Mullock, Ph. Terlecky, Ph. Chapter 1 Paul A. Walton, Ph. Chapter 6 Erik Snapp, Ph. Chapter 4 Chapter 9 Chapter 9 PREFACE The evolution of modern cell biology tools, such as confocal imaging techniques and advanced electron microscopy methodologies, has allowed for ever improving structural and functional characterizations of the cell. Such methods complement classical genetics and biochemistry in the ongoing effort to define cellular science.
This is especially apparent in the area of organelle biology. Studies dating back over years to the present have revealed the elaborate collection of distinctive membrane-bound cytoplasmic subcompartments, termed organelles, within the eukaryotic cell and defined their roles in mediating numerous specialized functions in cellular physiology. Organelles play an essential role in the cell in large part through ensuring a tight regulatory and functional separation of distinct chemical reactions, such as cellular respiration, and molecular processes, such as protein degradation and DNA replication.
Many organelles are common to virtually all cell types e. The unique characteristics of such heterogeneous cellular organelles are dictated by their particular biochemical composition and complement of biomolecules. The Biogenesis of Cellular Organelles seeks to describe the cellular and molecular mechanisms mediating the biogenesis, maintenance, and function of key eukaryotic organelles. This work consists of an initial discussion of the evolution of organelle biogenesis theory from early studies through recent findings, overviews of the prominent cellular machineries involved in the biogenesis and maintenance of cellular organelles, and reviews of the function and biogenesis of a number of key organelles common to nearly all eukaryotic cells, including the endoplasmic reticulum, the Golgi apparatus, the lysosome, the nucleus, the mitochondria, and the peroxisome.
All chapters strive to highlight recent findings and topical issues relating to organelle biology. The primary interests of this work are the biogenesis and functional events operating in mammalian cells and in some cases the analogous events in key lower eukaryotes, such as yeast and Drosophila. The reader should note that a wealth of organelles besides those covered here have also been described, such as the all important chloroplast present in plants and other photosynthetic organisms.
The general themes of each chapter are as follows: Chapter one offers a historical perspective of organelle biogenesis. This chapter recounts early discoveries that formed the foundation for the modern study of organelle biology, including the role of protein sorting in organelle maintenance and methods of organelle inheritance during cell division.
In this chapter the progression from early findings to more recent discoveries in developing our current views of organelle function and biogenesis are highlighted. Chapter two presents an in depth discussion of protein coats, which in concert with additional components of the cellular machinery operate to selectively sort proteins within intracellular and endocytic trafficking pathways.
In this function protein coats serve as key mediators of organelle biogenesis and maintenance. The protein coat constituents described include the adaptor protein AP complexes and clathrin, which operate in the late-secretory and endocytic pathways, and the COP complexes, which operate in the early secretory pathway. The recently defined adaptor-related coat proteins, the GGAs and Stoned B family members, are also reviewed. Chapter three describes the cooperative role played by lipids and proteins in maintaining organelle identity and function in the face of continuous biomolecular flux between compartments and to and from the plasma membrane.
Chapter four provides an extensive description of the organization, function, and maintenance of the endoplasmic reticulum. The remarkably dynamic nature and morphological variability of the endoplasmic reticulum are detailed along with its numerous cellular roles, including serving as the primary site for membrane protein synthesis and entry into the secretory pathway. The contribution of proliferation and differentiation of existing membranes to the generation of endoplasmic reticulum networks are also reviewed. Chapter five reviews classical and recent findings relating to the Golgi apparatus, which functions as a site for post-translational modifications of glycoproteins and glycolipids and for the selective sorting of secretory proteins to the plasma membranes or target sites within the cell.
The complex morphology of the Golgi, which allows compartmentalization of distinct Golgi functions, and the dynamics of its disassembly and reassembly during the cell cycle are highlighted. Chapter six discusses the function and biogenesis of the lysosome. The role of the lysosome, and the analogous yeast vacuole, as the primary degradative compartment in the cell and current models for the biogenesis of lysosomes and related compartments are discussed. The participation of the protein sorting machinery in lysosomal maintenance and function are described.
Also, the importance of the lysosome to cellular function is illustrated through discussions of a number of mutant phenotypes resulting from perturbation of lysosomal protein sorting. Chapter seven offers a review of nuclear biogenesis, or nucleogenesis. This chapter focuses on the dynamic disassembly and reassembly of the nuclear envelope during mitotic division and the cellular machinery mediating these processes. The biogenesis of nucleoli, the nuclear structures that serve as sites for ribosome biosynthesis, is also detailed.
