Molecular Neurobiology

, Volume 54, Issue 7, pp 5142–5155 | Cite as

Adenine Nucleotides Control Proliferation In Vivo of Rat Retinal Progenitors by P2Y1 Receptor

  • Luana de Almeida-Pereira
  • Camila Feitosa Magalhães
  • Marinna Garcia Repossi
  • Maria Luiza Prates Thorstenberg
  • Alfred Sholl-Franco
  • Robson Coutinho-Silva
  • Ana Lucia Marques Ventura
  • Lucianne Fragel-Madeira
Article

Abstract

Previous studies demonstrated that exogenous ATP is able to regulate proliferation of retinal progenitor cells (RPCs) in vitro possibly via P2Y1 receptor, a G protein-coupled receptor. Here, we evaluated the function of adenine nucleotides in vivo during retinal development of newborn rats. Intravitreal injection of apyrase, an enzyme that hydrolyzes nucleotides, reduced cell proliferation in retinas at postnatal day 2 (P2). This decrease was reversed when retinas were treated together with ATPγ-S or ADPβ-S, two hydrolysis-resistant analogs of ATP and ADP, respectively. During early postnatal days (P0 to P5), an increase in ectonucleotidase (E-NTPDase) activity was observed in the retina, suggesting a decrease in the availability of adenine nucleotides, coinciding with the end of proliferation. Interestingly, intravitreal injection of the E-NTPDase inhibitor ARL67156 increased proliferation by around 60 % at P5 rats. Furthermore, immunolabeling against P2Y1 receptor was observed overall in retina layers from P2 rats, including proliferating Ki-67-positive cells in the neuroblastic layer (NBL), suggesting that this receptor could be responsible for the action of adenine nucleotides upon proliferation of RPCs. Accordingly, intravitreal injection of MRS2179, a selective antagonist of P2Y1 receptors, reduced cell proliferation by approximately 20 % in P2 rats. Moreover, treatment with MRS 2179 caused an increase in p57KIP2 and cyclin D1 expression, a reduction in cyclin E and Rb phosphorylated expression and in BrdU-positive cell number. These data suggest that the adenine nucleotides modulate the proliferation of rat RPCs via activation of P2Y1 receptors regulating transition from G1 to S phase of the cell cycle.

Keywords

Retina Development Proliferation Purines P2Y1 receptor 

Supplementary material

12035_2016_59_Fig6_ESM.jpg (2 kb)
Figure S1

P2Y1 receptor identification in a newborn rat retina. a, b and c Negative control (a DAPI—blue, b without anti-P2Y1 primary antibody—red, c merge). d, e and f P2Y1 immunostaining (d DAPI—blue, e P2Y1—red, f merge). The P2Y1 receptor was found in all layers at P2 rat retina. In the GCL and IPL, it was uniformly distributed at the cell surface, but in the NBL, we observed a dotted staining to P2Y1 receptor. The retina photomicrography represents a 400× magnification under indirect fluorescence using a Leica microscope (DM2500). GCL = Ganglion Cell Layer; IPL = Inner Plexiform Layer; NBL = Neuroblastic Layer; Scale bar = 100 μM. (JPEG 1 kb)

12035_2016_59_MOESM1_ESM.tif (494 kb)
High Resolution Image (TIFF 494 kb)
12035_2016_59_Fig7_ESM.jpg (3 kb)
Figure S2

The treatment of 100 μM MRS 2179 did not induce cell death at rat retina. Neutral red staining at P2 rat retina control and treated with 100 μM MRS 2179 at different survival times. At any survival time, there was no observed difference in the amount of pyknotic nuclei between the control and treated animals. a Control 3 h; b 100 μM MRS 2179 3 h; c Control 6 h; d 100 μM MRS 2179 6 h; e Control 12 h; f 100 μM MRS 2179 12 h; g Control 16 h; h 100 μM MRS 2179 16 h; i Control 20 h; j 100 μM MRS 2179 20 h. The retina photomicrographs represent 400× magnification under differential interference contrast using a Leica microscope (DM2500). GCL = Ganglion Cell Layer; IPL = Inner Plexiform Layer; NBL = Neuroblastic Layer. Scale bar = 50 μm (JPEG 2 kb)

