Platelet activating factor blocks interkinetic nuclear migration in retinal progenitors through an arrest of the cell cycle at the S/G2 transition

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Fragel Madeira, Lucianne ^a   Meletti, Tamara ^a   Mariante, Rafael M ^a   Monteiro, Robson Q ^a   Einicker Lamas, Marcelo ^a   Bernardo, Robson R ^a   Lopes, Angela H ^a   Linden, Rafael ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

CHECKPOINT KINASE 1; CYCLIN B1; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; THROMBOCYTE ACTIVATING FACTOR; THROMBOCYTE ACTIVATING FACTOR RECEPTOR; FIBRINOGEN RECEPTOR; G PROTEIN COUPLED RECEPTOR; PROTEIN KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE S PHASE; CELL MIGRATION; CELL NUCLEUS; CELL PROLIFERATION; CONTROLLED STUDY; NEWBORN; NONHUMAN; RAT; RETINA DEVELOPMENT; RETINAL STEM CELL; SIGNAL TRANSDUCTION; STEM CELL; ANIMAL; CYTOLOGY; PHYSIOLOGY; RETINA; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CELL NUCLEUS; CELL PROLIFERATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; G2 PHASE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PLATELET ACTIVATING FACTOR; PLATELET MEMBRANE GLYCOPROTEINS; PROTEIN KINASES; RATS; RECEPTORS, G-PROTEIN-COUPLED; RETINA; S PHASE; STEM CELLS;

EID: 79551554497     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016058     Document Type: Article

References (95)

1. Boye E, Skjolberg HC, Grallert B (2009) Checkpoint regulation of DNA replication. Methods Mol Biol 521: 55-70.
2. Ciliberto A, Shah JV (2009) A quantitative systems view of the spindle a sembly checkpoint. EMBO J 28: 2162-2173.
3. Chin CF, Yeong FM (2010) Safeguarding entry into mitosis: the antephase checkpoint. Mol Cell Biol 30: 22-32.
4. Cook JG (2009) Replication licensing and the DNA damage checkpoint. Front Bisci 14: 5013-5030.
5. Chow JP, Siu WY, Ho HT, Ma KH, Ho CC, et al. (2003) Differential contribution of inhibitory phosphorylation of CDC2 and CDK2 for unperturbed cell cycle control and DNA integrity checkpoints. J Biol Chem 278: 40815-40828.
6. Petermann E, Caldecott KW (2006) Evidence that the ATR/Chk1 pathway maintains normal replication fork progression during unperturbed S phase. Cell Cycle 5: 2203-2209.
7. Miyata T (2008) Development of three-dimensional architecture of the neuroepithelium: role of pseudostratification and cellular 'community'. Dev Growth Differ 50(Suppl 1): S105-112.
8. Baye LM, Link BA (2008) Nuclear migration during retinal development. Brain Res 1192: 29-36.
9. Frade JM (2002) Interkinetic nuclear movement in the vertebrate neuroepithelium: encounters with an old acquaintance. Prog Brain Res 136: 67-71.
10. Del Bene F, Wehman AM, Link BA, Baier H (2008) Regulation of neurogenesis by interkinetic nuclear migration through an apical-basal notch gradient. Cell 134: 1055-1065.
11. Latasa MJ, Cisneros E, Frade JM (2009) Cell cycle control of Notch signaling and the functional regionalization of the neuroepithelium during vertebrate neurogenesis. Int J Dev Biol 53: 895-908.
12. Messier PE (1978) Microtubules, interkinetic nuclear migration and neurulation. Experientia 34: 289-296.
13. Carneiro AC, Fragel-Madeira L, Silva-Neto MA, Linden R (2008) A role for CK2 upon interkinetic nuclear migration in the cell cycle of retinal progenitor cells. Dev Neurobiol 68: 620-631.
14. Tsai JW, Chen Y, Kriegstein AR, Vallee RB (2005) LIS1 RNA interference blocks neural stem cell division, morphogenesis, and motility at multiple stages. J Cell Biol 170: 935-945.
15. Xie Z, Moy LY, Sanada K, Zhou Y, Buchman JJ, et al. (2007) Cep120 and TACCs control interkinetic nuclear migration and the neural progenitor pool. Neuron 56: 79-93.