Chapter eight reviews the function, intricate structure, and biogenesis of the mitochondria, which serves as the site of cellular respiration. The unique nature of this organelle, which has prokaryotic origins and still retains it own small genome, is described, as is its essential nature in the physiology of the cell. The mode of mitochondrial biogenesis through growth and division of pre-existing mitochondria is detailed. The pathways for mitochondrial protein import and export and ion trafficking are also reviewed.
Chapter nine presents an overview of peroxisome biogenesis and function. Potential modes of formation of the peroxisome, which represent an organelle rich in metabolic enzymes and activities, are discussed along with cellular factors that contribute to its biogenesis and function. This work also details the numerous peroxisomal disorders in humans, which highlights the need to address the many unanswered questions regarding the biology of this important organelle.
While the discoveries described in The Biogenesis of Cellular Organelles and elsewhere illustrate our growing understanding of the fundamental processes mediating organelle biogenesis and function, they also remind us of how much remains to be discovered. The pursuit of knowledge regarding organelle biology is essential to understanding the basic science of the cell as well as human physiology.
This is clearly evident from the growing observations that associate defects in organelle function to human disease. With the continued dedication of basic and clinical scientists to addressing these important questions ensured, the future of cellular biology is sure to be one of remarkable discovery. Chris Mullins, Ph. National Institutes of Health I would like to acknowledge Dr.
Josephine Briggs, Dr. Juan S. Bonifacino, and Dr. Leroy M. Nyberg, Jr. Special thanks are extended to Dr. Rosa Puertollano for her kind and generous advice and assistance during the completion of this book. Most of all I thank the many contributors for their valuable time, exhaustive effort, and patience in the development of this project. This work is dedicated to them and all the basic and clinical researchers who strive to understand the biology of the eukaryotic cell.
Paul Luzio Abstract O rganelles, defined as intracellular membrane-bound structures in eukaryotic cells, were described from the early days of light microscopy and the development of cell theory in the 19th century. During the 20th century, electron microscopy and subcellular fractionation enabled the discovery of additional organelles and, together with radiolabelling, allowed the first modern experiments on their biogenesis.
Over the past 30 years, the development of cell-free systems and the use of yeast genetics have together established the major pathways of delivery of newly synthesised proteins to organelles and the vesicular traffic system used to transfer cargo between organelles in the secretory and endocytic pathways. Mechanisms of protein sorting, retrieval and retention have been described and give each organelle its characteristic composition.
Insights have been gained into the mechanisms by which complex organelle morphology can be established. Organelle biogenesis includes the process of organelle inheritance by which organelles are divided between daughter cells during mitosis. Two inheritance strategies have been described, stochastic and ordered, which are not mutually exclusive.
Among the major challenges of the future are the need to understand the role of self-organization in ensuring structural stability and the mechanisms by which a cell senses the status of its organelles and regulates their biogenesis. Introduction Today, cell biologists are almost overwhelmed by molecular detail about organelle composition, structure, function and biogenesis. Nevertheless during the molecular era, which has encompassed the past half century, a conceptual framework has developed to explain processes such as protein sorting, membrane traffic and organelle biogenesis.
In this chapter we review this development, together with earlier work that established the existence of organelles and traffic to them. Necessarily, we cannot include specific detail about all organelles and we have concentrated, for the most part, on those found on the secretory and endocytic pathways. Definitions Organelles are defined as intracellular membrane-bound structures in eukaryotic cells, usually specialized for a particular function. Among the former are the nucleus, mitochondria and organelles in the secretory and endocytic pathways including the endoplasmic reticulum, Golgi complex, endosomes and lysosomes vacuoles in yeast , whereas the latter include chloroplasts restricted to the plant kingdom.
In mammalian cells there has been much study of cell type-specific specialist organelles and their relationship to common organelles. Many, if not all, of these are specialized structures in the secretory and endocytic pathways and include, for example, regulated secretory granules in neuroendocrine cells3 and melanosomes,4 which are clearly lysosome-like, in skin melanocytes. Organelle biogenesis is the process by which new organelles are made.
