Cell proliferation is a crucial cellular process which influences development. In plants, meristems are formed by actively proliferating cells, in which the main expression of proliferation is the existence of a cell division cycle. Many cell activities are influenced by the cell proliferation status and cell cycle progression, among them ribosome biogenesis, which is morphologically expressed as the nucleolus. The connection is established through nucleolar proteins, which regulate the synthesis and processing of preribosomal precursors and, at the same time, are targets of various cell cycle regulators, such as certain kinases. Nucleolin is one of these nucleolar proteins, whose level increases with cell proliferation and depends on the cell cycle stages. Not only the levels, but also other important features of the protein, such as its distribution in situ in the nucleolus, its phosphorylation and its physiological degradation, depend on these parameters. Furthermore, since the nucleolar structure is highly sensitive to functional variations, distinct nucleolar structures, regarding the nucleolar size and the distribution of nucleolar subcomponents, have been defined for each period of the cell cycle, using synchronized cells. In addition to increasing our knowledge of cellular physiology, these relationships can be used to mark the proliferative state of the cell and the periods of cell cycle.
ribosome; cell cycle; nucleolin; fibrillarin; Western blotting; electron microscopy
Beemster GTS, Fiorani F, Inze D: Cell cycle: the key to plant growth control? Trends Plant Sci 8:154-158, 2003.
Bogre L, Jonak C, Mink M et al.: Developmental and cell cycle regulation of alfalfa nucMs1, a plant homolog of the yeast Nsr1 and mammalian nucleolin. Plant Cell 8:417-428, 1996.
Bouche G, Caizergues-Ferrer M, Bugler B, Amalric F: Interrelations between the maturation of a 100 KDa nucleolar protein and pre-rRNA synthesis in CHO cells. Nucl Acids Res 12:3025-3035, 1984.
Bugler B, Caizergues-Ferrer M, Bouche G, Bourbon HM, Amalric F: Detection and localization of a class of proteins immunologically related to a 100-KDa nucleolar protein. Eur J Biochem 128:475-480, 1982.
Busch H, Ballal NR, Rao MRS, Choi YC, Rothblum LI: Factors affecting nucleolar rDNA readouts. In Busch H (ed.): The Cell Nucleus, vol. 5, Chromatin, part B. Academic Press, New York, San Francisco, London 1978, pp. 416-468.
Cerdido A, Medina FJ: Subnucleolar location of fibrillarin and variation in its levels during the cell cycle and during differentiation of plant cells. Chromosoma 103:625-634, 1995.
De Carcer G, Cerdido A, Medina FJ: NopA64, a novel nucleolar phosphoprotein from proliferating onion cells, sharing immunological determinants with mammalian nucleolin. Planta 201:487-495, 1997.
Dolan L, Janmaat K, Willemsen V et al.: Cellular organisation of the Arabidopsis thaliana root. Development 119:71-84, 1993.
Doree M, Galas S: The cyclin-dependent protein kinases and the control of cell division. FASEB J 8:1114-1121, 1994.
Fang SH, Yeh NH: The self-cleaving activity of nucleolin determines its molecular dynamics in relation to cell proliferation. Exp Cell Res 208:48-53, 1993.
Ginisty H, Sicard H, Roger B, Bouvet P: Structure and functions of nucleolin. J Cell Sci 112:761-772, 1999.
Gonzalez-Camacho F, Medina FJ: Identification of specific plant nucleolar phosphoproteins in a functional proteomic analysis. Proteomics 4:407-417, 2004.
Guiltinan MJ, Schelling ME, Ehtesham NZ, Thomas JC, Christensen ME: The nucleolar RNA binding protein B-36 is highly conserved among plants. Eur J Cell Biol 46:547-553, 1988.
Gutierrez C: Coupling cell proliferation and development in plants. Nature Cell Biol 7:535-541, 2005.
Hernandez-Verdun D, Roussel P: Regulators of nucleolar functions. Prog Cell Cycle Res 5:301-308, 2003.
Jimenez-Garcia LF, Rothblum LI, Busch H, Ochs RL: Nucleologenesis: use of nonisotopic "in situ" hybridization and immunocytochemistry to compare the localization of rDNA and nucleolar proteins during mitosis. Biol Cell 65:239-246, 1989.
Jordan EG, McGovern JH: The quantitative relationship of the fibrillar centres and other nucleolar components to changes in growth conditions, serum deprivation and low doses of actinomycin D in cultured diploid human fibroblasts (strain MRC-5). J Cell Sci 52:373-389, 1981.
