- Email: [email protected]
Coated vesicles
Cell 634
movie “Star Wars” was really episode 3. Although science is usually slow on the uptake, the series on Membrane Structure and Function by E. Edward Bittar adopts this trend with the release of volumes 1 and 3 but not 2. In general, the articles in these volumes are well written and attempt to give a broad, probing view of several areas of membrane biochemistry and biophysics. Though these areas are rapidly changing and the treatises include only literature published before summer, 1979, the articles present background material timely for people new to the field and raise important questions which have not yet been answered. The chapters provide good starting points for graduate students and investigators interested in obtaining an overview of certain membrane topics. The price of a single volume is not outrageous but is certainly sufficient to make one think twice before ordering the complete series for a personal library. Each volume contains four articles having from 100 to 442 references. Volume 1 considers the organization of biological membranes, model lipid systems and energy transduction. Only three topics are mentioned because articles by S. K. Malhotra and by J. M. Lackie both present a view of membrane organization. As a microscopist, Malhotra treats membrane organization and biogenesis with a sensitivity to how it relates to structures visible in the electron microscope. Lackie reiterates some of the structural concepts discussed by Malhotra and in addition discusses membrane functions such as phagocytosis and membrane fusion. Both authors attempt to cover large areas in a small space with occasionally incomplete results. The figures, although good quality photographs, generally do not highlight major concepts. In the chapter dealing with model lipid systems, Chapman raises many important questions relating to lipid organization in reconstituted lipid protein complexes. As a lipid physicist, however, he fails to treat the biochemical question of the “nativeness” of the protein in a reconstituted system. This information is germane to any conclusions to be drawn from studies of those systems. In the final chapter of Volume 1, Wilson provides a thoughtful treatise on energy transduction in biological membranes. It begins at a very basic level and through logical development considers many relevant aspects of the subject. The third volume of the Membrane Structure and Function Series begins with a comprehensive treatment of receptor-hormone interrelationships by Triggle. In a field replete with phenomenology, Triggle attempts to classify and organize the findings in a meaningful way. He presents experimental observations to defend or discredit current hypotheses. Many illustrative diagrams are provided to aid the reader in understanding the concepts in this very worthwhile chapter. Membrane fusion is discussed in the second chapter by Gratzl et al. Calcium ion fluxes dominate
current theories, but membrane fusion is not completely explained by this phenomenon. Although it does summarize some interesting observations on vesicle systems in vitro, the article leaves the reader stranded with “proteinaceous membrane components” and Ca++. Motility is creeping into all areas of cell biology, even membranes. The treatment of cell motility by Sleigh and Bell in the third chapter of this book is a well-considered treatise on the field. However, because motile systems in membranes have only been inferred from circumstantial evidence and microscopy, cell motility from the membrane viewpoint is a sparse topic. In the last chapter, De Mello provides a summary of intercellular communication and junctional permeability which is a good introduction to the field. It is well illustrated and treats both microscopic and electrical studies of junctions. Though information in several areas is incomplete, the books provide articles useful for graduate teaching or for the intellectually curious. Michael P. Sheetz Department of Physiology University of Connecticutt School of Medicine Farmington, Connecticutt
06032
A Budding Field in Cell Biology Coated Vesicles. C. D. Ockleford and A. Whyte, eds. Cambridge: Cambridge University Press. (1980). pp. $90.00.
