From signal to cell polarity: mitogen-activated protein kinases as sensors and effectors of cytoskeleton dynamicity.

Mitogen-activated protein kinases (MAPKs) are ubiquitous phosphorylation enzymes involved in signal transduction, gene expression and activation of diverse cytoskeletal proteins. MAPKs participate in the regulation of a broad range of crucial cellular processes including cell survival, division, polarization, stress responses, and metabolism. Phosphorylation of cytoskeletal proteins usually results in the rearrangement of cytoskeletal arrays leading to morphological changes and cell polarization. On the other hand, some cytoskeletal motor proteins, such as kinesins, could activate MAPK members and participate in signal delivery to the proper cellular destination (e.g. during cell division). Moreover, changes in the integrity of cytoskeletal elements have direct impacts on MAPK activity. Recent evidence suggests that there is bi-directional signalling between MAPK cascades and cytoskeleton. The focus here is on this cross-talk between MAPK signalling and the cytoskeleton in various eukaryotic systems including yeast, plants, and mammals and a role is proposed for MAPKs as sensors monitoring the cytoskeleton-dependent balance of forces within the cell.

[1]  K. Mortensen,et al.  Effects of cytochalasin D on the actin cytoskeleton: association of neoformed actin aggregates with proteins involved in signaling and endocytosis , 2003, Cellular and Molecular Life Sciences CMLS.

[2]  A. Aplin,et al.  Integrin and cytoskeletal regulation of growth factor signaling to the MAP kinase pathway , 1998 .

[3]  H. Hirt,et al.  MP2C, a plant protein phosphatase 2C, functions as a negative regulator of mitogen-activated protein kinase pathways in yeast and plants. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[4]  R. Landgraf,et al.  Human ERK1 Induces Filamentous Growth and Cell Wall Remodeling Pathways in Saccharomyces cerevisiae * , 2000, The Journal of Biological Chemistry.

[5]  F. Posas,et al.  A human homolog of the yeast Ssk2/Ssk22 MAP kinase kinase kinases, MTK1, mediates stress‐induced activation of the p38 and JNK pathways , 1997, The EMBO journal.

[6]  A. Sessions,et al.  Differential expression of members of the annexin multigene family in Arabidopsis. , 2001, Plant physiology.

[7]  I. Ota,et al.  Differential Regulation of the Cell Wall Integrity Mitogen-Activated Protein Kinase Pathway in Budding Yeast by the Protein Tyrosine Phosphatases Ptp2 and Ptp3 , 1999, Molecular and Cellular Biology.

[8]  J. Behlke,et al.  Phosphorylation and supramolecular organization of murine small heat shock protein HSP25 abolish its actin polymerization-inhibiting activity. , 1994, The Journal of biological chemistry.

[9]  L. Bardwell,et al.  Inhibitory and activating functions for MAPK Kss1 in the S. cerevisiae filamentous- growth signalling pathway , 1997, Nature.

[10]  D. Botstein,et al.  1 The Yeast Cytoskeleton , 1997 .

[11]  C. Mazzoni,et al.  The SLT2(MPK1) MAP kinase is activated during periods of polarized cell growth in yeast. , 1996, The EMBO journal.

[12]  R. Meagher,et al.  The Arabidopsis Cytoskeletal Genome , 2003, The arabidopsis book.

[13]  Michael J. Sailor,et al.  Remodeling of Synaptic Actin Induced by Photoconductive Stimulation , 2001, Cell.

[14]  M. Gaestel,et al.  Cytoskeletal Changes in Hypoxic Pulmonary Endothelial Cells Are Dependent on MAPK-activated Protein Kinase MK2* , 2002, The Journal of Biological Chemistry.

[15]  K. Irie,et al.  Expansion of the Cell Plate in Plant Cytokinesis Requires a Kinesin-like Protein/MAPKKK Complex , 2002, Cell.

[16]  Michael L. Dustin,et al.  The immunological synapse and the actin cytoskeleton: molecular hardware for T cell signaling , 2000, Nature Immunology.

