K-Cl - cotransporter 1 (KCC1) negatively regulates NGF-induced neurite outgrowth in PC12 cells

Cellular Physiology and Biochemistry

Volumn 30, Issue 3, 2012, Pages 538-551

  Nagao, Hikaru ^a,b   Nakajima, Ken Ichi ^a   Niisato, Naomi ^a,c   Hirota, Ryuichi ^b   Bando, Hideki ^b   Sakaguchi, Hirofumi ^b   Hisa, Yasuo ^b   Marunaka, Yoshinori ^a,c  

^a KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^b KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^c Takatsuki city   (Japan)

Author keywords

Chloride ion concentration; DIOA; NGF; SiRNA; SLC12 family

Indexed keywords

ALKANOIC ACID; MESSENGER RNA; NERVE GROWTH FACTOR; POTASSIUM CHLORIDE COTRANSPORTER; POTASSIUM CHLORIDE COTRANSPORTER 1; POTASSIUM CHLORIDE COTRANSPORTER 2; POTASSIUM CHLORIDE COTRANSPORTER 3; POTASSIUM CHLORIDE COTRANSPORTER 4; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; [(DIHYDRONINDENYL)OXY]ALKANOIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL STRAIN; CONTROLLED STUDY; EPITHELIUM CELL; GENE EXPRESSION; GENE SILENCING; MALE; NERVE FIBER GROWTH; NONHUMAN; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROSTATE CANCER; PROTEIN EXPRESSION; RAT;

RATTUS;

EID: 84863874509     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000341436     Document Type: Article

References (58)

