Advertisement

Role of T-Type Calcium Channels in Neuroendocrine Differentiation

  • Marine Warnier
  • Florian Gackière
  • Morad Roudbaraki
  • Pascal Mariot
Chapter

Abstract

Neuroendocrine cells release their secretory products into the extracellular environment via a calcium-dependent pathway. These particular cells share common morphological and molecular features, such as the expression of specific biomarkers, neurite outgrowth and dense-core secretory granules. In order to elucidate the signalling pathways leading from undifferentiated to differentiated neuroendocrine cells, the role of voltage-dependent calcium channels and central actors in excitation–secretion coupling has been comprehensively investigated. T-type calcium channels, comprising of three different molecular isoforms, appear to be one of the important calcium channel families involved in the neuroendocrine differentiation process. They also may participate in the development of neuroendocrine tumours.

Keywords

PC12 Cell Nerve Growth Factor LNCaP Cell Prostatic Acid Phosphatase Neurite Formation 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abrahamsson PA (1999) Neuroendocrine differentiation in prostatic carcinoma. Prostate 39:135–148PubMedGoogle Scholar
  2. Andres D, Keyser BM, Petrali J, Benton B, Hubbard KS, McNutt PM, Ray R (2013) Morphological and functional differentiation in BE(2)-M17 human neuroblastoma cells by treatment with Trans-retinoic acid. BMC Neurosci 14:49PubMedCentralPubMedGoogle Scholar
  3. Andrew A (1974) Further evidence that enterochromaffin cells are not derived from the neural crest. J Embryol Exp Morphol 31:589–598PubMedGoogle Scholar
  4. Angelsen A, Sandvik AK, Syversen U, Stridsberg M, Waldum HL (1998) NGF-beta, NE-cells and prostatic cancer cell lines. A study of neuroendocrine expression in the human prostatic cancer cell lines DU-145, PC-3, LNCaP, and TSU-pr1 following stimulation of the nerve growth factor-beta. Scand J Urol Nephrol 32:7–13PubMedGoogle Scholar
  5. Arnhold S, Andressen C, Angelov DN, Vajna R, Volsen SG, Hescheler J, Addicks K (2000) Embryonic stem-cell derived neurones express a maturation dependent pattern of voltage-gated calcium channels and calcium-binding proteins. Int J Dev Neurosci 18:201–212PubMedGoogle Scholar
  6. Artalejo CR, Adams ME, Fox AP (1994) Three types of Ca2+ channel trigger secretion with different efficacies in chromaffin cells. Nature 367:72–76PubMedGoogle Scholar
  7. Bang YJ, Pirnia F, Fang WG, Kang WK, Sartor O, Whitesell L, Ha MJ, Tsokos M, Sheahan MD, Nguyen P et al (1994) Terminal neuroendocrine differentiation of human prostate carcinoma cells in response to increased intracellular cyclic AMP. Proc Natl Acad Sci USA 91:5330–5334PubMedCentralPubMedGoogle Scholar
  8. Banno Y, Nemoto S, Murakami M, Kimura M, Ueno Y, Ohguchi K, Hara A, Okano Y, Kitade Y, Onozuka M, Murate T, Nozawa Y (2008) Depolarization-induced differentiation of PC12 cells is mediated by phospholipase D2 through the transcription factor CREB pathway. J Neurochem 104:1372–1386PubMedGoogle Scholar
  9. Berenguer C, Boudouresque F, Dussert C, Daniel L, Muracciole X, Grino M, Rossi D, Mabrouk K, Figarella-Branger D, Martin PM, Ouafik L (2008) Adrenomedullin, an autocrine/paracrine factor induced by androgen withdrawal, stimulates ‘neuroendocrine phenotype’ in LNCaP prostate tumor cells. Oncogene 27:506–518PubMedGoogle Scholar