344
One of the key steps in the translocation of membranes within cells has recently been glimpsed, and cell biologists with a variety of interests are focusing their attention and experimental skills on its further elucidation. That step is the formation of a membranous vesicle from a larger, preexisting membrane
VESICLE FORMATION
VESICLE TRANSLOCATION
VESICLE FUSION
Book 635
Reviews
compartment. This membrane “budding” is the first step in a dynamic process of membrane shuttling which is apparently occurring continuously in the Iiving cell, linking all of its internal membrane compartments with each other and with the plasma membrane at its surface (diagram). The essential steps of this membrane shuttling are vesicle formation from a “donor” compartment, vesicle translocation through the cytoplasm and vesicle fusion with an “acceptor” compartment. Carried along in the shuttle are, of course, small bites of the contents of the donor compartment, as well as the bit of membrane in the vesicle itself. The best known shuttle of this type-that worked out by Palade and colleagues-is the one that carries newly made proteins from the site of synthesis in the first membrane compartment, the one studded with ribosomes and called endoplasmic reticulum, through a series of intermediate compartments for protein processing and storage, until eventual discharge by vesicle fusion with the plasma membrane. A second well understood shuttle is that which carries bits of extracellular material into the cell by vesicle formation from the plasma membrane. Here, in the process of pinocytosis, is where the key new fact about membrane shuttling has emerged: the cell forms a special submembraneous network against the bit of membrane that is to be turned into a vesicle. Thus it generates a “coated vesicle.” The first multi-authored book to be spawned by that realization is appropriately called Coated Vesicles. It contains a series of reviews on how this realization came about, and what the submembranous network or “coat” might be doing. Unfortunately, the reviews in this book are for the most part very superficial, and they become irritatingly redundant when placed back to back, so the reader is forced to wade through heavy waters to glean the summaries of each author’s own particular contribution to this field. Unfortunately, too, the authors seem to have been chosen mainly by virtue of their proximity to the editors, either physically or by their common interest in protein pinocytosis through the placenta, rather than by the import of their contributions to the particular problem of coated vesicle formation. Missing from the list of authors are all the key figures in this field: -Tom Roth, who together with Keith Porter obtained the first electron micrographs of coated vesicles and showed that they originated by pinocytosis from the plasma membrane, and who has gone on since to study the construction and mechanism of formation of coated vesicles. -Ken Kadota, who first isolated and negatively stained coated vesicles, and had the interpretive brilliance to realize that the spiny coat seen in thin sections was actually a distorted image of a delicate cytoplasmic “basketwork” which surrounds such vesicles (photograph).
-Barbara Pearse, who first succeeded in purifying coated vesicles enough to determine their protein composition, who named their major protein “clathrin” by analogy with a chemical clathrate (which is a basket or cage-like structure surrounding something else) and who collaborated with expert structural biologists in Cambridge to carry the analysis of negatively stained coated vesicles to the level of the computer. (She was granted a one-page foreword in the book, which looks like an afterthought.) -Dick Anderson, Joe Goldstein and Mike Brown, who first showed that the membrane as well as the contents of forming coated vesicles is highly selected, and who have discovered a number of spontaneous human mutations that display distinct abnormalities in the mechanism by which this selection is brought about. (As an example of the shortcomings of this book, 8 of its 12 chapters review the work of these three investigators, each attempting to explain how that work illustrates the involvement of membrane receptors in the selection process. These reviews, however, are so garbled or abbreviated that they are barely intelligible, and only one of them focuses on the critical exciting issue of how the coat “recognizes” receptor-rich regions of the donor membrane compartment and selects them from the rest.)
Cell 636
The only substantive first-hand account in this book is the chapter by Rodewald, who has been the key figure in showing that coated vesicles are the shuttles for carrying membrane IgG receptors back and forth across cells in the neonatal intestine. This is how maternal antibodies get delivered unscathed to the infant’s circulation. Rodewald’s chapter is marred only by the stingy way his usually spectacular electron micrographs were cropped and reduced by the publisher (although they are still good compared with the other micrographs in this book, which are thoroughly second-rate). His chapter provides excellent reviews of work on the yoke sac and placenta, which are the other tissues that transfer antibodies and other proteins the way the intestine does. It thus eliminates the need for many of the other chapters. Another shortcoming of this book is that it focuses exclusively on the surface shuttle of pinocytosis and completely neglects all the internal membrane shuttles, where clathrin coats or “baskets” are just as involved in forming vesicles. Primary investigators not represented here include George Palade, Marilyn Farquhar, and associates, who have focused attention on the comings and goings of membranes shuttling through the Golgi apparatus inside the cell. They were the first to show that such shuttles are also coated vesicles, and they they are energy-dependent; yet no mention is made in this book of Palade’s recent demonstration that coats fall off the shuttle vesicles when cellular ATP is depleted (J. Cell Biol. 75, 371 a, 1977). [The only reference to the energetics or cellular control of this process made in the entire Coated Vesicle book-which is repeated in four chaptersis reference to an abstract of work performed by Nagura and Asai (J. Cell Biol. 70, 89A, 1976) which has still not been published in comprehensible form.] Also missing from the list of authors, and not referenced anywhere, is Jim Rothman, who has followed the transport of a viral product through the membrane compartments of infected cells, and has shown by advanced biochemical methods that the product becomes associated with clathrin-coated shuttle vesicles at two different stages in its maturation, once before and once after its residence in the Golgi apparatus. The cell biologist interested in this “budding” field could catch up more efficiently by reading a few of the appended references from the above-mentioned investigators, rather than wading through the catalog of second-hand reviews and speculations presented in this book. This would reveal much more clearly and directly the exciting problem of how all this vesicle shuttling is specified and controlled. For after all, membrane compartments in the cell remain physically separate and biochemically unique, in spite of the shuttling that goes on between them. Certainly, one step toward understanding the orderliness of this membrane circulation will come from an elucidation of
what role the clathrin coat plays in selecting and pinching off each membrane bit that is to be shuttled. John Heuser Department of Physiology Washington University School of Medicine St. Louis, Missouri 63110 References Farquhar, M. G. (1978). Traffic of products and membranes throughout the Golgi complex. Life Sciences Research Report 11, Transport of Macromolecules in Cellular Systems, S. Silverstein. ed. (Berlin: Dahlem Konferenzen). pp. 341-362. Goldstein, J.. Anderson, Ft. and Brown, N. (1979). Coated pits, coated vesicles, and receptor-mediated endocytosis. Nature 279, 679-685. Kanaseki, T. and Kadota. Cell Biol. 42, 202-220.