16. Zhang X, Lei K, Yuan X, Wu X, Zhuang Y, et al. (2009) SUN1/2 and Syne/ Nesprin-1/2 complexes connect centrosome to the nucleus during neurogenesis and neuronal migration in mice. Neuron 64: 173-187.
17. Tsai JW, Bremner KH, Vallee RB (2007) Dual subcellular roles for LIS1 and dynein in radial neuronal migration in live brain tissue. Nat Neurosci 10: 970-979.
18. Norden C, Young S, Link BA, Harris WA (2009) Actomyosin is the main driver of interkinetic nuclear migration in the retina. Cell 138: 1195-1208.
19. Schenk J, Wilsch-Brauninger M, Calegari F, Huttner WB (2009) Myosin II is required for interkinetic nuclear migration of neural progenitors. Proc Natl Acad Sci U S A 106: 16487-16492.
20. Pearson RA, Luneborg NL, Becker DL, Mobbs P (2005) Gap junctions modulate interkinetic nuclear movement in retinal progenitor cells. J Neurosci 25: 10803-10814.
21. Liu X, Hashimoto-Torii K, Torii M, Ding C, Rakic P (2010) Gap junctions/ hemichannels modulate interkinetic nuclear migration in the forebrain precursors. J Neurosci 30: 4197-4209.
22. Tsai LH, Gleeson JG (2005) Nucleokinesis in neuronal migration. Neuron 46: 383-388.
23. Morris NR, Efimov VP, Xiang X (1998) Nuclear migration, nucleokinesis and lissencephaly. Trends Cell Biol 8: 467-470.
24. Wynshaw-Boris A, Gambello MJ (2001) LIS1 and dynein motor function in neuronal migration and development. Genes Dev 15: 639-651.
25. Morris NR (2000) Nuclear migration. From fungi to the mammalian brain. J Cell Biol 148: 1097-1101.
26. Gambello MJ, Darling DL, Yingling J, Tanaka T, Gleeson JG, et al. (2003) Multiple dose-dependent effects of Lis1 on cerebral cortical development. J Neurosci 23: 1719-1729.
27. Arai H, Koizumi H, Aoki J, Inoue K (2002) Platelet-activating factor acetylhydrolase (PAF-AH). J Biochem 131: 635-640.
28. Stafforini DM, McIntyre TM, Zimmerman GA, Prescott SM (2003) Plateletactivating factor, a pleiotrophic mediator of physiological and pathological processes. Crit Rev Clin Lab Sci 40: 643-672.
29. Ishii S, Shimizu T (2000) Platelet-activating factor (PAF) receptor and genetically engineered PAF receptor mutant mice. Prog Lipid Res 39: 41-82.
30. Shukla SD (1996) Tyrosine kinase activation by PAF leads to downstream gene expression. Adv Exp Med Biol 416: 153-155.
31. Albrecht U, Abu-Issa R, Ratz B, Hattori M, Aoki J, et al. (1996) Plateletactivating factor acetylhydrolase expression and activity suggest a link between neuronal migration and platelet-activating factor. Dev Biol 180: 579-593.
32. Hirotsune S, Fleck MW, Gambello MJ, Bix GJ, Chen A, et al. (1998) Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat Genet 19: 333-339.
33. Bix GJ, Clark GD (1998) Platelet-activating factor receptor stimulation disrupts neuronal migration in vitro. J Neurosci 18: 307-318.
34. Tokuoka SM, Ishii S, Kawamura N, Satoh M, Shimada A, et al. (2003) Involvement of platelet-activating factor and LIS1 in neuronal migration. Eur J Neurosci 18: 563-570.
35. de Araujo EG, Linden R (1993) Trophic factors produced by retinal cells increase the survival of retinal ganglion cells in vitro. Eur J Neurosci 5: 1181-1188.
36. Alexiades MR, Cepko C (1996) Quantitative analysis of proliferation and cell cycle length during development of the rat retina. Dev Dyn 205: 293-307.
37. Dover R, Patel K (1994) Improved methodology for detecting bromodeoxyuridine in cultured cells and tissue sections by immunocytochemistry. Histochemistry 102: 383-387.
