Endocytosis, Actin Cytoskeleton, and Signaling

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