Neuropeptide Y stimulates retinal neural cell proliferation - Involvement of nitric oxide

Journal of Neurochemistry

Volumn 105, Issue 6, 2008, Pages 2501-2510

  Álvaro, Ana Rita ^a   Martins, João ^a,b   Araújo, Inês M ^a   Rosmaninho Salgado, Joana ^a   Ambrósio, António F ^a,b   Cavadas, Cláudia ^a,c  

^a UNIVERSITY OF COIMBRA   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF COIMBRA   (Portugal)

Author keywords

Cell proliferation; Neuropeptide Y; Neuropeptide Y receptors; Nitric oxide; Retina

Indexed keywords

CYCLIC GMP; GUANYLATE CYCLASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; N(G) NITROARGININE METHYL ESTER; NEUROPEPTIDE Y; NEUROPEPTIDE Y RECEPTOR; OXIDE; UO 126;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RETINA CELL;

ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CYCLIC GMP; MAP KINASE KINASE 2; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE 3; NEURONS; NEUROPEPTIDE Y; NITRIC OXIDE; RATS; RATS, WISTAR; RETINA; SIGNAL TRANSDUCTION;

RATTUS;

EID: 44649189136     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2008.05334.x     Document Type: Article

References (83)

1. Álvaro A. R., Rosmaninho-Salgado J., Santiago A. R. et al. (2007) NPY in rat retina is present in neurons, in endothelial cells and also in microglial and Müller cells. Neurochem. Int. 50, 757 763.
2. Ammar D. A., Hughes B. A. Thompson D. A. (1998) Neuropeptide Y and the retinal pigment epithelium: receptor subtypes, signaling, and bioelectrical responses. Invest. Ophthalmol. Vis. Sci. 39, 1870 1878.
3. Angers S., Salahpour A. Bouvier M. (2002) Dimerization: an emerging concept for G protein-coupled receptor ontogeny and function. Annu. Rev. Pharmacol. Toxicol. 42, 409 435.
4. Anitha M., Chandrasekharan B., Salgado J. R., Grouzmann E., Mwangi S., Sitaraman S. V. Srinivasan S. (2006) Glial-derived neurotrophic factor modulates enteric neuronal survival and proliferation through neuropeptide Y. Gastroenterology 131, 1164 1178.
5. Bagnoli P., Dal Monte M. Casini G. (2003) Expression of neuropeptides and their receptors in the developing retina of mammals. Histol. Histopathol. 18, 1219 1242.
6. Bal-Price A., Gartlon J. Brown G. C. (2006) Nitric oxide stimulates PC12 cell proliferation via cGMP and inhibits at higher concentrations mainly via energy depletion. Nitric Oxide 14, 238 246.
7. Berglund M. M., Schober D. A., Esterman M. A. Gehlert D. R. (2003) Neuropeptide Y Y4 receptor homodimers dissociate upon agonist stimulation. J. Pharmacol. Exp. Ther. 307, 1120 1126.
8. Bruun A., Tornqvist K. Ehinger B. (1986) Neuropeptide Y (NPY) immunoreactive neurons in the retina of different species. Histochemistry 86, 135 140.
9. Cai J., Jiang W. G., Ahmed A. Boulton M. (2006) Vascular endothelial growth factor-induced endothelial cell proliferation is regulated by interaction between VEGFR-2, SH-PTP1 and eNOS. Microvasc. Res. 71, 20 31.
10. Cano E. Mahadevan L. C. (1995) Parallel signal processing among mammalian MAPKs. Trends Biochem. Sci. 20, 117 122.
11. Cayre M., Malaterre J., Scotto-Lomassese S., Holstein G. R., Martinelli G. P., Forni C., Nicolas S., Aouane A., Strambi C. Strambi A. (2005) A role for nitric oxide in sensory-induced neurogenesis in an adult insect brain. Eur. J. Neurosci. 21, 2893 2902.
12. Cho Y. R. Kim C. W. (2004) Neuropeptide Y promotes beta-cell replication via extracellular signal-regulated kinase activation. Biochem. Biophys. Res. Commun. 314, 773 780.