K. (1969).
Palade. G. E. (1975). Intracellular synthesis. Science 789, 347-358. Pearse, 8. M. F. (1980). 131-134.
Coated
The “vesicle
aspects vesicles.
in a basket.”
of the process Trends
J.
of protein
Biochem.
Sci. ? 7 t,
Aodewald. Ft. (1980). Distribution of immunoglobulin G receptors the small intestine of the young rat. J. Cell Biol. 85. 18-32.
in
Rothman, J.. Bursztyn-Pettigrew. H. and Fine, R. E. (1980). Transport of the membrane protein of vesicular stomatitis virus to the cell surface in two stages of clathrin-coated vesicles. J. Cell Biol. 86, 162-171. Woodward, M. and Roth, T. (1978). Coated vesicles: characterization. selective dissociation, and reassembly. Proc. Nat. Acad. Sci. USA 75. 4394-4398.
Justice for Developmental Developmental Biology By L. W. Browder. Philadelphia: Saunders $22.00.
College.
Biology
(1980).
602
pp.
Leon Browder’s Developmental Biology is one of the very few texts that does justice to this complex subject. It closely approaches what I see as my responsibility to students: to instill a sense of history and respect for those individuals who laid the foundations of developmental biology, the concepts they developed and the preconceptions under which they worked, and to lead the next generation of developmental biologists along a profitable path. Browder fully presents both modern concepts and their origins, backing up new ideas with original data obtained from “developmental systems,” and filling in gaps with data obtained from “non-developmental systems” where a phenomenon seems to be related
movie “Star Wars” was really episode 3. Although science is usually slow on the uptake, the series on Membrane Structure and Function by E. Edward Bittar adopts this trend with the release of volumes 1 and 3 but not 2. In general, the articles in these volumes are well written and attempt to give a broad, probing view of several areas of membrane biochemistry and biophysics. Though these areas are rapidly changing and the treatises include only literature published before summer, 1979, the articles present background material timely for people new to the field and raise important questions which have not yet been answered. The chapters provide good starting points for graduate students and investigators interested in obtaining an overview of certain membrane topics. The price of a single volume is not outrageous but is certainly sufficient to make one think twice before ordering the complete series for a personal library. Each volume contains four articles having from 100 to 442 references. Volume 1 considers the organization of biological membranes, model lipid systems and energy transduction. Only three topics are mentioned because articles by S. K. Malhotra and by J. M. Lackie both present a view of membrane organization. As a microscopist, Malhotra treats membrane organization and biogenesis with a sensitivity to how it relates to structures visible in the electron microscope. Lackie reiterates some of the structural concepts discussed by Malhotra and in addition discusses membrane functions such as phagocytosis and membrane fusion. Both authors attempt to cover large areas in a small space with occasionally incomplete results. The figures, although good quality photographs, generally do not highlight major concepts. In the chapter dealing with model lipid systems, Chapman raises many important questions relating to lipid organization in reconstituted lipid protein complexes. As a lipid physicist, however, he fails to treat the biochemical question of the “nativeness” of the protein in a reconstituted system. This information is germane to any conclusions to be drawn from studies of those systems. In the final chapter of Volume 1, Wilson provides a thoughtful treatise on energy transduction in biological membranes. It begins at a very basic level and through logical development considers many relevant aspects of the subject. The third volume of the Membrane Structure and Function Series begins with a comprehensive treatment of receptor-hormone interrelationships by Triggle. In a field replete with phenomenology, Triggle attempts to classify and organize the findings in a meaningful way. He presents experimental observations to defend or discredit current hypotheses. Many illustrative diagrams are provided to aid the reader in understanding the concepts in this very worthwhile chapter. Membrane fusion is discussed in the second chapter by Gratzl et al. Calcium ion fluxes dominate
current theories, but membrane fusion is not completely explained by this phenomenon. Although it does summarize some interesting observations on vesicle systems in vitro, the article leaves the reader stranded with “proteinaceous membrane components” and Ca++. Motility is creeping into all areas of cell biology, even membranes. The treatment of cell motility by Sleigh and Bell in the third chapter of this book is a well-considered treatise on the field. However, because motile systems in membranes have only been inferred from circumstantial evidence and microscopy, cell motility from the membrane viewpoint is a sparse topic. In the last chapter, De Mello provides a summary of intercellular communication and junctional permeability which is a good introduction to the field. It is well illustrated and treats both microscopic and electrical studies of junctions. Though information in several areas is incomplete, the books provide articles useful for graduate teaching or for the intellectually curious. Michael P. Sheetz Department of Physiology University of Connecticutt School of Medicine Farmington, Connecticutt
06032
A Budding Field in Cell Biology Coated Vesicles. C. D. Ockleford and A. Whyte, eds. Cambridge: Cambridge University Press. (1980). pp. $90.00.
