TRPC channels are involved in calcium-dependent migration and proliferation in immortalized GnRH neurons

Cell Calcium

Volumn 49, Issue 6, 2011, Pages 387-394

  Ariano, Paolo ^a,c   Dalmazzo, Simona ^a   Owsianik, Grzegorz ^b   Nilius, Bernd ^b   Lovisolo, Davide ^a  

^a UNIVERSITY OF TURIN   (Italy)

^b LABORATORY OF MOLECULAR AND CELLULAR SIGNALING   (Belgium)

^c ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

Calcium; GN11; GnRH; Migration; TRPC

Indexed keywords

1 OLEIL 2 ACETYL SN GLYCEROL; 1 [2 (4 METHOXYPHENYL) 2 [3 (4 METHOXYPHENYL)PROPOXY]ETHYL] 1H IMIDAZOLE; CALCIUM; CATION CHANNEL; GONADORELIN; LANTHANUM; TRANSIENT RECEPTOR POTENTIAL CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL AFFECTING AGENT; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL IMMORTALIZATION; CELL LINE; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SUBPOPULATION; CONTROLLED STUDY; DEVELOPMENTAL STAGE; MOUSE; NERVE CELL; NERVE CELL DIFFERENTIATION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SERUM; TRANSPORT KINETICS;

VERTEBRATA;

EID: 79958094509     PISSN: 01434160     EISSN: 15321991     Source Type: Journal    
DOI: 10.1016/j.ceca.2011.03.007     Document Type: Article

References (64)