1. Russell JM: Sodium-potassium-chloride cotransport. Physiol Rev 2000;80:211-276.
2. Hebert SC, Mount DB, Gamba G: Molecular physiology of cation-coupled CI" cotransport: the SLC12 family. Pflugers Arch 2004;447:580-593.
3. Adragna NC, Di Fulvio M, Lauf PK: Regulation of K-Cl cotransport: from function to genes. Membr Biol 2004;201:109-137.
4. Chen YF, Chou CY, Ellory JC, Shen MR: The emerging role of KCl cotransport in tumor biology. Am Transi Res 2010;2:345-355.
5. Wei WC, Akerman C], Newey SE, Pan J, Clinch NW, Jacob Y, Shen MR, Wilkins R], Ellory JC: The potassium-chloride cotransporter 2 promotes cervical cancer cell migration and invasion by an ion transport-independent mechanism. J Physiol 2011;589:5349-5359.
6. Shen MR, Chou CY, Ellory JC: Volume-sensitive KCl cotransport associated with human cervical carcinogenesis. Pflugers Arch 2000;440:751-760.
7. Shen MR, Chou CY, Hsu KF, Hsu YM, Chiu WT, Tang MJ, Alper SL, Ellory JC: KCl cotransport is an important modulator of human cervical cancer growth and invasion. J Biol Chem 2003;278:39941-39950.
8. Shen MR, Lin AC, Hsu YM, Chang TJ, Tang MJ, Alper SL, Ellory JC, Chou CY: Insulin-like growth factor 1 stimulates KCl cotransport, which is necessary for invasion and proliferation of cervical cancer and ovarian cancer cells. J Cell Biol 2004;279:40017-40025.
9. Hsu YM, Chen YF, Chou CY, Tang MJ, Chen JH, Wilkins RJ, Ellory JC, Shen MR: KCl cotransporter-3 down-regulates E-cadherin/beta-catenin complex to promote epithelial-mesenchymal transition. Cancer Res 2007;67:11064-11073.
10. Pan D, Kalfa TA, Wang D, Risinger M, Crable S, Ottlinger A, Chandra S, Mount DB, Hubner CA, Franco RS, Joiner CH: K-Cl cotransporter gene expression during human and murine erythroid differentiation. J Biol Chem 2011;286:30492-30503.
11. Shiozaki A, Miyazaki H, Niisato N, Nakahari T, Iwasaki Y, Itoi H, Ueda Y, Yamagishi H, Marunaka Y: Furosemide, a blocker of NaVKV2Cl" cotransporter, diminishes proliferation of poorly differentiated human gastric cancer cells by affecting G^Gj state. J Physiol Sei 2006;56:401-406.
12. Shiozaki A, Otsuji E, Marunaka Y: Intracellular chloride regulates the GJS cell cycle progression in gastric cancer cells. World J Gastrointest Oncol 2011;3:119-122.
13. Ohsawa R, Miyazaki H, Niisato N, Shiozaki A, Iwasaki Y, Otsuji E, Marunaka Y: Intracellular chloride regulates cell proliferation through the activation of stress-activated protein kinases in MKN28 human gastric cancer cells. J Cell Physiol 2010;223:764-770.
14. Maki M, Miyazaki H, Niisato N, Morihara T, Marunaka Y, Kubo T: Blockers of IC/Cl" transporter/channels diminish proliferation of osteoblastic cells. Biomed Res 2009;30:137-140.
15. Marunaka Y, Niisato N, Taruno A, Ohta M, Miyazaki H, Hosogi S, Nakajima K, Kusuzaki K, Ashihara E, Nishio K, Iwasaki Y Nakahari T, Kubota T: Regulation of epithelial sodium transport via epithelial Nachannel. Biomed Biotechnol 2011;2011:978196.
16. Niisato N, Eaton DC, Marunaka Y: Involvement of cytosolic CI" in osmoregulation of alpha-ENaC gene expression. Am Physiol Renal Physiol 2004;287:F932-939.
17. Menegazzi R, Busetto S, Cramer R, Dri P, Patriarca P: Role of intracellular chloride in the reversible activation of neutrophil beta 2 integrins: a lesson from TNF stimulation. Immunol 2000;165:4606-4614.
18. Menegazzi R, Busetto S, Decleva E, Cramer R, Dri P, Patriarca P: Triggering of chloride ion efflux from human neutrophils as a novel function of leukocyte beta 2 integrins: relationship with spreading and activation of the respiratory burst. Immunol 1999;162:423-434.
19. Menegazzi R, Busetto S, Dri P, Cramer R, Patriarca P: Chloride ion efflux regulates adherence, spreading, and respiratory burst of neutrophils stimulated by tumor necrosis factor-alpha (TNF) on biologic surfaces. Cell Biol 1996;135:511-522.