12035_2016_59_MOESM2_ESM.tif (1 mb)
High Resolution Image (TIFF 1033 kb)

References

  1. 1.
    Barton A, Fendrik AJ (2015) Retinogenesis: stochasticity and the competency model. J Theor Biol 373:73–81. doi:10.1016/j.jtbi.2015.03.015 CrossRefPubMedGoogle Scholar
  2. 2.
    Masland RH (2012) The neuronal organization of the retina. Neuron 76:266–280. doi:10.1016/j.neuron.2012.10.002 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Cepko C (2014) Intrinsically different retinal progenitor cells produce specific types of progeny. Nat Rev Neurosci 15:615–627. doi:10.1038/nrn3767 CrossRefPubMedGoogle Scholar
  4. 4.
    Rapaport DH, Wong LL, Wood ED, et al. (2004) Timing and topography of cell genesis in the rat retina. J Comp Neurol 474:304–324. doi:10.1002/cne.20134 CrossRefPubMedGoogle Scholar
  5. 5.
    Bilitou A, Ohnuma SI (2010) The role of cell cycle in retinal development: cyclin-dependent kinase inhibitors co-ordinate cell-cycle inhibition, cell-fate determination and differentiation in the developing retina. Dev Dyn 239:727–736. doi:10.1002/dvdy.22223 CrossRefPubMedGoogle Scholar
  6. 6.
    Lim S, Kaldis P (2013) Cdks, cyclins and CKIs: roles beyond cell cycle regulation. Development 140:3079–3093. doi:10.1242/dev.091744 CrossRefPubMedGoogle Scholar
  7. 7.
    Xiong Y, Zhang H, Beach D (1992) D type cyclins associate with multiple protein kinases and the DNA replication and repair factor PCNA. Cell 71:505–514CrossRefPubMedGoogle Scholar
  8. 8.
    Bates S, Bonetta L, MacAllan D, et al. (1994) CDK6 (PLSTIRE) and CDK4 (PSK-J3) are a distinct subset of the cyclin-dependent kinases that associate with cyclin D1. Oncogene 9:71–79PubMedGoogle Scholar
  9. 9.
    Hatakeyama M, Brill JA, Fink GR, Weinberg RA (1994) Collaboration of G1 cyclins in the functional inactivation of the retinoblastoma protein. Genes Dev 8:1759–1771CrossRefPubMedGoogle Scholar
  10. 10.
    Bertoli C, Skotheim JM, de Bruin RAM (2013) Control of cell cycle transcription during G1 and S phases. Nat Rev Mol Cell Biol 14:518–528. doi:10.1038/nrm3629 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Suzuki-Takahashi I, Kitagawa M, Saijo M, et al. (1995) The interactions of E2F with pRB and with p107 are regulated via the phosphorylation of pRB and p107 by a cyclin-dependent kinase. Oncogene 10:1691–1698PubMedGoogle Scholar
  12. 12.
    Burke JR, Hura GL, Rubin SM (2012) Structures of inactive retinoblastoma protein reveal multiple mechanisms for cell cycle control. Genes Dev 26:1156–1166. doi:10.1101/gad.189837.112 CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Westendorp B, Mokry M, Groot Koerkamp MJA, et al. (2012) E2F7 represses a network of oscillating cell cycle genes to control S-phase progression. Nucleic Acids Res 40:3511–3523. doi:10.1093/nar/gkr1203 CrossRefPubMedGoogle Scholar
  14. 14.
    Koff A, Giordano A, Desai D, et al. (1992) Formation and activation of a cyclin E-cdk2 complex during the G1 phase of the human cell cycle. Science 257:1689–1694CrossRefPubMedGoogle Scholar
  15. 15.
    Ohtsubo M, Theodoras AM, Schumacher J, et al. (1995) Human cyclin E, a nuclear protein essential for the G1-to-S phase transition. Mol Cell Biol 15:2612–2624CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Jiang H, Wang YC (1996) Cyclin-dependent kinase inhibitors in mammal cells. Sheng Li Ke Xue Jin Zhan 27:107–112PubMedGoogle Scholar
  17. 17.