1. Schwarting G.A., Wierman M.E., Tobet S.A. Gonadotropin-releasing hormone neuronal migration. Semin. Reprod. Med. 2007, 25:305-312.
2. Charlton H. Hypothalamic control of anterior pituitary function: a history. J. Neuroendocrinol. 2008, 20:641-646.
3. Schwanzel-Fukuda M., Pfaff D.W. Origin of luteinizing hormone-releasing hormone neurons. Nature 1989, 338:161-164.
4. Wray S., Nieburgs A., Elkabes S. Spatiotemporal cell expression of luteinizing hormone-releasing hormone in the prenatal mouse: evidence for an embryonic origin in the olfactory placode. Brain Res. Dev. Brain Res. 1989, 46:309-318.
5. Wray S. Development of gonadotropin-releasing hormone-1 neurons. Front. Neuroendocrinol. 2002, 23:292-316.
6. Hardelin J.P., Dode C. The complex genetics of Kallmann syndrome: KAL1, FGFR1, FGF8, PROKR2, PROK2, et al. Sex Dev. 2008, 2:181-193.
7. Maggi R., Pimpinelli F., Molteni L., et al. Immortalized luteinizing hormone-releasing hormone neurons show a different migratory activity in vitro. Endocrinology 2000, 141:2105-2112.
8. Pimpinelli F., Redaelli E., Restano-Cassulini R., et al. Depolarization differentially affects the secretory and migratory properties of two cell lines of immortalized luteinizing hormone-releasing hormone (LHRH) neurons. Eur. J. Neurosci. 2003, 18:1410-1418.
9. Giacobini P., Giampietro C., Fioretto M., et al. Hepatocyte growth factor/scatter factor facilitates migration of GN-11 immortalized LHRH neurons. Endocrinology 2002, 143:3306-3315.
10. Giacobini P., Messina A., Wray S., et al. Hepatocyte growth factor acts as a motogen and guidance signal for gonadotropin hormone-releasing hormone-1 neuronal migration. J. Neurosci. 2007, 27:431-445.
11. Giacobini P., Messina A., Morello F., et al. Semaphorin 4D regulates gonadotropin hormone-releasing hormone-1 neuronal migration through PlexinB1-Met complex. J. Cell. Biol. 2008, 183:555-566.
12. Cariboni A., Hickok J., Rakic S., et al. Neuropilins and their ligands are important in the migration of gonadotropin-releasing hormone neurons. J. Neurosci. 2007, 27:2387-2395.
13. Giacobini P., Kopin A.S., Beart P.M., Mercer L.D., Fasolo A., Wray S. Cholecystokinin modulates migration of gonadotropin-releasing hormone-1 neurons. J. Neurosci. 2004, 24:4737-4748.
14. Norgren R.B., Brackenbury R. Cell adhesion molecules and the migration of LHRH neurons during development. Dev. Biol. 1993, 160:377-387.
15. Wray S. From nose to brain: development of gonadotrophin-releasing hormone-1 neurones. J. Neuroendocrinol. 2010, 22:743-753.
16. Radovick S., Wray S., Lee E., et al. Migratory arrest of gonadotropin-releasing hormone neurons in transgenic mice. Proc. Natl. Acad. Sci. U.S.A. 1991, 88:3402-3406.
17. Komuro H., Kumada T. Ca2+ transients control CNS neuronal migration. Cell Calcium 2005, 37:387-393.
18. Zheng J.Q., Poo M.M. Calcium signaling in neuronal motility. Annu. Rev. Cell Dev. Biol. 2007, 23:375-404.
19. Toba Y., Pakiam J.G., Wray S. Voltage-gated calcium channels in developing GnRH-1 neuronal system in the mouse. Eur. J. Neurosci. 2005, 22:79-92.
20. Zaninetti R., Tacchi S., Erriquez J., et al. Calcineurin primes immature gonadotropin-releasing hormone-secreting neuroendocrine cells for migration. Mol. Endocrinol. 2008, 22:729-736.
21. Pedersen S.F., Owsianik G., Nilius B. TRP channels: an overview. Cell Calcium 2005, 38:233-252.
22. Venkatachalam K., Montell C. TRP channels. Annu. Rev. Biochem. 2007, 76:387-417.
23. Nilius B., Owsianik G., Voets T., Peters J.A. Transient receptor potential cation channels in disease. Physiol. Rev. 2007, 87:165-217.
24. Abramowitz J., Birnbaumer L. Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J. 2009, 23:297-328.
25. Talavera K., Nilius B., Voets T. Neuronal TRP channels: thermometers, pathfinders and life-savers. Trends Neurosci. 2008, 31:287-295.
26. Tai Y., Feng S., Du W., Wang Y. Functional roles of TRPC channels in the developing brain. Pflugers Arch. 2009, 458:283-289.
27. Wang W., O'Connell B., Dykeman R., et al. Cloning of Trp1beta isoform from rat brain: immunodetection and localization of the endogenous Trp1 protein. Am. J. Physiol. 1999, 276:C969-C979.
28. Wes P.D., Chevesich J., Jeromin A., Rosenberg C., Stetten G., Montell C. TRPC1, a human homolog of a Drosophila store-operated channel. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:9652-9656.
29. Xu S.Z., Beech D.J. TrpC1 is a membrane-spanning subunit of store-operated Ca(2+) channels in native vascular smooth muscle cells. Circ. Res. 2001, 88:84-87.
30. Lentini D., Guzzi F., Pimpinelli F., et al. Polarization of caveolins and caveolae during migration of immortalized neurons. J. Neurochem. 2008, 104:514-523.
31. Kueng W., Silber E., Eppenberger U. Quantification of cells cultured on 96-well plates. Anal. Biochem. 1989, 182:16-19.
32. Zhang C., Roepke T.A., Kelly M.J., Ronnekleiv O.K. Kisspeptin depolarizes gonadotropin-releasing hormone neurons through activation of TRPC-like cationic channels. J. Neurosci. 2008, 28:4423-4434.
33. Bengtson C.P., Tozzi A., Bernardi G., Mercuri N.B. Transient receptor potential-like channels mediate metabotropic glutamate receptor EPSCs in rat dopamine neurones. J. Physiol. 2004, 555:323-330.
34. Fowler M.A., Sidiropoulou K., Ozkan E.D., Phillips C.W., Cooper D.C. Corticolimbic expression of TRPC4 and TRPC5 channels in the rodent brain. PLoS One 2007, 2:e573.
35. Jia Y., Zhou J., Tai Y., Wang Y. TRPC channels promote cerebellar granule neuron survival. Nat. Neurosci. 2007, 10:559-567.
