Differential regulation of TRPC4 in the vasopressin magnocellular system by water deprivation and hepatic cirrhosis in the rat

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 306, Issue 5, 2014, Pages

  Nedungadi, T Prashant ^a   Cunningham, J Thomas ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

Bile duct ligation; Osmolality; TRPC4; Vasopressin; Water deprivation

Indexed keywords

TRANSIENT RECEPTOR POTENTIAL CHANNEL 4; ARGIPRESSIN; MESSENGER RNA; PLASMA PROTEIN; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; TRPC4 ION CHANNEL; VASOPRESSIN; VASOPRESSIN DERIVATIVE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT LIGATION; CELL DIFFERENTIATION; CELL POPULATION; CONTROLLED STUDY; GENE EXPRESSION; HEMATOCRIT; IMMUNODETECTION; IMMUNOFLUORESCENCE; LASER CAPTURE MICRODISSECTION; LIVER CIRRHOSIS; LIVER WEIGHT; MAGNOCELLULAR NUCLEUS; MAGNOCELLULAR PARAVENTRICULAR NUCLEUS; MALE; NONHUMAN; PARAVENTRICULAR THALAMIC NUCLEUS; PLASMA OSMOLALITY; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SUPRAOPTIC NUCLEUS; TRANSCRIPTION INITIATION; VASOPRESSIN RELEASE; WATER DEPRIVATION; ANIMAL; BILE DUCT; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; HYPOTHALAMUS; LIGATION; METABOLISM; METHODOLOGY; NERVE CELL; OSMOLALITY; OSMOLARITY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; TRPC4; WESTERN BLOTTING;

BILE DUCT LIGATION; OSMOLALITY; TRPC4; VASOPRESSIN; WATER DEPRIVATION;

ANIMALS; ARGININE VASOPRESSIN; BILE DUCTS; BLOOD PROTEINS; BLOTTING, WESTERN; GENE EXPRESSION REGULATION; HYPOTHALAMUS; LIGATION; LIVER CIRRHOSIS; MALE; NEURONS; OSMOLAR CONCENTRATION; RATS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRPC CATION CHANNELS; VASOPRESSINS; WATER DEPRIVATION;

EID: 84899442405     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00388.2013     Document Type: Article

References (74)

