Endocytosis, Actin Cytoskeleton, and Signaling
Year: 2004
Type: review
Abstract: Endocytosis is the internalization of plasma membrane proteins and lipids, extracellular molecules, fluids, particles, exosomes, viruses, and bacteria. Endocytic internalization is a conserved process for all eukaryotic cells that is required for diverse cellular functions. These include turnover and degradation of plasma membrane proteins and receptors, transduction and dispersal of signals within the cell and between cells of an organized tissue, spread of morphogens, cell-to-cell communication at synapses, elimination of pathogenic microorganisms, establishment of symbiosis with microorganisms, and nutrient uptake. Endocytosis has played a crucial role in endosymbiosis during eukaryotic evolution and laid the foundation for the emergence of specialized organelles, such as mitochondria and plastids. Several basic forms of endocytosis have been defined according to the type of cargo and molecular machinery driving its internalization. The endocytic pathways include clathrin-mediated, caveolae/lipid raft-mediated, clathrin-, and caveolae-independent endocytosis, fluid-phase endocytosis, and phagocytosis. Among them, clathrin-dependent endocytosis represents the best studied form of endocytic internalization. During the last decade, a significant number of studies revealed that clathrin-mediated endocytosis is highly regulated by structural, adaptor, regulatory, and signaling proteins involved in the formation (budding) of endocytic vesicles, their pinching off the plasma membrane, trafficking and selective fusion with endosomal/lysosomal compartments (for review, see Brodsky et al., 2001). For example, the structural protein clathrin and several adaptor proteins build up the macromolecular lattice on the surface of endocytic vesicles (known as clathrin coat) that interacts with the large GTPase dynamin, as well as with cytoskeletal and signaling protein complexes (for review, see Engqvist-Goldstein and Drubin, 2003). Importantly, endocytosis is required not only for retrieval and desensitization of receptors, but also for efficient signal dispersal within the cell (for review, see Sorkin and von Zastrow, 2002; Piddini and Vincent, 2003). In this update, we highlight recent progress in plant endocytosis. We also discuss data revealing inherent interactions between endocytosis, the actin cytoskeleton, and mitogen-activated protein kinases (MAPKs) in mammalian models with possible implications for plant cells. Finally, we outline a perspective of future research in this emerging field of plant cell biology. We do not deal here with biosynthetic and vacuolar pathways merging eventually with endosomes since these have been covered elsewhere recently (Surpin and Raikhel, 2004). Endocytic pathways in mammals, such as clathrin-mediated, caveolae/lipid raft-mediated, clathrin- and caveolae-independent endocytosis, fluid-phase endocytosis, and phagocytosis, differ with regard to the nature of internalized cargo, the size of vesicles, the associated molecular machinery, and the type of regulation (for review, see Conner and Schmid, 2003). These considerable differences are highlighted in Tables I Overview of endocytosis in animals Homologous proteins found in plants. Overview of endocytosis in animals Homologous proteins found in plants. Links between endocytosis, actin cytoskeleton, and signaling Homologous proteins found in plants. Links between endocytosis, actin cytoskeleton, and signaling Homologous proteins found in plants. Endocytic pathways employ morphologically diverse membranous tubulo-vesicular compartments encompassing sorting endosomes (also called early endosomes), recycling endosomes, multivesicular bodies, late endosomes, and lysosomes. These endocytic compartments differ in their internal pH, enrichment in specific membrane lipids, and in membrane-associated small GTPases of the Rab family (Table III Classification of endosomes Classification of endosomes Based on structural studies, clathrin-mediated endocytosis in mammals was subdivided into distinct stages: (1) clathrin coat assembly on membranes, (2) vesicle invagination, (3) fission, (4) movement of vesicles into the cell interior, (5) vesicle uncoating, and (6) fusion with early endosomes. Adaptor proteins such as AP2, AP180, and epsins are interacting with plasma membrane phospholipids, cytoplasmic domains of receptors, and with synaptotagmin. When adaptor proteins are bound to the plasma membrane, they recruit clathrin and promote the assembly of the clathrin triskelion into a clathrin coat on the inner surface of the plasma membrane. Other proteins, such as β-arrestins, interact with receptors and the clathrin lattice. Additionally, β-arrestins are involved in signal transduction since they serve as scaffolds recruiting MAPK cascades onto endosomal vesicles (see below). Endophilin, a lysophosphatidic acid transferase, is involved in invagination of coated plasma membrane domains resulting in the formation of clathrin-coated pits (CCPs). The large GTPase dynamin is essential for fission of the clathrin-coated vesicles (CCVs) from the plasma membrane. Auxilin, Hsc70, and synaptojanin are likely