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A new take on the old
This section is our way of celebrating 50 years of magnificent cell biology in the pages of the Journal of Cell Biology. It is, to a first approximation, chronological, but by necessity far from exhaustive. We consciously set out to sketch some high points in the history of the Journal, but not to cover the entirety of cell biology. Papers from other journals are, however, always cited when appropriate.
The selection of articles to be covered will always be a subjective process. We tried to improve these judgements by using multiple sources of information: older review articles, citation frequencies and, most importantly, the recommendations of past and present JCB editorial board members. Sincere thanks to all those who provided suggestions and helped with context and first-hand accounts of research—research that happened many years ago but that provides many salient lessons for cell biologists working today.
The first forty years
After highlighting papers from the first 40 years of the JCB, this marks the completion, at least for now, of the “From the Archive” series. We hope you will use this series as a sampler, and continue to enjoy the astonishing work contained within the entire online JCB archive.
William Wells
News Editor
| From Past Issues: |
The
discovery of synaptic vesicles
The visualization of the messengers of the synapse — synaptic
vesicles — gives the hypothesis of quantal transmitter release a structural
correlate.
Catching sight of lysosomes
Lysosomes are identified by Christian deDuve when a membrane barrier gradually
dissolves, thus yielding the tell-tale release of an enzyme activity over
time.
The invention of freeze fracture
EM and the determination of membrane structure
Russell Steere introduces his home-made contraption for freeze fracture electron
microscopy (EM), and Daniel Branton uses it to conclude that membranes are
bilayers.
Cilia get arms for bending
Björn Afzelius identifies cilia arms and comes up with the filament sliding
model of cilia movement. The sliding is visualized first by Peter Satir and more
directly by Ian Gibbons.
Heterochromatin
is late
Antonio Lima-de-Faria shows that heterochromatin replicates later than euchromatin.
How to spot a satellite cell
Based on appearance alone, Alexander Mauro identifies satellite cells as a possible
muscle stem cell.
The nucleolar origin of rRNA
Base compositions and half-lives suggest to Jan-Erik Edström that the
nucleolus is the source of rRNA.
How vessels become leaky
Guido Majno and George Palade find that inflamed blood vessels leak when endothelial
cells loosen their grip on one another.
Autophagy unveiled
Autophagy is identified, given a function, and named.
There’s DNA in those
organelles
DNA is directly visualized in first chloroplasts and then mitochondria.
A cell line that is under control
George Todaro and Howard Green establish the 3T3 cell line — the first
well behaved, contact-inhibited cell line.
Defining junctional complexes
A mess of nomenclature is sorted out by Marilyn Farquhar and George Palade,
who use superb microscopy to define three of the four major types of cell–cell
junctions in the polarized epithelial cells of vertebrates.
Microtubules get a name
Microtubules are named, and recognized as a widespread phenomenon even outside
of the spindle.
Coated pits bring in the
yolk
A study of yolk protein uptake leads Thomas Roth and Keith Porter to propose
that endocytosis is specific to a particular cargo and that the vesicle coat
might be functioning in both selection and mechanical molding.
Sugars sprinkled onto proteins
in the Golgi
Glycosylation occurs in the Golgi complex, based on labeling with
tritiated glucose carried out by Marian Neutra and C.P. Leblond.
Excess secretory products
fuse with lysosomes
Robert Smith and Marilyn Farquhar find that excess secretory granules are not
stored but fuse with multivesicular bodies (MVBs) that then mature and fuse
with lysosomes.
Endothelial tight junctions
form the blood–brain barrier
What is the cellular correlate of the so called blood-brain barrier? Thomas
Reese and Morris Karnovsky find that it is the junctions between endothelial
cells in the brain vasculature. Their discovery comes thanks to three factors:
high resolution electron microscopy; the development of sensitive tracer methods;
and a fortuitous lunch date.
Microtubules
shape the cell
Based on cold treatment and correlation, Lewis Tilney and Keith Porter find
evidence that microtubule polymerization is important for the development and
maintenance of cell shape.
The discovery
of tubulin
Tubulin is isolated by Gary Borisy and Edwin Taylor as a colchicine-binding
activity, and by Ian Gibbon’s group from cilia.
How to
make a lysosome
Daniel Friend and Marilyn Farquhar find that transport pathways intersect:
synthesized enzyme meets endocytosed protein in the lysosome.
