Making parallel lines meet: Transferring information from microtubules to extracellular matrix.

2012·1.4 MB·English

by  Baskin, Tobias I.

CellAdhesion&Migration6:5,404–408;September/October2012;G2012LandesBioscience
Making parallel lines meet
Transferring information from microtubules to extracellular matrix
Tobias I. Baskin1,* and Ying Gu2
1BiologyDepartment;UniversityofMassachusetts;Amherst,MAUSA;2CenterforLignoCelluloseStructureandFormation;DepartmentofBiochemistryandMolecular
Biology;PennsylvaniaStateUniversity;UniversityPark,PAUSA
Theextracellularmatrixisconstructed to spaces both fascinating and useful. A
beyond the plasma membrane, contemporary case of parallel lines whose
challenging mechanisms for its control meeting is impossible but informative is
by the cell. In plants, the cell wall is offered by the humble vascular plant.
highlyordered,withcellulosemicrofibrils Perhaps of doubtful utility for readers of
aligned coherently over a scale spanning Cell Adhesion & Migration, this case
hundreds of cells. To a considerable neverthelesscouldfascinatethem,concern-
extent, deploying aligned microfibrils ing as it does the problem of information
determines mechanical properties of the flowing out of the cell, a flow that is a
cell wall, including strength and compli- hallmark of living things but far less well
ance. Cellulose microfibrils have long understood than is the typical receptor-
Keywords: cellulose microfibrils, cellulose been seen to be aligned in parallel with mediatedinwardflow.Andfascinationdoes
synthase, cellulose synthase interacting an array of microtubules in the cell beget utility, as non-Euclidean geometries
protein 1, cortical microtubules, plant cell cortex. How do these cortical microtu- proposedforpuremathematicalabstraction
wall, Pom-Pom2 bules affect the cellulose synthase com- havegivenrisetosolutionsinphysics.
Submitted: 04/13/12 plex?Thisquestionhasstoodforasmany Theplantcellissurroundedbyatough
years as the parallelism between the yet pliant extracellular matrix, called the
Revised: 05/31/12
elements has been observed, but now an cell wall (see Box 1 for definitions of
Accepted: 06/13/12 answer is emerging. Here, we review plant-specific terms). While animal cells
http://dx.doi.org/10.4161/cam.21121 recent work establishing that the link make an extracellular matrix, few of them
between microtubules and microfibrils is are surrounded by it as completely as is
*Correspondenceto:TobiasI.Baskin;
Email:[email protected] mediated by a protein named cellulose nearly every plant cell. The cell wall is so
synthase-interacting protein 1 (CSI1). ubiquitously and intimately associated
Commentaryto:LiS,LeiL,SomervilleCR,GuY. The protein binds both microtubules with the plant cell that one is tempted to
Cellulosesynthaseinteractiveprotein1(CSI1) andcomponentsofthecellulosesynthase consider the wall as one more organelle,
linksmicrotubulesandcellulosesynthasecom- complex. In the absence of CSI1, micro- albeit a large one. Indeed, the cell wall
plexes.ProcNatlAcadSciUSA2012;109:185–
fibrilsaresynthesizedbuttheiralignment space defines a compartment, known as
90;PMID:22190487;http://dx.doi.org/10.1073/
becomes uncoupled from the microtu- the apoplast. However, the cell wall is
pnas.1118560109
and bules,aneffectthatisphenocopiedinthe unquestionably outside of the plasma
BringmannM,LiE,SampathkumarA,KocabekT, wild type by depolymerizing the micro- membrane and for that reason extracellu-
HauserMT,PerssonS.POM-POM2/cellulose tubules. The characterization of CSI1 lar. Far from being a random entangled
synthaseinteracting1isessentialforthefunc-
significantly enhances knowledge of how network, for example like an agarose gel,
tionalassociationofcellulosesynthaseand
cellulose is aligned, a process that serves the cell wall is highly organized (Fig.1A).
microtubulesinArabidopsis.PlantCell2012;
24:163–77;PMID:22294619;http://dx.doi.org/10. as a paradigmatic example of how cells The organization makes the cell wall
1105/tpc.111.093575 dictate the construction of their extra- mechanically anisotropic, a property that
and cellular environment. is required by morphogenesis to channel
MeiY,GaoHB,YuanM,XueHW.The
expansion into anisotropic shapes, such as
ArabidopsisARCPprotein,CSI1,whichis
stems and leaves. How does information
requiredformicrotubulestability,isnecessary
forrootandantherdevelopment.PlantCell In Euclid’s geometry, parallel lines cannot from the cell flow across the plasma
2012;24:1066–80;PMID:22427339;http://dx.doi. meet, but Riemann and others found membrane to constrain the construction
org/10.1105/tpc.111.095059 geometries where they do meet, leading us of cell wall?
