Neuronal differentiation of NG108-15 cells has impact on nitric oxide- and membrane (natriuretic peptide receptor-A) cyclic GMP-generating proteins

Molecular and Cellular Endocrinology

Volumn 320, Issue 1-2, 2010, Pages 118-127

  Müller, Dieter ^a,b   Greenland, Karen J ^b   Speth, Robert C ^c   Middendorff, Ralf ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b UNIVERSITY OF HAMBURG   (Germany)

^c NOVA SOUTHEASTERN UNIVERSITY   (United States)

Author keywords

ANP; Desensitization; Neuron; NNOS; PP2A; SGC

Indexed keywords

ATRIAL NATRIURETIC FACTOR; BRAIN NATRIURETIC PEPTIDE; CYCLIC GMP; GUANYLATE CYCLASE; INSULIN RECEPTOR; NATRIURETIC PEPTIDE RECEPTOR A; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE; PHOSPHOPROTEIN PHOSPHATASE 2A;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; BRAIN TISSUE; CELL LINE; CONTROLLED STUDY; IMMUNOBLOTTING; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINE; CELL MEMBRANE; CYCLIC GMP; GUANYLATE CYCLASE; NEURONS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; PROTEIN PHOSPHATASE 2; PROTEIN SUBUNITS; RATS; RECEPTORS, ATRIAL NATRIURETIC FACTOR; RECEPTORS, CYTOPLASMIC AND NUCLEAR; SIGNAL TRANSDUCTION; UP-REGULATION;

EID: 77949566943     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2010.01.022     Document Type: Article

References (57)

