Distribution of Transglutaminase in Pear Pollen Tubes in Relation to Cytoskeleton and Membrane Dynamics1[W]

Distribution of a cell wall enzyme in pollen depends both on actin filaments and membrane trafficking. Transglutaminases (TGases) are ubiquitous enzymes that take part in a variety of cellular functions. In the pollen tube, cytoplasmic TGases are likely to be involved in the incorporation of primary amines at selected peptide-bound glutamine residues of cytosolic proteins (including actin and tubulin), while cell wall-associated TGases are believed to regulate pollen tube growth. Using immunological probes, we identified TGases associated with different subcellular compartments (cytosol, membranes, and cell walls). Binding of cytosolic TGase to actin filaments was shown to be Ca2+ dependent. The membrane TGase is likely associated with both Golgi-derived structures and the plasma membrane, suggesting a Golgi-based exocytotic delivery of TGase. Association of TGase with the plasma membrane was also confirmed by immunogold transmission electron microscopy. Immunolocalization of TGase indicated that the enzyme was present in the growing region of pollen tubes and that the enzyme colocalizes with cell wall markers. Bidimensional electrophoresis indicated that different TGase isoforms were present in distinct subcellular compartments, suggesting either different roles or different regulatory mechanisms of enzyme activity. The application of specific inhibitors showed that the distribution of TGase in different subcellular compartments was regulated by both membrane dynamics and cytoskeleton integrity, suggesting that delivery of TGase to the cell wall requires the transport of membranes along cytoskeleton filaments. Taken together, these data indicate that a cytoplasmic TGase interacts with the cytoskeleton, while a different TGase isoform, probably delivered via a membrane/cytoskeleton-based transport system, is secreted in the cell wall of pear (Pyrus communis) pollen tubes, where it might play a role in the regulation of apical growth.

[1]  R. Casadio,et al.  Expression of different forms of transglutaminases by immature cells of Helianthus tuberosus sprout apices , 2012, Amino Acids.

[2]  Tadashi Suzuki,et al.  A plant peptide: N-glycanase orthologue facilitates glycoprotein ER-associated degradation in yeast. , 2012, Biochimica et biophysica acta.

[3]  K. Ha,et al.  Transglutaminase 2 Promotes Both Caspase-dependent and Caspase-independent Apoptotic Cell Death via the Calpain/Bax Protein Signaling Pathway* , 2012, The Journal of Biological Chemistry.

[4]  Caleb M. Rounds,et al.  Calcium entry into pollen tubes. , 2012, Trends in plant science.

[5]  G. Pagliarani,et al.  Simulated environmental criticalities affect transglutaminase of Malus and Corylus pollens having different allergenic potential , 2012, Amino Acids.

[6]  L. Fésüs,et al.  Protein transamidation by transglutaminase 2 in cells: a disputed Ca2+‐dependent action of a multifunctional protein , 2011, The FEBS journal.

[7]  G. Distefano,et al.  Polyamines and transglutaminase activity are involved in compatible and self-incompatible pollination of Citrus grandis , 2011, Amino Acids.

[8]  W. Baumgartner,et al.  Beta-Actin is a Target for Transglutaminase Activity at Synaptic Endings in Chicken Telencephalic Cell Cultures , 2011, Journal of Molecular Neuroscience.

[9]  Teun Munnik,et al.  Understanding pollen tube growth: the hydrodynamic model versus the cell wall model. , 2011, Trends in plant science.

[10]  N. Chabot,et al.  Plasma Membrane Factor XIIIA Transglutaminase Activity Regulates Osteoblast Matrix Secretion and Deposition by Affecting Microtubule Dynamics , 2011, PloS one.

[11]  A. Emons,et al.  Distribution of Callose Synthase, Cellulose Synthase, and Sucrose Synthase in Tobacco Pollen Tube Is Controlled in Dissimilar Ways by Actin Filaments and Microtubules1[W] , 2010, Plant Physiology.

[12]  Y. Stierhof,et al.  Regulated trafficking of cellulose synthases. , 2010, Current opinion in plant biology.

[13]  C. Faleri,et al.  An extracellular transglutaminase is required for apple pollen tube growth. , 2010, The Biochemical journal.

[14]  Natalie S. Poulter,et al.  Regulation of actin dynamics by actin-binding proteins in pollen. , 2010, Journal of experimental botany.

[15]  K. Ha,et al.  Transglutaminase 2: a multi-functional protein in multiple subcellular compartments , 2010, Amino Acids.

[16]  G. Cai,et al.  Compatible and self-incompatible pollination in Pyrus communis displays different polyamine levels and transglutaminase activity , 2010, Amino Acids.

