The nitric oxide-cGKII system relays death and survival signals during embryonic retinal development via AKT-induced CREB1 activation

Cell Death and Differentiation

Volumn 21, Issue 6, 2014, Pages 915-928

  Socodato, R ^a   Brito, R ^a   Portugal, C C ^a   De Oliveira, N A ^a   Calaza, K C ^a   Paes De Carvalho, R ^a  

^a FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

Author keywords

AKT nuclear localization; apoptosis; cGMP; L arginine; sGC

Indexed keywords

ARGININE; CALCIUM; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIC GMP DEPENDENT PROTEIN KINASE 2; GUANYLATE CYCLASE; N ACETYL S NITROSOPENICILLAMINE; NITRIC OXIDE; PROTEIN KINASE B; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BIRD; CALCIUM TRANSPORT; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CHICK; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; NERVOUS SYSTEM DEVELOPMENT; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; RETINA DEVELOPMENT; RETINA NERVE CELL; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CHICK EMBRYO; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; RETINA;

AVES; MURINAE; VERTEBRATA;

ANIMALS; APOPTOSIS; ARGININE; CELL SURVIVAL; CHICK EMBRYO; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC GMP-DEPENDENT PROTEIN KINASE TYPE II; EMBRYONIC DEVELOPMENT; NEUROGENESIS; NITRIC OXIDE; PROTO-ONCOGENE PROTEINS C-AKT; RETINA; SIGNAL TRANSDUCTION;

EID: 84899978192     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2014.11     Document Type: Article

References (58)