13. Cobb M. H. (1999) MAP kinase pathways. Prog. Biophys. Mol. Biol. 71, 479 500.
14. D'Angelo I. Brecha N. C. (2004) Y2 receptor expression and inhibition of voltage-dependent Ca(2+) influx into rod bipolar cell terminals. Neuroscience 125, 1039 1049.
15. Dean M. K., Higgs C., Smith R. E., Bywater R. P., Snell C. R., Scott P. D., Upton G. J., Howe T. J. Reynolds C. A. (2001) Dimerization of G-protein-coupled receptors. J. Med. Chem. 44, 4595 4614.
16. Devi L. A. (2001) Heterodimerization of G-protein-coupled receptors: pharmacology, signaling and trafficking. Trends Pharmacol. Sci. 22, 532 537.
17. Dimitrijevic M., Stanojevic S., Micic S., Vujic V., Kovacevic-Jovanovic V., Mitic K., von Horsten S. Kosec D. (2006) Neuropeptide Y (NPY) modulates oxidative burst and nitric oxide production in carrageenan-elicited granulocytes from rat air pouch. Peptides 27, 3208 3215.
18. Ding J. D. Weinberg R. J. (2007) Distribution of soluble guanylyl cyclase in rat retina. J. Comp. Neurol. 502, 734 745.
19. Dinger M. C., Bader J. E., Kobor A. D., Kretzschmar A. K. Beck-Sickinger A. G. (2003) Homodimerization of neuropeptide y receptors investigated by fluorescence resonance energy transfer in living cells. J. Biol. Chem. 278, 10562 10571.
20. Du M., Islam M. M., Lin L., Ohmura Y., Moriyama Y. Fujimura S. (1997) Promotion of proliferation of murine BALB/C3T3 fibroblasts mediated by nitric oxide at lower concentrations. Biochem. Mol. Biol. Int. 41, 625 631.
21. Dumont Y., Martel J. C., Fournier A., St-Pierre S. Quirion R. (1992) Neuropeptide Y and neuropeptide Y receptor subtypes in brain and peripheral tissues. Prog. Neurobiol. 38, 125 167.
22. English J., Pearson G., Wilsbacher J., Swantek J., Karandikar M., Xu S. Cobb M. H. (1999) New insights into the control of MAP kinase pathways. Exp. Cell Res. 253, 255 270.
23. Ferriero D. M. Sagar S. M. (1989) Development of neuropeptide Y-immunoreactive neurons in the rat retina. Brain Res. Dev. Brain Res. 48, 19 26.
24. Frank S., Kampfer H., Podda M., Kaufmann R. Pfeilschifter J. (2000) Identification of copper/zinc superoxide dismutase as a nitric oxide-regulated gene in human (HaCaT) keratinocytes: implications for keratinocyte proliferation. Biochem. J. 346, 719 728.
25. Gomes I., Jordan B. A., Gupta A., Trapaidze N., Nagy V. Devi L. A. (2000) Heterodimerization of mu and delta opioid receptors: a role in opiate synergy. J. Neurosci. 20, RC110.
26. Gomes I., Jordan B. A., Gupta A., Rios C., Trapaidze N. Devi L. A. (2001) G protein coupled receptor dimerization: implications in modulating receptor function. J. Mol. Med. 79, 226 242.
27. Gotzes S., de Vente J. Muller F. (1998) Nitric oxide modulates cGMP levels in neurons of the inner and outer retina in opposite ways. Vis. Neurosci. 15, 945 955.
28. Grant M. B., Davis M. I., Caballero S., Feoktistov I., Biaggioni I. Belardinelli L. (2001) Proliferation, migration, and ERK activation in human retinal endothelial cells through A(2B) adenosine receptor stimulation. Invest. Ophthalmol. Vis. Sci. 42, 2068 2073.
29. Hajri A., Metzger E., Vallat F., Coffy S., Flatter E., Evrard S., Marescaux J. Aprahamian M. (1998) Role of nitric oxide in pancreatic tumour growth: in vivo and in vitro studies. Br. J. Cancer 78, 841 849.
30. Hansel D., Eipper BA Ronnet GV (2001) Neuropeptide Y functions as a neuroproliferative factor. Nature 410, 940 944.
31. Hashimoto T., Zhang X. M., Chen B. Y. Yang X. J. (2006) VEGF activates divergent intracellular signaling components to regulate retinal progenitor cell proliferation and neuronal differentiation. Development 133, 2201 2210.