404 CellAdhesion&Migration Volume6Issue5
COMMENTARY
Box1.Definingterms. powered by the energy released from
Apoplast:Thecontinuumformedbycellwalls,airspaces,anddeadcells,suchasthewater hydrolyzingUDP-glucoseorcrystallization.
conductingxylem.
Mechanistic details about the synthesis
Arabidopsisthaliana:The“fruitfly”ofplantbiology;thatis,aspecieschosenforutilityinresearch
ratherthanforitseconomicrelevance. of cellulose are scarce, primarily because
Cellwall:Thepolysaccharide-richextracellularmatrixthatsurroundseveryplantcell. the reaction proceeds with great difficulty
Cellulose:Thegeneralnameforpolymersofb1A4linkedglucoseassociatedintoacrystallineor in vitro,3 and frustratingly not at all in
semi-crystallinefibril. extracts from the model plant, Arabidopsis
Cellulosemicrofibril:Thetypicalformofcelluloseinvascularplants,withaminimaldiameterof
thaliana, the species in which most of the
~3nmandanindefinitelength.
Cellulosesynthase:Themulti-peptidecomplexattheplasmamembranethatsynthesizesa genetic evidence relating to cellulose
cellulosemicrofibril. synthesishasbeenobtained.Geneticshave
CellulosesynthaseA(CESA):Thepolypeptidethoughttoberesponsibleforcatalyzingthereaction implicated a family of putative glycosyl
whereUDPglucoseisaddedtothegrowingchainofpolymerizedglucose. transferases, called cellulose synthase A
Corticalarrayofmicrotubules:Anarrayofmainlyparallelmicrotubulesinthecellcortexassociated
(CESA), and it appears that a functional
closelywiththeplasmamembrane,presentinessentiallyallplantcellsduringinterphase.
Rosette:Asynonymforthecellulosesynthasecomplex,basedonitshexamericappearanceinthe cellulose synthase complex requires three
electronmicroscope. distinct CESA family members.1,2 An
antibody against a CESA labels a hexame-
In contrast to the animal cell’s extra- similartothescaleofthecellitself.Sucha ric structure, termed a rosette, that is
abundant in freeze-fracture images of the
cellularmatrix,theplantcellwallischiefly molecule could be packaged into a
plasma membrane.4 This, along with
polysaccharide. The functional analog of secretory vesicle only by wizardry and,
genetics and estimations of the lateral
theprotein,collagen,isthepolysaccharide, lacking magic wands, cells synthesize
dimensions of a microfibril have led to a
cellulose. Structurally, cellulose comprises cellulose at the plasma membrane. This
model where each cellulose synthase is a
unbranched polymers of glucose linked is accomplished by a multi-subunit com-
rosette,containing36CESApolypeptides,
side by side in a (partly) crystalline array plex called cellulose synthase. At its
with each (or possibly each pair) synthes-
and stabilized by a network of hydrogen cytosolic side, this complex reacts with
izing a glucose chain. However, we know
bonds dense enough to give cellulose a UDP-glucose and extrudes polymerized
neither how CESA proteins are organized
tensile strength rivaling steel.1,2 The crys- glucan chains into the extracellular space.