    Besson A, Dowdy SF, Roberts JM (2008) CDK inhibitors: cell cycle regulators and beyond. Dev Cell 14:159–169. doi:10.1016/j.devcel.2008.01.013 CrossRefPubMedGoogle Scholar
  18. 18.
    Burnstock G (2009) Purinergic signalling : past, present and future. Braz J Med Biol Res 42:3–8. doi:10.1590/S0100-879X2008005000037 CrossRefPubMedGoogle Scholar
  19. 19.
    Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H (2009) Purinergic signalling in the nervous system: an overview. Trends Neurosci 32:19–29. doi:10.1016/j.tins.2008.10.001 CrossRefPubMedGoogle Scholar
  20. 20.
    Zimmermann H (2011) Purinergic signaling in neural development. Semin Cell Dev Biol 22:194–204. doi:10.1016/j.semcdb.2011.02.007 CrossRefPubMedGoogle Scholar
  21. 21.
    Ulrich H, Abbracchio MP, Burnstock G (2012) Extrinsic purinergic regulation of neural stem/progenitor cells: implications for CNS development and repair. Stem Cell Rev Reports 8:755–767. doi:10.1007/s12015-012-9372-9 CrossRefGoogle Scholar
  22. 22.
    Newman EA (2001) Propagation of intercellular calcium waves in retinal astrocytes and Müller cells. J Neurosci 21:2215–2223PubMedPubMedCentralGoogle Scholar
  23. 23.
    Pearson RA, Dale N, Llaudet E, Mobbs P (2005) ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 46:731–744. doi:10.1016/j.neuron.2005.04.024 CrossRefPubMedGoogle Scholar
  24. 24.
    Illes P, Alexandre Ribeiro J (2004) Molecular physiology of P2 receptors in the central nervous system. Eur J Pharmacol 483:5–17. doi:10.1016/j.ejphar.2003.10.030 CrossRefPubMedGoogle Scholar
  25. 25.
    Burnstock G (2013) Purinergic signalling: pathophysiology and therapeutic potential. Keio J Med 62:63–73. doi:10.2302/kjm.2013-0003-RE CrossRefPubMedGoogle Scholar
  26. 26.
    Kaczmarek-Hájek K, Lörinczi E, Hausmann R, Nicke A (2012) Molecular and functional properties of P2X receptors—recent progress and persisting challenges. Purinergic Signal 8:375–417. doi:10.1007/s11302-012-9314-7 CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    North RA, Jarvis MF (2013) P2X receptors as drug targets. Mol Pharmacol 83:759–769. doi:10.1124/mol.112.083758 CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Chappell WH, Steelman LS, Long JM, et al. (2011) Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR inhibitors: rationale and importance to inhibiting these pathways in human health. Oncotarget 2:135–164CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    von Kügelgen I, Hoffmann K (2015) Pharmacology and structure of P2Y receptors. Neuropharmacology. doi:10.1016/j.neuropharm.2015.10.030 Google Scholar
  30. 30.
    Jacobson KA, Balasubramanian R, Deflorian F, Gao ZG (2012) G protein-coupled adenosine (P1) and P2Y receptors: ligand design and receptor interactions. Purinergic Signal 8:419–436. doi:10.1007/s11302-012-9294-7 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Puchałowicz K, Tarnowski M, Baranowska-Bosiacka I, et al. (2014) P2X and P2Y receptors—role in the pathophysiology of the nervous system. Int J Mol Sci 15:23672–23704. doi:10.3390/ijms151223672 CrossRefPubMedPubMedCentralGoogle Scholar
  32. 32.
    Novak I (2003) ATP as a signaling molecule: the exocrine focus. News Physiol Sci 18:12–17. doi:10.1152/nips.01409.2002 PubMedGoogle Scholar
  33. 33.
    Zimmermann H, Zebisch M, Sträter N (2012) Cellular function and molecular structure of ecto-nucleotidases. Purinergic Signal 8:437–502. doi:10.1007/s11302-012-9309-4 CrossRefPubMedPubMedCentralGoogle Scholar