[17]  Anja Geitmann,et al.  Microfilament orientation constrains vesicle flow and spatial distribution in growing pollen tubes. , 2009, Biophysical journal.

[18]  P. Matarrese,et al.  The adenine nucleotide translocator 1 acts as a type 2 transglutaminase substrate: implications for mitochondrial-dependent apoptosis , 2009, Cell Death and Differentiation.

[19]  K. Matsuoka,et al.  A Mobile Secretory Vesicle Cluster Involved in Mass Transport from the Golgi to the Plant Cell Exterior[W][OA] , 2009, The Plant Cell Online.

[20]  G. Cai,et al.  Effects of post-translational modifications catalysed by pollen transglutaminase on the functional properties of microtubules and actin filaments. , 2009, The Biochemical journal.

[21]  G. Cai,et al.  Changes in the accumulation of α- and β-tubulin during bud development in Vitis vinifera L. , 2009, Planta.

[22]  M. Piacentini,et al.  An overview of the first 50 years of transglutaminase research , 2009, Amino Acids.

[23]  Zhenbiao Yang,et al.  Tip growth: signaling in the apical dome. , 2008, Current opinion in plant biology.

[24]  Kirby N. Swatek,et al.  Pollen Proteins Bind to the C-terminal Domain of Nicotiana alata Pistil Arabinogalactan Proteins* , 2008, Journal of Biological Chemistry.

[25]  D. Serafini-Fracassini,et al.  Transglutaminases: widespread cross-linking enzymes in plants. , 2008, Annals of botany.

[26]  D. Serafini-Fracassini,et al.  Visualisation of transglutaminase-mediated cross-linking activity in germinating pollen by laser confocal microscopy , 2008 .

[27]  A. Cheung,et al.  Structural and signaling networks for the polar cell growth machinery in pollen tubes. , 2008, Annual review of plant biology.

[28]  C. Faleri,et al.  Sucrose Synthase Is Associated with the Cell Wall of Tobacco Pollen Tubes1[W] , 2008, Plant Physiology.

[29]  T. Munnik,et al.  Vesicle trafficking dynamics and visualization of zones of exocytosis and endocytosis in tobacco pollen tubes. , 2008, Journal of experimental botany.

[30]  J. Rodríguez-León,et al.  Exclusion of a Proton ATPase from the Apical Membrane Is Associated with Cell Polarity and Tip Growth in Nicotiana tabacum Pollen Tubes[W] , 2008, The Plant Cell Online.

[31]  N. Poulter,et al.  Microtubules Are a Target for Self-Incompatibility Signaling in Papaver Pollen1 , 2008, Plant Physiology.

[32]  J. Kunkel,et al.  Pollen Tube Growth Oscillations and Intracellular Calcium Levels Are Reversibly Modulated by Actin Polymerization1[OA] , 2008, Plant Physiology.

[33]  S. Sansavini,et al.  Pollen Transglutaminase in Pear Self Incompatibility and Relationships with S-RNases and S-Allele Variability. , 2008 .

[34]  Shaoling Zhang,et al.  Pyrus pyrifolia stylar S-RNase induces alterations in the actin cytoskeleton in self-pollen and tubes in vitro , 2007, Protoplasma.

[35]  P. Torrigiani,et al.  Transglutaminase activity changes during the hypersensitive reaction, a typical defense response of tobacco NN plants to TMV. , 2007, Physiologia plantarum.

[36]  I. Mikhailenko,et al.  Cell-surface transglutaminase undergoes internalization and lysosomal degradation: an essential role for LRP1 , 2007, Journal of Cell Science.

[37]  F. De Filippis,et al.  The Acropetal Wave of Developmental Cell Death of Tobacco Corolla Is Preceded by Activation of Transglutaminase in Different Cell Compartments1[C][W] , 2007, Plant Physiology.

[38]  S. Gilroy,et al.  Petunia Phospholipase C1 Is Involved in Pollen Tube Growth[W] , 2006, The Plant Cell Online.

[39]  K. Mehta,et al.  Tissue transglutaminase: from biological glue to cell survival cues. , 2006, Frontiers in bioscience : a journal and virtual library.

[40]  F. Baluška,et al.  Effects of Brefeldin A on Pollen Germination and Tube Growth. Antagonistic Effects on Endocytosis and Secretion1[W] , 2005, Plant Physiology.

[41]  F. Dupont,et al.  Sequential extraction and quantitative recovery of gliadins, glutenins, and other proteins from small samples of wheat flour. , 2005, Journal of agricultural and food chemistry.

[42]  A. Geitmann,et al.  Immunogold localization of arabinogalactan proteins, unesterified and esterified pectins in pollen grains and pollen tubes ofNicotiana tabacum L. , 1995, Protoplasma.