However, the amount of DNA in such organelles can encode only a very small number of the many proteins required.
Organelle biogenesis - Wikipedia
In general it is thought that new organelles are derived by proliferation of preexisting organelles. In , Brown observed and described the nucleus, the first organelle. By the early 20th century, the osmotic properties of red blood cells had extended the concept of the plasma membrane to mammalian cells, but it was not until the classic experiment of Gorter and Grendel published in that the basic structure of the plasma membrane was shown to consist of a bilayer of phospholipid.
In this experiment, the surface area of a compressed film of total lipid extracted from a known number of red blood cells was measured and found to be twice the total cell area. The phospholipid bilayer was incorporated as a central feature in many subsequent models of the structure of both the plasma membrane and intracellular membranes, culminating in the fluid mosaic model of Singer and Nicholson in which integral membrane proteins were distributed within the bilayer.
Brown8 had suggested the possibility of a nuclear membrane and in Flemming14 summarised the evidence for its reality. The nucleolus had been observed as a feature of some nuclei many times; over articles on the subject had appeared before the classic paper by Montgomery in The increasing use of chemicals, which preferentially stained some parts of the cell, led to more accurate descriptions of cell structure, although concerns over artefacts had to be addressed.
In , Golgi24 demonstrated the existence of the Golgi complex by staining with heavy metals such as silver nitrate or osmium tetroxide. The reality of this organelle, however, continued to be doubted until the mid s when electron micrographs became available. However, a parallel interest in taking cells apart and studying the nature of the separated components also yielded invaluable information; the existence of lysosomes was established before they were seen. Information as to the chemical nature and function of organelles was sought as early as by Bensley and Hoerr,26 who made a crude preparation of mitochondria.
Claude in used similar procedures with a crucial difference. He also examined the size, shape and fine structure of the particulates in the separated fractions and used an isotonic medium for homogenisation. In Hogeboom, Schneider and Palade 29 improved his methodology by using a Potter-Elvehjem homogeniser to achieve quantitative gentle breakage of liver cells and sucrose in place of saline. Enzymes such as cytochrome oxidase, which appeared mostly in the large granule fraction, were clearly mitochondrial. However, the work of de Duve from onwards demonstrated the existence of a group of enzymes, which were sedimented in the large granule fraction only if relatively high speeds were used in its preparation.
The large granule fraction could be separated into a heavy and a light fraction. The former contained the respiratory activity characteristic of mitochondria but the light fraction contained variegated hydrolases. These were only measurable when the preparation had been subjected to hypotonic media, detergents or other insults to membrane integrity. From these results, de Duve hypothesised the existence of organelles containing primarily hydrolases and named them lysosomes. This necessitated the development of adequate fixing, staining, embedding and sectioning techniques as well as the development of the instruments themselves.
However, the electron microscope also revealed structures which the light microscope was completely unable to resolve. The continuous nature of the meshes could only be demonstrated by tedious serial sectioning, although much more detailed structure could be observed and many different tissues examined to show the ubiquity of the organelle. The dynamic nature of such vesicles and of most other organelles began to be revealed when, in , Jamieson and Palade used radioactive tracers and electron microscopic autoradiography.
By , Palade, if not every worker in the field, believed that movement of material through these organelles depended on vesicular traffic. Phagocytosis was observed as early as , but the fact that endocytosis was of widespread occurrence in animal cells was recognized only in the mid s by electron microscopy. Quantitative electron microscopic investigations in by Steinman, Brodie and Cohn43 showed that tissue culture cells internalized plasma membrane at a rate which greatly exceeded their biosynthetic capacity. Therefore, a mechanism had to exist whereby endocytosed membrane could be recycled to the plasma membrane.
Protein Synthesis and Targeting Although Palade had established that newly synthesised secretory proteins crossed into the lumen of the endoplasmic reticulum, it required the experiments of Blobel and his colleagues to establish that this sorting and targeting event was mediated by a sequence motif within the primary sequence of the secretory protein, which was named the signal sequence. This cell-free system was a powerful forerunner of many others established elsewhere which faithfully recapitulated individual steps in organelle biogenesis pathways.