20. Busetto S, Trevisan E, Decleva E, Dri P, Menegazzi R: Chloride movements in human neutrophils during phagocytosis: characterization and relationship to granule release. Immunol 2007;179:4110-4124.
21. Nakajima K, Miyazaki H, Niisato N, Marunaka Y Essential role of NKCC1 in NGF-induced neurite outgrowth. Biochem Biophys Res Commun 2007;359:604-610.
22. Nakajima K, Miyazaki H, Niisato N, Marunaka Y Implication of chloride transporter, NKCC1, in neurite outgrowth. Physiol Sei 2007;57:S121.
23. Nakajima K, Niisato N, Marunaka Y Molecular mechanism of degradation and turnover of NKCC1. Physiol Sci2008;58:S205.
24. Nakajima K, Niisato N, Marunaka Y Genistein enhances the NGF-induced neurite outgrowth. Biomed Res 2011;32:351-356.
25. Nakajima K, Niisato N, Marunaka Y Quercetin stimulates NGF-induced neurite outgrowth in PC12 cells via activation of Na7K72Cl-cotransporter. Cell Physiol Biochem 2011;28:147-156.
26. Nakajima K, Niisato N, Marunaka Y Flavonoids stimulate NGF-induced neurite outgrowth in PC12 cells via activation of Na7K72Cl-cotransporter. Physiol Sei 2010;60:S106.
27. Nakajima K, Nagao H, Niisato N, Hisa Y Marunaka Y The role of potassium chloride cotransporter 1 in neurite outgrowth of PC12 cell. Physiol Sei 2011; 61:S260.
28. Niisato N, Ohta M, Eaton DC, Marunaka Y Hypotonic stress upregulates beta-and gamma-ENaC expression through suppression of ERK by inducing MKP-1. Am Physiol Renal Physiol 2012, in press.
29. Garay RP, Nazaret C, Hannaert PA, Cragoe E], Jr.: Demonstration of a [K*, Cr]-cotransport system in human red cells by its sensitivity to [(dihydroindenyl)oxy]alkanoic acids: regulation of cell swelling and distinction from the bumetanide-sensitive [Na*, K*, Cl~]-cotransport system. Mol Pharmacol 1988;33:696-701.
30. Su W, Shmukler BE, Chernova MN, Stuart-Tilley AK, de Franceschi L, Brugnara C, Alper SL: Mouse K-Cl cotransporter KCC1: cloning, mapping, pathological expression, and functional regulation. Am Physiol 1999;277:C899-912.
31. Shen MR, Chou CY, Hsu KF, Liu HS, Dunham PB, Holtzman E], Ellory JC: The KCl cotransporter isoform KCC3 can play an important role in cell growth regulation. Proc Natl Acad Sei USA 2001;98:14714-14719.
32. Pellegrino C, Gubkina O, Schaefer M, Becq H, Ludwig A, Mukhtarov M, Chudotvorova I, Corby S, Salyha Y Salozhin S, Bregestovski P, Medina I: Knocking down of the KCC2 in rat hippocampal neurons increases intracellular chloride concentration and compromises neuronal survival. Physiol 2011;589:2475-2496.
33. Mercado A, Song L, Vazquez N, Mount DB, Gamba G: Functional comparison of the K*-C1" cotransporters KCC1 and KCC4. Biol Chem 2000;275:30326-30334.
34. Fujii T, Ohira Y, Itomi Y, Takahashi Y, Asano S, Morii M, Takeguchi N, Sakai H: Inhibition of P-type ATPases by [(dihydroindenyl)oxy]acetic acid (DIOA), a K*-C1" cotransporter inhibitor. Eur Pharmacol 2007;560:123-126.
35. Arrazola A, Rota R, Hannaert P, Soler A, Garay RP: Cell volume regulation in rat thymocytes. Physiol 1993;465:403-414.
36. Lauf PK, Misri S, Chimote AA, Adragna NC: Apparent intermediate K conductance channel hyposmotic activation in human lens epithelial cells. Am Physiol Cell Physiol 2008;294:C820-832.
37. Keith CH: Neurite elongation is blocked if microtubule polymerization is inhibited in PC12 cells. Cell Motil Cytoskeleton 1990;17:95-105.
38. Yasui H, Katoh H, Yamaguchi Y Aoki J, Fujita H, Mori K, Negishi M: Differential responses to nerve growth factor and epidermal growth factor in neurite outgrowth of PC12 cells are determined by Racl activation systems. Biol Chem 2001;276:15298-15305.
39. Stein V, Hermans-Borgmeyer I, Jentsch T], Hubner CA: Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. Comp Neurol 2004;468:57-64.