involved in disassembly of the clathrin coat before endocytic vesicles fuse with early endosomes (for review, see Brodsky et al., 2001; Holstein, 2002 for plant cells). Caveolae/lipid raft-dependent endocytosis is characterized by its clathrin independence. Caveolae are membrane invaginations enriched in structural sterols, which might but do not need to be coated with caveolins, serving the internalization of some plasma membrane glycosphingolipids, glycosylphosphatidylinositol (GPI)-anchored proteins, extracellular ligands such as albumin and folic acid, bacterial toxins including tetanus and cholera, as well as uncoated Polyoma or Simian viruses (for review, see Parton and Richards, 2003). Interestingly, both caveolae and plasma membrane lipid rafts are enriched with cholesterol and sphingolipids, and they are involved in signaling events at the plasma membrane. In comparison to clathrin-dependent endocytosis, little is known about different stages of caveolae formation. Nevertheless, the study by Pelkmans et al. (2002) revealed that dynamin is essential for the fission step of caveolae from the plasma membrane. Pinosomes are large vesicles (0.5–5 μm in diameter) that internalize extracellular fluid. This extracellular fluid can be labeled by fluid phase markers such as Lucifer Yellow and rhodamin-labeled dextran. Several proteins, including phosphoinositol-dependent kinase and small GTPases of the Ras and Rho families, together with their effectors, including p21-activated kinase and ADP-ribosylation factor (ARF6), were shown to have a regulatory function during macropinocytosis (for review, see Cardelli, 2001). Besides the fission step, dynamin was also implicated in the formation of actin comet tails, which are necessary for the intracellular movement of macropinosomes (Orth et al., 2002). Phagocytosis is a special type of endocytosis occurring in free living unicellular organisms or specialized cells of higher organisms such as neutrophils and macrophages, when an entire foreign particle or microorganism is engulfed by the formation of phagocytic cups. Distinct stages have been identified during phagocytosis encompassing attachment of the particles to cell surface receptors, engulfment of the particle by dynamic shape changes dependent on the polymerization of actin and membrane exocytosis, and, finally, the formation of phago-lysosomes (for review, see Cardelli, 2001). All these phagocytic processes are dependent on rearrangements of the actin cytoskeleton. As highlighted by May and Machesky (2001), phosphoinositide lipids and multicomponent signaling complexes are important for signal transduction from phagocytic receptors to the actin cytoskeleton. Initially, the existence of endocytosis in plant cells was drawn into question because of their turgor pressure and rigid cell walls (Oparka et al., 1993; Hawes et al., 1995). However, numerous subsequent reports that used endocytic markers (for review, see Low and Chandra, 1994; Bahaji et al., 2001; Battey et al., 1999), as well as a number of recent localization and functional studies employing membrane-associated styryl FM dyes, filipin-labeled plant sterols, the fluid-phase marker Lucifer Yellow, green fluorescent protein (GFP)/yellow fluorescent protein (YFP)-tagged Rab GTPases, and BP-80 (a prevacuolar compartment/multivesicular body marker) and the fungal inhibitor of vesicular traffic, brefeldin A (BFA), clarified the existence and extraordinary dynamics of endocytic activity in plant cells (Geldner et al., 2001, 2003; Ueda et al., 2001; Baluška et al., 2002, 2004; Emans et al., 2002; Inaba et al., 2002; Grebe et al., 2003; Tse et al., 2004). In the light of recent published work on endocytosis, it is expected that at least four basic forms of endocytosis, including clathrin-dependent, lipid raft-dependent, phagocytosis, and fluid-phase endocytosis, operate in plants. Here, we briefly summarize the supporting evidence. Plants possess clathrin and they are equipped with most proteins necessary for clathrin-dependent endocytosis, including adaptor proteins involved in the formation of the clathrin coat on the surface of plasma membrane and endocytic vesicles (for review, see Holstein, 2002). In their recent work, Barth and Holstein (2004) biochemically and functionally characterized two of these adaptor proteins, AP180 and αC-adaptin, in Arabidopsis. Plant AP180 functions as a clathrin assembly protein while αC-adaptin binds AP180 and mammalian endocytic proteins, including amphiphysin, Eps15, and dynamin. Interestingly, plant CCVs have smaller sizes (70–90 nm; Barth and Holstein, 2004) in comparison to their mammalian counterparts (average size 120 nm; Conner and Schmid, 2003), which might be a consequence of endocytic internalization against higher turgor pressure in some plant cell types. Direct involvement of CCVs in regulated (ligand/receptor-mediated) endocytosis has not been demonstrated yet. Other studies reported endocytic uptake of plant- or pathogen-derived elicitors, such as oligogalacturonic acid, glycoproteins, and exopolysaccharides, which are produced during plant defense (Romanenko et al., 2002). While molecular links between receptor-mediated endocytosis