Membrane microdomains, caveolae, and caveolar endocytosis of sphingolipids (Review)

Caveolae are flask-shape membrane invaginations of the plasma membrane that have been implicated in endocytosis, transcytosis, and cell signaling. Recent years have witnessed the resurgence of studies on caveolae because they have been found to be involved in the uptake of some membrane components such as glycosphingolipids and integrins, as well as viruses, bacteria, and bacterial toxins. Accumulating evidence shows that endocytosis mediated by caveolae requires unique structural and signaling machinery (caveolin-1, src kinase), which indicates that caveolar endocytosis occurs through a mechanism which is distinct from other forms of lipid microdomain-associated, clathrin-independent endocytosis. Furthermore, a balance of glycosphingolipids, cholesterol, and caveolin-1 has been shown to be important in regulating caveolae endocytosis.

[1]  R. Pagano,et al.  The glycosphingolipid, lactosylceramide, regulates beta1-integrin clustering and endocytosis. , 2005, Cancer research.

[2]  L. Pelkmans,et al.  Assembly and trafficking of caveolar domains in the cell , 2005, The Journal of cell biology.

[3]  M. Kirkham,et al.  Ultrastructural identification of uncoated caveolin-independent early endocytic vehicles , 2005, The Journal of cell biology.

[4]  Lucas Pelkmans,et al.  Clathrin- and caveolin-1–independent endocytosis , 2005, The Journal of cell biology.

[5]  C. ffrench-Constant,et al.  Integrins: versatile integrators of extracellular signals. , 2004, Trends in cell biology.

[6]  J. Sottile,et al.  Fibronectin matrix turnover occurs through a caveolin-1-dependent process. , 2004, Molecular biology of the cell.

[7]  R. Pagano,et al.  Elevated endosomal cholesterol levels in Niemann-Pick cells inhibit rab4 and perturb membrane recycling. , 2004, Molecular biology of the cell.

[8]  L. Pelkmans,et al.  Caveolin-Stabilized Membrane Domains as Multifunctional Transport and Sorting Devices in Endocytic Membrane Traffic , 2004, Cell.

[9]  J. E. Larsen,et al.  Cholera toxin toxicity does not require functional Arf6- and dynamin-dependent endocytic pathways. , 2004, Molecular biology of the cell.

[10]  N. Naslavsky,et al.  Characterization of a nonclathrin endocytic pathway: membrane cargo and lipid requirements. , 2004, Molecular biology of the cell.

[11]  R. Simari,et al.  Selective stimulation of caveolar endocytosis by glycosphingolipids and cholesterol. , 2004, Molecular biology of the cell.

[12]  A. Malik,et al.  Role of Src-induced Dynamin-2 Phosphorylation in Caveolae-mediated Endocytosis in Endothelial Cells* , 2004, Journal of Biological Chemistry.

[13]  I. Nabi,et al.  Ganglioside GM1 levels are a determinant of the extent of caveolae/raft-dependent endocytosis of cholera toxin to the Golgi apparatus , 2004, Journal of Cell Science.

[14]  Ira,et al.  Nanoscale Organization of Multiple GPI-Anchored Proteins in Living Cell Membranes , 2004, Cell.

[15]  María Yáñez-Mó,et al.  Caveolae are a novel pathway for membrane-type 1 matrix metalloproteinase traffic in human endothelial cells. , 2003, Molecular biology of the cell.

[16]  Varpu Marjomäki,et al.  Clustering induces a lateral redistribution of alpha 2 beta 1 integrin from membrane rafts to caveolae and subsequent protein kinase C-dependent internalization. , 2003, Molecular biology of the cell.

[17]  V. Puri,et al.  Selective caveolin-1-dependent endocytosis of glycosphingolipids. , 2003, Molecular biology of the cell.

[18]  Ivan R. Nabi,et al.  Caveolae/raft-dependent endocytosis , 2003, The Journal of cell biology.

[19]  R. Pagano,et al.  Glycosphingolipids Internalized via Caveolar-related Endocytosis Rapidly Merge with the Clathrin Pathway in Early Endosomes and Form Microdomains for Recycling* , 2003, The Journal of Biological Chemistry.

[20]  S. Hakomori Structure, organization, and function of glycosphingolipids in membrane , 2003, Current opinion in hematology.

[21]  Richard G. W. Anderson,et al.  Dual control of caveolar membrane traffic by microtubules and the actin cytoskeleton , 2002, Journal of Cell Science.

[22]  Richard O Hynes,et al.  Integrins Bidirectional, Allosteric Signaling Machines , 2002, Cell.

[23]  N. Hogg,et al.  Mechanisms contributing to the activity of integrins on leukocytes , 2002, Immunological reviews.