  10. Bergeron F, Leduc R, Day R (2000) Subtilase-like pro-protein convertases: from molecular specificity to therapeutic applications. J Mol Endocrinol 24:1–22PubMedGoogle Scholar
  11. Bertolesi GE, Jollimore CA, Shi C, Elbaum L, Denovan-Wright EM, Barnes S, Kelly ME (2003) Regulation of alpha1G T-type calcium channel gene (CACNA1G) expression during neuronal differentiation. Eur J Neurosci 17:1802–1810PubMedGoogle Scholar
  12. Bertolesi GE, Walia Da Silva R, Jollimore CA, Shi C, Barnes S, Kelly ME (2006) Ca(v)3.1 splice variant expression during neuronal differentiation of Y-79 retinoblastoma cells. Neuroscience 141:259–268PubMedGoogle Scholar
  13. Boczek T, Lisek M, Kowalski A, Pikula S, Niewiarowska J, Wiktorska M, Zylinska L (2012) Downregulation of PMCA2 or PMCA3 reorganizes Ca(2+) handling systems in differentiating PC12 cells. Cell Calcium 52:433–444PubMedGoogle Scholar
  14. Bosch MA, Hou J, Fang Y, Kelly MJ, Ronnekleiv OK (2009) 17Beta-estradiol regulation of the mRNA expression of T-type calcium channel subunits: role of estrogen receptor alpha and estrogen receptor beta. J Comp Neurol 512:347–358PubMedCentralPubMedGoogle Scholar
  15. Bournaud R, Hidalgo J, Yu H, Jaimovich E, Shimahara T (2001) Low threshold T-type calcium current in rat embryonic chromaffin cells. J Physiol 537:35–44PubMedCentralPubMedGoogle Scholar
  16. Carabelli V, Marcantoni A, Comunanza V, Carbone E (2007a) Fast exocytosis mediated by T- and L-type channels in chromaffin cells: distinct voltage-dependence but similar Ca2+-dependence. Eur Biophys J 36:753–762PubMedGoogle Scholar
  17. Carabelli V, Marcantoni A, Comunanza V, de Luca A, Diaz J, Borges R, Carbone E (2007b) Chronic hypoxia up-regulates alpha1H T-type channels and low-threshold catecholamine secretion in rat chromaffin cells. J Physiol 584:149–165PubMedCentralPubMedGoogle Scholar
  18. Carbone E, Giancippoli A, Marcantoni A, Guido D, Carabelli V (2006) A new role for T-type channels in fast “low-threshold” exocytosis. Cell Calcium 40:147–154PubMedGoogle Scholar
  19. Catterall WA (2011) Voltage-gated calcium channels. Cold Spring Harb Perspect Biol 3:a003947PubMedCentralPubMedGoogle Scholar
  20. Cazillis M, Gonzalez BJ, Billardon C, Lombet A, Fraichard A, Samarut J, Gressens P, Vaudry H, Rostene W (2004) VIP and PACAP induce selective neuronal differentiation of mouse embryonic stem cells. Eur J Neurosci 19:798–808PubMedGoogle Scholar
  21. Chafai M, Basille M, Galas L, Rostene W, Gressens P, Vaudry H, Gonzalez BJ, Louiset E (2011) Pituitary adenylate cyclase-activating polypeptide and vasoactive intestinal polypeptide promote the genesis of calcium currents in differentiating mouse embryonic stem cells. Neuroscience 199:103–115PubMedGoogle Scholar
  22. Chemin J, Nargeot J, Lory P (2002) Neuronal T-type alpha 1H calcium channels induce neuritogenesis and expression of high-voltage-activated calcium channels in the NG108-15 cell line. J Neurosci 22:6856–6862PubMedGoogle Scholar
  23. Chemin J, Nargeot J, Lory P (2004) Ca(v)3.2 calcium channels control an autocrine mechanism that promotes neuroblastoma cell differentiation. Neuroreport 15:671–675PubMedGoogle Scholar
  24. Chen H, Sun Y, Wu C, Magyar CE, Li X, Cheng L, Yao JL, Shen S, Osunkoya AO, Liang C, Huang J (2012) Pathogenesis of prostatic small cell carcinoma involves the inactivation of the P53 pathway. Endocr Relat Cancer 19:321–331PubMedCentralPubMedGoogle Scholar