  34. 34.
    Yegutkin GG (2014) Enzymes involved in metabolism of extracellular nucleotides and nucleosides: functional implications and measurement of activities. Crit Rev Biochem Mol Biol 49:473–497. doi:10.3109/10409238.2014.953627 CrossRefPubMedGoogle Scholar
  35. 35.
    Robson SC, Sévigny J, Zimmermann H (2006) The E-NTPDase family of ectonucleotidases: structure function relationships and pathophysiological significance. Purinergic Signal 2:409–430. doi:10.1007/s11302-006-9003-5 CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Kukulski F, Lévesque SA, Sévigny J (2011) Impact of ectoenzymes on p2 and p1 receptor signaling. Adv Pharmacol. doi:10.1016/B978-0-12-385526-8.00009-6 PubMedGoogle Scholar
  37. 37.
    Sugioka M, Zhou WL, Hofmann HD, Yamashita M (1999) Involvement of P2 purinoceptors in the regulation of DNA synthesis in the neural retina of chick embryo. Int J Dev Neurosci 17:135–144. doi:10.1016/S0736-5748(98)00066-5 CrossRefPubMedGoogle Scholar
  38. 38.
    Pearson R, Catsicas M, Becker D, Mobbs P (2002) Purinergic and muscarinic modulation of the cell cycle and calcium signaling in the chick retinal ventricular zone. J Neurosci 22:7569–7579PubMedGoogle Scholar
  39. 39.
    Sanches G, de Alencar LS, Ventura ALM (2002) ATP induces proliferation of retinal cells in culture via activation of PKC and extracellular signal-regulated kinase cascade. Int J Dev Neurosci 20:21–27CrossRefPubMedGoogle Scholar
  40. 40.
    França GR, Freitas RCC, Ventura a. LM (2007) ATP-induced proliferation of developing retinal cells: regulation by factors released from postmitotic cells in culture. Int J Dev Neurosci 25:283–291. doi: 10.1016/j.ijdevneu.2007.05.006
  41. 41.
    Sholl-Franco A, Fragel-Madeira L, Macamaa DCC, et al. (2010) ATP controls cell cycle and induces proliferation in the mouse developing retina. Int J Dev Neurosci 28:63–73. doi:10.1016/j.ijdevneu.2009.09.004 CrossRefPubMedGoogle Scholar
  42. 42.
    Battista AG, Ricatti MJ, Pafundo DE, et al. (2009) Extracellular ADP regulates lesion-induced in vivo cell proliferation and death in the zebrafish retina. J Neurochem 111:600–613. doi:10.1111/j.1471-4159.2009.06352.x CrossRefPubMedGoogle Scholar
  43. 43.
    Fragel-Madeira L, Meletti T, Mariante RM, et al. (2011) Platelet activating factor blocks interkinetic nuclear migration in retinal progenitors through an arrest of the cell cycle at the S/G2 transition. PLoS One 6:e16058. doi:10.1371/journal.pone.0016058 CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Chan KM, Delfert D, Junger KD (1986) A direct colorimetric assay for Ca2+-stimulated ATPase activity. Anal Biochem 157:375–380CrossRefPubMedGoogle Scholar
  45. 45.
    Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3 CrossRefPubMedGoogle Scholar
  46. 46.
    Schafer R, Sedehizade F, Welte T, Reiser G (2003) ATP- and UTP-activated P2Y receptors differently regulate proliferation of human lung epithelial tumor cells. Am J Physiol Lung Cell Mol Physiol 285:L376–L385. doi:10.1152/ajplung.00447.2002 CrossRefPubMedGoogle Scholar
  47. 47.
    Horckmans M, Robaye B, Léon-Gόmez E, et al. (2012) P2Y(4) nucleotide receptor: a novel actor in post-natal cardiac development. Angiogenesis 15:349–360. doi:10.1007/s10456-012-9265-1 CrossRefPubMedGoogle Scholar
  48. 48.