The signal hypothesis also led directly to the concept that specific sequences within a protein could direct its targeting to a particular organelle. Thus, different consensus sequences have since been recognized as targeting motifs for import into mitochondria,46 chloroplasts,47 peroxisomes,48 nuclei49 and for the targeting of membrane proteins on secretory and endocytic pathways. Subsequent to the discovery of consensus sequences targeting proteins to particular organelles, there has been much work over the past 20 years identifying the protein machinery required for transport into such organelles, leading to an extensive understanding of transport to the mitochondrial matrix,46 inner membrane,50 outer membrane,51 into chloroplasts,52 into peroxisomes53 and through nuclear pores.
The discovery of clathrin by Pearse in the s61 provided the first coat component of vesicles involved in membrane traffic. However, it was during the s that elucidation of the molecular machinery of vesicular traffic started in earnest with the reconstitution of individual traffic steps in cell-free systems from animal cells62 and the isolation of secretory mutants in yeast. Vesicular traffic resulted in addition of radioactive N-acetylglucosamine to the VSV-G as a result of the activity of the transferase in the wild type Golgi membranes.
This assay led directly to the discovery of COPI coat protein I coated vesicles65 and the discovery of components of the general cytosolic fusion machinery required for vesicle fusion with acceptor membranes throughout the secretory and endocytic pathways. Similarly, cell-free assays were established to look at the breakdown and reformation of organelles during cell division. The isolation of secretion sec mutants in the budding yeast Saccharomyces cerevisiae63 provided a powerful approach to identify proteins required for traffic through the secretory pathway and to study their function.
Throughout the s and s many proteins necessary for membrane traffic on the secretory pathway were identified almost at the same time, either by fractionating mammalian cytosol or through characterization of yeast mutants. Mechanisms for organelle biogenesis in the secretory and endocytic pathways. A Vesicular traffic. A coated vesicle buds from a donor organelle, loses its coat and fuses with an acceptor organelle. The coat made up of cytosolic proteins denoted by black ovals and gray circles - refer to legend for designations of individual factors both deforms the donor membrane to form the vesicle and sorts into the vesicle only those proteins checked boxes selected for delivery.
B Maturation. An organelle is formed from the preceding organelle in a pathway by retrieval of those proteins hatched boxes which should not be in the final organelle, using retrograde vesicular traffic to deliver them to an earlier stage in the pathway. Additional proteins stippled boxes may be delivered to the organelle by vesicular traffic from other sources e. Thus, when organelles are formed by anterograde vesicular traffic, retrieval may still be used to ensure that mis-sorted proteins are returned to their correct residence.
Very soon it was realized that there were at least two classes of clathrin coated vesicles in cells, one predominantly Golgi-associated, subsequently shown to be involved in budding from the trans-Golgi network and the other at the plasma membrane responsible for a major endocytic uptake route. The two classes of clathrin-coated vesicles were distinguished by the presence of two different heterotetrameric adaptor protein complexes, AP-1 at the trans-Golgi network and AP-2 at the plasma membrane.
Work in several laboratories showed that the adaptors were involved in cargo sorting as well as recruitment of clathrin to the membrane.
In mammalian cells GGAs are important in trafficking mannose 6-phosphate receptors and associated newly synthesised mannose 6-phosphate—tagged acid hydrolases to the endosomes for delivery to lysosomes. AP-1 is most likely involved in traffic back to the trans-Golgi network of the empty mannose 6-phosphate receptors. AP-3 is required for efficient delivery of newly synthesised membrane proteins to lysosomes and lysosome-related organelles.
Mutations in AP-3 occur naturally in animals including fruit flies i. Once mechanical invagination of the donor membrane to form the vesicle is complete, pinching off occurs, mediated at least in part by the action of the GTPase dynamin. The first coat to be identified for vesicular traffic in this part of the secretory pathway was COPI using the cell-free assays described above.
These five proteins are necessary and sufficient to produce COPII vesicles from endoplasmic reticulum microsomes or from chemically defined liposomes. Indeed they might be regarded as the first organelles to be reconstituted solely from purified components since they fulfill the essential criteria to be called organelles in being intracellular membrane-bound structures in eukaryotic cells. Vesicular traffic between donor and acceptor organelles in the secretory and endocytic pathways requires not only vesicle formation, but subsequent loss of the vesicle coat and fusion with the acceptor organelle.