1. Marquardt T, Gruss P. Generating neuronal diversity in the retina: one for nearly all. Trends Neurosci 2002; 25: 32.
2. Yang XJ. Roles of cell-extrinsic growth factors in vertebrate eye pattern formation and retinogenesis. Semin Cell Dev Biol 2004; 15: 91-103.
3. Wiesinger H. Arginine metabolism and the synthesis of nitric oxide in the nervous system. Prog Neurobiol 2001; 64: 365-391.
4. Knowles RG, Palacios M, Palmer RM, Moncada S. Formation of nitric oxide from L-arginine in the central nervous system: a transduction mechanism for stimulation of the soluble guanylate cyclase. Proc Natl Acad Sci USA 1989; 86: 5159-5162.
5. Krumenacker JS, Hanafy KA, Murad F. Regulation of nitric oxide and soluble guanylyl cyclase. Brain Res Bull 2004; 62: 505-515.
6. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 2001; 3: 193-197.
7. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 2005; 6: 150-166.
8. Liu L, Stamler JS. NO: an inhibitor of cell death. Cell Death Differ 1999; 6: 937-942.
9. Boehning D, Snyder SH. Novel neural modulators. Annu Rev Neurosci 2003; 26: 105-131.
10. Peunova N, Enikolopov G. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 1995; 375: 68-73.
11. Magalhaes CR, Socodato RES, Paes-de-Carvalho R. Nitric oxide regulates the proliferation of chick embryo retina cells by a cyclic GMP-independent mechanism. Int J Dev Neurosci 2006; 24: 53-60.
12. Mej́ia-Garcia TA, Paes-de-Carvalho R. Nitric oxide regulates cell survival in purified cultures of avian retinal neurons: involvement of multiple transduction pathways. J Neurochem 2007; 100: 382-394.
13. Cossenza M, Paes-de-Carvalho R. L-arginine uptake and release by cultured avian retinal cells: differential cellular localization in relation to nitric oxide synthase. J Neurochem 2000; 74: 1885-1894.
14. Portugal CC, da Encarnação TG, Socodato R, Moreira SR, Brudzewsky D, Ambrósio AFet al. Nitric oxide modulates sodium vitamin C transporter 2 (SVCT-2) protein expression via protein kinase G (PKG) and nuclear factor-kappaB (NF-kB). J Biol Chem 2012; 287: 3860-3872.
15. Socodato R, Santiago FN, Portugal CC, Domingues AF, Santiago AR, Relvas JB et al. Calcium-permeable a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors trigger neuronal nitric-oxide synthase activation to promote nerve cell death in an Src kinase-dependent fashion. J Biol Chem 2012; 287: 38680-38694.
16. Hofmann F, Feil R, Kleppisch T, Schlossmann J. Function of cGMP-dependent protein kinases as revealed by gene deletion. Physiol Rev 2006; 86: 1-23.
17. Feil R, Lohmann SM, de Jonge H, Walter U, Hofmann F. Cyclic GMP-dependent protein kinases and the cardiovascular system insights from genetically modified mice. Circ Res 2003; 93: 907-916.
18. Surks HK, Mochizuki N, Kasai Y, Georgescu SP, Tang KM, Ito M et al. Regulation of myosin phosphatase by a specific interaction with cGMP-dependent protein kinase I±. Science 1999; 286: 1583-1587.
19. Arancio O, Antonova I, Gambaryan S, Lohmann SM, Wood JS, Lawrence DS et al. Presynaptic role of cGMP-dependent protein kinase during long-lasting potentiation. J Neurosci 2001; 21: 143-149.
20. Serulle Y, Zhang S, Ninan I, Puzzo D, McCarthy M, Khatri L et al. A GluR1-cGKII interaction regulates AMPA receptor trafficking. Neuron 2007; 56: 670-688.
21. Wang H-G, Lu F-M, Jin I, Udo H, Kandel ER, de Vente J et al. Presynaptic and postsynaptic roles of NO, cGK, and RhoA in long-lasting potentiation and aggregation of synaptic proteins. Neuron 2005; 45: 389-403.
22. Mej́ia-García TA, Portugal CC, Encarnação TG, Prado MA, Paes-de-Carvalho R. Nitric oxide regulates AKT phosphorylation and nuclear translocation in cultured retinal cells. Cell Signal 2013; 25: 2424-2439.
23. Socodato RES, Magalhães CR, Paes-de-Carvalho R. Glutamate and nitric oxide modulate ERK and CREB phosphorylation in the avian retina: evidence for direct signaling from neurons to Müller glial cells. J Neurochem 2009; 108: 417-429.
24. Lonze BE, Ginty DD. Function and regulation of CREB family transcription factors in the nervous system. Neuron 2002; 35: 605-623.
25. Shaywitz AJ, Greenberg ME. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu Rev Biochem 1999; 68: 821-861.
26. West AE, Griffith EC, Greenberg ME. Regulation of transcription factors by neuronal activity. Nat Rev Neurosci 2002; 3: 921-931.
27. Socodato R, Brito R, Calaza KC, Paes-de-Carvalho R. Developmental regulation of neuronal survival by adenosine in the in vitro and in vivo avian retina depends on a shift of signaling pathways leading to CREB phosphorylation or dephosphorylation. J Neurochem 2011; 116: 227-239.
28. O'Driscoll C, O'Connor J, O'Brien CJ, Cotter TG. Basic fibroblast growth factor-induced protection from light damage in the mouse retina in vivo. J Neurochem 2008; 105: 524-536.
29. Riccio A, Alvania RS, Lonze BE, Ramanan N, Kim T, Huang Y et al. A nitric oxide signaling pathway controls CREB-mediated gene expression in neurons. Mol Cell 2006; 21: 283-294.
30. Paes-de-Carvalho R, Maia GA, Ferreira JM. Adenosine regulates the survival of avian retinal neurons and photoreceptors in culture. Neurochem Res 2003; 2003:1583-1590.