    Certal M, Vinhas A, Pinheiro AR, et al. (2015) Calcium signaling and the novel anti-proliferative effect of the UTP-sensitive P2Y11 receptor in rat cardiac myofibroblasts. Cell Calcium 58:518–533. doi:10.1016/j.ceca.2015.08.004 CrossRefPubMedGoogle Scholar
  49. 49.
    Eun SY, Ko YS, Park SW, et al. (2015) IL-1β enhances vascular smooth muscle cell proliferation and migration via P2Y2 receptor-mediated RAGE expression and HMGB1 release. Vasc Pharmacol 72:108–117. doi:10.1016/j.vph.2015.04.013 CrossRefGoogle Scholar
  50. 50.
    Ricatti MJ, Battista AG, Zorrilla Zubilete M, Faillace MP (2011) Purinergic signals regulate daily S-phase cell activity in the ciliary marginal zone of the zebrafish retina. J Biol Rhythm 26:107–117. doi:10.1177/0748730410395528 CrossRefGoogle Scholar
  51. 51.
    Suyama S, Sunabori T, Kanki H, et al. (2012) Purinergic signaling promotes proliferation of adult mouse subventricular zone cells. J Neurosci 32:9238–9247. doi:10.1523/JNEUROSCI.4001-11.2012 CrossRefPubMedGoogle Scholar
  52. 52.
    Cao X, Li L-P, Qin X-H, et al. (2013) Astrocytic adenosine 5′-triphosphate release regulates the proliferation of neural stem cells in the adult hippocampus. Stem Cells 31:1633–1643. doi:10.1002/stem.1408 CrossRefPubMedGoogle Scholar
  53. 53.
    Xia M, Zhu Y (2014) Fibronectin enhances spinal cord astrocyte proliferation by elevating P2Y1 receptor expression. J Neurosci Res 92:1078–1090. doi:10.1002/jnr.23384 CrossRefPubMedGoogle Scholar
  54. 54.
    Maraula G, Lana D, Coppi E, et al. (2014) The selective antagonism of P2X7 and P2Y1 receptors prevents synaptic failure and affects cell proliferation induced by oxygen and glucose deprivation in rat dentate gyrus. PLoS One 9:e115273. doi:10.1371/journal.pone.0115273 CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Fries JE, Wheeler-Schilling TH, Kohler K, Guenther E (2004) Distribution of metabotropic P2Y receptors in the rat retina: a single-cell RT-PCR study. Mol Brain Res 130:1–6. doi:10.1016/j.molbrainres.2004.06.041 CrossRefPubMedGoogle Scholar
  56. 56.
    Fries JE, Wheeler-Schilling TH, Guenther E, Kohler K (2004) Expression of P2Y1, P2Y2, P2Y4, and P2Y6 receptor subtypes in the rat retina. Investig Ophthalmol Vis Sci 45:3410–3417. doi:10.1167/iovs.04-0141 CrossRefGoogle Scholar
  57. 57.
    Dyer MA, Cepko CL (2000) p57(Kip2) regulates progenitor cell proliferation and amacrine interneuron development in the mouse retina. Development 127:3593–3605PubMedGoogle Scholar
  58. 58.
    Sicinski P, Donaher JL, Parker SB, et al. (1995) Cyclin D1 provides a link between development and oncogenesis in the retina and breast. Cell 82:621–630CrossRefPubMedGoogle Scholar
  59. 59.
    Fantl V, Stamp G, Andrews A, et al. (1995) Mice lacking cyclin D1 are small and show defects in eye and mammary gland development. Genes Dev 9:2364–2372CrossRefPubMedGoogle Scholar
  60. 60.
    Ornelas IM, Ventura ALM (2010) Involvement of the PI3K/AKT pathway in ATP-induced proliferation of developing retinal cells in culture. Int J Dev Neurosci 28:503–511. doi:10.1016/j.ijdevneu.2010.06.001 CrossRefPubMedGoogle Scholar
  61. 61.
    Sheppard KE, McArthur GA (2013) The cell-cycle regulator CDK4: an emerging therapeutic target in melanoma. Clin Cancer Res 19:5320–5328. doi:10.1158/1078-0432.CCR-13-0259 CrossRefPubMedGoogle Scholar
  62. 62.