withinarosettenorwhatotherproteins,if
talline array comprises a few dozen of the Eachsynthasecomplexprobablymakes18
any, are also components of the complex,
unbranchedpolymers,formingastructural to 36 chains that somehow associate or
although sucrose synthase is likely.5
unit called the cellulose microfibril. The crystallize into a microfibril. As the chains
Knowledgeaboutcellulosesynthesishas
degree of polymerization of each glucose are extended, the cellulose synthase moves
recently been enhanced by the develop-
chain is on the order of ten thousand, along the plasma membrane, presumably
ment of a system whereby the movement
of the synthase can be imaged in living
cells.6 A specific CESA sequence is tagged
with a fluorescent protein and introduced
into a background where the correspond-
ing native gene has been inactivated
mutationally; when imaged through a
spinning-disc confocalfluorescencemicro-
scope, the tagged cellulose synthase com-
plexes are seen as spots at the plasma
membrane. Over time, the spots move
(see Fig.2A and C). The velocity,
~0.3 mm min21, along with the density
of the complexes per unit area, plausibly
account for rates of cellulose synthesis
measured in bulk. In the absence of in
vitro enzymology, imaging the tagged
CESA in living cells provides a readout
of the reaction rate that is particularly
Figure1.Parallellines.(A)CellwalloftheinflorescencestemofA.thalianaimagedwithfield valuable.
emissionscanningelectronmicroscopy.Formethod,seereference23.(B)Methacrylatesection Insofar as cellulose constitutes about
throughtherootofA.thalianastainedwithanantibodyagainsttubulin.Thesectionplanepasses one third of the cell wall mass and is, by
throughthemiddleofafileofwidecellsandthroughthecortexofafileofnarrowcells;cortical far, its longest and stiffest component, the
microtubulesareviewedend-onintheformerandinfaceviewinthelatter.Formethod,see
cell goes some way toward guiding the
reference24.Scalebars:(A)=600nm,(B)=10mm.
assembly of the cell wall by constraining
www.landesbioscience.com CellAdhesion&Migration 405
Figure2.Co-localizationofCSI1,CESAcomplexes,andmicrotubules.(A)Wild-typeseedlingsco-expressingGFP-CESA6andRFP-CSI1:theco-alignmentof
CSI1andCESAcomplexesisevidentinthemergedtime-averagedimage.(B)Wild-typeseedlingsco-expressingYFP-TUA5andRFP-CSI1:theco-
alignmentofCSI1andmicrotubulesisevidentinthemergedtime-averagedimage.(C)Wild-typeseedlingsco-expressingRFP-TUA5andYFP-CESA6:the
co-alignmentofCESAcomplexesandmicrotubulesisevidentinthemergedtime-averagedimage.(D)Incsi1seedlingsco-expressingYFP-CESA6and
RFP-TUA5,CESAparticlesarerandomlydistributed,theirtime-averagedtrajectoriesareapparentlyshorterandrarelyco-localizedwithmicrotubules.
Notethatthelarge,roughlycircularstructuresintheGFP-CESA6(A)andYFP-CESA6(C)imagesareGolgibodies.Thetime-averagedimagesare
projectionsof60frames(~5min)acquiredat5secintervals.Bars=10mm.Methodsdescribedfurtherinreference15.
the orientation in which the cellulose array of microtubules, called the cortical there appear to be exceptions, these many
microfibrils form. Given that microfibrils array.8,9 Like those in animal cells, micro- examples make clear that microfibrils are
are long and stiff, and synthesized within tubules in the cortical array turn over oriented with respect to the microtubules.
the confined, essentially two-dimensional rapidly and exhibit dynamic instability; But the hypothesis remains incomplete
space between plasma membrane and however, unlike most other arrays, the because the mechanism behind this flow
extant cell wall, self-assembly probably cortical array lacks a microtubule organiz- of orientation information has remained
contributes to the parallel arrangement of ingcenterandthepolarityofmicrotubules obscure.