1. Acharya JK, Jalink K, Hardy RW, Hartenstein V, Zuker CS. InsP3 receptor is essential for growth and differentiation but not for vision in Drosophila. Neuron 18: 881-887, 1997.
2. Alessandri-Haber N, Dina OA, Chen X, Levine JD. TRPC1 and TRPC6 channels cooperate with TRPV4 to mediate mechanical hyperalgesia and nociceptor sensitization. J Neurosci 29: 6217-6228, 2009.
3. Amaral MD, Pozzo-Miller L. TRPC3 channels are necessary for brainderived neurotrophic factor to activate a nonselective cationic current and to induce dendritic spine formation. J Neurosci 27: 5179-5189, 2007.
4. Armstrong WE. Morphological and electrophysiological classification of hypothalamic supraoptic neurons. Prog Neurobiol 47: 291-339, 1995.
5. Better OS, Aisenbrey GA, Berl T, Anderson RJ, Handelman WA, Linas SL, Guggenheim SJ, Schrier RW. Role of antidiuretic hormone in impaired urinary dilution associated with chronic bile-duct ligation. Clin Sci (Lond) 58: 493-500, 1980.
6. Bezzerides VJ, Ramsey IS, Kotecha S, Greka A, Clapham DE. Rapid vesicular translocation and insertion of TRP channels. Nat Cell Biol 6: 709-720, 2004.
7. Bourque CW. Central mechanisms of osmosensation and systemic osmoregulation. Nat Rev Neurosci 9: 519-531, 2008.
8. Briski KP, Nedungadi TP, Koshy Cherian A. Effects of hypoglycaemia on neurotransmitter and hormone receptor gene expression in laserdissected arcuate neuropeptide Y/agouti-related peptide neurones. J Neuroendocrinol 22: 599-607, 2010.
9. Brond L, Hadrup N, Salling N, Torp M, Graebe M, Christensen S, Nielsen S, Jonassen TE. Uncoupling of vasopressin signaling in collecting ducts from rats with CBL-induced liver cirrhosis. Am J Physiol Renal Physiol 287: F806-F815, 2004.
10. 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 296: R454-R466, 2009.
11. Carreno FR, Walch JD, Dutta M, Nedungadi TP, Cunningham JT. Brain-derived neurotrophic factor-tyrosine kinase B pathway mediates NMDA receptor NR2B subunit phosphorylation in the supraoptic nuclei following progressive dehydration. J Neuroendocrinol 23: 894-905, 2011.
12. Carreño FR, Walch JD, Dutta M, Nedungadi TP, Cunningham JT. BDNF-TrkB pathway mediates NMDA receptor NR2B subunit phosphorylation in the supraoptic nuclei following progressive dehydration. J Neuroendocrinol 23: 894-905, 2011.
13. Chatterjee K. Neurohormonal activation in congestive heart failure and the role of vasopressin. Am J Cardiol 95: 8-13, 2005.
14. Clapham DE, Runnels LW, Strubing C. The TRP ion channel family. Nat Rev Neurosci 2: 387-396, 2001.
15. Cunningham JT, Nedungadi TP, Walch JD, Nestler EJ, Gottlieb HB. DeltaFosB in the supraoptic nucleus contributes to hyponatremia in rats with cirrhosis. Am J Physiol Regul Integr Comp Physiol 303: R177-R185, 2012.
16. 2+ rise in primary sensory cells. Neurosci Bull 27: 135-142, 2011.
17. Ding J, Zhang JR, Wang Y, Li CL, Lu D, Guan SM, Chen J. Effects of a non-selective TRPC channel blocker, SKF-96365, on melittin-induced spontaneous persistent nociception and inflammatory pain hypersensitivity. Neurosci Bull 28: 173-181, 2012.
18. Doignon I, Julien B, Serrière-Lanneau V, Garcin I, Alonso G, Nicou A, Monnet F, Gigou M, Humbert L, Rainteau D, Azoulay D, Castaing D, Gillon MC, Samuel D, Duclos-Vallée JC, Tordjmann T. Immediate neuroendocrine signaling after partial hepatectomy through acute portal hyperpressure and cholestasis. J Hepatol 54: 481-488, 2011.
19. 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 52: 3212-3219, 1973.
20. Ferguson AV, Latchford KJ. Local circuitry regulates the excitability of rat neurohypophysial neurones. Exp Physiol 85: 153S-161S, 2000.
21. 2+ entry and embryonic rat neural stem cell proliferation. J Neurosci 25: 2687-2701, 2005.
22. Fowler MA, Sidiropoulou K, Ozkan ED, Phillips CW, Cooper DC. Corticolimbic expression of TRPC4 and TRPC5 channels in the rodent brain. PloS One 2: e573, 2007.
23. Gimpl G, Fahrenholz F. The oxytocin receptor system: structure, function, and regulation. Physiol Rev 81: 629-683, 2001.
24. Goel M, Sinkins WG, Schilling WP. Selective association of TRPC channel subunits in rat brain synaptosomes. J Biol Chem 277: 48303-48310, 2002.
25. Goldsmith SR. Current treatments and novel pharmacologic treatments for hyponatremia in congestive heart failure. Am J Cardiol 95: 14-23, 2005.