    Zhang SS, Fu XY, Barnstable CJ (2002) Tissue culture studies of retinal development. Methods 28:439–447CrossRefPubMedGoogle Scholar
  63. 63.
    Heavner W, Pevny L (2012) Eye development and retinogenesis. Cold Spring Harb Perspect Biol 4:a008391. doi:10.1101/cshperspect.a008391 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Dyer MA, Cepko CL (2001) p27Kip1 and p57Kip2 regulate proliferation in distinct retinal progenitor cell populations. J Neurosci 21:4259–4271PubMedGoogle Scholar
  65. 65.
    Donovan SL, Dyer MA (2004) Developmental defects in Rb-deficient retinae. Vis Res 44:3323–3333. doi:10.1016/j.visres.2004.08.007 CrossRefPubMedGoogle Scholar
  66. 66.
    Davis DM, Dyer MA (2010) Retinal progenitor cells, differentiation, and barriers to cell cycle reentry. Curr Top Dev Biol. doi:10.1016/B978-0-12-385044-7.00006-0 PubMedGoogle Scholar
  67. 67.
    Nunes PHC, Calaza KDC, Albuquerque LM, et al. (2007) Signal transduction pathways associated with ATP-induced proliferation of cell progenitors in the intact embryonic retina. Int J Dev Neurosci 25:499–508. doi:10.1016/j.ijdevneu.2007.09.007 CrossRefPubMedGoogle Scholar
  68. 68.
    Resta V, Novelli E, Di Virgilio F, Galli-Resta L (2005) Neuronal death induced by endogenous extracellular ATP in retinal cholinergic neuron density control. Development 132:2873–2882. doi:10.1242/dev.01855 CrossRefPubMedGoogle Scholar
  69. 69.
    He M-L, Gonzalez-Iglesias AE, Tomic M, Stojilkovic SS (2005) Release and extracellular metabolism of ATP by ecto-nucleotidase eNTPDase 1-3 in hypothalamic and pituitary cells. Purinergic Signal 1:135–144. doi:10.1007/s11302-005-6208-y CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Lutty GA, McLeod DS (1992) A new technique for visualization of the human retinal vasculature. Arch Ophthalmol 110:267–276CrossRefPubMedGoogle Scholar
  71. 71.
    Lutty GA, McLeod DS (2005) Phosphatase enzyme histochemistry for studying vascular hierarchy, pathology, and endothelial cell dysfunction in retina and choroid. Vis Res 45:3504–3511. doi:10.1016/j.visres.2005.08.022 CrossRefPubMedPubMedCentralGoogle Scholar
  72. 72.
    Anccasi RM, Ornelas IM, Cossenza M, et al. (2013) ATP induces the death of developing avian retinal neurons in culture via activation of P2X7 and glutamate receptors. Purinergic Signal 9:15–29. doi:10.1007/s11302-012-9324-5 CrossRefPubMedGoogle Scholar
  73. 73.
    Puthussery T, Fletcher EL (2007) Neuronal expression of P2X3 purinoceptors in the rat retina. Neuroscience 146:403–414. doi:10.1016/j.neuroscience.2007.01.055 CrossRefPubMedGoogle Scholar
  74. 74.
    Bigonnesse F, Levesque SA, Kukulski F, et al. (2004) Cloning and characterization of mouse nucleoside triphosphate diphosphohydrolase-8. Biochemistry 43:5511–5519. doi:10.1021/bi0362222 CrossRefPubMedGoogle Scholar
  75. 75.
    Fausther M, Lecka J, Kukulski F, et al. (2007) Cloning, purification, and identification of the liver canalicular ecto-ATPase as NTPDase8. Am J Physiol Gastrointest Liver Physiol 292:G785–G795. doi:10.1152/ajpgi.00293.2006 CrossRefPubMedGoogle Scholar
  76. 76.
    Kiss DS, Zsarnovszky A, Horvath K, et al. (2009) Ecto-nucleoside triphosphate diphosphohydrolase 3 in the ventral and lateral hypothalamic area of female rats: morphological characterization and functional implications. Reprod Biol Endocrinol 7:31. doi:10.1186/1477-7827-7-31 CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Massé K, Bhamra S, Eason R, et al. (2007) Purine-mediated signalling triggers eye development. Nature 449:1058–1062. doi:10.1038/nature06189 CrossRefPubMedGoogle Scholar
