Antiproliferative effect of nitric oxide on epidermal growth factor-responsive human neuroblastoma cells

Journal of Neurochemistry

Volumn 83, Issue 1, 2002, Pages 119-131

  Murillo Carretero, Maribel ^a   Ruano, María José ^b   Matarredona, Esperanza R ^a   Villalobo, Antonio ^b   Estrada, Carmen ^a  

^a UNIVERSITY OF CÁDIZ   (Spain)

^b CSIC   (Spain)

Author keywords

Cell proliferation; DNA synthesis; NB69 cell line; Neuroblasts; Nitric oxide donors; Nitric oxide synthase

Indexed keywords

2 (N,N DIETHYLAMINO)DIAZENOLATE 2 OXIDE; ANTIMITOTIC AGENT; CYCLIC GMP; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE DONOR; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL LYSATE; CELL PROLIFERATION; CELL VIABILITY; CONTROLLED STUDY; CYTOSTASIS; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; NEUROBLASTOMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SERUM; WESTERN BLOTTING;

APOPTOSIS; BLOTTING, WESTERN; CELL DIVISION; CELL SURVIVAL; CULTURE MEDIA; CYCLIC GMP; ENZYME ACTIVATION; EPIDERMAL GROWTH FACTOR; HUMANS; HYDRAZINES; IMMUNOHISTOCHEMISTRY; ISOENZYMES; NEUROBLASTOMA; NITRIC OXIDE; NITRIC OXIDE DONORS; NITRIC OXIDE SYNTHASE; NITROGEN OXIDES; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 0036787295     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2002.01116.x     Document Type: Article

References (47)

