllen R.M., Pennington G.L., McKinley M.J. Osmoresponsive units in sheep median preoptic nucleus. Am. J. Physiol. 1990, 259:R593-R600.
41. McKinley M.J., Gerstberger R., Mathai M.L., Oldfield B.J., Schmid H. The lamina terminalis and its role in fluid and electrolyte homeostasis. J. Clin. Neurosci. 1999, 6:289-301.
42. McKinley M.J., Mathai M.L., McAllen R.M., McClear R.C., Miselis R.R., Pennington G.L., Vivas L., Wade J.D., Oldfield B.J. Vasopressin secretion: osmotic and hormonal regulation by the lamina terminalis. J. Neuroendocrinol. 2004, 16:340-347.
43. Monet M., Gkika D., Lehen'kyi V., Pourtier A., Vanden Abeele F., Bidaux G., Juvin V., Rassendren F., Humez S., Prevarsakaya N. Lysophospholipids stimulate prostate cancer cell migration via TRPV2 channel activation. Biochim. Biophys. Acta 2009, 1793:528-539.
44. Moran M.M., McAlexander M.A., Bíró T., Szallasi A. Transient receptor potential channels as therapeutic targets. Nat. Rev. Drug Discov. 2011, 10:601-620.
45. Moreira T.S., Takakura A.C., Colombari E., Guyenet P.G. Central chemoreceptors and sympathetic vasomotor outflow. J. Physiol. 2006, 577:369-386.
46. Muraki K., Iwata Y., Katanosaka Y., Ito T., Ohya S., Shigekawa M., Imaizumi Y. TRPV2 is a component of osmotically sensitive cation channels in murine aortic myocytes. Circ. Res. 2003, 93:829-838.
47. Nagasawa M., Nakagawa Y., Tanaka S., Kojima I. Chemotactic peptide fMetLeuPhe induces translocation of the TRPV2 channel in macrophages. J. Cell. Physiol. 2007, 210:692-702.
48. Nedungadi T.P., Carreno F.R., Walch J.D., Bathina C.S., Cunningham J.T. Region-specific changes in transient receptor potential vanilloid channel expression in the vasopressin magnocellular system in hepatic cirrhosis-induced hyponatraemia. J. Neuroendocrinol. 2012, 24:642-652.
49. Oliet S.H., Bourque C.W. Properties of supraoptic magnocellular neurones isolated from the adult rat. J. Physiol. 1992, 455:291-306.
50. Oliet S.H., Bourque C.W. Mechanosensitive channels transduce osmosensitivity in supraoptic neurons. Nature 1993, 364:341-343.
51. O'Neil R.G., Heller S. The mechanosensitive nature of TRPV channels. Pflugers Arch. 2005, 451:193-203.
52. Park U., Vastani N., Guan Y., Raja S.N., Koltzenburg M., Caterina M.J. TRP vanilloid 2 knock-out mice are susceptible to perinatal lethality but display normal thermal and mechanical nociception. J. Neurosci. 2011, 31:11425-11436.
53. Paxinos G. Chemoarchitectonic Atlas of the Rat Brainstem 1999, Academic Press, San Diego.
54. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1997, Academic Press, San Diego.
55. Penna A., Juvin V., Chemin J., Compan V., Monet M., Rassendren F.A. PI3-kinase promotes TRPV2 activity independently of channel translocation to the plasma membrane. Cell Calcium 2006, 39:495-507.
56. Renaud L.P., Bourque C.W. Neurophysiology and neuropharmacology of hypothalamic magnocellular neurons secreting vasopressin and oxytocin. Prog. Neurobiol. 1991, 36:131-169.
57. Rinaman L. Visceral sensory inputs to the endocrine hypothalamus. Front. Neuroendocrinol. 2007, 28:50-60.
58. Rinaman L. Hindbrain noradrenergic A2 neurons: diverse roles in autonomic, endocrine, cognitive, and behavioral functions. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2011, 300:R222-R235.
59. Rutter A.R., Ma Q.P., Leveridge M., Bonnert T.P. Heteromerization and colocalization of TrpV1 and TrpV2 in mammalian cell lines and rat dorsal root ganglia. Neuroreport 2005, 16:1735-1739.
60. Sara S.J. The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. Neurosci. 2009, 10:211-223.
61. Scotland R.S., Chauhan S., Davis C., De Felipe C., Hunt S., Kabir J., Kotsonis P., Oh U., Ahluwalia A. Vanilloid receptor TRPV1, sensory C-fibers, and vascular autoregulation: a novel mechanism involved in myogenic constriction. Circ. Res. 2004, 95:1027-1034.
62. Sharif Naeini R., Witty M.F., Seguela P., Bourque C.W. An N-terminal variant of Trpv1 channel is required for osmosensory transduction. Nat. Neurosci. 2006, 9:93-98.
63. Sharif-Naeini R., Ciura S., Zhang Z., Bourque C.W. Contribution of TRPV channels to osmosensory transduction, thirst, and vasopressin release. Kidney Int. 2008, 73:811-815.
64. Shibasaki K., Murayama N., Ono K., Ishizaki Y., Tominaga M. TRPV2 enhances axon outgrowth through its activation by membrane stretch in developing sensory and motor neurons. J. Neurosci. 2010, 30:4601-4612.
65. Sudbury J.R., Ciura S., Sharif-Naeini R., Bourque C.W. Osmotic and thermal control of magnocellular neurosecretory neurons-role of an N-terminal variant of trpv1. Eur. J. Neurosci. 2010, 32:2022-2030.
66. Szallasi A., Blumberg P.M. Vanilloid (Capsaicin) receptors and mechanisms. Pharmacol. Rev. 1999, 51:159-212.
67. Taylor A.C., McCarthy J.J., Stocker S.D. Mice lacking the transient receptor vanilloid potential 1 channel display normal thirst responses and central Fos activation to hypernatremia. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294:R1285-R1293.
68. Tominaga M., Caterina M.J. Thermosensation and pain. J. Neurobiol. 2004, 61:3-12.
69. Venkatachalam K., Montell C. TRP channels. Annu. Rev. Biochem. 2007, 76:387-417.
70. Wainwright A., Rutter A.R., Seabrook G.R., Reilly K., Oliver K.R. Discrete expression of TRPV2 within the hypothalamo-neurohypophysial system: implications for regulatory activity within the hypothalamic-pituitary-adrenal axis. J. Comp. Neurol. 2004, 474:24-42.
71. Watson R.E., Wiegland S.J., Clough R.W., Hoffman G.E. Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology. Peptides 1986, 7:155-159. (New York, N.Y.: 1980).
72. Welsh D.G., Morielli A.D., Nelson M.T., Brayden J.E. Transient receptor potential channels regulate myogenic tone of resistance arteries. Circ. Res. 2002, 90:248-250.
73. Yamashiro K., Sasano T., Tojo K., Namekata I., Kurokawa J., Sawada N., Suganami T., Kamei Y., Tanaka H., Tajima N., Utsunomiya K., Ogawa Y., Furukawa T. Role of transient receptor potential vanilloid 2 in LPS-induced cytokine production in macrophages. Biochem. Biophys. Res. Commun. 2010, 398:284-289.
74. Yamashita H., Inenaga K., Dyball R.E. Thermal, osmotic and chemical modulation of neural activity in the paraventricular nucleus: in vitro studies. Brain Res. Bull. 1988, 20:825-829.