  78. 78.
    Gampe K, Haverkamp S, Robson SC, et al. (2014) NTPDase2 and the P2Y1 receptor are not required for mammalian eye formation. Purinergic Signal 11:155–160. doi:10.1007/s11302-014-9440-5 CrossRefPubMedPubMedCentralGoogle Scholar
  79. 79.
    Siow NL, Choi RCY, Xie HQ, et al. (2010) ATP induces synaptic gene expressions in cortical neurons: transduction and transcription control via P2Y1 receptors. Mol Pharmacol 78:1059–1071. doi:10.1124/mol.110.066506 CrossRefPubMedPubMedCentralGoogle Scholar
  80. 80.
    Liu X, Hashimoto-Torii K, Torii M, et al. (2008) The role of ATP signaling in the migration of intermediate neuronal progenitors to the neocortical subventricular zone. Proc Natl Acad Sci U S A 105:11802–11807. doi:10.1073/pnas.0805180105 CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Foster DA, Yellen P, Xu L, Saqcena M (2010) Regulation of G1 cell cycle progression: distinguishing the restriction point from a nutrient-sensing cell growth checkpoint(s). Genes Cancer 1:1124–1131. doi:10.1177/1947601910392989 CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Cuyàs E, Corominas-faja B, Joven J, Menendez JA (2014) Cell Cycle Control. doi:10.1007/978-1-4939-0888-2
  83. 83.
    Kim M, Nakamoto T, Nishimori S, et al. (2008) A new ubiquitin ligase involved in p57KIP2 proteolysis regulates osteoblast cell differentiation. EMBO Rep 9:878–884. doi:10.1038/embor.2008.125 CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Lu Z, Hunter T (2010) Ubiquitylation and proteasomal degradation of the p21(Cip1), p27(Kip1) and p57(Kip2) CDK inhibitors. Cell Cycle 9:2342–2352CrossRefPubMedPubMedCentralGoogle Scholar
  85. 85.
    Nishimori S, Tanaka Y, Chiba T, et al. (2001) Smad-mediated transcription is required for transforming growth factor-beta 1-induced p57(Kip2) proteolysis in osteoblastic cells. J Biol Chem 276:10700–10705. doi:10.1074/jbc.M007499200 CrossRefPubMedGoogle Scholar
  86. 86.
    El-Deiry WS, Tokino T, Velculescu VE, et al. (1993) WAF1, a potential mediator of p53 tumor suppression. Cell 75:817–825. doi:10.1016/0092-8674(93)90500-P CrossRefPubMedGoogle Scholar
  87. 87.
    Vuong L, Conley SM, Al-Ubaidi MR (2012) Expression and role of p53 in the retina. Invest Ophthalmol Vis Sci 53:1362–1371. doi:10.1167/iovs.11-8909 CrossRefPubMedGoogle Scholar
  88. 88.
    Das G, Choi Y, Sicinski P, Levine EM (2009) Cyclin D1 fine-tunes the neurogenic output of embryonic retinal progenitor cells. Neural Dev 4:15. doi:10.1186/1749-8104-4-15 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Luana de Almeida-Pereira
    • 1
  • Camila Feitosa Magalhães
    • 1
  • Marinna Garcia Repossi
    • 1
  • Maria Luiza Prates Thorstenberg
    • 2
  • Alfred Sholl-Franco
    • 2
  • Robson Coutinho-Silva
    • 2
  • Ana Lucia Marques Ventura
    • 1
  • Lucianne Fragel-Madeira
    • 1
    • 3
  1. 1.Department of Neurobiology, Institute of BiologyFluminense Federal UniversityNiteróiBrazil
  2. 2.Institute of Biophysics Carlos Chagas FilhoFederal University of Rio de JaneiroRio de JaneiroBrazil
  3. 3.Laboratório de Desenvolvimento e Regeneração Neural, Departmento de NeurobiologiaUniversidade Federal FluminenseNiteróiBrazil

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