KCl stimulation increases norepinephrine transporter function in PC12 cells

Journal of Neurochemistry

Volumn 98, Issue 5, 2006, Pages 1521-1530

  Mandela, Prashant ^a   Ordway, Gregory A ^b  

^a UNIVERSITY OF MISSISSIPPI MEDICAL CENTER   (United States)

^b East Tennessee State University   (United States)

Author keywords

Antidepressant; Noradrenergic; Norepinephrine; Norepinephrine transporter; Regulation; Release

Indexed keywords

1 (5 CHLORO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; 1 (5 IODO 1 NAPHTHALENESULFONYL)HEXAHYDRO 1H 1,4 DIAZEPINE; CALCIUM ION; MYOSIN LIGHT CHAIN KINASE INHIBITOR; N [2 [[N [3 (4 CHLOROPHENYL) 2 PROPENYL] N METHYLAMINO]METHYL]PHENYL] N (2 HYDROXYETHYL) 4 METHOXYBENZENESULFONAMIDE; NORADRENALIN; NORADRENALIN TRANSPORTER; OKADAIC ACID; PHORBOL 13 ACETATE 12 MYRISTATE; PHOSPHOTRANSFERASE INHIBITOR; POTASSIUM CHLORIDE; PROTEIN KINASE (CALCIUM,CALMODULIN); TRITIUM; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE TRANSPORT; CELL STRAIN; CONTROLLED STUDY; CULTURE MEDIUM; NONHUMAN; NORADRENALIN RELEASE; NORADRENALIN UPTAKE; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; WHOLE CELL;

ANALYSIS OF VARIANCE; ANIMALS; BIOLOGICAL TRANSPORT; CALCIUM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME INHIBITORS; FLUOXETINE; NOREPINEPHRINE; PC12 CELLS; POTASSIUM CHLORIDE; PROTEIN BINDING; RATS; TIME FACTORS; TRITIUM;

EID: 33746953638     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04062.x     Document Type: Article

References (52)