[43]  D. Serafini-Fracassini,et al.  Transglutaminases of higher, lower plants and fungi. , 2005, Progress in experimental tumor research.

[44]  T. Baskin,et al.  Enhanced fixation reveals the apical cortical fringe of actin filaments as a consistent feature of the pollen tube , 2005, Planta.

[45]  D. Caparros-Ruiz,et al.  AtPng1p. The First Plant Transglutaminase , 2004 .

[46]  A. Trewavas,et al.  Pollen tubes exhibit regular periodic membrane trafficking events in the absence of apical extension , 2003, Journal of Cell Science.

[47]  Rita Casadio,et al.  Transglutaminases: nature's biological glues. , 2002, The Biochemical journal.

[48]  C. Ritzenthaler,et al.  Brefeldin A: Deciphering an Enigmatic Inhibitor of Secretion , 2002, Plant Physiology.

[49]  J. Mollet,et al.  Arabinogalactan proteins, pollen tube growth, and the reversible effects of Yariv phenylglycoside , 2002, Protoplasma.

[50]  L. Vidali,et al.  Actin polymerization is essential for pollen tube growth. , 2001, Molecular biology of the cell.

[51]  K. Baek,et al.  Phospholipase Cδ1 Is a Guanine Nucleotide Exchanging Factor for Transglutaminase II (Gαh) and Promotes α1B-Adrenoreceptor-mediated GTP Binding and Intracellular Calcium Release* , 2001, The Journal of Biological Chemistry.

[52]  K. Baek,et al.  Phospholipase Cdelta1 is a guanine nucleotide exchanging factor for transglutaminase II (Galpha h) and promotes alpha 1B-adrenoreceptor-mediated GTP binding and intracellular calcium release. , 2001, The Journal of biological chemistry.

[53]  H. Qian,et al.  Integrin-like proteins in the pollen tube: detection, localization and function. , 2000, Plant & cell physiology.

[54]  E. Nothnagel,et al.  The multiple roles of arabinogalactan proteins in plant development. , 2000, Plant physiology.

[55]  J. Woessner,et al.  A transglutaminase immunologically related to tissue transglutaminase catalyzes cross-linking of cell wall proteins in Chlamydomonas reinhardtii. , 1999, Plant physiology.

[56]  J. Feijó,et al.  Growing Pollen Tubes Possess a Constitutive Alkaline Band in the Clear Zone and a Growth-dependent Acidic Tip , 1999, The Journal of cell biology.

[57]  M. Piacentini,et al.  Identification of ‘tissue’ transglutaminase binding proteins in neural cells committed to apoptosis , 1999, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[58]  Lilley,et al.  Detection of Ca2+-dependent transglutaminase activity in root and leaf tissue of monocotyledonous and dicotyledonous plants , 1998, Plant physiology.

[59]  C. Bergamini,et al.  Transglutaminase-catalyzed modification of cytoskeletal proteins by polyamines during the germination of Malus domestica pollen , 1997, Sexual Plant Reproduction.

[60]  Tami L. Bach,et al.  Colocalization of tissue transglutaminase and stress fibers in human vascular smooth muscle cells and human umbilical vein endothelial cells. , 1997, Experimental cell research.

[61]  H. Kang,et al.  Purification and properties of transglutaminase from soybean (Glycine max) leaves. , 1996, Biochemical and biophysical research communications.

[62]  D. Serafini-Fracassini,et al.  First evidence for polyamine conjugation mediated by an enzymic activity in plants. , 1988, Plant physiology.

[63]  R. Takashi A novel actin label: a fluorescent probe at glutamine-41 and its consequences. , 1988, Biochemistry.

[64]  N. Bagni,et al.  In vitro interactions between polyamines and pectic substances. , 1987, Biochemical and biophysical research communications.

[65]  R. Wattiaux,et al.  Presence of a transglutaminase activity in rat liver lysosomes. , 1984, European journal of cell biology.

[66]  D. Russell,et al.  Intracellular distribution of transglutaminase activity during rat liver regeneration , 1982, Journal of cellular physiology.

[67]  N. Bagni,et al.  RNA, proteins and polyamines during tube growth in germinating apple pollen. , 1981, Plant physiology.

[68]  W. Kunau,et al.  Degradation of unsaturated fatty acids in peroxisomes. Existence of a 2,4-dienoyl-CoA reductase pathway. , 1981, The Journal of biological chemistry.

[69]  H. Towbin,et al.  Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[70]  P. J. Birckbichler,et al.  Differential transglutaminase distribution in normal rat liver and rat hepatoma. , 1976, Cancer research.

[71]  U. K. Laemmli,et al.  Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4 , 1970, Nature.