[17]  Y. Goda,et al.  Actin-Dependent Regulation of Neurotransmitter Release at Central Synapses , 2000, Neuron.

[18]  R. Nishihama,et al.  The NPK1 mitogen-activated protein kinase kinase kinase is a regulator of cell-plate formation in plant cytokinesis. , 2001, Genes & development.

[19]  M. Craxton.  Genomic analysis of synaptotagmin genes. , 2001, Genomics.

[20]  J. Blenis,et al.  Cargo of Kinesin Identified as Jip Scaffolding Proteins and Associated Signaling Molecules , 2001, The Journal of cell biology.

[21]  S. Halpain.  Actin in a supporting role , 2003, Nature Neuroscience.

[22]  P. Maness,et al.  A MAP Kinase-Signaling Pathway Mediates Neurite Outgrowth on L1 and Requires Src-Dependent Endocytosis , 2000, The Journal of Neuroscience.

[23]  Y. Nagamine,et al.  Cytoskeleton Reorganization Induces the Urokinase-type Plasminogen Activator Gene via the Ras/Extracellular Signal-regulated Kinase (ERK) Signaling Pathway* , 1997, The Journal of Biological Chemistry.

[24]  S. Grewal,et al.  Extracellular-signal-regulated kinase signalling in neurons , 1999, Current Opinion in Neurobiology.

[25]  J. Xu,et al.  Inactivation of the mitogen-activated protein kinase Mps1 from the rice blast fungus prevents penetration of host cells but allows activation of plant defense responses. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Jonathan A. Cooper,et al.  p42 mitogen-activated protein kinase in brain: Prominent localization in neuronal cell bodies and dendrites , 1993, Neuroscience.

[27]  M. Gustin,et al.  Positioning of cell growth and division after osmotic stress requires a map kinase pathway , 1994, Yeast.

[28]  H. Hirt,et al.  MAP kinases in plant signal transduction , 1999, Cellular and Molecular Life Sciences CMLS.

[29]  H. Hirt,et al.  MAP kinase pathways: molecular plug-and-play chips for the cell , 2000, Plant Molecular Biology.

[30]  D. Preuss,et al.  Pollen tube targeting and axon guidance: parallels in tip growth mechanisms. , 2000, Trends in cell biology.

[31]  T. Chambers,et al.  Microtubule inhibitors elicit differential effects on MAP kinase (JNK, ERK, and p38) signaling pathways in human KB-3 carcinoma cells. , 2000, Experimental cell research.

[32]  J. Mathur,et al.  Microtubules and Microfilaments in Cell Morphogenesis in Higher Plants , 2002, Current Biology.

[33]  H. Hirt.  Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathway. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[34]  P. McPherson,et al.  Signaling on the Endocytic Pathway , 2001, Traffic.

[35]  E. Krebs,et al.  Association of mitogen-activated protein kinase with the microtubule cytoskeleton. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[36]  P. Grabham,et al.  Recruitment of the Arp2/3 complex and Mena for the stimulation of actin polymerization in growth cones by nerve growth factor , 2000, Journal of neuroscience research.

[37]  A. Jungk.  Root hairs and the acquisition of plant nutrients from soil , 2001 .

[38]  M. Yuan,et al.  Jasplakinolide reversibly disrupts actin filaments in suspension-cultured tobacco BY-2 cells , 2002, Protoplasma.

[39]  R. Klemke,et al.  Regulation of Cell Contraction and Membrane Ruffling by Distinct Signals in Migratory Cells , 1999, The Journal of cell biology.

[40]  Michael Loran Dustin,et al.  Neural and Immunological Synaptic Relations , 2002, Science.

[41]  T. Okuno,et al.  The mitogen-activated protein kinase gene MAF1 is essential for the early differentiation phase of appressorium formation in Colletotrichum lagenarium. , 2002, Molecular plant-microbe interactions : MPMI.

[42]  C. Wilson,et al.  A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cells. , 1998, Journal of cell science.