and signaling cascades are still missing in plants, receptor-like kinases were by Holstein (2002) as for internalization clathrin-mediated endocytosis. in this et al. (2002) demonstrated that the protein endocytosis of a can likely form a together with et al., 2002). In the it be to study can internalization and this signal is and to cellular cells were with two in green and in of both on endosomes is shown in the that the is a endosomal marker in plant cells. is known about endocytosis in plants. are published data on and this protein is missing in plant Nevertheless, existence of lipid rafts and their with proteins was in et al., 2003; et al., 2004). in this are equipped with the structural and that are in lipid rafts in cholesterol et al., 2001). Grebe et al. reported that plant structural of the plasma membrane labeled with fluorescent were internalized and with on endosomes. structural were implicated to a role in localization of the et al., 2003). Additionally, it has been that recycling of some proteins be dependent on structural and lipid rafts et al., 2003; et al., 2003). these that membrane a role in plant endocytosis. are internalized into plant cells phagocytosis during with of plants. These the by of a invagination from the of the the and are to the inner cells. are internalized into cells of the of the in which (for review, see and In a recent et al. found that the small GTPase is essential for phagocytosis of bacterial that were reported to be internalized in et al., research et al., 2003; et al., recently identified factor receptors in and their in the internalization of in In the it be to study these receptors receptor-mediated endocytosis to factor The of a large of both plant and bacterial in all stages of the between and efficient as well as the cell to this be in involved in into plant cells. While cells are for of in these cells also fluid-phase endocytosis as revealed by internalization of the fluid phase marker Lucifer Yellow in et al., 2004). fluid-phase endocytosis at and in These data that endocytic events in plant cells such as phagocytosis and fluid-phase endocytosis are important for interactions with and for of some plant cells and Endocytosis in from the plasma membrane and plasma membrane-associated in plasma membrane plasma membrane structural sterols, and membrane protein to cell by small GTPase and within The and dynamin both with plasma membrane and and can be eventually to the from both of cell be by to compartments is to cells. of of cell with with from Grebe et al., 2003). of to and cell by to on compartments in cells with for are with The of are dependent on the and as well as the For et al. reported that with for are still compartments are from and endosomes. of with most of the of are in cells et al., and eventually with of the the is of a of vesicles and membranous compartments of different and from the endocytic it was that the represents a membranous vesicular by both endosomal and et al., 2002; 2002; et al., 2002; see also A was reported for cells et al., and In of plants, the is by of in a with most the see also Grebe et al., 2003). Importantly, some and such as and in these of the (see and in Grebe et al., 2003). the both endocytic vesicles plasma membrane (Geldner et al., 2001, 2003; Baluška et al., as well as plasma membrane et al., 2003), in vesicles of the is a this assembly of diverse vesicles can together in the and be that some proteins to the proteins are involved in its that of the for the of vesicles in the of compartments is the type of internalized membrane, for example, its enrichment in structural important can be the type of membrane since coated by clathrin (a coat on plasma membrane and vesicles but not on or up in vesicles coated with proteins at the of This was reported by et al. for are the for in mammalian cells. The plant ADP-ribosylation factor which is a small GTPase of the Ras family regulated was to on the plasma membrane in cells and to the compartments in cells et al., 2002; This work the that a protein associated with the is on endosomal The localization of to was by et al. A recent study by et al. revealed that the endosomal an represents a of in plant cells. at endosomal which also A protein was and were The of protein to in to Additionally, both shape and size of endosomes labeled with were in from these plants. However, recycling of proteins, such as and to be or of that are or different molecular involved in their endocytic these data that can recycling of its to endosomes (Geldner et al., 2003). trafficking and possible of the actin in an actin polymerization together with of dynamin endocytic recycling of receptors, and cell and by the pinching off the endocytic vesicles and by actin on these vesicles dependent on such as both with endosomal vesicles and the actin cytoskeleton. Additionally, of actin regulated by and are to as a structural in to and signaling and regulatory molecules, including within the vesicle trafficking of and endocytic as well as between and endosomes. Several important for endocytosis were recently within of including dynamin et al., actin et al., et al., 2003), et al., and protein protein et al., 2003). The actin has been