344
One of the key steps in the translocation of membranes within cells has recently been glimpsed, and cell biologists with a variety of interests are focusing their attention and experimental skills on its further elucidation. That step is the formation of a membranous vesicle from a larger, preexisting membrane
VESICLE FORMATION
VESICLE TRANSLOCATION
VESICLE FUSION
Book 635
Reviews
compartment. This membrane “budding” is the first step in a dynamic process of membrane shuttling which is apparently occurring continuously in the Iiving cell, linking all of its internal membrane compartments with each other and with the plasma membrane at its surface (diagram). The essential steps of this membrane shuttling are vesicle formation from a “donor” compartment, vesicle translocation through the cytoplasm and vesicle fusion with an “acceptor” compartment. Carried along in the shuttle are, of course, small bites of the contents of the donor compartment, as well as the bit of membrane in the vesicle itself. The best known shuttle of this type-that worked out by Palade and colleagues-is the one that carries newly made proteins from the site of synthesis in the first membrane compartment, the one studded with ribosomes and called endoplasmic reticulum, through a series of intermediate compartments for protein processing and storage, until eventual discharge by vesicle fusion with the plasma membrane. A second well understood shuttle is that which carries bits of extracellular material into the cell by vesicle formation from the plasma membrane. Here, in the process of pinocytosis, is where the key new fact about membrane shuttling has emerged: the cell forms a special submembraneous network against the bit of membrane that is to be turned into a vesicle. Thus it generates a “coated vesicle.” The first multi-authored book to be spawned by that realization is appropriately called Coated Vesicles. It contains a series of reviews on how this realization came about, and what the submembranous network or “coat” might be doing. Unfortunately, the reviews in this book are for the most part very superficial, and they become irritatingly redundant when placed back to back, so the reader is forced to wade through heavy waters to glean the summaries of each author’s own particular contribution to this field. Unfortunately, too, the authors seem to have been chosen mainly by virtue of their proximity to the editors, either physically or by their common interest in protein pinocytosis through the placenta, rather than by the import of their contributions to the particular problem of coated vesicle formation. Missing from the list of authors are all the key figures in this field: -Tom Roth, who together with Keith Porter obtained the first electron micrographs of coated vesicles and showed that they originated by pinocytosis from the plasma membrane, and who has gone on since to study the construction and mechanism of formation of coated vesicles. -Ken Kadota, who first isolated and negatively stained coated vesicles, and had the interpretive brilliance to realize that the spiny coat seen in thin sections was actually a distorted image of a delicate cytoplasmic “basketwork” which surrounds such vesicles (photograph).
-Barbara Pearse, who first succeeded in purifying coated vesicles enough to determine their protein composition, who named their major protein “clathrin” by analogy with a chemical clathrate (which is a basket or cage-like structure surrounding something else) and who collaborated with expert structural biologists in Cambridge to carry the analysis of negatively stained coated vesicles to the level of the computer. (She was granted a one-page foreword in the book, which looks like an afterthought.) -Dick Anderson, Joe Goldstein and Mike Brown, who first showed that the membrane as well as the contents of forming coated vesicles is highly selected, and who have discovered a number of spontaneous human mutations that display distinct abnormalities in the mechanism by which this selection is brought about. (As an example of the shortcomings of this book, 8 of its 12 chapters review the work of these three investigators, each attempting to explain how that work illustrates the involvement of membrane receptors in the selection process. These reviews, however, are so garbled or abbreviated that they are barely intelligible, and only one of them focuses on the critical exciting issue of how the coat “recognizes” receptor-rich regions of the donor membrane compartment and selects them from the rest.)