1. Basu M., Biswas R. and Das M. (1984) 42,000-Molecular weight EGF receptor has protein kinase activity. Nature 311, 477-480.
2. Bauer P. M., Buga G. M., Fukuto J. M., Pegg A. E. and Ignarro L. J. (2001) Nitric oxide inhibits omithine decarboxylase via S-nitrosylation of cysteine 360 in the active site of the enzyme. J. Biol. Chem. 276, 34458-34464.
3. Bredt D. S. and Snyder S. H. (1994) Transient nitric oxide synthase neurons in embryonic cerebral cortical plate, sensory ganglia and olfactory epithelium. Neuron 13, 301-313.
4. Browning D. D., Windes N. D. and Ye R. D. (1999) Activation of p38 mitogen-activated protein kinase by lipopolysaccharide in human neutrophils requires nitric oxide-dependent cGMP accumulation. J. Biol. Chem. 274, 537-542.
5. Buga G. M., Wei L. H., Bauer P. M., Fukuto J. M. and Ignarro L. J. (1998) NG-hydroxy-L-arginine and nitric oxide inhibit Caco-2 tumor cell proliferation by distinct mechanisms. Am. J. Physiol. 275, 1256-1264.
6. Craig C. G., Tropepe V., Morshead C. M., Reynolds B. A., Weiss S. and Van der Kooy D. (1996) In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J. Neurosci. 16, 2649-2658.
7. Doetsch F., Garcia-Verdugo J. M. and Alvarez-Buylla A. (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J. Neurosc. 17, 5046-5061.
8. Dotsch J., Harmjanz A., Christiansen H., Hanze J., Lampert F. and Rascher W. (2000) Gene expression of neuronal nitric oxide synthase and adrenomedullin in human neuroblastoma using real-time PCR. Int. J. Cancer 88, 172-175.
9. Estrada C., Gomez C., Martin-Nieto J., De Frutos T, Jimenez A. and Villalobo A. (1997) Nitric oxide reversibly inhibits the epidermal growth factor receptor tyrosine kinase. Biochem. J. 326, 369-376.
10. Feelisch M. and Stamler J. S. (1996) Methods in Nitric Oxide Research, pp. 71-115. John Wiley & Sons, UK.
11. Fujisawa H., Ogura T., Kurashima Y., Yokoyama T, Yamashita J. and Esumi H. (1994) Expression of two types of nitric oxide synthase mRNA in human neuroblastoma cell lines. J. Neurochem. 63, 140-145.
12. Garg U. C. and Hassid A. (1989) Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J. Clin. Invest. 83, 1774-1777.
13. Garg U. C. and Hassid A. (1990) Nitric oxide-generating vasodilators inhibit mitogenesis and proliferation of BALB/c 3T3 fibroblasts by a cyclic GMP-independent mechanism. Biochem. Biophys. Res. Commun. 171, 474-479.
14. Ghigo D., Priotto C., Migliorino D., Geromin D., Franchino C., Todde R., Costamagna C., Pescarmona G. and Bosia A. (1998) Retinoic acid-induced differentiation in a human neuroblastoma cell line is associated with an increase in nitric oxide synthesis. J. Cell. Physiol. 174, 99-106.
15. Giuili G., Luzi A., Poyard M. and Guellaën G. (1994) Expression of mouse brain soluble guanylyl cyclase and NO synthase during ontogeny. Dev. Brain Res. 81, 269-283.
16. Gonzalez C., Barroso C., Martin C., Gulbenkian S. and Estrada C. (1997) Neuronal nitric oxide synthase activation by vasoactive intestinal peptide in bovine cerebral arteries. J. Cereb. Blood Flow Metab. 17, 977-984.
17. Gritti A., Frölichstal-Schoeller P., Galli R., Parati E. A., Cova L., Pagano S. E., Bjorson C. R. and Vescovi A.L. (1999) Epidermal and fibroblast growth factors behave as mitogenic regulators for a single multipotent stem cell-like population from the subventricular region of the adult mouse forebrain. J. Neurosci. 19, 3287-3297.
18. Gu M., Lynch J. and Brecher P. (2000) Nitric oxide increases p21 (Waf1/Cip1) expression by a cGMP-dependent pathway that includes activation of extracellular signal-regulated kinase and p70 (S6k). J. Biol. Chem. 275, 11389-11396.
19. Ho Y. S., Wang Y. J. and Lin J. K. (1996) Induction of p53 and p21/WAF1/CIP1 expression by nitric oxide and their association with apoptosis in human cancer cells. Mol. Carcinog. 16, 20-31.
20. Jaffrey S. R., Erdjument-Bromage H., Ferris C. D., Tempst P. and Snyder S. H. (2001) Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat. Cell Biol. 3, 193-197.
21. Janssens M. Y., Verovski V. N., Van den Berge D. L., Monsaert C. and Storme G. A. (1999) Radiosensitization of hypoxic tumour cells by S-nitroso-N-acetylpenicillamine implicates a bioreductive mechanism of nitric oxide generation. Br. J. Cancer 79, 1085-1089.
22. Kashiba-Iwatsuki M., Kitoh K., Kasahara E. Yu H., Nisikawa M., Matsuo M. and Inoue M. (1997) Ascorbic acid and reducing agents regulate the fates and functions of S-nitrosothiols. J. Biochem. (Tokyo) 122, 1208-1214.