  25. Collado B, Gutierrez-Canas I, Rodriguez-Henche N, Prieto JC, Carmena MJ (2004) Vasoactive intestinal peptide increases vascular endothelial growth factor expression and neuroendocrine differentiation in human prostate cancer LNCaP cells. Regul Pept 119:69–75PubMedGoogle Scholar
  26. Collado B, Sanchez MG, Diaz-Laviada I, Prieto JC, Carmena MJ (2005) Vasoactive intestinal peptide (VIP) induces c-fos expression in LNCaP prostate cancer cells through a mechanism that involves Ca2+ signalling. Implications in angiogenesis and neuroendocrine differentiation. Biochim Biophys Acta 1744:224–233PubMedGoogle Scholar
  27. Cox ME, Deeble PD, Bissonette EA, Parsons SJ (2000) Activated 3',5'-cyclic AMP-dependent protein kinase is sufficient to induce neuroendocrine-like differentiation of the LNCaP prostate tumor cell line. J Biol Chem 275:13812–13818PubMedGoogle Scholar
  28. Day R, Salzet M (2002) The neuroendocrine phenotype, cellular plasticity, and the search for genetic switches: redefining the diffuse neuroendocrine system. Neuro Endocrinol Lett 23:447–451PubMedGoogle Scholar
  29. Deeble PD, Murphy DJ, Parsons SJ, Cox ME (2001) Interleukin-6- and cyclic AMP-mediated signaling potentiates neuroendocrine differentiation of LNCaP prostate tumor cells. Mol Cell Biol 21:8471–8482PubMedCentralPubMedGoogle Scholar
  30. DeLellis RA (2001) The neuroendocrine system and its tumors: an overview. Am J Clin Pathol 115(Suppl):S5–S16PubMedGoogle Scholar
  31. Diaz M, Abdul M, Hoosein N (1998) Modulation of neuroendocrine differentiation in prostate cancer by interleukin-1 and -2. Prostate Suppl 8:32–36PubMedGoogle Scholar
  32. Dizeyi N, Hedlund P, Bjartell A, Tinzl M, Austild-Tasken K, Abrahamsson PA (2011) Serotonin activates MAP kinase and PI3K/Akt signaling pathways in prostate cancer cell lines. Urol Oncol 29:436–445PubMedGoogle Scholar
  33. Elhamdani A, Brown ME, Artalejo CR, Palfrey HC (2000) Enhancement of the dense-core vesicle secretory cycle by glucocorticoid differentiation of PC12 cells: characteristics of rapid exocytosis and endocytosis. J Neurosci 20:2495–2503PubMedGoogle Scholar
  34. Farini D, Puglianiello A, Mammi C, Siracusa G, Moretti C (2003) Dual effect of pituitary adenylate cyclase activating polypeptide on prostate tumor LNCaP cells: short- and long-term exposure affect proliferation and neuroendocrine differentiation. Endocrinology 144:1631–1643PubMedGoogle Scholar
  35. Feyrter F (1938) Uber diffuse endokrine epitheliale Organe. JA Barth, Leipzig, GermanyGoogle Scholar
  36. Flourakis M, Lehen’kyi V, Beck B, Raphael M, Vandenberghe M, Abeele FV, Roudbaraki M, Lepage G, Mauroy B, Romanin C, Shuba Y, Skryma R, Prevarskaya N (2010) Orai1 contributes to the establishment of an apoptosis-resistant phenotype in prostate cancer cells. Cell Death Dis 1:e75PubMedCentralPubMedGoogle Scholar
  37. Froelich F (1949) Die “Helle Zelle” der Bronchialschleimhaut und ihre Beziehungen zum Problem der Chemoreceptoren. Frankfurt Z Pathol 60:517–559Google Scholar
  38. Fujita T, Kobayashi S, Yui R (1980) Paraneuron concept and its current implications. Adv Biochem Psychopharmacol 25:321–325PubMedGoogle Scholar
  39. Gackiere F, Bidaux G, Delcourt P, Van Coppenolle F, Katsogiannou M, Dewailly E, Bavencoffe A, Van Chuoi-Mariot MT, Mauroy B, Prevarskaya N, Mariot P (2008) CaV3.2T-type calcium channels are involved in calcium-dependent secretion of neuroendocrine prostate cancer cells. J Biol Chem 283:10162–10173PubMedGoogle Scholar