[43]  G. Drewes,et al.  Glycogen synthase kinase‐3 and the Alzheimer‐like state of microtubule‐associated protein tau , 1992, FEBS letters.

[44]  T. A. Ryan,et al.  Actin has a molecular scaffolding, not propulsive, role in presynaptic function , 2003, Nature Neuroscience.

[45]  R. Meagher,et al.  Isovariant Dynamics Expand and Buffer the Responses of Complex Systems: The Diverse Plant Actin Gene Family , 1999, Plant Cell.

[46]  M. C. Ruíz-Roldan,et al.  PTK1, a mitogen-activated-protein kinase gene, is required for conidiation, appressorium formation, and pathogenicity of Pyrenophora teres on barley. , 2001, Molecular plant-microbe interactions : MPMI.

[47]  H. Hirt,et al.  Complexity, cross talk and integration of plant MAP kinase signalling. , 2002, Current opinion in plant biology.

[48]  J. Millar,et al.  A MAP kinase-dependent actin checkpoint ensures proper spindle orientation in fission yeast , 2001, Nature.

[49]  C. L. Wang,et al.  Phosphotyrosine-dependent targeting of mitogen-activated protein kinase in differentiated contractile vascular cells. , 1995, Circulation research.

[50]  A. Holzinger,et al.  Jasplakinolide, a novel actin targeting peptide, inhibits cell growth and induces actin filament polymerization in the green alga Micrasterias. , 1997, Cell motility and the cytoskeleton.

[51]  M. Camps,et al.  The nucleus, a site for signal termination by sequestration and inactivation of p42/p44 MAP kinases. , 2001, Journal of cell science.

[52]  J. L. Tomsig,et al.  Copines: a ubiquitous family of Ca2+-dependent phospholipid-binding proteins , 2002, Cellular and Molecular Life Sciences CMLS.

[53]  L. Brodin,et al.  Impaired recycling of synaptic vesicles after acute perturbation of the presynaptic actin cytoskeleton , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[54]  L. Vidali,et al.  Polarized cell growth in higher plants. , 2001, Annual review of cell and developmental biology.

[55]  J. Xu,et al.  MAP kinase and cAMP signaling regulate infection structure formation and pathogenic growth in the rice blast fungus Magnaporthe grisea. , 1996, Genes & development.

[56]  M. Gustin,et al.  MAP Kinase Pathways in the YeastSaccharomyces cerevisiae , 1998, Microbiology and Molecular Biology Reviews.

[57]  Y. Matsuura,et al.  Association of Frabin with the Actin Cytoskeleton Is Essential for Microspike Formation through Activation of Cdc42 Small G Protein* , 1999, The Journal of Biological Chemistry.

[58]  P. Hussey,et al.  Actin-binding proteins in the Arabidopsis genome database: properties of functionally distinct plant actin-depolymerizing factors/cofilins. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[59]  H. Hirt,et al.  A MAP Kinase Is Activated Late in Plant Mitosis and Becomes Localized to the Plane of Cell Division , 1999, Plant Cell.

[60]  J. Sweatt,et al.  Molecular psychology: roles for the ERK MAP kinase cascade in memory. , 2002, Annual review of pharmacology and toxicology.

[61]  M. Cobb,et al.  MEKK1 interacts with alpha-actinin and localizes to stress fibers and focal adhesions. , 1999, Cell motility and the cytoskeleton.

[62]  J. A. Kaltschmidt,et al.  Planar polarity and actin dynamics in the epidermis of Drosophila , 2002, Nature Cell Biology.

[63]  K. Clark,et al.  Pheromone Response in Yeast: Association of Bem1p with Proteins of the MAP Kinase Cascade and Actin , 1995, Science.

[64]  F. Ausubel,et al.  MAP kinase signalling cascade in Arabidopsis innate immunity , 2002, Nature.

[65]  F. Baluška,et al.  Involvement of the mitogen‐activated protein kinase SIMK in regulation of root hair tip growth , 2002, The EMBO journal.

[66]  G. Wasteneys,et al.  Remodeling the cytoskeleton for growth and form: an overview with some new views. , 2003, Annual review of plant biology.

