دورية أكاديمية

Cell cycle regulation by ADP and IGF-1 in cultured late developing glia progenitors of the avian retina.

التفاصيل البيبلوغرافية
العنوان: Cell cycle regulation by ADP and IGF-1 in cultured late developing glia progenitors of the avian retina.
المؤلفون: Ornelas IM; Department of Physiological Sciences, Federal University of Espírito Santo, Vitória, Espírito Santo, 29047-105, Brazil., Silva TM; Department of Neurobiology, Neuroscience Program, Federal Fluminense University, Rua Prof. M.W. de Freitas Reis, bloco M, sala 409, São Domingos, Niterói, Rio de Janeiro, CEP 24210-201, Brazil., Pereira MR; Department of Neurobiology, Neuroscience Program, Federal Fluminense University, Rua Prof. M.W. de Freitas Reis, bloco M, sala 409, São Domingos, Niterói, Rio de Janeiro, CEP 24210-201, Brazil., França GR; Department of Physiological Sciences, Federal University of the State of Rio de Janeiro, Rua Frei Caneca 94, Centro, Rio de Janeiro, RJ, CEP 20211-040, Brazil., Ventura ALM; Department of Neurobiology, Neuroscience Program, Federal Fluminense University, Rua Prof. M.W. de Freitas Reis, bloco M, sala 409, São Domingos, Niterói, Rio de Janeiro, CEP 24210-201, Brazil. almvuff@gmail.com.
المصدر: Purinergic signalling [Purinergic Signal] 2023 Dec 27. Date of Electronic Publication: 2023 Dec 27.
Publication Model: Ahead of Print
نوع المنشور: Journal Article
اللغة: English
بيانات الدورية: Publisher: Springer Country of Publication: Netherlands NLM ID: 101250499 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1573-9546 (Electronic) Linking ISSN: 15739538 NLM ISO Abbreviation: Purinergic Signal Subsets: MEDLINE
أسماء مطبوعة: Original Publication: Dordrecht, the Netherlands : Springer
مستخلص: In the avian retina, ADP induces the proliferation of late developing glia progenitors. Here, we show that in serum-containing retinal cell cultures, ADP-induced increase in [ 3 H]-thymidine incorporation can be prevented by the IGF-1 receptor antagonists AG1024 and I-OMe-Tyrphostin AG 538, suggesting the participation of IGF-1 in ADP-mediated progenitor proliferation. In contrast, no increase in [ 3 H]-thymidine incorporation is observed in retinal cultures treated only with IGF-1. Under serum starvation, while no increase in cell proliferation is detected in cultures treated only with ADP or IGF-1, a significant increase in [ 3 H]-thymidine incorporation and number of PCNA expressing cells is observed in cultures treated concomitantly with ADP plus IGF-1, suggesting that both molecules are required to induce proliferation of retinal progenitors. In serum-starved cultures, although an increase in cell viability is detected by MTT assays in IGF-1-treated cultures, no significant increase in viability of [ 3 H]-thymidine labeled progenitors is observed, suggesting that IGF-1 may contribute to survival of postmitotic cells in culture. While only ADP increases intracellular calcium, only IGF-1 induces the phosphorylation of Akt in the retinal cultures. IGF-1 through the PI3K/Akt pathway induces a significant increase in the transcription and expression of CDK1 with a decrease in phospho-histone H3 expression that is concomitant with an increase in the expression of cyclins D1 and E and CDK2. These findings suggest that IGF-1 stimulates CDK-1 mRNA and protein expression that enable progenitors to progress through the cell cycle. However, signaling of ADP in the presence IGF-I seems to be required for DNA synthesis.
(© 2023. The Author(s), under exclusive licence to Springer Nature B.V.)
References: 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:. https://doi.org/10.1242/dev.01855.
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:. https://doi.org/10.1007/s11302-012-9324-5.
Silva TM, França GR, Ornelas IM, et al (2015) Involvement of nucleotides in glial growth following scratch injury in avian retinal cell monolayer cultures. Purinergic Signal 11:. https://doi.org/10.1007/s11302-015-9444-9.