Junera HR, Masson C, Geraud G, Hernandez-Verdun D: The three-dimensional organization of ribosomal genes and the architecture of the nucleoli vary with G1, S and G2 phases. J Cell Sci 108:3427-3441, 1995.
Klein J, Grummt I: Cell cycle-dependent regulation of RNA polymerase I transcription: the nucleolar transcription factor UBF is inactive in mitosis and early G1. Proc Natl Acad Sci USA 96:6096-6101, 1999.
Kwiatkowska M, Maszewski J: Changes in the activity of RNA polymerase detected in situ and the intensity of 3H uridine incorporation into the nucleolus and the nucleus of interphase cells in antheridial filaments of Chara vulgaris L. Folia Histochem. Cytochem 17:275-286, 1979.
Medina FJ, Risueno MC, Moreno Diaz de la Espina S: 3-D Reconstruction and morphometry of fibrillar centres in plant cells in relation to nucleolar activity. Biol Cell 48:31-38, 1983.
Medina FJ, Cerdido A, Fernandez-Gomez ME: Components of the nucleolar processing complex (pre-rRNA, fibrillarin and nucleolin) colocalize during mitosis and are incorporated to daughter cell nucleoli. Exp Cell Res 221:111-125, 1995.
Medina FJ, Cerdido A, De Carcer G: The functional organization of the nucleolus in proliferating plant cells. Eur J Histochem 44:117-131, 2000.
Medina FJ, Gonzalez-Camacho F, Cerdido A, De Carcer G: In situ localization of the onion nucleolar protein NopA64 is dependent on cell proliferation mechanisms and cell cycle phases. In Dini L and Catalano M (eds.): Proc. 5th Multinational Congress on Electron Microscopy. Rinton Press Inc., Princeton, New Jersey. 2001, pp. 197-207.
Medina FJ, Gonzalez-Camacho F: Nucleolar proteins and cell proliferation in plant cells. Recent Res Devel Plant Biol 3:55-68, 2003.
Moreno Diaz de la Espina S, Medina FJ, Risueno MC.: Correlation of nucleolar activity and nucleolar vacuolation in plant cells. Eur J Cell Biol 22:724-729, 1980.
Ochs RL, Lischwe MA, O'Leary P, Busch H: Localization of nucleolar phosphoproteins B23 and C23 during mitosis. Exp Cell Res 146:139-149, 1983.
Olson MOJ: The role of proteins in nucleolar structure and function. In Strauss PR and Wilson SH (eds.): The Eukaryotic Nucleus. Molecular Biochemistry and Macromolecular Assemblies. The Telford Press, Caldwell, New Jersey 1991, pp. 519-559.
Pih KT, Yi MJ, Liang YS et al.: Molecular cloning and targeting of a fibrillarin homolog from Arabidopsis. Plant Physiol 123:51-58, 2000.
Reichler SA, Balk J, Brown ME et al.: Light differentially regulates cell division and the mRNA abundance of pea nucleolin during de-etiolation. Plant Physiol 125:339-350, 2001.
Riera M, Peracchia G, Pages M: Distinctive features of plant protein kinase CK2. Mol Cell Biochem 227:119-127, 2001.
Risueno MC, Medina FJ: The nucleolar structure in plant cells. Cell Biol Rews (RBC) 7:1-154, 1986.
Risueno MC, Medina FJ, Moreno Diaz de la Espina S: Nucleolar fibrillar centres in plant meristematic cells: ultrastructure, cytochemistry and autoradiography. J Cell Sci 58:313-329, 1982.
Sirri V, Roussel P, Gendron MC, Hernandez-Verdun D: Amount of the two major AgNOR proteins, nucleolin and protein B23 is cellcycle dependent. Cytometry 28:147-156, 1997.
Srivastava M, Pollard HB: Molecular dissection of nucleolin's role in growth and cell proliferation: new insights. FASEB J 13:1911-1922, 1999.
Tuteja R, Tuteja N: Nucleolin: a multifunctional major nucleolar protein. CRC Crit. Rev Biochem Mol Biol 33:407-436, 1998.
Volkov RA, Medina FJ, Zentgraf U, Hemleben V: Organization and molecular evolution of rDNA, nucleolar dominance, and nucleolus structure. Prog Botany 65:106-146, 2004.
Stepinski D: Immunodetection of nucleolar proteins and ultrastructure of nucleoli of soybean root meristematic cells treated with chilling stress and after recovery. Protoplasma 235:77-89, 2009.
Matia I, Van Loon JWA, Carnero-Diaz E, Marco R, Medina FJ: Seed germination and seedling growth under simulated microgravity causes alterations in plant cell proliferation and ribosome biogenesis. Microgravity Sci Technol 21:169-174, 2009.