26. Gottlieb HB, Ji LL, Jones H, Penny ML, Fleming T, Cunningham JT. Differential effects of water and saline intake on water deprivationinduced c-Fos staining in the rat. Am J Physiol Regul Integr Comp Physiol 290: R1251-R1261, 2006.
27. Groschner K, Hingel S, Lintschinger B, Balzer M, Romanin C, Zhu X, Schreibmayer W. Trp proteins form store-operated cation channels in human vascular endothelial cells. FEBS Lett 437: 101-106, 1998.
28. Haanwinckel MA, Elias LK, Favaretto AL, Gutkowska J, McCann SM, Antunes-Rodrigues J. Oxytocin mediates atrial natriuretic peptide release and natriuresis after volume expansion in the rat. Proc Natl Acad Sci USA 92: 7902-7906, 1995.
29. Hindmarch C, Yao S, Beighton G, Paton J, Murphy D. A comprehensive description of the transcriptome of the hypothalamoneurohypophyseal system in euhydrated and dehydrated rats. Proc Natl Acad Sci USA 103: 1609-1614, 2006.
30. Huang WC, Young JS, Glitsch MD. Changes in TRPC channel expression during postnatal development of cerebellar neurons. Cell Calcium 42: 1-10, 2007.
31. Ji LL, Fleming T, Penny ML, Toney GM, Cunningham JT. Effects of water deprivation and rehydration on c-Fos and FosB staining in the rat supraoptic nucleus and lamina terminalis region. Am J Physiol Regul Integr Comp Physiol 288: R311-R321, 2005.
32. Kato AS, Knierman MD, Siuda ER, Isaac JT, Nisenbaum ES, Bredt DS. Glutamate receptor delta2 associates with metabotropic glutamate receptor 1 (mGluR1), protein kinase C, and canonical transient receptor potential 3 and regulates mGluR1-mediated synaptic transmission in cerebellar Purkinje neurons. J Neurosci 32: 15296-15308, 2012.
33. Knight WD, Ji LL, Little JT, Cunningham JT. Dehydration followed by sham rehydration contributes to reduced neuronal activation in vasopressinergic supraoptic neurons after water deprivation. Am J Physiol Regul Integr Comp Physiol 299: R1232-R1240, 2010.
34. Li HS, Xu XZ, Montell C. Activation of a TRPC3-dependent cation current through the neurotrophin BDNF. Neuron 24: 261-273, 1999.
35. Li Y, Jia YC, Cui K, Li N, Zheng ZY, Wang YZ, Yuan XB. Essential role of TRPC channels in the guidance of nerve growth cones by brainderived neurotrophic factor. Nature 434: 894-898, 2005.
36. Liedtke W, Friedman JM. Abnormal osmotic regulation in trpv4-/-mice. Proc Natl Acad Sci USA 100: 13698-13703, 2003.
37. 2+-sensitive cation channels. J Biol Chem 275: 27799-27805, 2000.
38. Ludwig M, Leng G. Dendritic peptide release and peptide-dependent behaviours. Nat Rev Neurosci 7: 126-136, 2006.
39. Miller M, Shi J, Zhu Y, Kustov M, Tian JB, Stevens A, Wu M, Xu J, Long S, Yang P, Zholos AV, Salovich JM, Weaver CD, Hopkins CR, Lindsley CW, McManus O, Li M, Zhu MX. Identification of ML204, a novel potent antagonist that selectively modulates native TRPC4/C5 ion channels. J Biol Chem 286: 33436-33446, 2011.
40. Min MY, Shih PY, Wu YW, Lu HW, Lee ML, Yang HW. Neurokinin 1 receptor activates transient receptor potential-like currents in noradrenergic A7 neurons in rats. Mol Cell Neurosci 42: 56-65, 2009.
41. Minke B, Cook B. TRP channel proteins and signal transduction. Physiol Rev 82: 429-472, 2002.
42. 2+ channel isoforms in mouse brain. Neuroreport 9: 507-515, 1998.
43. Munsch T, Freichel M, Flockerzi V, Pape HC. Contribution of transient receptor potential channels to the control of GABA release from dendrites. Proc Natl Acad Sci USA 100: 16065-16070, 2003.
44. Nedungadi TP, Carreno FR, Walch JD, Bathina CS, Cunningham JT. Region-specific changes in transient receptor potential vanilloid channel expression in the vasopressin magnocellular system in hepatic cirrhosisinduced hyponatraemia. J Neuroendocrinol. 24: 642-652, 2012.
45. Nedungadi TP, Dutta M, Bathina CS, Caterina MJ, Cunningham JT. Expression and distribution of TRPV2 in rat brain. Exp Neurol 237: 223-237, 2012.
46. 2+ to trigger exocytosis in neuroendocrine cells. J Biol Chem 277: 16172-16178, 2002.
47. 2+-permeable cation channel that is constitutively activated and enhanced by stimulation of G protein-coupled receptor. J Biol Chem 274: 27359-27370, 1999.
48. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic Press, 1997.
49. Petersen CC, Berridge MJ, Borgese MF, Bennett DL. Putative capacitative calcium entry channels: expression of Drosophila trp and evidence for the existence of vertebrate homologues. Biochem J 311: 41-44, 1995.