Seeing peroxisomes
Christian de Duve’s group isolates and characterizes peroxisomes.
Not actin,
not myosin, but intermediate
They are neither thick nor thin: Howard Holtzer identifies intermediate filaments
as a completely new kind of filament.
Tension
gets chromosomes oriented
Using grasshopper cells in meiosis, Bruce Nicklas and Carol Koch show that
attachments of mono-oriented chromosomes can be stabilized using a glass needle
to pull on one of the chromosomes. Thus tension between two kinetochores, generated
only in the bi-oriented state, might discriminate between correct and incorrect
attachments.
Actin in non-muscle cells
Howard Holtzer’s group uses heavy meromyosin as a probe to
find actin filaments in non-muscle cells.
Growth cones make proteins,
too
The recent discovery that elongating axons can synthesize proteins locally
is pre-dated by 30 years by Virginia Tennyson’s discovery that growth
cones have ribosomes.
Actin in locomotion
Ken Yamada, Brian Spooner and Norman Wessels use the newly discovered drug
cytochalasin B to show that actin filaments drive cell locomotion.
Spectrin is peripheral
S. Jonathan Singer, Garth Nicolson, and Vincent Marchesi use red cell ghosts
to provide strong evidence for the existence of peripheral membrane proteins.
A macrophage mystery leads
to dendritic discovery
In the days before MHC function is defined, digestion of antigens
in macrophages is mistakenly taken as evidence against the cells’ role
in antigen presentation. But the study leads Ralph Steinman and Zanvil Cohn
to their vital discovery of dendritic cells.
Curbside recycling at the
synapse
When John Heuser and Thomas Reese visualize neurotransmitter 'quanta'
being released, they also catch sight of endocytic recycling that forms new
synaptic vesicles. Ralph Steinman confirms that significant plasma membrane
recycling must also be occurring in other cell types.
Actin pushes in bizarre places
Lewis Tilney discovers that actin polymerization is a means of force
generation. His studies use unorthodox systems: the acrosomal reaction in
both starfish and sea cucumber sperm and the cell-to-cell motility of the Listeria
monocytogenes bacterium.
Powered by gel
Thomas Stossel and John Hartwig nab the very first actin-binding
protein, find that it spurs actin fibers in vitro to coalesce into a mesh,
and tie this process to what happens in vivo during phagocytosis.
EGF is internalized and degraded
Occupied growth factor receptors do not remain
statically at the cell surface, say Graham Carpenter and Stanley Cohen, but
are internalized to allow continued signaling or downregulation.
Contacting the matrix
Can the extracellular matrix (ECM) act as an inducer? Using an ingenious
combination of biochemistry and tissue culture on Nucleopore filters, Elizabeth
Hay and Stephen Meier show that direct contact with ECM is necessary for corneal
epithelium to differentiate.
Myosin powers cytokinesis
Issei Mabuchi and Makoto Okuno, in the first use of antibodies as protein inhibitors
in live cells, show that myosin interacts with actin to provide the force
behind cell cleavage.
The sticky business of discovering
cadherins
A change in the recipe for a trypsin solution allows Masatoshi Takeichi to
distinguish calcium-dependent adhesion.
Microtubules as a gyroscope
for cells on the go
Harry Malech, Richard Root, and John Gallin make neutrophils switch their direction,
and thus find that microtubules orient and organize the internal structure of
migrating cells.
Basal lamina instructs innervation
Joshua Sanes and Jack McMahan show that regenerating nerve axons take their
cues for new synapse formation from the extracellular matrix (ECM) of muscle
cells and not from the muscle cells themselves.
Actin and microtubules interact
via MAP
A viscometer allows Linda Griffith and Tom Pollard to demonstrate that actin
and microtubules interact via MAPs.
The isolation of the nuclear
lamina
Aaronson, Blobel, and Gerace define the extent and composition of the nuclear
lamina.
'Porterplasm' and the microtrabecular
lattice
At the end of a long, distinguished career, Keith Porter tangles with
a possible EM artifact.
Viruses catch an endocytic
ride into the cell
Ari Helenius puts together snapshots of virus entry to form a coherent
sequence of events.
What the cytoskeleton really
looks like
Freeze drying gives John Heuser a far more complete view of the cytoskeleton.