38. Campos CB, Bedard PA, Linden R (2002) Activation of p38 mitogen-activated protein kinase during normal mitosis in the developing retina. Neuroscience 112: 583-591.
39. Hayes NL, Nowakowski RS (2000) Exploiting the dynamics of S-phase tracers in developing brain: interkinetic nuclear migration for cells entering versus leaving the S-phase. Dev Neurosci 22: 44-55.
40. Yavin E, Zutra A (1977) Separation and analysis of 32P-labeled phospholipids by a simple and rapid thin-layer chromatographic procedure and its application to cultured neuroblastoma cells. Anal Biochem 80: 430-437.
41. Sambasivarao K, McCluer RH (1963) Thin-Layer Chromatographic Separation of Sphingosine and Related Bases. J Lipid Res 4: 106-108.
42. Kubrusly RC, Panizzutti R, Gardino PF, Stutz B, Reis RA, et al. (2008) Expression of functional dopaminergic phenotype in purified cultured Muller cells from vertebrate retina. Neurochem Int 53: 63-70.
43. Monteiro RQ, Carlini CR, Guimaraes JA, Bon C, Zingali RB (1997) Distinct bothrojaracin isoforms produced by individual jararaca (Bothrops jararaca) snakes. Toxicon 35: 649-657.
44. Sarkaria JN, Busby EC, Tibbetts RS, Roos P, Taya Y, et al. (1999) Inhibition of ATM and ATR kinase activities by the radiosensitizing agent, caffeine. Cancer Res 59: 4375-4382.
45. Linden R, Cavalcante LA, Barradas PC (1986) Mononuclear phagocytes in the retina of developing rats. Histochemistry 85: 335-339.
46. Marrache AM, Gobeil F, Jr., Bernier SG, Stankova J, Rola-Pleszczynski M, et al. (2002) Proinflammatory gene induction by platelet-activating factor mediated via its cognate nuclear receptor. J Immunol 169: 6474-6481.
47. Mazzotti G, Rizzoli R, Galanzi A, Papa S, Vitale M, et al. (1990) Highresolution detection of newly synthesized DNA by anti-bromodeoxyuridine antibodies identifies specific chromatin domains. J Histochem Cytochem 38: 13-22.
48. Grallert B, Boye E (2008) The multiple facets of the intra-S checkpoint. Cell Cycle 7: 2315-2320.
49. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA doublestranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868.
50. Nojima H (2006) Protein kinases that regulate chromosome stability and their downstream targets. Genome Dyn 1: 131-148.
51. Tarricone C, Perrina F, Monzani S, Massimiliano L, Kim MH, et al. (2004) Coupling PAF signaling to dynein regulation: structure of LIS1 in complex with PAF-acetylhydrolase. Neuron 44: 809-821.
52. Han G, Liu B, Zhang J, Zuo W, Morris NR, et al. (2001) The Aspergillus cytoplasmic dynein heavy chain and NUDF localize to microtubule ends and affect microtubule dynamics. Curr Biol 11: 719-724.
53. Zhuang SH, Hung YE, Hung L, Robey RW, Sackett DL, et al. (2007) Evidence for microtubule target engagement in tumors of patients receiving ixabepilone. Clin Cancer Res 13: 7480-7486.
54. Yamada M, Toba S, Yoshida Y, Haratani K, Mori D, et al. (2008) LIS1 and NDEL1 coordinate the plus-end-directed transport of cytoplasmic dynein. EMBO J 27: 2471-2483.
55. Stark GR, Taylor WR (2006) Control of the G2/M transition. Mol Biotechnol 32: 227-248.
56. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, 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: 348-360.
57. Callegari AJ, Kelly TJ (2006) UV irradiation induces a postreplication DNA damage checkpoint. Proc Natl Acad Sci U S A 103: 15877-15882.
58. Faretta M, Bergamaschi D, Taverna S, Ronzoni S, Pantarotto M, et al. (1998) Characterization of cyclin B1 expression in human cancer cell lines by a new three-parameter BrdUrd/cyclin B1/DNA analysis. Cytometry 31: 53-59.