[67]  S. Horwitz,et al.  Selective potentiation of paclitaxel (taxol)-induced cell death by mitogen-activated protein kinase kinase inhibition in human cancer cell lines. , 2001, Molecular pharmacology.

[68]  David A. Cheresh,et al.  Regulation of Cell Motility by Mitogen-activated Protein Kinase , 1997, The Journal of cell biology.

[69]  Matthias Peter,et al.  MAP kinase dynamics in response to pheromones in budding yeast , 2001, Nature Cell Biology.

[70]  K. Morgan,et al.  Extracellular regulated kinase (ERK) interaction with actin and the calponin homology (CH) domain of actin-binding proteins. , 1999, The Biochemical journal.

[71]  H. Hirt,et al.  Salt stress induces changes in amounts and localization of the mitogen-activated protein kinase SIMK in alfalfa roots , 2000, Protoplasma.

[72]  R. Segal,et al.  Location, location, location: a spatial view of neurotrophin signal transduction , 2002, Trends in Neurosciences.

[73]  S. Grinstein,et al.  Involvement of the actin network in insulin signalling. , 1997, Society of General Physiologists series.

[74]  D. Menzel,et al.  The anti-proliferative agent jasplakinolide rearranges the actin cytoskeleton of plant cells. , 1999, European journal of cell biology.

[75]  M. Gustin,et al.  Osmotic stress and the yeast cytoskeleton: phenotype-specific suppression of an actin mutation , 1992, The Journal of cell biology.

[76]  M. Braun,et al.  Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. , 2000, Developmental biology.

[77]  M. Coptcoat,et al.  PSK, a Novel STE20-like Kinase Derived from Prostatic Carcinoma That Activates the c-Jun N-terminal Kinase Mitogen-activated Protein Kinase Pathway and Regulates Actin Cytoskeletal Organization* , 2000, The Journal of Biological Chemistry.

[78]  Frantisek Baluska,et al.  Polar transport of auxin: carrier-mediated flux across the plasma membrane or neurotransmitter-like secretion? , 2003, Trends in cell biology.

[79]  C. Marshall,et al.  Specificity of receptor tyrosine kinase signaling: Transient versus sustained extracellular signal-regulated kinase activation , 1995, Cell.

[80]  D. Ingber,et al.  Regulation of cytoskeletal mechanics and cell growth by myosin light chain phosphorylation. , 1998, The American journal of physiology.

[81]  Jay X. Tang,et al.  Cytoskeletal targeting of calponin in differentiated, contractile smooth muscle cells of the ferret , 1998, The Journal of physiology.

[82]  Gerald R. Fink,et al.  MAP Kinases with Distinct Inhibitory Functions Impart Signaling Specificity during Yeast Differentiation , 1997, Cell.

[83]  C. Mazzoni,et al.  The SLT2 (MPK1) MAP kinase homolog is involved in polarized cell growth in Saccharomyces cerevisiae , 1993, The Journal of cell biology.

[84]  Sakae Tanaka,et al.  Extracellular signal-regulated kinase mediates phosphorylation of tropomyosin-1 to promote cytoskeleton remodeling in response to oxidative stress: impact on membrane blebbing. , 2003, Molecular biology of the cell.

[85]  T. Miyano,et al.  Localisation of phosphorylated MAP kinase during the transition from meiosis I to meiosis II in pig oocytes , 2000, Zygote.

[86]  G. Fink,et al.  Ras2 signals via the Cdc42/Ste20/mitogen-activated protein kinase module to induce filamentous growth in Saccharomyces cerevisiae. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

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

[88]  Mu-ming Poo,et al.  Adaptation in the chemotactic guidance of nerve growth cones , 2002, Nature.

[89]  H. Hirt,et al.  Opposite changes in membrane fluidity mimic cold and heat stress activation of distinct plant MAP kinase pathways. , 2002, The Plant journal : for cell and molecular biology.