40. Uvarov P, Ludwig A, Markkanen M, Pruunsild P, Kaila K, Delpire E, Timmusk T, Rivera C, Airaksinen MS: A novel N-terminal isoform of the neuron-specific K-Cl cotransporter KCC2. Biol Chem 2007;282:30570-30576.
41. Lauf PK, Di Fulvio M, Srivastava V, Sharma N, Adragna NC: KCC2a expression in a human fetal lens epithelial cell line. Cell Physiol Biochem 2012;29:303-312.
42. Payne JA, Antrobus SP, Lytle C: K-Cl cotransporter-2 (KCC2) expression in chicken cardiomyocytes. FASEB 2012;26:694.691.
43. Payne JA, Stevenson TJ, Donaldson LF: Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform. J Biol Chem 1996;271:16245-16252.
44. Chelly J, Kaplan JC, Maire P, Gautron S, Kahn A: Transcription of the dystrophin gene in human muscle and non-muscle tissue. Nature 1988;333:858-860.
45. Rivera C, Li H, Thomas-Crusells J, Lahtinen H, Viitanen T, Nanobashvili A, Kokaia Z, Airaksinen MS, Voipio J, Kaila K, Saarma M: BDNF-induced TrkB activation down-regulates the K*-C1" cotransporter KCC2 and impairs neuronal CI" extrusion. J Cell Biol 2002;159:747-752.
46. Akiyama N, Hatori Y, Takashiro Y Hirabayashi T, Saito T, Murayama T: Nerve growth factor-induced up-regulation of cytosolic phospholipase A2alpha level in rat PC12 cells. Neurosci Lett 2004;365:218-222.
47. Suzuki X Kurahashi H, Ichinose H: Ras/MEK pathway is required for NGF-induced expression of tyrosine hydroxylase gene. Biochem Biophys Res Commun 2004;315:389-396.
48. Naranjo-Suarez S, Castellanos MC, Alvarez-Tejado M, Vara A, Landazuri MO, del Peso L: Down-regulation of hypoxia-inducible factor-2 in PC12 cells by nerve growth factor stimulation. J Biol Chem 2003;278:31895-31901.
49. Kurbannazarova RS, Bessonova SV, Okada Y Sabirov RZ: Swelling-activated anion channels are essential for volume regulation of mouse thymocytes. Int J Mol Sei 2011;12:9125-9137.
50. Miyazaki H, Shiozaki A, Niisato N, Ohsawa R, Itoi H, Ueda Y, Otsuji E, Yamagishi H, Iwasaki Y, Nakano T, Nakahari T, Marunaka Y: Chloride ions control the Gj/S cell-cycle checkpoint by regulating the expression of p21 through a p53-independent pathway in human gastric cancer cells. Biochem Biophys Res Commun 2008;366:506-512.
51. Hiraoka K, Miyazaki H, Niisato N, Iwasaki Y Kawauchi A, Miki T, Marunaka Y Chloride ion modulates cell proliferation of human androgen-independent prostatic cancer cell. Cell Physiol Biochem 2010;25:379-388.
52. Maki M, Miyazaki H, Nakajima K, Yamane J, Niisato N, Morihara T, Kubo T, Marunaka Y Chloride-dependent acceleration of cell cycle via modulation of Rb and cdc2 in osteoblastic cells. Biochem Biophys Res Commun 2007;361:1038-1043.
53. Ohsawa R, Miyazaki H, Otsuji E, Niisato N, Marunaka Y Intracellular chloride-dependent mechanism of stress-activated protein kinases in human gastric cancer MKN28 cells. J Physiol Sei 2009;59:S303.
54. Ohsawa R, Miyazaki H, Shiozaki A, Otsuji E, Niisato N, Marunaka Y Reduction of intracellular CI" concentration induces the Gj/S cell cycle arrest through the activation of stress-activated protein kinases in MKN28 human gastric cancer cells. Physiol Sei 2008;58:S207.
55. Hiraoka K, Miyazaki H, Niisato N, Marunaka Y Intracellular chloride regulates cell proliferation of androgen-independent prostate cancer PC3 cell. Physiol Sei 2009;59:S303.
56. Miyazaki H, Shiozaki A, Niisato N, Marunaka Y Cl-dependent regulatory mechanisms of proliferation of human gastric cancer cells via G^Gj arrest. Physiol Sei 2007;57:S20.
57. Miyazaki H, Shiozaki A, Niisato N, Marunaka Y Physiological significance of hypotonicity-induced regulatory volume decrease: reduction in intracellular CI" concentration acting as an intracellular signaling. Am Physiol Renal Physiol 2007;292:F1411-F1417.
58. Miyazaki H, Ohsawa R, Shiozaki A, Niisato N, Marunaka Y Intracellular chloride regulates the Gj/S cell cycle checkpoint in MKN28 human gastric cancer cells. Physiol Sei 2008;58:S207.