Cell 636
The only substantive first-hand account in this book is the chapter by Rodewald, who has been the key figure in showing that coated vesicles are the shuttles for carrying membrane IgG receptors back and forth across cells in the neonatal intestine. This is how maternal antibodies get delivered unscathed to the infant’s circulation. Rodewald’s chapter is marred only by the stingy way his usually spectacular electron micrographs were cropped and reduced by the publisher (although they are still good compared with the other micrographs in this book, which are thoroughly second-rate). His chapter provides excellent reviews of work on the yoke sac and placenta, which are the other tissues that transfer antibodies and other proteins the way the intestine does. It thus eliminates the need for many of the other chapters. Another shortcoming of this book is that it focuses exclusively on the surface shuttle of pinocytosis and completely neglects all the internal membrane shuttles, where clathrin coats or “baskets” are just as involved in forming vesicles. Primary investigators not represented here include George Palade, Marilyn Farquhar, and associates, who have focused attention on the comings and goings of membranes shuttling through the Golgi apparatus inside the cell. They were the first to show that such shuttles are also coated vesicles, and they they are energy-dependent; yet no mention is made in this book of Palade’s recent demonstration that coats fall off the shuttle vesicles when cellular ATP is depleted (J. Cell Biol. 75, 371 a, 1977). [The only reference to the energetics or cellular control of this process made in the entire Coated Vesicle book-which is repeated in four chaptersis reference to an abstract of work performed by Nagura and Asai (J. Cell Biol. 70, 89A, 1976) which has still not been published in comprehensible form.] Also missing from the list of authors, and not referenced anywhere, is Jim Rothman, who has followed the transport of a viral product through the membrane compartments of infected cells, and has shown by advanced biochemical methods that the product becomes associated with clathrin-coated shuttle vesicles at two different stages in its maturation, once before and once after its residence in the Golgi apparatus. The cell biologist interested in this “budding” field could catch up more efficiently by reading a few of the appended references from the above-mentioned investigators, rather than wading through the catalog of second-hand reviews and speculations presented in this book. This would reveal much more clearly and directly the exciting problem of how all this vesicle shuttling is specified and controlled. For after all, membrane compartments in the cell remain physically separate and biochemically unique, in spite of the shuttling that goes on between them. Certainly, one step toward understanding the orderliness of this membrane circulation will come from an elucidation of
what role the clathrin coat plays in selecting and pinching off each membrane bit that is to be shuttled. John Heuser Department of Physiology Washington University School of Medicine St. Louis, Missouri 63110 References Farquhar, M. G. (1978). Traffic of products and membranes throughout the Golgi complex. Life Sciences Research Report 11, Transport of Macromolecules in Cellular Systems, S. Silverstein. ed. (Berlin: Dahlem Konferenzen). pp. 341-362. Goldstein, J.. Anderson, Ft. and Brown, N. (1979). Coated pits, coated vesicles, and receptor-mediated endocytosis. Nature 279, 679-685. Kanaseki, T. and Kadota. Cell Biol. 42, 202-220.
K. (1969).
Palade. G. E. (1975). Intracellular synthesis. Science 789, 347-358. Pearse, 8. M. F. (1980). 131-134.
Coated
The “vesicle
aspects vesicles.
in a basket.”
of the process Trends
J.
of protein
Biochem.
Sci. ? 7 t,
Aodewald. Ft. (1980). Distribution of immunoglobulin G receptors the small intestine of the young rat. J. Cell Biol. 85. 18-32.
in
Rothman, J.. Bursztyn-Pettigrew. H. and Fine, R. E. (1980). Transport of the membrane protein of vesicular stomatitis virus to the cell surface in two stages of clathrin-coated vesicles. J. Cell Biol. 86, 162-171. Woodward, M. and Roth, T. (1978). Coated vesicles: characterization. selective dissociation, and reassembly. Proc. Nat. Acad. Sci. USA 75. 4394-4398.
Justice for Developmental Developmental Biology By L. W. Browder. Philadelphia: Saunders $22.00.
College.
Biology
(1980).
602
pp.
Leon Browder’s Developmental Biology is one of the very few texts that does justice to this complex subject. It closely approaches what I see as my responsibility to students: to instill a sense of history and respect for those individuals who laid the foundations of developmental biology, the concepts they developed and the preconceptions under which they worked, and to lead the next generation of developmental biologists along a profitable path. Browder fully presents both modern concepts and their origins, backing up new ideas with original data obtained from “developmental systems,” and filling in gaps with data obtained from “non-developmental systems” where a phenomenon seems to be related