Sugioka M, Zhou WL, Hofmann HD, Yamashita M (1999) Ca2+ mobilization and capacitative Ca2+ entry regulate DNA synthesis in cultured chick retinal neuroepithelial cells. International Journal of Developmental Neuroscience 17:. https://doi.org/10.1016/S0736-5748(99)00027-1.
Moll V WMMIKHRABA (2002) P2Y receptor-mediated stimulation of Müller glial DNA synthesis. In: Invest Ophthalmol Vis Sci. 2002 Mar;43(3):766–73. PMID: 11867596. https://pubmed.ncbi.nlm.nih.gov/11867596/ . Accessed 14 Aug 2023.
Pearson RA, Catsicas M, Becker DL, et al (2004) Ca2+ signalling and gap junction coupling within and between pigment epithelium and neural retina in the developing chick. European Journal of Neuroscience 19:. https://doi.org/10.1111/j.0953-816X.2004.03338.x.
Milenkovic I, Weick M, Wiedemann P, et al (2003) P2Y receptor-mediated stimulation of Müller glial cell DNA synthesis: Dependence on EGF and PDGF receptor transactivation. Invest Ophthalmol Vis Sci 44:. https://doi.org/10.1167/iovs.02-0260.
Sholl-Franco A, Fragel-Madeira L, Macama A da CC, et al (2010) ATP controls cell cycle and induces proliferation in the mouse developing retina. International Journal of Developmental Neuroscience 28:. https://doi.org/10.1016/j.ijdevneu.2009.09.004.
Sanches G, Alencar LS de, Ventura ALM (2002) ATP induces proliferation of retinal cells in culture via activation of PKC and extracellular signal-regulated kinase cascade. International Journal of Developmental Neuroscience 20:. https://doi.org/10.1016/S0736-5748(02)00004-7.
França GR, Freitas RCC, Ventura ALM (2007) ATP-induced proliferation of developing retinal cells: regulation by factors released from postmitotic cells in culture. International Journal of Developmental Neuroscience 25:. https://doi.org/10.1016/j.ijdevneu.2007.05.006.
Sugioka M, Fukuda Y, Yamashita M (1996) Ca2+ responses to ATP via purinoceptors in the early embryonic chick retina. Journal of Physiology 493:. https://doi.org/10.1113/jphysiol.1996.sp021428.
Nunes PHC, Calaza K da C, 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:. https://doi.org/10.1016/j.ijdevneu.2007.09.007.
Jacques FJ, Silva TM, da Silva FE, et al (2017) Nucleotide P2Y13-stimulated phosphorylation of CREB is required for ADP-induced proliferation of late developing retinal glial progenitors in culture. Cell Signal 35:. https://doi.org/10.1016/j.cellsig.2017.03.019.
Rajala RVS (2010) Phosphoinositide 3-kinase signaling in the vertebrate retina. J Lipid Res 51 https://doi.org/10.1194/jlr.R000232.
Kermer P, Klöcker N, Labes M, Bähr M (2000) Insulin-like growth factor-I protects axotomized rat retinal ganglion cells from secondary death via PI3-K-dependent Akt phosphorylation and inhibition of caspase-3 in vivo. Journal of Neuroscience 20:. https://doi.org/10.1523/jneurosci.20-02-00722.2000.
Yang X, Wei A, Liu Y et al (2013) IGF-1 protects retinal ganglion cells from hypoxia-induced apoptosis by activating the Erk-1/2 and Akt pathways. Mol Vis 19:1901. (PMID: 240494363774573)
Kalluri HSG, Vemuganti R, Dempsey RJ (2007) Mechanism of insulin-like growth factor I-mediated proliferation of adult neural progenitor cells: Role of Akt. European Journal of Neuroscience 25:. https://doi.org/10.1111/j.1460-9568.2007.05336.x.