31. Adler R, Hatlee M. Plasticity and differentiation of embryonic retinal cells after terminal mitosis. Science 1989; 243: 391-393.
32. Bredt DS, Hwang PM, Snyder SH. Localization of nitric oxide synthase indicating a neural role for nitric oxide. Nature 1990; 347: 768.
33. Bredt DS, Snyder SH. Nitric oxide mediates glutamate-linked enhancement of cGMP levels in the cerebellum. Proc Natl Acad Sci USA 1989; 86: 9030-9033.
34. Arnelle DR, Stamler JS. NO +, NO., and NO-donation by S-nitrosothiols: implications for regulation of physiological functions by S-nitrosylation and acceleration of disulfide formation. Arch Biochem Biophys 1995; 318: 279-285.
35. Zeller A, Wenzl MV, Beretta M, Stessel H, Russwurm M, Koesling D et al. Mechanisms underlying activation of soluble guanylate cyclase by the nitroxyl donor Angeli's salt. Mol Pharmacol 2009; 76:1115-1122.
36. Irvine JC, Ritchie RH, Favaloro JL, Andrews KL, Widdop RE, Kemp-Harper BK. Nitroxyl (HNO): the Cinderella of the nitric oxide story. Trends Pharmacol Sci 2008; 29: 601-608.
37. Hardingham GE, Arnold FJ, Bading H. Nuclear calcium signaling controls CREB-mediated gene expression triggered by synaptic activity. Nat Neurosci 2001; 4: 261-267.
38. Hardingham GE, Fukunaga Y, Bading H. Extrasynaptic NMDARs oppose synaptic NMDARs by triggering CREB shut-off and cell death pathways. Nat Neurosci 2002; 5: 405-414.
39. Kornhauser JM, Cowan CW, Shaywitz AJ, Dolmetsch RE, Griffith EC, Hu LS et al. CREB transcriptional activity in neurons is regulated by multiple, calcium-specific phosphorylation events. Neuron 2002; 34: 221-233.
40. Datta SR, Brunet A, Greenberg ME. Cellular survival: a play in three Akts. Genes Dev 1999; 13:2905-2927.
41. Lee SB, Xuan Nguyen TL, Choi JW, Lee KH, Cho SW, Liu Z et al. Nuclear Akt interacts with B23/NPM and protects it from proteolytic cleavage, enhancing cell survival. Proc Natl Acad Sci USA 2008; 105:16584-16589.
42. Ahn JY, Liu X, Liu Z, Pereira L, Cheng D, Peng J et al. Nuclear Akt associates with PKC-phosphorylated Ebp1, preventing DNA fragmentation by inhibition of caspase-activated DNase. EMBO J 2006; 25: 2083-2095.
43. Hu Y, Yao J, Liu Z, Liu X, Fu H, Ye K. Akt phosphorylates acinus and inhibits its proteolytic cleavage, preventing chromatin condensation. EMBO J 2005; 24: 3543-3554.
44. Jain V, Baitharu I, Prasad D, Ilavazhagan G. Enriched environment prevents hypobaric hypoxia induced memory impairment and neurodegeneration: role of BDNF/PI3K/GSK3beta pathway coupled with CREB activation. PLoS One 2013; 8: e62235.
45. Simao F, Matte A, Pagnussat AS, Netto CA, Salbego CG. Resveratrol prevents CA1 neurons against ischemic injury by parallel modulation of both GSK-3beta and CREB through PI3-K/Akt pathways. Eur J Neurosci 2012; 36: 2899-2905.
46. Paquet-Durand F, Hauck SM, Van Veen T, Ueffing M, Ekström P. PKG activity causes photoreceptor cell death in two retinitis pigmentosa models. J Neurochem 2008; 108: 796-810.
47. Wu GY, Deisseroth K, Tsien RW. Activity-dependent CREB phosphorylation: convergence of a fast, sensitive calmodulin kinase pathway and a slow, less sensitive mitogen-activated protein kinase pathway. Proc Natl Acad Sci USA 2001; 98: 2808-2813.
48. Rameau GA, Tukey DS, Garcin-Hosfield ED, Titcombe RF, Misra C, Khatri L et al. Biphasic coupling of neuronal nitric oxide synthase phosphorylation to the NMDA receptor regulates AMPA receptor trafficking and neuronal cell death. J Neurosci 2007; 27: 3445-3455.
49. Brown GC. Nitric oxide and neuronal death. Nitric Oxide Biol Chem 2010; 23: 153-165.
50. Walton MR, Dragunow I. Is CREB a key to neuronal survival? Trends Neurosci 2000; 23: 48-53.
51. Fusco S, Ripoli C, Podda MV, Ranieri SC, Leone L, Toietta G et al. A role for neuronal cAMP responsive-element binding (CREB)-1 in brain responses to calorie restriction. Proc Natl Acad Sci USA 2012; 109: 621-626.
52. Beltran WA, Allore HG, Johnson E, Towle V, Tao W, Acland GM et al. CREB1/ATF1 activation in photoreceptor degeneration and protection. Invest Ophthalmol Vis Sci 2009; 50: 5355-5363.
53. Yamamoto KK, Gonzalez GA, Biggs WH 3rd, Montminy MR. Phosphorylation- induced binding and transcriptional efficacy of nuclear factor CREB. Nature 1988; 334: 494-498.
54. Gonzalez GA, Montminy MR. Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 1989; 59: 675-680.
55. Mali RS, Zhang XM, Chintala SK. A decrease in phosphorylation of cAMP-response element-binding protein (CREBP) promotes retinal degeneration. Exp Eye Res 2011; 92: 528-536.
56. Takeda H, Kitaoka Y, Hayashi Y, Kumai T, Munemasa Y, Fujino H et al. Calcium/calmodulin-dependent protein kinase II regulates the phosphorylation of CREB in NMDA-induced retinal neurotoxicity. Brain Res 2007; 1184: 306-315.
57. Nagai-Kusuhara A, Nakamura M, Mukuno H, Kanamori A, Negi A, Seigel GM. cAMP-responsive element binding protein mediates a cGMP/protein kinase G-dependent anti-apoptotic signal induced by nitric oxide in retinal neuro-glial progenitor cells. Exp Eye Res 2007; 84: 152-162.
58. Anccasi RM, Ornelas IM, Cossenza M, Persechini PM, Ventura ALM ATP. induces the death of developing avian retinal neurons in culture via activation of P2X7 and glutamate receptors. Purinergic Signal 2013; 9: 15-29.