implicated in vesicular in cells et al., 2001). In The of with the of actin at the et al., 2002). GTPases of the of family a role in both and the in and 2002). We that actin processes an important role during vesicle and movement of endosomes This is with recent in data movement of early endosomes labeled with Rab GTPases and or with in of and and In to the function of actin in endocytosis, actin and serve as molecular for vesicles and associated regulatory and signaling including et al., 2002, 2004). cells changes in their surface to was by et al. As of the plasma membrane is only about of surface and it is that and endocytosis events are processes in the of cells of and revealed that and of was associated with fusion and fission of vesicles at the plasma membrane. et al. have shown that internalization of the endocytic from the cell surface in was with the of surface by of these vesicles during the of Additionally, recent important work by et al. (2004) reports about endocytosis of plasma membrane and in cells. These data that is during the is likely that these recycling vesicles are with cell as shown here and reported for et al., or cell of by and the on was by of the endosomal et al., 2002). Endocytosis is by in plant cells et al., 2002). several of that endocytosis is essential for of is a large GTPase implicated to an essential role in all forms of endocytosis in higher including fission of clathrin- and vesicles and movement of and et al., 2002; for review, see and 2003). is a protein that interacts with a of proteins, including that with the actin (for review, see and 2003). For example, dynamin interacts its with and with proteins while its as domains were identified in and of them, with clathrin and was to to actin et al., 2001). Plants a large family of proteins et al., work has for a role of the in plasma membrane et al., In plants, the plasma membrane was with invaginations et al., fission of plant dynamin, with CCVs and with the plasma membrane et al., 2002; et al., All this that at least some in endocytosis in plant cells. are data interactions between endocytosis and the actin in and mammals (for review, see May and 2001; Engqvist-Goldstein and Drubin, 2003). In an actin is necessary for all forms of endocytosis. Additionally, actin is required in to from the plasma membrane domains into early endosomes and for of the MAPK signaling et al., see for on signaling A number of proteins have been implicated as functional at the between the endocytic internalization and the actin cytoskeleton. In mammals, some of these proteins, dynamin, amphiphysin, and and were as molecular between endocytosis and the actin (Table Other molecular between dynamin and actin are by and (for review, see et al., Engqvist-Goldstein and Drubin, 2003; Several endocytic actin was shown that actin polymerization at the plasma membrane both the and of the internalization step, and of early endosomes from the plasma membrane into the (for review, see Engqvist-Goldstein and Drubin, 2003). Nevertheless, the function of actin in endocytosis is from For it is not known for which of endocytosis the actin is Several have been for the actin such as endocytosis into plasma membrane and invagination of plasma membrane, of vesicle formation as a rigid vesicle fission and from the plasma membrane, vesicle the and vesicle fusion (for review, see et al., In two recent studies, a role of actin in endocytic vesicles was by et al. and actin were identified as of endocytosis in cells et al., 2003). A recent study revealed that both the endocytic and the actin assembly work in in endocytic as actin in to of the et al., 2004). This recent inherent and dynamic interactions between endocytosis and the actin cytoskeleton. Importantly, is that such endocytic functions of actin are to and dynamic actin In the of the actin in the nature of the internalized cargo is not However, it be in to the in plant cells et al., 2002; et al., of the cell are internalized and actin endocytosis. Plants possess some of the molecular between endocytic and including proteins, and the important known from eukaryotic such as proteins and their and were not found in plants. In and dynamin interacting proteins, including and are also missing from the plant (for review, see Holstein, 2002; et al., 2002). Nevertheless, several recent studies reported that the actin is required for endocytosis in plant cells on evidence. was shown that actin by or two the formation of large endocytic which recycling plasma membrane and cell (Geldner et al., 2001; Baluška et al., 2002; et al., 2002; et al., 2002). we reported that and a or fluid phase endocytosis of Lucifer Yellow into cells et al., 2004). Endocytic of is also dependent on the actin as revealed by with and studies of the et al., 2003). All these an essential role of actin in endocytic internalization. The function of the actin in plant endocytosis, to be and be expected from studies on cell and During the last a body of has from the study on mammalian cell that of MAPK signaling pathways in their with signaling endosomes et al., et al., 2001; for review, see Sorkin and von Zastrow, 2002). Additionally, several of MAPK signaling interact or with the actin