Once the vesicle reaches its target acceptor organelle, membrane fusion can occur, utilizing a common cytosolic fusion machinery and cognate interacting membrane proteins specific to the particular vesicle and organelle. Discovery of the common cytosolic fusion machinery derived from the observation that low concentrations of the alkylating agent N-ethylmaleimide NEM inhibited many membrane traffic steps reconstituted in cell-free systems. A classification of SNAREs based on sequence alignments of the helical domains and structural features observed in the crystal structure of the synaptic SNARE fusion complex82 has been proposed.
Theory of Organelle Biogenesis: A Historical Perspective 9 Although cognate SNARE proteins can be reconstituted into liposomes and themselves act as phospholipid bilayer fusion catalysts,80,85,86 membrane fusion within the cell requires the functional involvement of other proteins. Most current models of fusion suggest three steps, tethering of the vesicle to the target organelle, SNARE complex formation and phospholipid bilayer fusion.
A class of small GTPases known as rab proteins was identified as generally important when it was shown that different rabs localize to different organelles on the secretory and endocytic pathways. To allow the organelles to retain their integrity as well as to ensure efficient traffic of cargo by vesicles requires mechanisms for sorting proteins into vesicles, to retrieve proteins that have been inappropriately delivered to another organelle and to retain proteins in an organelle Fig. Efficient sorting of cell surface membrane receptors into clathrin coated pits was recognized at an early stage in their biochemical characterization.
By the late s it was recognised that while some receptors are concentrated into clathrin-coated pits, other plasma membrane proteins are effectively excluded such that the pits act as molecular filters. The mutation leading to this phenotype was an amino acid substitution in the cytoplasmic domain resulting in a cysteine replacing a tyrosine.
Cytoplasmic tail sequence motifs containing tyrosine and dileucine are now recognized as being important not only for internalization from the cell surface but also for targeting to organelles within the secretory and endocytic pathways. Different coated vesicle adaptor proteins show subtle differences in specificity for such sequences. The structural basis for such differences is unclear. The concept of retrieval derived initially from studies of lumenal proteins in the endoplasmic reticulum. The identity of an organelle is not maintained solely by retrieval but also by retention.
Perhaps the clearest example of this is in the cisternae of the Golgi complex where a variety of glycosyl transferases must be retained to carry out their function in the biosynthesis of glycoproteins. These enzymes are type II membrane proteins with trans-membrane domains that are, on average, five amino acids shorter than the trans-membrane domains of plasma membrane proteins. A dramatic example of this is seen in the case of the Golgi complex where it is clear that the observed morphology in part reflects the interaction of the structure with the cytoskeleton via appropriate motor proteins and in part the function of matrix proteins in the organization of the cisternae.
In the case of the Golgi complex, there has long been a debate about how secreted proteins pass through it. However, electron microscopy studies of large macromolecules, including algal scales and collagen aggregates favoured a maturation model with new cisternae forming on the cis-side and mature ones fragmenting from the trans-side. The cisternal maturation model has been refined to encompass data on retrograde vesicular traffic in COPI coated vesicles such that the present consensus is that most, if not all, anterograde movement through the Golgi complex is the result of cisternal progression with retrograde vesicular traffic ensuring that the polarized distribution of Golgi enzymes in the cisternal stack is maintained Fig.
Theory of Organelle Biogenesis: A Historical Perspective 11 Experiments in which secreted proteins tagged with green fluorescent protein have been imaged as they leave the Golgi complex in living cells have shown that large tubular carriers are particularly important for constitutive traffic to the cell surface.
As in the secretory pathway, vesicular traffic between individual organelles does not explain all steps in the pathway. Clathrin-coated vesicles budding from the plasma membrane comprise a very important, but not sole, mechanism of delivery from the plasma membrane to early endosomes defined historically as the first endosomal compartment to be entered by endocytosed ligands. Traffic from early to late endosomes, found deeper within the cell, has been studied extensively and is mediated by large endocytic carrier vesicles which some regard as matured early endosomes.
In addition to heterotypic fusion between late endosomes and lysosomes, the endocytic pathway is characterized by the occurrence of homotypic fusions between early endosomes and between late endosomes. These homotypic fusion events are also SNARE-mediated, and allow continuous remodelling of these organelles. Organelles in the late endocytic pathway are characterised by the presence of numerous internal vesicles, leading to the alternative description of late endosomes as multivesicular bodies. Some cell surface receptors are sorted into such vesicles after internalization from the plasma membrane and prior to degradation.