1. Amara S. G. and Kuhar M. J. (1993) Neurotransmitter transporters: recent progress. Annu. Rev. Neurosci. 16, 73-93.
2. Apparsundaram S., Galli A., DeFelice L. J., Hartzell H. C. and Blakely R. D. (1998a) Acute regulation of norepinephrine transport: I. Protein kinase C-linked muscarinic receptors influence transport capacity and transporter density in SK-N-SH cells. J. Pharmacol. Exp. Ther. 287, 733-743.
3. Apparsundaram S., Schroeter S., Giovanetti E. and Blakely R. D. (1998b) Acute regulation of norepinephrine transport. II. PKC-modulated surface expression of human norepinephrine transporter proteins. J. Pharmacol. Exp. Ther. 287, 744-751.
4. Apparsundaram S., Sung U., Price R. D. and Blakely R. D. (2001) Trafficking-dependent and -independent pathways of neurotransmitter transporter regulation differentially involving p38 mitogen-activated protein kinase revealed in studies of insulin modulation of norepinephrine transport in SK-N-SH cells. J. Pharmacol. Exp. Ther. 299, 666-677.
5. Axelrod J. and Kopin I. J. (1969) The uptake, storage, release and metabolism of noradrenaline in sympathetic nerves. Prog. Brain Res. 31, 21-32.
6. Bauman A. L., Apparsundaram S., Ramamoorthy S., Wadzinski B. E., Vaughan R. A. and Blakely R. D. (2000) Cocaine and antidepressant-sensitive biogenic amine transporters exist in regulated complexes with protein phosphatase 2A. J. Neurosci. 20, 7571-7578.
7. Bonisch H., Hammermann R. and Bruss M. (1998) Role of protein kinase C and second messengers in regulation of the norepinephrine transporter. Adv. Pharmacol. 42, 183-186.
8. Braun A. P. and Schulman H. (1995) The multifunctional calcium/calmodulin-dependent protein kinase: from form to function. Annu. Rev. Physiol. 57, 417-445.
9. Bryan-Lluka L. J., Paczkowski F. A. and Bonisch H. (2001) Effects of short- and long-term exposure to c-AMP and c-GMP on the noradrenaline transporter. Neuropharmacology 40, 607-617.
10. Distelmaier F., Wiedemann P., Bruss M. and Bonisch H. (2004) Functional importance of the C-terminus of the human norepinephrine transporter. J. Neurochem. 91, 537-546.
11. Dupont J. L., Janoshazi A., Bellahcene M., de Mykita S. and B. J. (2000) Reversible protein kinase C activation in PC12 cells: effect of NGF treatment. Eur. J. Neurosci. 12, 215-226.
12. Friedrich U. and Bonisch H. (1986) The neuronal noradrenaline transport system of PC-12 cells: kinetic analysis of the interaction between noradrenaline, Na+ and Cl- in transport. Naunyn Schmiedebergs Arch. Pharmacol. 333, 246-252.
13. Gillis C. N. (1963) Increased retention of exogenous norepinephrine by cat atria after electrical stimulation of the cardioaccelerator nerves. Biochem. Pharmacol. 12, 593-595.
14. Gillis C. N., Schneider F. H., Van Orden L. S. and Giarman N. J. (1966) Biochemical and microfluorometric studies of norepinephrine redistribution accompanying sympathetic nerve stimulation. J. Pharmacol. Exp. Ther. 151, 46-54.
15. +/calmodulin- dependent protein kinases. Annu. Rev. Biochem. 61, 559-601.
16. Ishikawa T., Chijiwa T., Hagiwara M., Mamiya S., Saitoh M. and Hidaka H. (1988) ML-9 inhibits the vascular contraction via the inhibition of myosin light chain phosphorylation. Mol. Pharmacol. 33, 598-603.
17. Iwasaki S., Kataoka M., Sekiguchi M., Shimazaki Y., Sato K. and Takahashi M. (2000) Two distinct mechanisms underlie the stimulation of neurotransmitter release by phorbol esters in clonal rat pheochromocytoma PC12 cells. J. Biochem. (Tokyo) 128, 407-414.
18. Jayanthi L. D., Ramamoorthy S., Mahesh V. B., Leibach F. H. and Ganapathy V. (1994) Calmodulin-dependent regulation of the catalytic function of the human serotonin transporter in placental choriocarcinoma cells. J. Biol. Chem. 269, 14 424-14 429.
19. Jayanthi L. D., Samuvel D. J. and Ramamoorthy S. (2004) Regulated internalization and phosphorylation of the native norepinephrine transporter in response to phorbol esters. Evidence for localization in lipid rafts and lipid raft-mediated internalization. J. Biol. Chem. 279, 19 315-19 326.
20. +- and calmodulin-dependent phosphorylation and synaptic vesicles. J. Neurosci. 19, 3801-3808.
21. Kantor L., Hewlett G. H., Park Y. H., Richardson-Burns S. M., Mellon M. J. and Gnegy M. E. (2001) Protein kinase C and intracellular calcium are required for amphetamine-mediated dopamine release via the norepinephrine transporter in undifferentiated PC12 cells. J. Pharmacol. Exp. Ther. 297, 1016-1024.
22. Katz B. and Miledi R. (1965) The effect of calcium on acetylcholine release from motor nerve terminals. Proc. R. Soc. Lond. B Biol. Sci. 161, 496-503.
23. Katz B. and Miledi R. (1967) Ionic requirements of synaptic transmitter release. Nature 215, 651.
24. Katz B. and Miledi R. (1968) The role of calcium in neuromuscular facilitation. J. Physiol. 195, 481-492.
25. Katz B. and Miledi R. (1970) Further study of the role of calcium in synaptic transmission. J. Physiol. 207, 789-801.
26. Kippenberger A. G., Palmer D. J., Comer A. M., Lipski J., Burton L. D. and Christie D. L. (1999) Localization of the noradrenaline transporter in rat adrenal medulla and PC12 cells: evidence for its association with secretory granules in PC12 cells. J. Neurochem. 73, 1024-1032.