59. Fung TK, Poon RY (2005) A roller coaster ride with the mitotic cyclins. Semin Cell Dev Biol 16: 335-342.
60. Francis D (2008) The G2/M transition in eukaryotes. SEB Exp Biol Ser 59: 81-98.
61. Cerella C, Scherer C, Cristofanon S, Henry E, Anwar A, et al. (2009) Cell cycle arrest in early mitosis and induction of caspase-dependent apoptosis in U937 cells by diallyltetrasulfide (Al2S4). Apoptosis 14: 641-654.
62. Bort R, Signore M, Tremblay K, Martinez Barbera JP, Zaret KS (2006) Hex homeobox gene controls the transition of the endoderm to a pseudostratified, cell emergent epithelium for liver bud development. Dev Biol 290: 44-56.
63. Marques M, Pei Y, Southall MD, Johnston JM, Arai H, et al. (2002) Identification of platelet-activating factor acetylhydrolase II in human skin. J Invest Dermatol 119: 913-919.
64. Wang H, Chakrabarty S (2003) Platelet-activating factor activates mitogenactivated protein kinases, inhibits proliferation, induces differentiation and suppresses the malignant phenotype of human colon carcinoma cells. Oncogene 22: 2186-2191.
65. Bulavin DV, Amundson SA, Fornace AJ (2002) p38 and Chk1 kinases: different conductors for the G(2)/M checkpoint symphony. Curr Opin Genet Dev 12: 92-97.
66. Shiromizu T, Goto H, Tomono Y, Bartek J, Totsukawa G, et al. (2006) Regulation of mitotic function of Chk1 through phosphorylation at novel sites by cyclin-dependent kinase 1 (Cdk1). Genes Cells 11: 477-485.
67. Chou YH, Ho YS, Wu CC, Chai CY, Chen SC, et al. (2007) Tubulozoleinduced G2/M cell cycle arrest in human colon cancer cells through formation of microtubule polymerization mediated by ERK1/2 and Chk1 kinase activation. Food Chem Toxicol 45: 1356-1367.
68. Mogila V, Xia F, Li WX (2006) An intrinsic cell cycle checkpoint pathway mediated by MEK and ERK in Drosophila. Dev Cell 11: 575-582.
69. Stracker TH, Usui T, Petrini JH (2009) Taking the time to make important decisions: the checkpoint effector kinases Chk1 and Chk2 and the DNA damage response. DNA Repair (Amst) 8: 1047-1054.
70. Martins MA, Silva PM, Castro HC, Neto F, Lima MC, et al. (1987) Interactions between local inflammatory and systemic haematological effects of PAF-acether in the rat. Eur J Pharmacol 136: 353-360.
71. Castro-Faria-Neto HC, Silva PM, Martins MA, Silva PS, Henriques MG, et al. (1990) Pharmacological modulation of 2-methyl-carbamate-PAF induced rat paw oedema. J Pharm Pharmacol 42: 203-204.
72. Vasquez-Bravo YL, Russo M, Jancar S (1993) Differential sensitivity of mouse strains to platelet activating factor-induced vasopermeability and mortality: effect of antagonists. J Lipid Mediat 8: 135-144.
73. McCormick C, Jones RL, Kennedy S, Wadsworth RM (2010) Activation of prostanoid EP receptors by prostacyclin analogues in rabbit iliac artery: implications for anti-restenotic potential. Eur J Pharmacol 641: 160-167.
74. Weltzin MM, Schulte MK (2010) Pharmacological characterization of the allosteric modulator desformylflustrabromine and its interaction with alpha4- beta2 neuronal nicotinic acetylcholine receptor orthosteric ligands. J Pharmacol Exp Ther 334: 917-926.
75. Panaro MA, Cianciulli A, Acquafredda A, Lisi S, Mitolo CI, et al. (2007) Modeling of granulocyte cytoskeletal responses following fMLP challenging. Immunopharmacol Immunotoxicol 29: 201-224.
76. Kanno T, Suga S, Nakano K, Kamimura N, Wakui M (1999) Corticotropinreleasing factor modulation of Ca2+ influx in rat pancreatic beta-cells. Diabetes 48: 1741-1746.