  40. Gackiere F, Bidaux G, Lory P, Prevarskaya N, Mariot P (2006) A role for voltage gated T-type calcium channels in mediating “capacitative” calcium entry? Cell Calcium 39:357–366PubMedGoogle Scholar
  41. Gackiere F, Warnier M, Katsogiannou M, Derouiche S, Delcourt P, Dewailly E, Slomianny C, Humez S, Prevarskaya N, Roudbaraki M, Mariot P (2013) Functional coupling between large-conductance potassium channels and Cav3.2 voltage-dependent calcium channels participates in prostate cancer cell growth. Biol Open 2:941–991PubMedCentralPubMedGoogle Scholar
  42. Garber SS, Hoshi T, Aldrich RW (1989) Regulation of ionic currents in pheochromocytoma cells by nerve growth factor and dexamethasone. J Neurosci 9:3976–3987PubMedGoogle Scholar
  43. Giancippoli A, Novara M, de Luca A, Baldelli P, Marcantoni A, Carbone E, Carabelli V (2006) Low-threshold exocytosis induced by cAMP-recruited CaV3.2 (alpha1H) channels in rat chromaffin cells. Biophys J 90:1830–1841PubMedCentralPubMedGoogle Scholar
  44. Greene LA, Tischler AS (1976) Establishment of a noradrenergic clonal line of rat adrenal pheochromocytoma cells which respond to nerve growth factor. Proc Natl Acad Sci USA 73:2424–2428PubMedCentralPubMedGoogle Scholar
  45. Greka A, Navarro B, Oancea E, Duggan A, Clapham DE (2003) TRPC5 is a regulator of hippocampal neurite length and growth cone morphology. Nat Neurosci 6:837–845PubMedGoogle Scholar
  46. Grumolato L, Elkahloun AG, Ghzili H, Alexandre D, Coulouarn C, Yon L, Salier JP, Eiden LE, Fournier A, Vaudry H, Anouar Y (2003) Microarray and suppression subtractive hybridization analyses of gene expression in pheochromocytoma cells reveal pleiotropic effects of pituitary adenylate cyclase-activating polypeptide on cell proliferation, survival, and adhesion. Endocrinology 144:2368–2379PubMedGoogle Scholar
  47. Grumolato L, Ghzili H, Montero-Hadjadje M, Gasman S, Lesage J, Tanguy Y, Galas L, Ait-Ali D, Leprince J, Guerineau NC, Elkahloun AG, Fournier A, Vieau D, Vaudry H, Anouar Y (2008) Selenoprotein T is a PACAP-regulated gene involved in intracellular Ca2+ mobilization and neuroendocrine secretion. FASEB J 22:1756–1768PubMedGoogle Scholar
  48. Gong J, Lee J, Akio H, Schlegel PN, Shen R (2007) Attenuation of apoptosis by chromogranin A-induced Akt and survivin pathways in prostate cancer cells. Endocrinology 148:4489–4499PubMedGoogle Scholar
  49. Gu X, Spitzer NC (1993) Low-threshold Ca2+ current and its role in spontaneous elevations of intracellular Ca2+ in developing Xenopus neurons. J Neurosci 13:4936–4948PubMedGoogle Scholar
  50. Gustafsson BI, Kidd M, Modlin IM (2008) Neuroendocrine tumors of the diffuse neuroendocrine system. Curr Opin Oncol 20:1–12PubMedGoogle Scholar
  51. Gutierrez-Canas I, Juarranz MG, Collado B, Rodriguez-Henche N, Chiloeches A, Prieto JC, Carmena MJ (2005) Vasoactive intestinal peptide induces neuroendocrine differentiation in the LNCaP prostate cancer cell line through PKA, ERK, and PI3K. Prostate 63:44–55PubMedGoogle Scholar
  52. Hansson J, Abrahamsson PA (2003) Neuroendocrine differentiation in prostatic carcinoma. Scand J Urol Nephrol Suppl 28–36Google Scholar
  53. Heo DK, Chung WY, Park HW, Yuan JP, Lee MG, Kim JY (2012) Opposite regulatory effects of TRPC1 and TRPC5 on neurite outgrowth in PC12 cells. Cell Signal 24:899–906PubMedGoogle Scholar