23. Kashima T., Vinters H. V. and Campagnoni A. T. (1995) Unexpected expression of intermediate filament protein genes in human oligodendroglioma cell lines. J. Neuropathol. Exp. Neurol. 54, 23-31.
24. Keilhoff G., Seidel B., Noack H., Tischmeyer W., Stanek D. and Wolf G. (1996) Patterns of nitric oxide synthase at the messenger RNA and protein levels during early rat brain development. Neuroscience 75, 41193-41201.
25. Kuhn H. G., Winkler J., Kempermann, G., Thal L. J. and Gage F. H. (1997) Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J. Neurosci. 17, 5820-5829.
26. Kurien B. T., Jackson K. and Scofield R. H. (1998) Immunoblotting of multiple antigenic peptides. Electrophoresis 19, 1659-1661.
27. Kuzin B., Regulski M., Stasiv Y., Scheinker V., Tully T. and Enikolopov G. (2000) Nitric oxide interacts with the retinoblastoma pathway to control eye development in Drosophila. Curr. Biol. 10, 459-462.
28. Kuzin B., Roberts I., Peunova N. and Enikolopov G. (1996) Nitric oxide regulates cell proliferation during Drosophila development. Cell 87, 639-649.
29. Laemmli U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
30. Lepoivre M., Flaman J. M., Bobe P., Lemaire G. and Henry Y. (1994) Quenching of the tyrosyl free radical of ribonucleotide reductase by nitric oxide. Relationship to cytostasis induced in tumor cells by cytotoxic macrophages. J. Biol. Chem. 269, 21891-21897.
31. Lois C. and Alvarez-Buylla A. (1993) Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA 90, 2074-2077.
32. McManus M. F., Chen L. C., Vallejo I. and Vallejo M. (1999) Astroglial differentiation of cortical precursor cells triggered by activation of the cAMP-dependent signaling pathway. J. Neurosci. 19, 9004-9015.
33. Moncada S., Palmer R. M. and Higgs E. A. (1991) Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43, 109-142.
34. Moreno-López B., Noval J. A., Gonzalez-Bonet L. G. and Estrada C. (2000) Morphological bases for a role of nitric oxide in adult neurogenesis. Brain Res. 869, 244-250.
35. Muñoz-Fernandez M. A., Cano E., O'Donnell C. A., Doyle J., Liew F. Y. and Fresno M. (1994) Tumor necrosis factor-alpha (TNF-alpha), interferon-gamma, and interleukin-6 but not TNF-beta induce differentiation of neuroblastoma cells: the role of nitric oxide. J. Neurochem. 62, 1330-1336.
36. Nakaya N., Lowe S. W., Taya Y., Chenchik A. and Enikolopov G. (2000) Specific pattern of p53 phosphorylation during nitric oxide-induced cell cycle arrest. Oncogene 19, 6369-6375.
37. Obregon E., Punzon M. C., Gonzalez-Nicolas J., Fernandez-Cruz E., Fresno M. and Munoz-Fernandez M. A. (1997) Induction of adhesion/differentiation of human neuroblastoma cells by tumour necrosis factor-alpha requires the expression of an inducible nitric oxide synthase. Eur. J. Neurosci. 9, 1184-1193.
38. Ogura T. and Esumi H. (1996) Nitric oxide synthase expression in human neuroblastoma cell line induced by cytokines. Neuroreport 7, 853-856.
39. Peunova N. and Enikolopov G. (1995) Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 375, 68-73.
40. Peunova N., Scheinker V., Cline H. and Enikolopov G. (2001) Nitric oxide is an essential negative regulator of cell proliferation in Xenopus brain. J. Neurosci. 21, 8809-8818.
41. Phung Y. T., Bekker J. M., Hallmark O. G. and Black S. M. (1999) Both neuronal NO synthase and nitric oxide are required for PC12 cell differentiation: a cGMP independent pathway. Brain Res. Mol. Brain Res. 64, 165-178.
42. Reynolds B. A. and Weiss S. (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710.
43. Rodriguez-Martin E., Casarejos M. J., Bazan E., Canals S., Herranz A. S. and Mena M. A. (2000) Nitric oxide induces differentiation in the NB69 human catecholamine-rich cell line. Neuropharmacology 39, 2090-2100.
44. Stamler J. S. (1995) S-nitrosothiols and the bioregulatory actions of nitrogen oxides through reactions with thiol groups. Curr. Top. Microbiol. Immunol. 196, 19-36.
45. Telford W. G., King L. E. and Fraker P. J. (1994) Rapid quantitation of apoptosis in pure and heterogeneous cell populations using flow cytometry. J. Immunol. Methods 172, 1-16.
46. Uttenthal L. O., Alonso D., Fernandez A. P., Campbell R. O., Moro M. A., Leza J. C., Lizasoain I., Esteban F. J., Barroso J. B., Valderrama R., Pedrosa J. A., Peinado M. A., Serrano J., Richart A., Bentura M. L., Santacana M., Martinez-Murillo R. and Rodrigo J. (1998) Neuronal and inducible nitric oxide synthase and nitrotyrosine immunoreactivities in the cerebral cortex of the aging rat. Microsc. Res. Techn. 43, 75-88.
47. Weiss A. and Schlessinger J. (1998) Switching signals on or off by receptor dimerization. Cell 94, 277-280.