Cui QL, Almazan G (2007) IGF-I-induced oligodendrocyte progenitor proliferation requires PI3K/Akt, MEK/ERK, and Src-like tyrosine kinases. J Neurochem 100:. https://doi.org/10.1111/j.1471-4159.2006.04329.x.
de Figueiredo CS, Raony Í, Medina SV, et al (2023) Insulin-like growth factor-1 stimulates retinal cell proliferation via activation of multiple signaling pathways. Current Research in Neurobiology 4:. https://doi.org/10.1016/j.crneur.2022.100068.
Bassnett S, Beebe DC (1990) Localization of insulin-like growth factor-1 binding sites in the embryonic chicken eye. In: Invest Ophthalmol Vis Sci . https://pubmed.ncbi.nlm.nih.gov/2167301/ . Accessed 14 Aug 2023.
Waldbillig RJ, Arnold DR, Fletcher RT, Chader GJ (1991) Insulin and IGF-I binding in developing chick neural retina and pigment epithelium: A characterization of binding and structural differences. Exp Eye Res 53:. https://doi.org/10.1016/0014-4835(91)90139-6.
Hernández-Sánchez C, López-Carranza A, Alarcón C, et al (1995) Autocrine/paracrine role of insulin-related growth factors in neurogenesis: Local expression and effects on cell proliferation and differentiation in retina. Proc Natl Acad Sci U S A 92:. https://doi.org/10.1073/pnas.92.21.9834.
Calvaruso G, Vento R, Giuliano M, et al (1996) Insulin-like growth factors in chick embryo retina during development. Regul Pept 61:. https://doi.org/10.1016/0167-0115(95)00132-8.
Frade JM, Martí E, Bovolenta P, et al (1996) Insulin-like growth factor-I stimulates neurogenesis in chick retina by regulating expression of the α6 integrin subunit. Development 122:. https://doi.org/10.1242/dev.122.8.2497.
Roberts EC, Shapiro PS, Nahreini TS, et al (2002) Distinct Cell Cycle Timing Requirements for Extracellular Signal-Regulated Kinase and Phosphoinositide 3-Kinase Signaling Pathways in Somatic Cell Mitosis. Mol Cell Biol 22:. https://doi.org/10.1128/mcb.22.20.7226-7241.2002.
Shtivelman E, Sussman J, Stokoe D (2002) A role for PI 3-kinase and PKB activity in the G2/M phase of the cell cycle. Current Biol 12:. https://doi.org/10.1016/S0960-9822(02)00843-6.
Ornelas IM, Silva TM, Fragel-Madeira L, Ventura ALM (2013) Inhibition of PI3K/Akt Pathway Impairs G2/M Transition of Cell Cycle in Late Developing Progenitors of the Avian Embryo Retina. PLoS One 8:. https://doi.org/10.1371/journal.pone.0053517.
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:. https://doi.org/10.1016/j.ijdevneu.2010.06.001.
Honegger A, Humbel RE (1986) Insulin-like growth factors I and II in fetal and adult bovine serum. Purification, primary structures, and immunological cross-reactivities. J Biol Chem 261:569–575. https://doi.org/10.1016/S0021-9258(17)36130-6. (PMID: 10.1016/S0021-9258(17)36130-63941093)
Celis JE, Celis A (1985) Cell cycle-dependent variations in the distribution of the nuclear protein cyclin proliferating cell nuclear antigen in cultured cells: Subdivision of S phase. Proc Natl Acad Sci U S A 82:. https://doi.org/10.1073/pnas.82.10.3262.
Barton KM, Levine EM (2008) Expression patterns and cell cycle profiles of PCNA, MCM6, cyclin D1, cyclin A2, cyclin B1, and phosphorylated histone H3 in the developing mouse retina. Developmental Dynamics 237:. https://doi.org/10.1002/dvdy.21449.
Hendzel MJ, Wei Y, Mancini MA, et al (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106:. https://doi.org/10.1007/s004120050256.
Sanches G, Ventura ALM (1998) Inhibition of carbachol-induced inositol phosphate accumulation in the embryonic retina promoted by kainate and veratridine. Brazil J Med Biol Res 31:. https://doi.org/10.1590/S0100-879X1998000700009.