  54. Hill J, Chan SA, Kuri B, Smith C (2011) Pituitary adenylate cyclase-activating peptide (PACAP) recruits low voltage-activated T-type calcium influx under acute sympathetic stimulation in mouse adrenal chromaffin cells. J Biol Chem 286:42459–42469PubMedCentralPubMedGoogle Scholar
  55. Hirooka K, Bertolesi GE, Kelly ME, Denovan-Wright EM, Sun X, Hamid J, Zamponi GW, Juhasz AE, Haynes LW, Barnes S (2002) T-Type calcium channel alpha1G and alpha1H subunits in human retinoblastoma cells and their loss after differentiation. J Neurophysiol 88:196–205PubMedGoogle Scholar
  56. Holliday J, Spitzer NC (1990) Spontaneous calcium influx and its roles in differentiation of spinal neurons in culture. Dev Biol 141:13–23PubMedGoogle Scholar
  57. Homma K, Kitamura Y, Ogawa H, Oka K (2006) Serotonin induces the increase in intracellular Ca2+ that enhances neurite outgrowth in PC12 cells via activation of 5-HT3 receptors and voltage-gated calcium channels. J Neurosci Res 84:316–325PubMedGoogle Scholar
  58. Huang J, Yao JL, di Sant’Agnese PA, Yang Q, Bourne PA, Na Y (2006) Immunohistochemical characterization of neuroendocrine cells in prostate cancer. Prostate 66:1399–1406PubMedGoogle Scholar
  59. Jeon S, Park JK, Bae CD, Park J (2010) NGF-induced moesin phosphorylation is mediated by the PI3K, Rac1 and Akt and required for neurite formation in PC12 cells. Neurochem Int 56:810–818PubMedGoogle Scholar
  60. Jones SE, Palmer TM (2012) Protein kinase A-mediated phosphorylation of RhoA on serine 188 triggers the rapid induction of a neuroendocrine-like phenotype in prostate cancer epithelial cells. Cell Signal 24:1504–1514PubMedCentralPubMedGoogle Scholar
  61. Kiermayer S, Biondi RM, Imig J, Plotz G, Haupenthal J, Zeuzem S, Piiper A (2005) Epac activation converts cAMP from a proliferative into a differentiation signal in PC12 cells. Mol Biol Cell 16:5639–5648PubMedCentralPubMedGoogle Scholar
  62. Kim J, Adam RM, Freeman MR (2002) Activation of the Erk mitogen-activated protein kinase pathway stimulates neuroendocrine differentiation in LNCaP cells independently of cell cycle withdrawal and STAT3 phosphorylation. Cancer Res 62:1549–1554PubMedGoogle Scholar
  63. Kirschenbaum A, Liu XH, Yao S, Leiter A, Levine AC (2011) Prostatic acid phosphatase is expressed in human prostate cancer bone metastases and promotes osteoblast differentiation. Ann N Y Acad Sci 1237:64–70PubMedGoogle Scholar
  64. Kiryushko D, Korshunova I, Berezin V, Bock E (2006) Neural cell adhesion molecule induces intracellular signaling via multiple mechanisms of Ca2+ homeostasis. Mol Biol Cell 17:2278–2286PubMedCentralPubMedGoogle Scholar
  65. Kumar S, Chakraborty S, Barbosa C, Brustovetsky T, Brustovetsky N, Obukhov AG (2012) Mechanisms controlling neurite outgrowth in a pheochromocytoma cell line: the role of TRPC channels. J Cell Physiol 227:1408–1419PubMedCentralPubMedGoogle Scholar
  66. Kushmerick C, Romano-Silva MA, Gomez MV, Prado MA (2001) Changes in Ca(2+) channel expression upon differentiation of SN56 cholinergic cells. Brain Res 916:199–210PubMedGoogle Scholar
  67. Lazarovici P, Jiang H, Fink D Jr (1998) The 38-amino-acid form of pituitary adenylate cyclase-activating polypeptide induces neurite outgrowth in PC12 cells that is dependent on protein kinase C and extracellular signal-regulated kinase but not on protein kinase A, nerve growth factor receptor tyrosine kinase, p21(ras) G protein, and pp60(c-src) cytoplasmic tyrosine kinase. Mol Pharmacol 54:547–558PubMedGoogle Scholar