32. Hecquet C., Lefevre G., Valtink M., Engelmann K. Mascarelli F. (2002) cAMP inhibits the proliferation of retinal pigmented epithelial cells through the inhibition of ERK1/2 in a PKA-independent manner. Oncogene 21, 6101 6112.
33. Hood J. Granger H. J. (1998) Protein kinase G mediates vascular endothelial growth factor-induced Raf-1 activation and proliferation in human endothelial cells. J. Biol. Chem. 273, 23504 23508.
34. Howell O. W., Scharfman H. E., Herzog H., Sundstrom L. E., Beck-Sickinger A. Gray W. P. (2003) Neuropeptide Y is neuroproliferative for post-natal hippocampal precursor cells. J. Neurochem. 86, 646 659.
35. Howell O. W., Doyle K., Goodman J. H., Scharfman H. E., Herzog H., Pringle A., Beck-Sickinger A. G. Gray W. P. (2005) Neuropeptide Y stimulates neuronal precursor proliferation in the post-natal and adult dentate gyrus. J. Neurochem. 93, 560 570.
36. Howell O. W., Silva S., Scharfman H. E., Sosunov A. A., Zaben M., Shatya A., McKhann G. 2nd., Herzog H., Laskowski A. Gray W. P. (2007) Neuropeptide Y is important for basal and seizure-induced precursor cell proliferation in the hippocampus. Neurobiol. Dis. 26, 174 188.
37. Hutsler J. J. Chalupa L. M. (1994) Neuropeptide Y immunoreactivity identifies a regularly arrayed group of amacrine cells within the cat retina. J. Comp. Neurol. 346, 481 489.
38. Hutsler J. J. Chalupa L. M. (1995) Development of neuropeptide Y immunoreactive amacrine and ganglion cells in the pre- and postnatal cat retina. J. Comp. Neurol. 361, 152 164.
39. Jen P. Y., Li W. W. Yew D. T. (1994) Immunohistochemical localization of neuropeptide Y and somatostatin in human fetal retina. Neuroscience 60, 727 735.
40. Johns P. R. (1977) Growth of the adult goldfish eye. III. Source of the new retinal cells. J. Comp. Neurol. 176, 343 357.
41. Jotwani G., Itoh K. Wadhwa S. (1994) Immunohistochemical localization of tyrosine hydroxylase, substance P, neuropeptide-Y and leucine-enkephalin in developing human retinal amacrine cells. Brain Res. Dev. Brain Res. 77, 285 289.
42. Kim K. Y., Moon J. I., Lee E. J., Lee Y. J., Kim I. B., Park C. K., Oh S. J. Chun M. H. (2002) The effect of L-arginine, a nitric oxide synthase substrate, on retinal cell proliferation in the postnatal rat. Dev. Neurosci. 24, 313 321.
43. Kitlinska J., Abe K., Kuo L. et al. (2005) Differential effects of neuropeptide Y on the growth and vascularization of neural crest-derived tumors. Cancer Res. 65, 1719 1728.
44. Krischel V., Bruch-Gerharz D., Suschek C., Kroncke K. D., Ruzicka T. Kolb-Bachofen V. (1998) Biphasic effect of exogenous nitric oxide on proliferation and differentiation in skin derived keratinocytes but not fibroblasts. J. Invest. Dermatol. 111, 286 291.
45. Leal E. C., Manivannan A., Hosoya K., Terasaki T., Cunha-Vaz J., Ambrósio A. F. Forrester J. V. (2007) Inducible nitric oxide synthase isoform is a key mediator of leukostasis and blood-retinal barrier breakdown in diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 48, 5257 5265.
46. Lee E. W., Michalkiewicz M., Kitlinska J. et al. (2003) Neuropeptide Y induces ischemic angiogenesis and restores function of ischemic skeletal muscles. J. Clin. Invest. 111, 1853 1862.
47. Lopez-Costa J. J., Goldstein J. Saavedra J. P. (1997) Neuronal and macrophagic nitric oxide synthase isoforms distribution in normal rat retina. Neurosci. Lett. 232, 155 158.