[24]  Ludger Johannes,et al.  Clathrin‐Dependent or Not: Is It Still the Question? , 2002, Traffic.

[25]  Ken Jacobson,et al.  A Role for Lipid Shells in Targeting Proteins to Caveolae, Rafts, and Other Lipid Domains , 2002, Science.

[26]  B. Nichols A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex , 2002, Nature Cell Biology.

[27]  Lucas Pelkmans,et al.  Local Actin Polymerization and Dynamin Recruitment in SV40-Induced Internalization of Caveolae , 2002, Science.

[28]  R. Fässler,et al.  Integrins in invasive growth. , 2002, The Journal of clinical investigation.

[29]  Pranav Sharma,et al.  GPI-anchored proteins are delivered to recycling endosomes via a distinct cdc42-regulated, clathrin-independent pinocytic pathway. , 2002, Developmental cell.

[30]  Jason S. Mitchell,et al.  Lipid Microdomain Clustering Induces a Redistribution of Antigen Recognition and Adhesion Molecules on Human T Lymphocytes1 , 2002, The Journal of Immunology.

[31]  N. Hogg,et al.  The involvement of lipid rafts in the regulation of integrin function. , 2002, Journal of cell science.

[32]  I. Nabi,et al.  Caveolin-1 Is a Negative Regulator of Caveolae-mediated Endocytosis to the Endoplasmic Reticulum* , 2002, The Journal of Biological Chemistry.

[33]  David S. Park,et al.  Caveolae-deficient Endothelial Cells Show Defects in the Uptake and Transport of Albumin in Vivo * , 2001, The Journal of Biological Chemistry.

[34]  M. Lisanti,et al.  Caveolins and caveolae: molecular and functional relationships. , 2001, Experimental cell research.

[35]  B. Deurs,et al.  Internalization of cholera toxin by different endocytic mechanisms. , 2001, Journal of cell science.

[36]  M. Drab,et al.  Loss of Caveolae, Vascular Dysfunction, and Pulmonary Defects in Caveolin-1 Gene-Disrupted Mice , 2001, Science.

[37]  V. Puri,et al.  Clathrin-dependent and -independent internalization of plasma membrane sphingolipids initiates two Golgi targeting pathways , 2001, The Journal of cell biology.

[38]  C. Mineo,et al.  Potocytosis. Robert Feulgen Lecture. , 2001, Histochemistry and cell biology.

[39]  Lucas Pelkmans,et al.  Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER , 2001, Nature Cell Biology.

[40]  A. Dautry‐Varsat,et al.  Interleukin 2 receptors and detergent-resistant membrane domains define a clathrin-independent endocytic pathway. , 2001, Molecular cell.

[41]  S. Peiró,et al.  Epidermal Growth Factor-mediated Caveolin Recruitment to Early Endosomes and MAPK Activation , 2000, The Journal of Biological Chemistry.

[42]  H. Hamm,et al.  Endothelial Cell-Surface Gp60 Activates Vesicle Formation and Trafficking via Gi-Coupled Src Kinase Signaling Pathway , 2000, The Journal of cell biology.

[43]  M. Masserini,et al.  Use of a photoactivable GM1 ganglioside analogue to assess lipid distribution in caveolae bilayer , 2000, Glycoconjugate Journal.

[44]  Ruixiang Li,et al.  Induction of Endocytic Vesicles by Exogenous C6-ceramide* , 1999, The Journal of Biological Chemistry.

[45]  A. Pol,et al.  The “early‐sorting” endocytic compartment of rat hepatocytes is involved in the intracellular pathway of caveolin‐1 (VIP‐21) , 1999, Hepatology.

[46]  G. Morel,et al.  Caveolar internalization of growth hormone. , 1999, Experimental cell research.

[47]  J. Engelman,et al.  Molecular genetics of the caveolin gene family: implications for human cancers, diabetes, Alzheimer disease, and muscular dystrophy. , 1998, American journal of human genetics.

[48]  R. Pagano,et al.  Use of BODIPY‐labeled Sphingolipids to Study Membrane Traffic along the Endocytic Pathway a , 1998, Annals of the New York Academy of Sciences.

[49]  P. Orlandi,et al.  Filipin-dependent Inhibition of Cholera Toxin: Evidence for Toxin Internalization and Activation through Caveolae-like Domains , 1998, The Journal of cell biology.

[50]  A. Malik,et al.  Gp60 Activation Mediates Albumin Transcytosis in Endothelial Cells by Tyrosine Kinase-dependent Pathway* , 1997, The Journal of Biological Chemistry.

[51]  W. Gunning,et al.  Clustering of GPI-Anchored Folate Receptor Independent of Both Cross-Linking and Association with Caveolin , 1997, The Journal of Membrane Biology.