  68. Le Douarin NM (1988) On the origin of pancreatic endocrine cells. Cell 53:169–171PubMedGoogle Scholar
  69. Lewis DL, Goodman MB, St John PA, Barker JL (1988) Calcium currents and fura-2 signals in fluorescence-activated cell sorted lactotrophs and somatotrophs of rat anterior pituitary. Endocrinology 123:611–621PubMedGoogle Scholar
  70. Lichvarova L, Jaskova K, Lacinova L (2012) NGF-induced neurite outgrowth in PC12 cells is independent of calcium entry through L-type calcium channels. Gen Physiol Biophys 31:473–478PubMedGoogle Scholar
  71. Lory P, Bidaud I, Chemin J (2006) T-type calcium channels in differentiation and proliferation. Cell Calcium 40:135–146PubMedGoogle Scholar
  72. Louhivuori LM, Louhivuori V, Wigren HK, Hakala E, Jansson LC, Nordstrom T, Castren ML, Akerman KE (2013) Role of low voltage activated calcium channels in neuritogenesis and active migration of embryonic neural progenitor cells. Stem Cells Dev 22:1206–1219PubMedGoogle Scholar
  73. Lopez-Dominguez AM, Espinosa JL, Navarrete A, Avila G, Cota G (2006) Nerve growth factor affects Ca2+ currents via the p75 receptor to enhance prolactin mRNA levels in GH3 rat pituitary cells. J Physiol 574:349–365PubMedCentralPubMedGoogle Scholar
  74. Lukyanetz EA (1998) Diversity and properties of calcium channel types in NG108-15 hybrid cells. Neuroscience 87:265–274PubMedGoogle Scholar
  75. Manecka DL, Mahmood SF, Grumolato L, Lihrmann I, Anouar Y (2013) Pituitary adenylate cyclase-activating polypeptide (PACAP) promotes both survival and neuritogenesis in PC12 cells through activation of nuclear factor kappa B (NF-kappaB) pathway: involvement of extracellular signal-regulated kinase (ERK), calcium and c-REL. J Biol Chem 288:14936–14948PubMedCentralPubMedGoogle Scholar
  76. Mansvelder HD, Kits KS (2000) All classes of calcium channel couple with equal efficiency to exocytosis in rat melanotropes, inducing linear stimulus-secretion coupling. J Physiol 526:327–339PubMedCentralPubMedGoogle Scholar
  77. Mariot P, Vanoverberghe K, Lalevee N, Rossier MF, Prevarskaya N (2002) Overexpression of an alpha 1H (Cav3.2) T-type calcium channel during neuroendocrine differentiation of human prostate cancer cells. J Biol Chem 277:10824–10833PubMedGoogle Scholar
  78. Monet M, Lehen’kyi V, Gackiere F, Firlej V, Vandenberghe M, Roudbaraki M, Gkika D, Pourtier A, Bidaux G, Slomianny C, Delcourt P, Rassendren F, Bergerat JP, Ceraline J, Cabon F, Humez S, Prevarskaya N (2010) Role of cationic channel TRPV2 in promoting prostate cancer migration and progression to androgen resistance. Cancer Res 70:1225–1235PubMedGoogle Scholar
  79. Mori S, Murakami-Mori K, Bonavida B (1999) Interleukin-6 induces G1 arrest through induction of p27(Kip1), a cyclin-dependent kinase inhibitor, and neuron-like morphology in LNCaP prostate tumor cells. Biochem Biophys Res Commun 257:609–614PubMedGoogle Scholar
  80. Mudado MA, Rodrigues AL, Prado VF, Beirao PS, Cruz JS (2004) CaV3.1 and CaV3.3 account for T-type Ca2+ current in GH3 cells. Braz J Med Biol Res 37:929–935PubMedGoogle Scholar
  81. Nagasawa K, Tarui T, Yoshida S, Sekiguchi F, Matsunami M, Ohi A, Fukami K, Ichida S, Nishikawa H, Kawabata A (2009) Hydrogen sulfide evokes neurite outgrowth and expression of high-voltage-activated Ca2+ currents in NG108-15 cells: involvement of T-type Ca2+ channels. J Neurochem 108:676–684PubMedGoogle Scholar