1. Abbey S.E., Potter L.R. Lysophosphatidic acid inhibits C-type natriuretic peptide activation of guanylyl cyclase-B. Endocrinology 2003, 144:240-246.
2. Agulló L., Garcia-Dorado D., Escalona N., Ruiz-Meana M., Mirabet M., Inserte J., Soler-Soler J. Membrane association of nitric oxide-sensitive guanylyl cyclase in cardiomyocytes. Cardiovasc. Res. 2005, 68:65-74.
3. Ahern G.P., Klyachko V.A., Jackson M.B. cGMP and S-nitrosylation: two routes for modulation of neuronal excitability by NO. Trends Neurosci. 2002, 25:510-517.
4. Akama K.T., McEwen B.S. Estrogen stimulates postsynaptic density-95 rapid protein synthesis via the Akt/protein kinase B pathway. J. Neurosci. 2003, 23:2333-2339.
5. Alderton W.K., Cooper C.E., Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 2001, 357:593-615.
6. Authier F., Cameron P.H., Merlen C., Kouach M., Briand G. Endosomal proteolysis of glucagon at neutral pH generates the bioactive degradation product miniglucagon-(19-29). Endocrinology 2003, 144:5353-5364.
7. Bromberg K.D., Ma'ayan A., Neves S.R., Iyengar R. Design logic of a cannabinoid receptor signaling network that triggers neurite outgrowth. Science 2008, 320:903-909.
8. Bryan P.M., Potter L.R. The atrial natriuretic peptide receptor (NPR-A/GC-A) is dephosphorylated by distinct microcystin-sensitive and magnesium-dependent protein phosphatases. J. Biol. Chem. 2002, 277:16041-16047.
9. Burette A., Zabel U., Weinberg R.J., Schmidt H.H., Valtschanoff J.G. Synaptic localization of nitric oxide synthase and soluble guanylyl cyclase in the hippocampus. J. Neurosci. 2002, 22:8961-8970.
10. Cao L.-H., Yang X.-L. Natriuretic peptides and their receptors in the central nervous system. Prog. Neurobiol. 2008, 84:234-248.
11. Chen J.J., Barber L.A., Dymshitz J., Vasko M.R. Peptidase inhibitors improve recovery of substance P and calcitonin gene-related peptide release from rat spinal cord slices. Peptides 1996, 17:31-37.
12. Cheng Chew S.B., Leung P.Y., Fiscus R.R. Preincubation with atrial natriuretic peptide protects NG108-15 cells against the toxic/proapoptotic effects of the nitric oxide donor S-nitroso-N-acetylpenicillamine. Histochem. Cell. Biol. 2003, 120:163-171.
13. Dinerman J.L., Dawson T.M., Schell M.J., Snowman A., Snyder S.H. Endothelial nitric oxide synthase localized to hippocampal pyramidal cells: implications for synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A. 1994, 91:4214-4218.
14. Fortin Y., De Lean A. Role of cyclic GMP and calcineurin in homologous and heterologous desensitization of natriuretic peptide receptor-A. Can. J. Physiol. Pharmacol. 2006, 84:539-546.
15. Fukami S., Watanabe K., Iwata N., Haraoka J., Lu B., Gerard N.P., Gerard C., Fraser P., Westaway D., George-Hyslop P.St., Saido T.C. Abeta-degrading endopeptidase, neprilysin, in mouse brain: synaptic and axonal localization inversely correlating with Abeta pathology. Neurosci. Res. 2002, 43:39-56.
16. Garthwaite J. Dynamics of cellular NO-cGMP signaling. Front Biosci. 2005, 10:1868-1880.
17. Garthwaite J. Concepts of neural nitric oxide-mediated transmission. Eur. J. Neurosci. 2008, 27:2783-2802.
18. Guidone D., Müller D., Vogt K., Mukhopadhyay A.K. Characterization of VIP and PACAP receptors in cultured rat penis corpus cavernosum smooth muscle cells and their interaction with guanylate cyclase-B receptors. Regul. Pept. 2002, 108:63-72.
19. Gutkowska J., Antunes-Rodrigues J., McCann S.M. Atrial natriuretic peptide in brain and pituitary gland. Physiol. Rev. 1997, 77:465-515.
20. Hardman J.G., Beavo J.A., Gray J.P., Chrisman T.D., Patterson W.D., Sutherland E.W. The formation and metabolism of cyclic GMP. Ann. N. Y. Acad. Sci. 1971, 185:27-35.