27. Klimek V., Stockmeier C., Overholser J., Meltzer H. Y., Kalka S., Dilley G. and Ordway G. A. (1997) Reduced levels of norepinephrine transporters in the locus coeruleus in major depression. J. Neurosci. 17, 8451-8458.
28. Kocabas A. M., Rudnick G. and Kilic F. (2003) Functional consequences of homo- but not hetero-oligomerization between transporters for the biogenic amine neurotransmitters. J. Neurochem. 85, 1513-1520.
29. Kongsamut S. and Miller R. J. (1986) Nerve growth factor modulates the drug sensitivity of neurotransmitter release from PC-12 cells. Proc. Natl Acad. Sci. USA 83, 2243-2247.
30. - cotransport in Ehrlich cells: regulation by protein phosphatases and kinases. Am. J. Physiol. 275, C239-C250.
31. Kumar G. K., Overholt J. L., Bright G. R., Hui K. Y., Lu H., Gratzl M. and Prabhakar N. R. (1998) Release of dopamine and norepinephrine by hypoxia from PC-12 cells. Am. J. Physiol. 274, C1592-C1600.
32. Mandela P. and Ordway G. A. (2006) The norepinephrine transporter and its regulation. J. Neurochem. 97, 310-333.
33. Mao W., Qin F., Iwai C., Vulapalli R., Keng P. C. and Liang C. S. (2004) Extracellular norepinephrine reduces neuronal uptake of norepinephrine by oxidative stress in PC12 cells. Am. J. Physiol. Heart Circ. Physiol. 287, H29-H39.
34. Nashat A. H. and Langer R. (2003) Temporal characteristics of activation, deactivation, and restimulation of signal transduction following depolarization in the pheochromocytoma cell line PC12. Mol. Cell Biol. 23, 4788-4795.
35. Nichols R. A., Sihra T. S., Czernik A. J., Nairn A. C. and Greengard P. (1990) Calcium/calmodulin-dependent protein kinase II increases glutamate and noradrenaline release from synaptosomes. Nature 343, 647-651.
36. Pacholczyk T., Blakely R. D. and Amara S. G. (1991) Expression cloning of a cocaine- and antidepressant-sensitive human noradrenaline transporter. Nature 350, 350-354.
37. Page G., Barc-Pain S., Pontcharraud R., Cante A., Piriou A. and Barrier L. (2004) The up-regulation of the striatal dopamine transporter's activity by cAMP is PKA-, CaMK II- and phosphatase-dependent. Neurochem. Int. 45, 627-632.
38. Robinson M. B. (2002) Regulated trafficking of neurotransmitter transporters: common notes but different melodies. J. Neurochem. 80, 1-11.
39. Saitoh M., Ishikawa T., Matsushima S., Naka M. and Hidaka H. (1987) Selective inhibition of catalytic activity of smooth muscle myosin light chain kinase. J. Biol. Chem. 262, 7796-7801.
40. Savchenko V., Sung U. and Blakely R. D. (2003) Cell surface trafficking of the antidepressant-sensitive norepinephrine transporter revealed with an ectodomain antibody. Mol. Cell Neurosci. 24, 1131-1150.
41. Schroeter S., Apparsundaram S., Wiley R. G., Miner L. H., Sesack S. R. and Blakely R. D. (2000) Immunolocalization of the cocaine- and antidepressant-sensitive 1-norepinephrine transporter. J. Comp. Neurol. 420, 211-232.
42. Shoji-Kasai Y., Itakura M., Kataoka M., Yamamori S. and Takahashi M. (2002) Protein kinase C-mediated translocation of secretory vesicles to plasma membrane and enhancement of neurotransmitter release from PC12 cells. Eur. J. Neurosci. 15, 1390-1394.
43. Soderling T. R. (2000) CaM-kinases: modulators of synaptic plasticity. Curr. Opin. Neurobiol. 10, 375-380.
44. Stober G., Hebebrand J., Cichon S. et al. (1999) Tourette syndrome and the norepinephrine transporter gene: results of a systematic mutation screening. Am. J. Med. Genet. 88, 158-163.
45. Sung U., Apparsundaram S., Galli A., Kahlig K. M., Savchenko V., Schroeter S., Quick M. W. and Blakely R. D. (2003) A regulated interaction of syntaxin 1A with the antidepressant-sensitive norepinephrine transporter establishes catecholamine clearance capacity. J. Neurosci. 23, 1697-1709.
46. Tansey M. G., Word R. A., Hidaka H., Singer H. A., Schworer C. M., Kamm K. E. and Stull J. T. (1992) Phosphorylation of myosin light chain kinase by the multifunctional calmodulin-dependent protein kinase II in smooth muscle cells. J. Biol. Chem. 267, 12 511-12 516.
47. 2+ sensitivity of light chain phosphorylation within smooth muscle cells. J. Biol. Chem. 269, 9912-9920.
48. Uchida J., Kiuchi Y., Ohno M., Yura A. and Oguchi K. (1998) Ca(2+)-dependent enhancement of [3H]noradrenaline uptake in PC12 cells through calmodulin-dependent kinases. Brain Res. 809, 155-164.
49. Uchikawa T., Kiuchi Y., Yura A., Nakachi N., Yamazaki Y., Yokomizo C. and Oguchi K. (1995) Ca(2+)-dependent enhancement of [3H]dopamine uptake in rat striatum: possible involvement of calmodulin-dependent kinases. J. Neurochem. 65, 2065-2071.
50. Ungerer M., Chlistalla A. and Richardt G. (1996) Upregulation of cardiac uptake 1 carrier in ischemic and nonischemic rat heart. Circ. Res. 78, 1037-1043.
51. Yang H. and Raizada M. K. (1998) MAP kinase-independent signaling in angiotensin II regulation of neuromodulation in SHR neurons. Hypertension 32, 473-481.
52. Zhu M. Y., Shamburger S., Li J. and Ordway G. A. (2000) Regulation of the human norepinephrine transporter by cocaine and amphetamine. J. Pharmacol. Exp. Ther. 295, 951-959.