77. Qiu J, Wang P, Jing Q, Zhang W, Li X, et al. (2001) Rapid activation of ERK1/ 2 mitogen-activated protein kinase by corticosterone in PC12 cells. Biochem Biophys Res Commun 287: 1017-1024.
78. Moriguchi S, Shioda N, Han F, Yeh JZ, Narahashi T, et al. (2009) Galantamine enhancement of long-term potentiation is mediated by calcium/calmodulindependent protein kinase II and protein kinase C activation. Hippocampus 19: 844-854.
79. Beauchamp MH, Marrache AM, Hou X, Gobeil F, Jr., Bernier SG, et al. (2002) Platelet-activating factor in vasoobliteration of oxygen-induced retinopathy. Invest Ophthalmol Vis Sci 43: 3327-3337.
80. Bussolino F, Gremo F, Tetta C, Pescarmona GP, Camussi G (1986) Production of platelet-activating factor by chick retina. J Biol Chem 261: 16502-16508.
81. Yousufzai SY, Abdel-Latif AA (1985) Effects of platelet-activating factor on the release of arachidonic acid and prostaglandins by rabbit iris smooth muscle. Inhibition by calcium channel antagonists. Biochem J 228: 697-706.
82. Janero DR, Burghardt B, Burghardt C (1988) Specific binding of 1-O-alkyl-2- acetyl-sn-glycero-3-phosphocholine (platelet-activating factor) to the intact canine platelet. Thromb Res 50: 789-802.
83. Chew LJ, King WC, Kennedy A, Gallo V (2005) Interferon-gamma inhibits cell cycle exit in differentiating oligodendrocyte progenitor cells. Glia 52: 127-143.
84. Oshima K, Teo DT, Senn P, Starlinger V, Heller S (2007) LIF promotes neurogenesis and maintains neural precursors in cell populations derived from spiral ganglion stem cells. BMC Dev Biol 7: 112.
85. Wu Y, Peng H, Cui M, Whitney NP, Huang Y, et al. (2009) CXCL12 increases human neural progenitor cell proliferation through Akt-1/FOXO3a signaling pathway. J Neurochem 109: 1157-1167.
86. Hume DA, Perry VH, Gordon S (1983) Immunohistochemical localization of a macrophage-specific antigen in developing mouse retina: phagocytosis of dying neurons and differentiation of microglial cells to form a regular array in the plexiform layers. J Cell Biol 97: 253-257.
87. Nakayama R, Udagawa H, Kumagai H (1997) Changes in PAF (plateletactivating factor) production during cell cycle of yeast Saccharomyces cerevisiae. Biosci Biotechnol Biochem 61: 631-635.
88. Boije H, Edqvist PH, Hallbook F (2009) Horizontal cell progenitors arrest in G2- phase and undergo terminal mitosis on the vitreal side of the chick retina. Dev Biol 330: 105-113.
89. Hardy P, Beauchamp M, Sennlaub F, Gobeil F, Jr., Tremblay L, et al. (2005) New insights into the retinal circulation: inflammatory lipid mediators in ischemic retinopathy. Prostaglandins Leukot Essent Fatty Acids 72: 301-325.
90. Bazan NG (2007) Omega-3 fatty acids, pro-inflammatory signaling and neuroprotection. Curr Opin Clin Nutr Metab Care 10: 136-141.
91. Rotstein NP, Miranda GE, Abrahan CE, German OL (2010) Regulating survival and development in the retina: key roles for simple sphingolipids. J Lipid Res 51: 1247-1262.
92. Nelson RJ, Young KA (1998) Behavior in mice with targeted disruption of single genes. Neurosci Biobehav Rev 22: 453-462.
93. Satyanarayana A, Kaldis P (2009) Mammalian cell-cycle regulation: several Cdks, numerous cyclins and diverse compensatory mechanisms. Oncogene 28: 2925-2939.
94. Matzinger P (2002) The danger model: a renewed sense of self. Science 296: 301-305.
95. Hardy P, Beauchamp M, Sennlaub F, Gobeil F, Jr., Mwaikambo B, et al. (2005) Inflammatory lipid mediators in ischemic retinopathy. Pharmacol Rep 57(Suppl): 169-190.