  82. Nakashima S, Ikeno Y, Yokoyama T, Kuwana M, Bolchi A, Ottonello S, Kitamoto K, Arioka M (2003) Secretory phospholipases A2 induce neurite outgrowth in PC12 cells. Biochem J 376:655–666PubMedCentralPubMedGoogle Scholar
  83. Novara M, Baldelli P, Cavallari D, Carabelli V, Giancippoli A, Carbone E (2004) Exposure to cAMP and beta-adrenergic stimulation recruits Ca(V)3 T-type channels in rat chromaffin cells through Epac cAMP-receptor proteins. J Physiol 558:433–449PubMedCentralPubMedGoogle Scholar
  84. Oesterling JE, Hauzeur CG, Farrow GM (1992) Small cell anaplastic carcinoma of the prostate: a clinical, pathological and immunohistological study of 27 patients. J Urol 147:804–807PubMedGoogle Scholar
  85. Panner A, Wurster RD (2006) T-type calcium channels and tumor proliferation. Cell Calcium 40:253–259PubMedGoogle Scholar
  86. Pearse AG (1968) Common cytochemical and ultrastructural characteristics of cells producing polypeptide hormones (the APUD series) and their relevance to thyroid and ultimobranchial C cells and calcitonin. Proc R Soc Lond B Biol Sci 170:71–80PubMedGoogle Scholar
  87. Pretl K (1944) Zur Frage der Endokrinie der menschlichen Vorsteherdruse. Virchows Arch 312:392–404Google Scholar
  88. Ravni A, Bourgault S, Lebon A, Chan P, Galas L, Fournier A, Vaudry H, Gonzalez B, Eiden LE, Vaudry D (2006) The neurotrophic effects of PACAP in PC12 cells: control by multiple transduction pathways. J Neurochem 98:321–329PubMedGoogle Scholar
  89. Roussel JP, Mateu G, Astier H (1992) Blockade of potassium or calcium channels provokes modifications in TRH-induced TSH release from rat perifused pituitaries. Endocr Regul 26:163–170PubMedGoogle Scholar
  90. Sagnak L, Topaloglu H, Ozok U, Ersoy H (2011) Prognostic significance of neuroendocrine differentiation in prostate adenocarcinoma. Clin Genitourin Cancer 9:73–80PubMedGoogle Scholar
  91. Sainz RM, Mayo JC, Tan DX, Leon J, Manchester L, Reiter RJ (2005) Melatonin reduces prostate cancer cell growth leading to neuroendocrine differentiation via a receptor and PKA independent mechanism. Prostate 63:29–43PubMedGoogle Scholar
  92. Seidah NG (2011) What lies ahead for the proprotein convertases? Ann N Y Acad Sci 1220:149–161PubMedGoogle Scholar
  93. Shen R, Dorai T, Szaboles M, Katz AE, Olsson CA, Buttyan R (1997) Transdifferentiation of cultured human prostate cancer cells to a neuroendocrine cell phenotype in a hormone-depleted medium. Urol Oncol 3:67–75PubMedGoogle Scholar
  94. Sherwood NT, Lesser SS, Lo DC (1997) Neurotrophin regulation of ionic currents and cell size depends on cell context. Proc Natl Acad Sci USA 94:5917–5922PubMedCentralPubMedGoogle Scholar
  95. Shitaka Y, Matsuki N, Saito H, Katsuki H (1996) Basic fibroblast growth factor increases functional L-type Ca2+ channels in fetal rat hippocampal neurons: implications for neurite morphogenesis in vitro. J Neurosci 16:6476–6489PubMedGoogle Scholar
  96. Silver RA, Bolsover SR (1991) Expression of T-type calcium current precedes neurite extension in neuroblastoma cells. J Physiol Paris 85:79–83PubMedGoogle Scholar
  97. Tarui T, Fukami K, Nagasawa K, Yoshida S, Sekiguchi F, Kawabata A (2010) Involvement of Src kinase in T-type calcium channel-dependent neuronal differentiation of NG108-15 cells by hydrogen sulfide. J Neurochem 114:512–519PubMedGoogle Scholar