Sugioka M, Yamashita M (2003) Calcium signaling to nucleus via store-operated system during cell cycle in retinal neuroepithelium. Neurosci Res 45:. https://doi.org/10.1016/S0168-0102(03)00004-X.
Seigel GM, Chiu L, Paxhia A (2000) Inhibition of neuroretinal cell death by insulin-like growth factor-1 and its analogs. Mol Vis 6:157–163. (PMID: 10973501)
Politi LE, Rotstein NP, Salvador G, et al (2001) Insulin-like growth factor-I is a potential trophic factor for amacrine cells. J Neurochem 76:. https://doi.org/10.1046/j.1471-4159.2001.00128.x.
Katayama K, Fujita N, Tsuruo T (2005) Akt/Protein Kinase B-Dependent Phosphorylation and Inactivation of WEE1Hu Promote Cell Cycle Progression at G 2 /M Transition . Mol Cell Biol 25:. https://doi.org/10.1128/mcb.25.13.5725-5737.2005.
Okumura E, Fukuhara T, Yoshida H, et al (2002) Akt inhibits Myt1 in the signalling pathway that leads to meiotic G2/M-phase transition. Nat Cell Biol 4:. https://doi.org/10.1038/ncb741.
Surmacz E, Nugent P, Pietrzkowski Z, Baserga R (1992) The role of the IGF1 receptor in the regulation of cdc2 mRNA levels in fibroblasts. Exp Cell Res 199:. https://doi.org/10.1016/0014-4827(92)90435-B.
Kalebic T TMHLJ (1994) In vivo treatment with antibody against IGF-1 receptor suppresses growth of human rhabdomyosarcoma and down-regulates p34cdc2. In: Cancer Res. . https://pubmed.ncbi.nlm.nih.gov/7923191/ . Accessed 14 Aug 2023.
Walker MP, DiAugustine RP, Zeringue E, et al (2010) An IGF1/insulin receptor substrate-1 pathway stimulates a mitotic kinase (cdk1) in the uterine epithelium during the proliferative response to estradiol. J Endocrinol 207:. https://doi.org/10.1677/JOE-10-0102.
Min J, Singh S, Fitzgerald-Bocarsly P, Wood TL (2012) Insulin-like growth factor I regulates G2/M progression through mammalian target of rapamycin signaling in oligodendrocyte progenitors. Glia 60:. https://doi.org/10.1002/glia.22387.
Gurley LR, D’Anna JA, Barham SS, et al (1978) Histone Phosphorylation and Chromatin Structure during Mitosis in Chinese Hamster Cells. Eur J Biochem 84:. https://doi.org/10.1111/j.1432-1033.1978.tb12135.x.
Van Hooser A, Goodrich DW, David Allis C, et al (1998) Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. J Cell Sci 111:. https://doi.org/10.1242/jcs.111.23.3497.
Wieser S, Pines J (2015) The biochemistry of mitosis. Cold Spring Harb Perspect Biol 7:. https://doi.org/10.1101/cshperspect.a015776.
Sherr CJ, Roberts JM (2004) Living with or without cyclins and cyclin-dependent kinases. Genes Dev. 18(22):2699–2711. https://doi.org/10.1101/gad.1256504. (PMID: 10.1101/gad.125650415545627)
معلومات مُعتمدة: CAPES-AUXPE-PNPD2808/2010 Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior; CAPES-AUXPE-PNPD2808/2010 Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior; CAPES-AUXPE-PNPD2808/2010 Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior; FAPERJ- E26-111.327/2013 Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro; CNPq-303018/2016-0 Conselho Nacional de Desenvolvimento Científico e Tecnológico
فهرسة مساهمة: Keywords: Calcium; Cell proliferation; P2Y receptors; PI3K/Akt; Retina development
تواريخ الأحداث: Date Created: 20231227 Latest Revision: 20231227
رمز التحديث: 20231228
DOI: 10.1007/s11302-023-09982-7
PMID: 38151691
قاعدة البيانات: MEDLINE