[90]  D. Helfman,et al.  Post-transcriptional down-regulation of ROCKI/Rho-kinase through an MEK-dependent pathway leads to cytoskeleton disruption in Ras-transformed fibroblasts. , 2002, Molecular biology of the cell.

[91]  D. Helfman,et al.  Post-transcriptional down-regulation of ROCKI/Rho-kinase through an MEK-dependent pathway leads to cytoskeleton disruption in Ras-transformed fibroblasts. , 2002 .

[92]  H. Hosoya,et al.  Phosphorylation by MAPKAP kinase 2 activates Mg(2+)-ATPase activity of myosin II. , 1996, Biochemical and biophysical research communications.

[93]  J. Landry,et al.  Regulation of actin filament dynamics by p38 map kinase-mediated phosphorylation of heat shock protein 27. , 1997, Journal of cell science.

[94]  G L Johnson,et al.  Organization and regulation of mitogen-activated protein kinase signaling pathways. , 1999, Current opinion in cell biology.

[95]  Karl Deisseroth,et al.  Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology , 2001, Nature Neuroscience.

[96]  M. West-Eberhard,et al.  Evolution in the light of developmental and cell biology, and vice versa. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[97]  E Schaefer,et al.  The MAP kinase kinase kinase MLK2 co‐localizes with activated JNK along microtubules and associates with kinesin superfamily motor KIF3 , 1998, The EMBO journal.

[98]  W. Reenstra,et al.  ECM‐stimulated actin bundle formation in embryonic corneal epithelia is tyrosine phosphorylation dependent , 1999, The Anatomical record.

[99]  R. Lefkowitz,et al.  Serotonin 5-HT1A Receptor-mediated Erk Activation Requires Calcium/Calmodulin-dependent Receptor Endocytosis* , 1999, The Journal of Biological Chemistry.

[100]  S. Ross,et al.  A Role for the p38 Mitogen-activated Protein Kinase/Hsp 27 Pathway in Cholecystokinin-induced Changes in the Actin Cytoskeleton in Rat Pancreatic Acini* , 1998, The Journal of Biological Chemistry.

[101]  K. Thai,et al.  NO Inhibits Stretch-induced MAPK Activity by Cytoskeletal Disruption* , 2000, The Journal of Biological Chemistry.

[102]  John R. Pringle,et al.  Bni1p, a Yeast Formin Linking Cdc42p and the Actin Cytoskeleton During Polarized Morphogenesis , 1997, Science.

[103]  J. Landry,et al.  Modulation of actin microfilament dynamics and fluid phase pinocytosis by phosphorylation of heat shock protein 27. , 1993, The Journal of biological chemistry.

[104]  R. Somwar,et al.  Actin Filaments Facilitate Insulin Activation of the Src and Collagen Homologous/Mitogen-activated Protein Kinase Pathway Leading to DNA Synthesis and c-fos Expression* , 1998, The Journal of Biological Chemistry.

[105]  A. Catling,et al.  Active MAP Kinase in Mitosis: Localization at Kinetochores and Association with the Motor Protein CENP-E , 1998, The Journal of cell biology.

[106]  F. Baluška,et al.  The architecture of polarized cell growth: the unique status of elongating plant cells. , 2003, BioEssays : news and reviews in molecular, cellular and developmental biology.

[107]  T. Yuzyuk,et al.  The MEK kinase Ssk2p promotes actin cytoskeleton recovery after osmotic stress. , 2002, Molecular biology of the cell.

[108]  Kazuo Shinozaki,et al.  Mitogen-activated protein kinase cascades in plants: a new nomenclature. , 2002, Trends in plant science.

[109]  M. Cobb,et al.  MAP kinase becomes stably activated at metaphase and is associated with microtubule-organizing centers during meiotic maturation of mouse oocytes. , 1993, Developmental biology.

[110]  R. Nishihama,et al.  The NPK1 mitogen-activated protein kinase kinase kinase contains a functional nuclear localization signal at the binding site for the NACK1 kinesin-like protein. , 2002, The Plant journal : for cell and molecular biology.