48. Lopez-Ilasaca M. (1998) Signaling from G-protein-coupled receptors to mitogen-activated protein (MAP)-kinase cascades. Biochem. Pharmacol. 56, 269 277.
49. Luczak K., Balcerczyk A., Soszynski M. Bartosz G. (2004) Low concentration of oxidant and nitric oxide donors stimulate proliferation of human endothelial cells in vitro. Cell Biol. Int. 28, 483 486.
50. Magalhaes C. R., Socodato R. E. Paes-de-Carvalho R. (2006) Nitric oxide regulates the proliferation of chick embryo retina cells by a cyclic GMP-independent mechanism. Int. J. Dev. Neurosci. 24, 53 60.
51. Maggio R., Barbier P., Colelli A., Salvadori F., Demontis G. Corsini G. U. (1999) G protein-linked receptors: pharmacological evidence for the formation of heterodimers. J. Pharmacol. Exp. Ther. 291, 251 257.
52. Matarredona E. R., Murillo-Carretero M., Moreno-Lopez B. Estrada C. (2005) Role of nitric oxide in subventricular zone neurogenesis. Brain Res. Brain Res. Rev. 49, 355 366.
53. Mayer E. J., Hughes E. H., Carter D. A. Dick A. D. (2003) Nestin positive cells in adult human retina and in epiretinal membranes. Br. J. Ophthalmol. 87, 1154 1158.
54. Mayer E. J., Carter D. A., Ren Y., Hughes E. H., Rice C. M., Halfpenny C. A., Scolding N. J. Dick A. D. (2005) Neural progenitor cells from postmortem adult human retina. Br. J. Ophthalmol. 89, 102 106.
55. 2+ and calmodulin/MAP kinase kinase/extracellular signal-regulated protein kinase signalling pathway in the mitogenic and antimitogenic effect of nitric oxide in glia- and neurone-derived cell lines. Eur. J. Neurosci. 23, 1690 1700.
56. Mejia-Garcia T. A. Paes-de-Carvalho R. (2007) Nitric oxide regulates cell survival in purified cultures of avian retinal neurons: involvement of multiple transduction pathways. J. Neurochem. 100, 382 394.
57. Milenkovic I., Weick M., Wiedemann P., Reichenbach A. Bringmann A. (2004) Neuropeptide Y-evoked proliferation of retinal glial (Muller) cells. Graefes Arch. Clin. Exp. Ophthalmol. 242, 944 950.
58. Movafagh S., Hobson J. P., Spiegel S., Kleinman H. K. Zukowska Z. (2006) Neuropeptide Y induces migration, proliferation, and tube formation of endothelial cells bimodally via Y1, Y2, and Y5 receptors. FASEB J. 20, 1924 1926.
59. Mullins D. E., Zhang X. Hawes B. E. (2002) Activation of extracellular signal regulated protein kinase by neuropeptide Y and pancreatic polypeptide in CHO cells expressing the NPY Y1, Y2, Y4 and Y5 receptor subtypes. Regul. Pept. 105, 65 73.
60. Oh S. J., D'Angelo I., Lee E. J., Chun M. H. Brecha N. C. (2002) Distribution and synaptic connectivity of neuropeptide Y-immunoreactive amacrine cells in the rat retina. J. Comp. Neurol. 446, 219 234.
61. Overton M. C. Blumer K. J. (2000) G-protein-coupled receptors function as oligomers in vivo. Curr. Biol. 10, 341 344.
62. Packer M. A., Stasiv Y., Benraiss A., Chmielnicki E., Grinberg A., Westphal H., Goldman S. A. Enikolopov G. (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proc. Natl Acad. Sci. USA 100, 9566 9571.
63. Perron M. Harris W. A. (2000) Retinal stem cells in vertebrates. Bioessays 22, 685 688.
64. Piehl L., Capani F., Facorro G., Lopez E. M., de Celis E. R., Pustovrh C., Hager A., Coirini H. Lopez-Costa J. J. (2007) Nitric oxide increases in the rat retina after continuous illumination. Brain Res. 1156, 112 119.
65. Rosmaninho-Salgado J., Araújo I., Álvaro A. R., Duarte E. Cavadas C. (2007) Intracellular signalling mechanisms mediating catecholamine release upon activation of NPY Y1 receptors in mouse chromaffin cells. J. Neurochem. 103, 896 903.