21. Iijima-Ando K., Hearn S.A., Granger L., Shenton C., Gatt A., Chiang H.C., Hakker I., Zhong Y., Iijima K. Overexpression of neprilysin reduces alzheimer amyloid-beta42 (Abeta42)-induced neuron loss and intraneuronal Abeta42 deposits but causes a reduction in cAMP-responsive element-binding protein-mediated transcription, age-dependent axon pathology, and premature death in Drosophila. J. Biol. Chem. 2008, 283:19066-19076.
22. Janssens V., Goris J. Protein phosphatase 2A: a highly regulated family of serine/threonine phosphatases implicated in cell growth and signalling. Biochem. J. 2001, 353:417-439.
23. Komeima K., Hayashi Y., Naito Y., Watanabe Y. Inhibition of neuronal nitric-oxide synthase by calcium/calmodulin-dependent protein kinase IIalpha through Ser847 phosphorylation in NG108-15 neuronal cells. J. Biol. Chem. 2000, 275:28139-28143.
24. Kranenburg O., Scharnhorst V., Van der Eb A.J., Zantema A. Inhibition of cyclin-dependent kinase activity triggers neuronal differentiation of mouse neuroblastoma cells. J. Cell Biol. 1995, 131:227-234.
25. Kuhn M. Structure, regulation, and function of mammalian membrane guanylyl cyclase receptors, with a focus on guanylyl cyclase-A. Circ. Res. 2003, 93:700-709.
26. Kuhn M. Function and dysfunction of mammalian membrane guanylyl cyclase receptors: lessons from genetic mouse models and implications for human diseases. Handb. Exp. Pharmacol. 2009, 191:47-69.
27. Lelièvre V., Pineau N., Hu Z., Ioffe Y., Byun J.Y., Muller J.M., Waschek J.A. Proliferative actions of natriuretic peptides on neuroblastoma cells Involvement of guanylyl cyclase and non-guanylyl cyclase pathways. J. Biol. Chem. 2001, 276:43668-43676.
28. Lelièvre V., Hu Z., Ioffe Y., Byun J.Y., Flores A., Seksenyan A., Waschek J.A. Paradoxical antagonism of PACAP receptor signaling by VIP in Xenopus oocytes via the type-C natriuretic peptide receptor. Cell Signal. 2006, 18:2013-2021.
29. Lin L.H., Taktakishvili O., Talman W.T. Identification and localization of cell types that express endothelial and neuronal nitric oxide synthase in the rat nucleus tractus solitarii. Brain Res. 2007, 1171:42-51.
30. Madhusoodanan K.S., Guo D., McGarrigle D.K., Maack T., Huang X.Y. Csk mediates G-protein-coupled lysophosphatidic acid receptor-induced inhibition of membrane-bound guanylyl cyclase activity. Biochemistry 2006, 45:3396-3403.
31. Matsukawa N., Grzesik W.J., Takahashi N., Pandey K.N., Pang S., Yamauchi M., Smithies O. The natriuretic peptide clearance receptor locally modulates the physiological effects of the natriuretic peptide system. Proc. Natl. Acad. Sci. U.S.A. 1999, 96:7403-7408.
32. Müller D., Baumeister H., Buck F., Richter D. Atrial natriuretic peptide (ANP) is a high-affinity substrate for rat insulin-degrading enzyme. Eur. J. Biochem. 1991, 202:285-292.
33. Müller D., Schulze C., Baumeister H., Buck F., Richter D. The rat insulin-degrading enzyme: cleavage pattern of the natriuretic peptide hormones ANP, BNP and CNP revealed by HPLC and mass spectrometry. Biochemistry 1992, 31:11138-11143.
34. Müller D., Middendorff R., Olcese J., Mukhopadhyay A.K. Central nervous system-specific glycosylation of the type A natriuretic peptide receptor. Endocrinology 2002, 143:23-29.
35. Müller D., Mukhopadhyay A.K., Speth R.C., Guidone G., Potthast R., Potter L.R., Middendorff R. Spatiotemporal regulation of the two atrial natriuretic peptide receptors in testis. Endocrinology 2004, 145:1392-1401.
36. Müller D., Cortes-Dericks L., Budnik L.T., Brunswig-Spickenheier B., Pancratius M., Speth R.C., Mukhopadhyay A.K., Middendorff R. Homologous and lysophosphatidic acid (LPA)-induced desensitization of the atrial natriuretic peptide receptor, guanylyl cyclase-A, in MA-10 Leydig cells. Endocrinology 2006, 147:2974-2985.
37. Müller D., Hida B., Guidone G., Speth R.C., Michurina T.V., Enikolopov G., Middendorff R. Expression of guanylyl cyclase (GC)-A and GC-B during brain development: evidence for a role of GC-B in perinatal neurogenesis. Endocrinology 2009, 150:5520-5529.