and they are involved in actin dynamics (for review, see et al., 2004). was reported that endocytosis is required for MAPK signaling regulated kinase because dynamin were in both the formation of endocytic vesicles and the of and its et al., et al., was at the plasma membrane and endocytic vesicles but not within the et al., proteins such as β-arrestins, which receptors factor for endocytosis, are also necessary for et al., et al., it was revealed that β-arrestins proteins that not only of but also both and to endosomes et al., et al., 2001). Besides the vesicular signaling of dependent on the of signaling endosomes, et al. demonstrated that mammalian endocytosis by formation between inhibitor and a small GTPase on early endosomes. The data that signaling endosomes in cells serve as assembly for diverse signaling pathways recruiting complexes of proteins, MAPK as well as their and interacting These also that endocytosis a crucial role in signal dispersal and within the cell (for review, see Sorkin and von Zastrow, 2002). Additionally, signaling is required for bacterial and phagocytosis. For example, and is necessary for of cells by et al., In plants, of and are well known as of and endocytosis (for review, see et al., 2001). we reported that between MAPK the actin cytoskeleton, and vesicular trafficking is involved in regulation of et al., 2002). was in of In with both and from while into to the cytoplasmic actin of the MAPK with (a inhibitor in mammalian and changes in vacuolar vesicular traffic, and of as revealed by Importantly, vesicular trafficking and of were not when a of were with et al., a role of in vesicular and were to in the of plant cells et al., 2002). The nature of these Nevertheless, it was recently reported that an of endocytosis and in cells et al., 2003), is to which is to protein kinase et al., 2002). these were not with proteins together endocytic trafficking and signaling et al., 2001). is a plant protein required for cell of as well as for cell formation during of plant which membrane recycling et al., 2003). studies on light on the interactions between endocytosis, and MAPK Endocytosis is an essential cellular process occurring in all eukaryotic cells. progress revealed that endocytosis in plants, in to mammals, is involved in the internalization and recycling of plasma membrane including membrane proteins and (Geldner et al., 2001, 2003; Baluška et al., 2002; Grebe et al., 2003), in the uptake of extracellular et al., and phagocytosis of et al., 2003). plant cells are to internalize cell such as with and et al., 2002; et al., 2002). These are with the that endocytosis not only the of plasma membrane proteins but also the of cell be to study cell in actin as functionally in this In mammals and the actin is required for endocytosis (for review, see et al., Engqvist-Goldstein and Drubin, 2003; et al., 2003; et al., and is also involved in endocytic internalization in (Geldner et al., 2001; Baluška et al., 2002, 2004; Grebe et al., 2003). During the last it was demonstrated that endocytosis in mammals is to signaling cascades regulated by in are to signaling endosomes and to cellular (for review, see Sorkin and von Zastrow, 2002). In future studies, it be important to this of signal transduction and endocytosis and signaling endosomes in plants. between actin and MAPK signaling were that rearrangements of the actin and of MAPK signal transduction cascades and their (for review, see et al., 2004). be that to be some basic differences in endocytosis between and higher at the molecular for not and for review, see Holstein, 2002; Engqvist-Goldstein and Drubin, 2003; and and clathrin and do not significant in endocytosis 2003), that a type of endocytosis is important for a regulated also to and of protein recycling between endosomes and plasma membrane known from mammals (for review, see and 2004) and (for a of the regulated type of endocytosis, is missing in but in not only as a for but is also necessary for endocytosis that clathrin and in mammals et al., 2003). Additionally, some and plant cell but not are to phagocytosis of pathogenic or bacteria. and differ in the of their molecular links between endocytosis and the actin cytoskeleton, since proteins such as and or proteins such as and were found in the plant (for review, see Holstein, 2002; et al., 2002). the and proteins the which are required for vesicle fission and endosomal to be conserved in (for review, see and 2003; et al., it was demonstrated in mammalian cells that two different endocytic pathways the of a was shown that clathrin-mediated endocytosis signaling of the the was internalized and caveolae et al., 2003). this for of plant receptors is not As progress has been and is likely to in this can that crucial endocytic be identified and functionally characterized at a The recently as an protein (Geldner et al., is a cell and study to the interactions endocytosis, the actin cytoskeleton, and signaling cascades in plant cells. We for with the for and for of We are to Holstein, and for of the We to work has not been to
Source: PLANT PHYSIOLOGY
Language: English
Subfield: Cell Biology
Domain: Life Sciences
Open Access status: green
OpenAlex ID: W2063400445