66. Santiago A. R., Pereira T. S., Garrido M. J., Cristovao A. J., Santos P. F. Ambrosio A. F. (2006) High glucose and diabetes increase the release of [3H]-D-aspartate in retinal cell cultures and in rat retinas. Neurochem. Int. 48, 453 458.
67. Sherr C. J. (1996) Cancer cell cycles. Science 274, 1672 1677.
68. Silva A. P., Cavadas C. Grouzmann E. (2002) Neuropeptide Y and its receptors as potential therapeutic drug targets. Clin. Chim. Acta 326, 3 25.
69. Silva A. P., Carvalho A. P., Carvalho C. M. Malva J. O. (2003) Functional interaction between neuropeptide Y receptors and modulation of calcium channels in the rat hippocampus. Neuropharmacology 44, 282 292.
70. Sinclair J. R. Nirenberg S. (2001) Characterization of neuropeptide Y-expressing cells in the mouse retina using immunohistochemical and transgenic techniques. J. Comp. Neurol. 432, 296 306.
71. Southam E. Garthwaite J. (1993) The nitric oxide-cyclic GMP signalling pathway in rat brain. Neuropharmacology 32, 1267 1277.
72. Spence J. R., Madhavan M., Aycinena J. C. Del Rio-Tsonis K. (2007) Retina regeneration in the chick embryo is not induced by spontaneous Mitf downregulation but requires FGF/FGFR/MEK/Erk dependent upregulation of Pax6. Mol. Vis. 13, 57 65.
73. Steinle J. J., Meininger C. J., Chowdhury U., Wu G. Granger H. J. (2003) Role of ephrin B2 in human retinal endothelial cell proliferation and migration. Cell. Signal. 15, 1011 1017.
74. Straznicky C. Hiscock J. (1989) Neuropeptide Y-like immunoreactivity in neurons of the human retina. Vision Res. 29, 1041 1048.
75. Tao J., Tu Y. T., Li J. W., Feng A. P., Huang C. Z., Wu Y. Shen G. X. (2006) Endogenous production of nitric oxide contributes to proliferation effect of vascular endothelial growth factor-induced malignant melanoma cell. Clin. Exp. Dermatol. 31, 94 99.
76. Troger J., Sellemond S., Kieselbach G., Kralinger M., Schmid E., Teuchner B., Nguyen Q. A., Schretter-Irschick E. Gottinger W. (2003) Inhibitory effect of certain neuropeptides on the proliferation of human retinal pigment epithelial cells. Br. J. Ophthalmol. 87, 1403 1408.
77. Turner D. L. Cepko C. L. (1987) A common progenitor for neurons and glia persists in rat retina late in development. Nature 328, 131 136.
78. Ulibarri J. A., Mozdziak P. E., Schultz E., Cook C. Best T. M. (1999) Nitric oxide donors, sodium nitroprusside and S-nitroso-N-acetylpencillamine, stimulate myoblast proliferation in vitro. In Vitro Cell. Dev. Biol. Anim. 35, 215 218.
79. Villalobo A. (2006) Nitric oxide and cell proliferation. FEBS J. 273, 2329 2344.
80. Wettstein J. G., Earley B. Junien J. L. (1995) Central nervous system pharmacology of neuropeptide Y. Pharmacol. Ther. 65, 397 414.
81. Zhang R., Wang L., Zhang L., Chen J., Zhu Z., Zhang Z. Chopp M. (2003) Nitric oxide enhances angiogenesis via the synthesis of vascular endothelial growth factor and cGMP after stroke in the rat. Circ. Res. 92, 308 313.
82. Zhu X. J., Hua Y., Jiang J., Zhou Q. G., Luo C. X., Han X., Lu Y. M. Zhu D. Y. (2006) Neuronal nitric oxide synthase-derived nitric oxide inhibits neurogenesis in the adult dentate gyrus by down-regulating cyclic AMP response element binding protein phosphorylation. Neuroscience 141, 827 836.
83. Zukowska-Grojec Z., Karwatowska-Prokopczuk E., Fisher T. A. Ji H. (1998) Mechanisms of vascular growth-promoting effects of neuropeptide Y: role of its inducible receptors. Regul. Pept. 75-76, 231 238.