50. Phelan KD, Mock MM, Kretz O, Shwe UT, Kozhemyakin M, Greenfield LJ, Dietrich A, Birnbaumer L, Freichel M, Flockerzi V, Zheng F. Heteromeric canonical transient receptor potential 1 and 4 channels play a critical role in epileptiform burst firing and seizure-induced neurodegeneration. Mol Pharmacol 81: 384-392, 2012.
51. Philipp S, Cavalie A, Freichel M, Wissenbach U, Zimmer S, Trost C, Marquart A, Murakami M, Flockerzi V. A mammalian capacitative calcium entry channel homologous to Drosophila TRP and TRPL. EMBO J 15: 6166-6171, 1996.
52. Philipp S, Hambrecht J, Braslavski L, Schroth G, Freichel M, Murakami M, Cavalie A, Flockerzi V. A novel capacitative calcium entry channel expressed in excitable cells. EMBO J 17: 4274-4282, 1998.
53. Putney JW. Physiological mechanisms of TRPC activation. Pflügers Arch 451: 29-34, 2005.
54. Raghu P, Colley NJ, Webel R, James T, Hasan G, Danin M, Selinger Z, Hardie RC. Normal phototransduction in Drosophila photoreceptors lacking an InsP(3) receptor gene. Mol Cell Neurosci 15: 429-445, 2000.
55. Riccio A, Medhurst AD, Mattei C, Kelsell RE, Calver AR, Randall AD, Benham CD, Pangalos MN. mRNA distribution analysis of human TRPC family in CNS and peripheral tissues. Brain Res Mol Brain Res 109: 95-104, 2002.
56. Schaefer M, Plant TD, Obukhov AG, Hofmann T, Gudermann T, Schultz G. Receptor-mediated regulation of the nonselective cation channels TRPC4 and TRPC5. J Biol Chem 275: 17517-17526, 2000.
57. Schaefer M, Plant TD, Stresow N, Albrecht N, Schultz G. Functional differences between TRPC4 splice variants. J Biol Chem 277: 3752-3759, 2002.
58. Schaefer M, Plant TD, Stresow N, Albrecht N, Schultz G. Functional differences between TRPC4 splice variants. J Biol Chem 277: 3752-3759, 2002.
59. Schrier RW. Water and sodium retention in edematous disorders: role of vasopressin and aldosterone. Am J Med 119: S47-S53, 2006.
60. Schrier RW. Water and sodium retention in edematous disorders: role of vasopressin and aldosterone. Am J Med 119: S47-S53, 2006.
61. Schrier RW, Ohara M. Dilemmas in human and rat pregnancy: proposed mechanisms relating to arterial vasodilation. J Neuroendocrinol 22: 400-406, 2010.
62. Simard M, Nedergaard M. The neurobiology of glia in the context of water and ion homeostasis. Neuroscience 129: 877-896, 2004.
63. Son SJ, Filosa JA, Potapenko ES, Biancardi VC, Zheng H, Patel KP, Tobin VA, Ludwig M, Stern JE. Dendritic peptide release mediates interpopulation crosstalk between neurosecretory and preautonomic networks. Neuron 78: 1036-1049, 2013.
64. Stocker SD, Cunningham JT, Toney GM. Water deprivation increases Fos immunoreactivity in PVN autonomic neurons with projections to the spinal cord and rostral ventrolateral medulla. Am J Physiol Regul Integr Comp Physiol 287: R1172-R1183, 2004.
65. Stocker SD, Hunwick KJ, Toney GM. Hypothalamic paraventricular nucleus differentially supports lumbar and renal sympathetic outflow in water-deprived rats. J Physiol 563: 249-263, 2005.
66. Strubing C, Krapivinsky G, Krapivinsky L, Clapham DE. TRPC1 and TRPC5 form a novel cation channel in mammalian brain. Neuron 29: 645-655, 2001.
67. Sudbury JR, Ciura S, Sharif-Naeini R, Bourque CW. Osmotic and thermal control of magnocellular neurosecretory neurons-role of an N-terminal variant of trpv1. Eur J Neurosci 32: 2022-2030, 2010.
68. Verbalis JG. Disorders of body water homeostasis. Best Pract Res Clin Endocrinol Metab 17: 471-503, 2003.
69. Verbalis JG. Osmotic inhibition of neurohypophysial secretion. Ann N Y Acad Sci 689: 146-160, 1993.
70. Walch JD, Carreno FR, Cunningham JT. Intracerebroventricular losartan infusion modulates angiotensin II type 1 receptor expression in the subfornical organ and drinking behaviour in bile-duct-ligated rats. Exp Physiol 98: 922-933, 2013.
71. Wu D, Huang W, Richardson PM, Priestley JV, Liu M. TRPC4 in rat dorsal root ganglion neurons is increased after nerve injury and is necessary for neurite outgrowth. J Biol Chem 283: 416-426, 2008.
72. Wu X, Zagranichnaya TK, Gurda GT, Eves EM, Villereal ML. A TRPC1/TRPC3-mediated increase in store-operated calcium entry is required for differentiation of H19-7 hippocampal neuronal cells. J Biol Chem 279: 43392-43402, 2004.
73. Xu XZ, Li HS, Guggino WB, Montell C. Coassembly of TRP and TRPL produces a distinct store-operated conductance. Cell 89: 1155-1164, 1997.
74. 2+-permeable cation channel activated by calcium store depletion. Neuron 16: 1189-1196, 1996.