[52]  T. Fujimoto,et al.  Crosslinked Plasmalemmal Cholesterol Is Sequestered to Caveolae: Analysis with a New Cytochemical Probe , 1997, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[53]  Charles C. Wykoff,et al.  Recombinant Expression of Caveolin-1 in Oncogenically Transformed Cells Abrogates Anchorage-independent Growth* , 1997, The Journal of Biological Chemistry.

[54]  E. Ikonen,et al.  Functional rafts in cell membranes , 1997, Nature.

[55]  L. Norkin,et al.  Bound simian virus 40 translocates to caveolin-enriched membrane domains, and its entry is inhibited by drugs that selectively disrupt caveolae. , 1996, Molecular biology of the cell.

[56]  T. Fujimoto,et al.  GPI-anchored proteins, glycosphingolipids, and sphingomyelin are sequestered to caveolae only after crosslinking. , 1996, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[57]  M. Roth,et al.  Different biosynthetic transport routes to the plasma membrane in BHK and CHO cells , 1996, The Journal of cell biology.

[58]  F. Wieland,et al.  VIP21/caveolin is a cholesterol-binding protein. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[59]  R. Parton,et al.  De novo formation of caveolae in lymphocytes by expression of VIP21-caveolin. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[60]  P. Oh,et al.  Separation of caveolae from associated microdomains of GPI-anchored proteins , 1995, Science.

[61]  D. Harris,et al.  Glycolipid-anchored proteins in neuroblastoma cells form detergent- resistant complexes without caveolin , 1995, The Journal of cell biology.

[62]  R. Parton,et al.  Detergent-insoluble glycolipid microdomains in lymphocytes in the absence of caveolae. , 1994, The Journal of biological chemistry.

[63]  R. Parton,et al.  Regulated internalization of caveolae , 1994, The Journal of cell biology.

[64]  R. Pagano,et al.  Internalization and sorting of a fluorescent analogue of glucosylceramide to the Golgi apparatus of human skin fibroblasts: utilization of endocytic and nonendocytic transport mechanisms , 1994, The Journal of cell biology.

[65]  R. Parton,et al.  Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. , 1994, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[66]  M. Lisanti,et al.  Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells , 1993, The Journal of cell biology.

[67]  T. Sasaki,et al.  Regulatory role of GM3 ganglioside in alpha 5 beta 1 integrin receptor for fibronectin-mediated adhesion of FUA169 cells. , 1993, The Journal of biological chemistry.

[68]  P. Dupree,et al.  VIP21, a 21-kD membrane protein is an integral component of trans-Golgi- network-derived transport vesicles , 1992, The Journal of cell biology.

[69]  Richard G. W. Anderson,et al.  Caveolin, a protein component of caveolae membrane coats , 1992, Cell.

[70]  Deborah A. Brown,et al.  Sorting of GPI-anchored proteins to glycolipid-enriched membrane subdomains during transport to the apical cell surface , 1992, Cell.

[71]  White Ca,et al.  Solubility and posttranslational regulation of GP130/F11--a neuronal GPI-linked cell adhesion molecule enriched in the neuronal membrane skeleton. , 1992 .

[72]  R. Haugland,et al.  A novel fluorescent ceramide analogue for studying membrane traffic in animal cells: accumulation at the Golgi apparatus results in altered spectral properties of the sphingolipid precursor , 1991, The Journal of cell biology.

[73]  R. G. Anderson,et al.  Cholesterol controls the clustering of the glycophospholipid-anchored membrane receptor for 5-methyltetrahydrofolate , 1990, The Journal of cell biology.

[74]  E. Yamada THE FINE STRUCTURE OF THE GALL BLADDER EPITHELIUM OF THE MOUSE , 1955, The Journal of biophysical and biochemical cytology.

[75]  Robert G Parton,et al.  Clathrin-independent endocytosis: new insights into caveolae and non-caveolar lipid raft carriers. , 2005, Biochimica et biophysica acta.

[76]  S. Hakomori Organization and function of glycosphingolipids in membrane , 2005 .

[77]  L. Valentino,et al.  Gangliosides regulate tumor cell adhesion to collagen , 2004, Clinical & Experimental Metastasis.

[78]  T. Hyypiä,et al.  Clustering induces a lateral redistribution of α 2 β 1 integrin from membrane rafts to caveolae and subsequent PKC-dependent internalization , 2003 .

[79]  K. Roepstorff,et al.  Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. , 2002, Molecular biology of the cell.

[80]  R. Pagano,et al.  Changes in the spectral properties of a plasma membrane lipid analog during the first seconds of endocytosis in living cells. , 1997, Biophysical journal.

[81]  C. White,et al.  Solubility and posttranslational regulation of GP130/F11--a neuronal GPI-linked cell adhesion molecule enriched in the neuronal membrane skeleton. , 1992, European Journal of Cell Biology.