Microtubules park parallel
in the half-spindle
By defining microtubule polarity in the mitotic spindle, Richard McIntosh
narrows down the possible mechanisms used during mitosis.
Isolating SRP
Walter, Blobel, Warren and Dobberstein pin down the proteins (and RNA) that
grab onto signal sequences.
Roll-your-own endothelial tubes
Tom Maciag and Michael Stemerman find
the critical factor that keeps endothelial cells alive and controls their tube
formation.
Tagging an organelle
Warren, Louvard, and Reggio isolate the first Golgi-specific
antibodies.
A portrait of the nuclear pore complex
Ron Milligan and Nigel Unwin get a closer
look at nuclear pore architecture.
More than one way to attach
Wen-Tien Chen and S. Jonathan Singer define different connections between membrane
receptors and extracellular matrix.
Dishing up bone formation
Hiroaki Kodama establishes a cell line of osteoblasts (bone-forming
cells) that mineralize in vitro.
Yeast becomes a cell biologist
Adams, Pringle, and Kilmartin introduce new antibody techniques, and budding
yeast makes its debut as a cell biology workhorse.
Frog egg extracts can do a
cell’s work
Manfred Lohka and Yoshio Masui show that frog egg extracts can be used
to recreate complex in vivo processes.
Pursuing the middleman: the
hunt for integrins
A group of labs use antibodies to find integrins and define their function.
Building a case for the chromosome scaffold
William Earnshaw and Margarete Heck localize topo 2 to the base supports of
the radial loops of chromatin.
A big BiP on the radar screen
David Bole and John Kearney track BiP movements
and gather evidence for its role as a chaperone.
Microtubules turn over rapidly
Eric Schulze and Marc Kirschner chemically label microtubules to define their dynamics.
Sticking it out with tight junctions
With persistence and a species change, tight junction proteins are isolated.
Filling in the gap: cloning a connexin
Paul, Goodenough, Kumar and Gilula clone the first connexin proteins.
MAP1c is a motor
Bryce Paschal and Richard Vallee show that dynein is the other motor.
Making tendons
David Birk and Robert Trelstad discover how the cell manipulates collagen to form a tendon.
Lipid raft idea is floated
Gerrit van Meer and Kai Simons get the first hints of lipid rafts based on lipid sorting experiments.
Passenger proteins check in
Carol Cooke and William Earnshaw identify the first passenger proteins and catalog their strange movements.
Centrosome choreography
Tony Hyman investigates how centrosome movements are choreographed, and how they determine the division axis.
Active neuronal death
Eugene Johnson shows that neurons lacking trophic factors actively kill themselves.
Cadherin as a tumor suppressor
Behrens and Birchmeier find that cells cut free from their cadherin moorings can metastasize.
BFA sends proteins back
Jon Yewdell uses Brefeldin A to detect retrograde trafficking.
Microtubules get dynamic
Tim Mitchison makes photoactivatable tubulin, allowing him to track flux in the spindle.
ECM signals ECM degradation
Damsky and Zena Werb show that changes in ECM interaction change expression of ECM-modifying enzymes.
Chromosome snatching by lateral microtubules
Conly Rieder gets kinetochore capture on tape.
In vitro nuclear import
In vitro nuclear import assays lead Gerace and Blobel to the importance of the Ran GTPase.
Skeleton crew
Anne Ridley and Alan Hall find that rho and its relatives control actin dynamics.
Cyclin localization controls activity
Jonathon Pines and Tony Hunter show that cyclin activity is controlled by location.
The kinetochore uncoiled
Bill Brinkley and Raymond Zinkowski pull apart the kinetochore.
ECM determines fate
Streuli and Bissell find that extracellular matrix can tell a cell what to do and what to become.
The Hunting of the snRNP
Carmo-Fonseca and Lamond track the nuclear travels of snRNPs.
Integrin signal transduction
Keith Burridge and Lewis Romer identify FAK as a key relay for passing integrin signals into the cell.
Dying On Cue
Yuri Lazebnik and William Earnshaw create a system for in vitro apoptosis.
Hold on for dear life
Steve Frisch and Hunter Francis find that epithelial cells that lose touch with the extracellular matrix kill themselves by anoikis.
An unattached kinetochore screams: “Wait!”
Schultz, Rieder and Sluder find that unattached kinetochores tell mitotic cells to wait before dividing.