36. Merritt J.E., Armstrong W.P., Benham C.D., et al. SK&F 96365, a novel inhibitor of receptor-mediated calcium entry. Biochem. J. 1990, 271:515-522.
37. Schwarz G., Droogmans G., Nilius B. Multiple effects of SK&F 96365 on ionic currents and intracellular calcium in human endothelial cells. Cell Calcium 1994, 15:45-54.
38. Barbiero G., Munaron L., Antoniotti S., Baccino F.M., Bonelli G., Lovisolo D. Role of mitogen-induced calcium influx in the control of the cell cycle in Balb-c 3T3 fibroblasts. Cell Calcium 1995, 18:542-556.
39. Ahmmed G.U., Mehta D., Vogel S., et al. Protein kinase Calpha phosphorylates the TRPC1 channel and regulates store-operated Ca2+ entry in endothelial cells. J. Biol. Chem. 2004, 279:20941-20949.
40. Faber E.S., Sedlak P., Vidovic M., Sah P. Synaptic activation of transient receptor potential channels by metabotropic glutamate receptors in the lateral amygdala. Neuroscience 2006, 137:781-794.
41. Antoniotti S., Lovisolo D., Fiorio Pla A., Munaron L. Expression and functional role of bTRPC1 channels in native endothelial cells. FEBS Lett. 2002, 510:189-195.
42. Kim S.J., Kim Y.S., Yuan J.P., Petralia R.S., Worley P.F., Linden D.J. Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 2003, 426:285-291.
43. Malarkey E.B., Ni Y., Parpura V. Ca2+ entry through TRPC1 channels contributes to intracellular Ca2+ dynamics and consequent glutamate release from rat astrocytes. Glia 2008, 56:821-835.
44. Venkatachalam K., Zheng F., Gill D.L. Regulation of canonical transient receptor potential (TRPC) channel function by diacylglycerol and protein kinase C. J. Biol. Chem. 2003, 278:29031-29040.
45. Zhang L., Guo F., Kim J.Y., Saffen D. Muscarinic acetylcholine receptors activate TRPC6 channels in PC12D cells via Ca2+ store-independent mechanisms. J. Biochem. 2006, 139:459-470.
46. Sydorenko V., Shuba Y., Thebault S., et al. Receptor-coupled, DAG-gated Ca2+-permeable cationic channels in LNCaP human prostate cancer epithelial cells. J. Physiol. 2003, 548:823-836.
47. Saleh S.N., Albert A.P., Peppiatt-Wildman C.M., Large W.A. Diverse properties of store-operated TRPC channels activated by protein kinase C in vascular myocytes. J. Physiol. 2008, 586:2463-2476.
48. Lucas P., Ukhanov K., Leinders-Zufall T., Zufall F. A diacylglycerol-gated cation channel in vomeronasal neuron dendrites is impaired in TRPC2 mutant mice: mechanism of pheromone transduction. Neuron 2003, 40:551-561.
49. Rohacs T., Nilius B. Regulation of transient receptor potential (TRP) channels by phosphoinositides. Pflugers Arch. 2007, 455:157-168.
50. Magni P., Dozio E., Ruscica M., et al. Leukemia inhibitory factor induces the chemomigration of immortalized gonadotropin-releasing hormone neurons through the independent activation of the Janus kinase/signal transducer and activator of transcription 3, mitogen-activated protein kinase/extracellularly regulated kinase 1/2, and phosphatidylinositol 3-kinase/Akt signaling pathways. Mol. Endocrinol. 2007, 21:1163-1174.
51. Constantin S., Caligioni C.S., Stojilkovic S., Wray S. Kisspeptin-10 facilitates a plasma membrane-driven calcium oscillator in gonadotropin-releasing hormone-1 neurons. Endocrinology 2009, 150:1400-1412.
52. Rao J.N., Platoshyn O., Golovina V.A., et al. TRPC1 functions as a store-operated Ca2+ channel in intestinal epithelial cells and regulates early mucosal restitution after wounding. Am. J. Physiol. Gastrointest. Liver Physiol. 2006, 290:G782-G792.
53. Waning J., Vriens J., Owsianik G., et al. A novel function of capsaicin-sensitive TRPV1 channels: involvement in cell migration. Cell Calcium 2007, 42:17-25.
54. Fabian A., Fortmann T., Dieterich P., et al. TRPC1 channels regulate directionality of migrating cells. Pflugers Arch. 2008, 457:475-484.
55. Damann N., Owsianik G., Li S., Poll C., Nilius B. The calcium-conducting ion channel transient receptor potential canonical 6 is involved in macrophage inflammatory protein-2-induced migration of mouse neutrophils. Acta Physiol. (Oxf.) 2009, 195:3-11.
56. Shimizu T., Owsianik G., Freichel M., Flockerzi V., Nilius B., Vennekens R. TRPM4 regulates migration of mast cells in mice. Cell Calcium 2009, 45:226-232.
57. Gomez T.M., Zheng J.Q. The molecular basis for calcium-dependent axon pathfinding. Nat. Rev. Neurosci. 2006, 7:115-125.
58. Ramsey I.S., Delling M., Clapham D.E. An introduction to TRP channels. Annu. Rev. Physiol. 2006, 68:619-647.
59. Dalmazzo S., Antoniotti S., Ariano P., Gilardino A., Lovisolo D. Expression and localisation of TRPC channels in immortalised GnRH neurons. Brain Res. 2008, 1230:27-36.
60. Flockerzi V., Jung C., Aberle T., et al. Specific detection and semi-quantitative analysis of TRPC4 protein expression by antibodies. Pflugers Archiv.: Eur. J. Physiol. 2005, 451:81-86.
61. Juvin V., Penna A., Chemin J., Lin Y.L., Rassendren F.A. Pharmacological characterization and molecular determinants of the activation of transient receptor potential V2 channel orthologs by 2-aminoethoxydiphenyl borate. Mol. Pharmacol. 2007, 72:1258-1268.
62. Singh A., Hildebrand M.E., Garcia E., Snutch T.P. The transient receptor potential channel antagonist SKF96365 is a potent blocker of low-voltage-activated T-type calcium channels. Br. J. Pharmacol. 2010, 160:1464-1475.
63. Dolmetsch R.E., Xu K., Lewis R.S. Calcium oscillations increase the efficiency and specificity of gene expression. Nature 1998, 392:933-936.
64. Gu X., Spitzer N.C. Distinct aspects of neuronal differentiation encoded by frequency of spontaneous Ca2+ transients. Nature 1995, 375:784-787.