38. Nausch L.W., Ledoux J., Bonev A.D., Nelson M.T., Dostmann W.R. Differential patterning of cGMP in vascular smooth muscle cells revealed by single GFP-linked biosensors. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:365-370.
39. Nelson P., Christian C., Nirenberg M. Synapse formation between clonal neuroblastoma X glioma hybrid cells and striated muscle cells. Proc. Natl. Acad. Sci. U.S.A. 1976, 73:123-127.
40. Neves S.R., Tsokas P., Sarkar A., Grace E.A., Rangamani P., Taubenfeld S.M., Alberini C.A., Schaff J.C., Blitzer R.D., Moraru I.I., Iyengar R. Cell shape and negative links in regulatory motifs together control spatial information flow in signaling networks. Cell 2008, 133:666-680.
41. Nishiyama M., von Schimmelmann M.J., Togashi K., Findley W.M., Hong K. Membrane potential shifts caused by diffusible guidance signals direct growth-cone turning. Nat. Neurosci. 2008, 11:762-771.
42. Oh J.E., Karlmark Raja K., Shin J.H., Pollak A., Hengstschläger M., Lubec G. Cytoskeleton changes following differentiation of N1E-115 neuroblastoma cell line. Amino Acids 2006, 31:289-298.
43. Pattanaik P., Fromondi L., Ng K.P., He J., van den Akker F. Expression, purification, and characterization of the intra-cellular domain of the ANP receptor. Biochimie 2009, 91:888-893.
44. Plouffe B., Guimond M.O., Beaudry H., Gallo-Payet N. Role of tyrosine kinase receptors in angiotensin II AT2 receptor signaling: involvement in neurite outgrowth and in p42/p44mapk activation in NG108-15 cells. Endocrinology 2006, 147:4646-4654.
45. Potter L.R., Garbers D.L. Dephosphorylation of the guanylyl cyclase-A receptor causes desensitization. J. Biol. Chem. 1992, 267:14531-14534.
46. Potter L.R. Phosphorylation-dependent regulation of the guanylyl cyclase-linked natriuretic peptide receptor B: dephosphorylation is a mechanism of desensitization. Biochemistry 1998, 37:2422-2429.
47. Potter L.R., Abbey-Hosch S., Dickey D.M. Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocrine Rev. 2006, 27:47-72.
48. Rose R.A., Giles W.R. Natriuretic peptide C receptor signalling in the heart and vasculature. J. Physiol. 2008, 586:353-366.
49. Russwurm M., Wittau N., Koesling D. Guanylyl cyclase/PSD-95 interaction: targeting of the nitric oxide-sensitive alpha2beta1 guanylyl cyclase to synaptic membranes. J. Biol. Chem. 2001, 276:44647-44652.
50. Seidman K.J., Barsuk J.H., Johnson R.F., Weyhenmeyer J.A. Differentiation of NG108-15 neuroblastoma cells by serum starvation or dimethyl sulfoxide results in marked differences in angiotensin II receptor subtype expression. J. Neurochem. 1996, 66:1011-1018.
51. Song T., Hatano N., Kume K., Sugimoto K., Yamaguchi F., Tokuda M., Watanabe Y. Inhibition of neuronal nitric-oxide synthase by phosphorylation at Threonine1296 in NG108-15 neuronal cells. FEBS Lett. 2005, 579:5658-5662.
52. Tohda M., Nomura Y. Serotonin stimulates both cytosolic and membrane-bound guanylate cyclase in NG108-15 cells. J. Neurochem. 1990, 55:1800-1805.
53. Tojima T., Yamane Y., Takahashi M., Ito E. Acquisition of neuronal proteins during differentiation of NG108-15 cells. Neurosci. Res. 2000, 37:153-161.
54. Tojima T., Ito E. Signal transduction cascades underlying de novo protein synthesis required for neuronal morphogenesis in differentiating neurons. Prog. Neurobiol. 2004, 72:183-193.
55. Toki S., Morishita Y., Sano T., Matsuda Y. HS-142-1, a novel non-peptide ANP antagonist, blocks the cyclic GMP production elicited by natriuretic peptides in PC12 and NG108-15 cells. Neurosci. Lett. 1992, 135:117-120.
56. Wang X., Robinson P.J. Cyclic GMP-dependent protein kinase and cellular signaling in the nervous system. J. Neurochem. 1997, 68:443-456.
57. Wykes V., Bellamy T.C., Garthwaite J. Kinetics of nitric oxide-cyclic GMP signalling in CNS cells and its possible regulation by cyclic GMP. J. Neurochem. 2002, 83:37-47.