Recently, insights have been gained into the molecular mechanisms by which proteins are sorted into these vesicles, which have a different lipid composition from the limiting membrane of the organelle. Such mechanisms include partitioning into lipid microdomains, dependent on the composition of trans-membrane domains, and ubiquitination of cytoplamic tail domains followed by recognition of the ubiquinated domain by protein complexes involved in inward vesiculation. During the cell cycle, each organelle must double in size, divide and be delivered appropriately to the daughter cells.
Historically, the inheritance of organelles was recognised as occurring over the same period of the late 19th and early 20th centuries as the basic mechanics of mitosis were being described. The first is stochastic, relying on the presence of multiple copies of an organelle randomly distributed throughout the cytoplasm and the second is ordered, often, but not always, using the mitotic spindle as a means of partitioning Fig.
The morphology of many organelles may differ in different cell types, which itself may be related to the use of one or other of these strategies to a greater or lesser extent. Mitochondria, for example are, in many cells, multiple copies of small bean shaped structures, but in the budding yeast S.
The steady-state morphology of mitochondria which continuously grow, divide and fuse throughout the cell cycle is 12 The Biogenesis of Cellular Organelles Figure 2. Mechanisms for organelle inheritance during mitosis. These are apportioned by chance to the daughter cells where the organelle is reassembled. In contrast to mitochondria, the endoplasmic reticulum is always a single copy organelle, albeit a dynamic reticulum. This breaks down into tubular vesicular elements during cell division to a variable extent.
It often fragments little, thus segregation of equal amounts into daughter cells during mitosis may rely mainly on the uniform and extensive distribution of the endoplasmic reticulum network throughout the cytoplasm of the mother cell. At the end of mitosis the nuclear envelope rapidly reassembles around daughter chromosomes. During the s, nuclear envelope breakdown in animal cells was shown to involve depolymerisation of the lamina underlying the membrane, fragmentation of the membrane and dissassembly of nuclear pore complexes.
Using Xenopus oocytes, which contain many nuclear components stored for use in early development, it was observed that injection Theory of Organelle Biogenesis: A Historical Perspective 13 of bacteriophage lambda DNA or its addition to cell-free extracts was sufficient to trigger nuclear assembly. In the first, proposed by Warren, the Golgi complex breaks down into vesicle clusters and shed vesicles which are distributed stochastically between the daughter cells where they reassemble in telophase.
Kondo and colleagues recently found that prevention of Golgi dissassembly, by microinjection of a nonphosphorylated mutant form of a soluble protein required for this process, had no effect on equal partitioning of the Golgi to daughter cells. Recently Misteli has suggested that the generation of an overall stable configuration in such dynamic structures is consistent with organelle morphology being determined by self-organization. Self-organization will ensure structural stability without loss of plasticity.
Self-organization is an interesting concept, but how organelles self-organize is unclear. What is certain is that future investigations will lead us to a better understanding of the molecular machinery of organelle biogenesis and inheritance. Such investigations are likely to address a number of questions to which we have few answers at present. These include the role of lipids, in particular lipid-protein interactions in microdomains, in determining morphology and the regulation of the size, shape and number of organelles in cells.
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Bestselling Series. Harry Potter. Popular Features. New Releases. Description The Biogenesis of Cellular Organelles represents a comprehensive summary of recent advances in the study of the biogenesis and functional dynamics of the major organelles operating in the eukaryotic cell. This book begins by placing the study of organelle biogenesis in a historical perspective by describing past scientific strategies, theories, and findings and relating these foundations to current investigations.
Reviews of protein and lipid mediators important for organelle biogenesis are then presented, and are followed by summaries focused on the endoplasmic reticulum, Golgi, lysosome, nucleus, mitochondria, and peroxisome. Product details Format Paperback pages Dimensions x x Other books in this series. Stage-Structured Populations Bryan Manly.
Add to basket. Immunobiology of Carbohydrates Simon Wong. Calreticulin Paul Eggleton. Zinc Finger Proteins Shiro Luchi. Lipid transfer and metabolism across the endolysosomal-mitochondrial boundary. Tiziana Daniele , Maria Vittoria Schiaffino. Savushkin , Alexander D Dergunov. Mitochondrial activity in T cells. References Publications referenced by this paper. Sandip Patel , Roberto Docampo. Friedman , Brant M. Webster , David N.