  98. Tojima T, Yamane Y, Takahashi M, Ito E (2000) Acquisition of neuronal proteins during differentiation of NG108-15 cells. Neurosci Res 37:153–161PubMedGoogle Scholar
  99. Vanden Abeele F, Shuba Y, Roudbaraki M, Lemonnier L, Vanoverberghe K, Mariot P, Skryma R, Prevarskaya N (2003) Store-operated Ca2+ channels in prostate cancer epithelial cells: function, regulation, and role in carcinogenesis. Cell Calcium 33:357–373PubMedGoogle Scholar
  100. Vanoverberghe K, Lehen’kyi V, Thebault S, Raphael M, Vanden Abeele F, Slomianny C, Mariot P, Prevarskaya N (2012) Cytoskeleton reorganization as an alternative mechanism of store-operated calcium entry control in neuroendocrine-differentiated cells. PLoS One 7:e45615PubMedCentralPubMedGoogle Scholar
  101. Vanoverberghe K, Vanden Abeele F, Mariot P, Lepage G, Roudbaraki M, Bonnal JL, Mauroy B, Shuba Y, Skryma R, Prevarskaya N (2004) Ca2+ homeostasis and apoptotic resistance of neuroendocrine-differentiated prostate cancer cells. Cell Death Differ 11:321–330PubMedGoogle Scholar
  102. Weiss N, Hameed S, Fernandez-Fernandez JM, Fablet K, Karmazinova M, Poillot C, Proft J, Chen L, Bidaud I, Monteil A, Huc-Brandt S, Lacinova L, Lory P, Zamponi GW, De Waard M (2012) A Ca(v)3.2/syntaxin-1A signaling complex controls T-type channel activity and low-threshold exocytosis. J Biol Chem 287:2810–2818PubMedCentralPubMedGoogle Scholar
  103. Weiss N, Zamponi GW (2013) Control of low-threshold exocytosis by T-type calcium channels. Biochim Biophys Acta 1828:1579–1586PubMedGoogle Scholar
  104. Westerink RH, Ewing AG (2008) The PC12 cell as model for neurosecretion. Acta Physiol (Oxf) 192:273–285Google Scholar
  105. Wu C, Huang J (2007) Phosphatidylinositol 3-kinase-AKT-mammalian target of rapamycin pathway is essential for neuroendocrine differentiation of prostate cancer. J Biol Chem 282:3571–3583PubMedGoogle Scholar
  106. Yao JL, Madeb R, Bourne P, Lei J, Yang X, Tickoo S, Liu Z, Tan D, Cheng L, Hatem F, Huang J, Anthony di Sant’Agnese P (2006) Small cell carcinoma of the prostate: an immunohistochemical study. Am J Surg Pathol 30:705–712PubMedGoogle Scholar
  107. Yuan TC, Veeramani S, Lin FF, Kondrikou D, Zelivianski S, Igawa T, Karan D, Batra SK, Lin MF (2006) Androgen deprivation induces human prostate epithelial neuroendocrine differentiation of androgen-sensitive LNCaP cells. Endocr Relat Cancer 13:151–167PubMedGoogle Scholar
  108. Yuan TC, Veeramani S, Lin MF (2007) Neuroendocrine-like prostate cancer cells: neuroendocrine transdifferentiation of prostate adenocarcinoma cells. Endocr Relat Cancer 14:531–547PubMedGoogle Scholar
  109. Zhang XQ, Kondrikov D, Yuan TC, Lin FF, Hansen J, Lin MF (2003) Receptor protein tyrosine phosphatase alpha signaling is involved in androgen depletion-induced neuroendocrine differentiation of androgen-sensitive LNCaP human prostate cancer cells. Oncogene 22:6704–6716PubMedGoogle Scholar

Copyright information

© Springer-Verlag Wien 2015

Authors and Affiliations

  • Marine Warnier
    • 1
    • 2
  • Florian Gackière
    • 1
    • 2
  • Morad Roudbaraki
    • 1
    • 2
  • Pascal Mariot
    • 1
    • 2
  1. 1.Laboratoire de Physiologie Cellulaire, Inserm U1003Université des Sciences et Technologies de Lille 1Villeneuve d’AscqFrance
  2. 2.Laboratory of Excellence, Ion Channels Science and TherapeuticsUniversité des Sciences et Technologies de Lille 1Villeneuve d’AscqFrance

Personalised recommendations