microfibrils, driven by entropic and within the array is apparently random. Indeed, the most popular model for
van der Waals forces, which apparently Cortical microtubules are well ordered how microtubules influence cellulose
also drive orientation of cytoskeletal fila- (Fig.1B), and their alignment usually posits no mechanism at all.9,12 Instead,
ments.7However,microfibrilsareoriented parallels that of the cellulose microfibrils. the model envisions the microtubules as a
on the macroscopic scale. For example, in In fact, microtubules were first imaged in kind of molecular guard rail, constraining
thestemsampledfor Figure1,microfibrils plantcellsandwerehypothesizedtoorient movement of the cellulose synthase steri-
arealignedperpendiculartothatstemover cellulose microfibrils based on the congru- cally but not interacting with the complex
a distance on order of a centimeter and entalignmentbetweentheseelements,even specifically. Although this model accounts
throughout thousands of cells. Macro- thoughmicrotubulesareinsidethecelland for the parallelism, it leaves an important
scopic order on this scale is beyond the microfibrilsareoutside.10,11Sincethen,this function (ordering the microfibrils) essen-
reach of self-assembly based on molecular hypothesis has been confirmed in general tiallytochance.Moreover,the“guard-rail”
forces and thus the cell must supplement but not in detail. The overall claim of the model makes no provision for activity of
intrinsic self-assembly with information hypothesisisconfirmedbycountlessexam- the microtubules in addition to ordering
specifying cellular polarity. ples where microtubules parallel microfi- the microfibrils. Cells are parsimonious;
Whatbetterwaytospecifypolaritythan brils and countless more where depoly- along with specifying orientational order,
through the cytoskeleton? Just inside the merizing the microtubules impairs the microtubules might have a concomitant
plasma membrane, plant cells contain an alignment among microfibrils.12 Although role in assisting with cellulose synthesis
406 CellAdhesion&Migration Volume6Issue5
itself.13 That is, while there is no require- loss-of-functionmutantsforCSI1(aback- reconstitute at least part of this motility
mentformicrotubulesperseforaplantto grounddenotedhereascsi1butalsoknown system in vitro so that this molecular
make cellulose, microtubules could con- as pom-pom2) have morphological pheno- anatomy can be dissected.
dition the properties of the synthesized types associated with aberrant cortical Fascinating. But even granting that
material. microtubules,14,16 some of which can be Earth’s biomass is mostly cellulosic, what
But at last, a mechanism is being ameliorated by transgenic expression of an is the lesson for the animal biologist? Like
discovered. Three papers published nearly animal microtubule-associated protein the plant cell wall, the animal cell
simultaneously characterize the first pro- (MAP4) that is absent from plants. Taken extracellular matrix, whether bone, shell,
tein known to link cortical microtubules together, this evidence shows that CSI1, spicule or tendon, is highly oriented.
and cellulose microfibrils.14-16 Previously, althoughdiscoveredbasedonitsrelationto Where does the order come from? Not
the protein, named cellulose synthase- cellulose synthase,17 associates with micro- entirely from self-assembly, because while
interacting protein (CSI1), had been tubules, pivotally supporting its hypothet- this is powerful on the small (sub-cellular)
fished out of a yeast two-hybrid screen icalroleasamessengerservicefromcytosol scale, the matrix is organized on a
for proteins that interact with CESA; the tocellwall. macroscopic scale and requires input from
proteinispresentattheplasmamembrane Perhaps the most interesting results in the organism. Although not that well
andmovesinlineartrajectoriesresembling the new papers are those concerning the elucidated, the order might come, as in
those of CESA, and loss-of-function velocity anddirectionalityofCESAmove- plants, from the cytoskeleton, albeit from
mutants synthesize less crystalline cel- ment. In the csi1 background, CESA actin rather than microtubules.
lulose.17 The new work extends our complexes move at about 70% percent of In biomineralization, the general term
knowledge of CSI1 and links it to the the rate of the wild type, and when used to describe constructing extracellular
cortical microtubules. microtubules are depolymerized, the matrix rich in inorganic compounds, as in
Tobeginwith,twopapersconfirmthat reduction in velocity is similar.15 Further boneorshell,secretedproteinscanserveas
CSI1 and cellulose synthase are associated attestingtoCSI1mediatingalinkbetween templates for crystallization and vesicles
intimately.14,15 In the original publica- microtubules and CESA, in the csi1 can be delivered selectively to seed crys-
tion,17 CSI1 and CESA were co-localized background, CESA trajectories lose their tallizationappropriately,18,19butingeneral
almost completely and both moved bi- close association with microtubules14,15 it is not known how large-scale order is
directionally, at all but indistinguishable (Fig.2C and D) and deviate somewhat imposed or whether the cytoskeleton is
velocities;thesefindingsarereproducedin from their linear character observed in the involved. One exception is patterning of
the new work but with a distinct CESA wild type. Notably similar wandering thesilica-richextracellularmatrix(frustule)
familymember(Fig.2A).Furthermore,an CESA trajectories occur when microtu- ofthediatom,whichdependsontheactin
inhibitor of cellulose synthesis, which bules are depolymerized, again fingering cytoskeleton;20 while diatoms are as
depletes the membrane of CESA com- CSI1 as the microtubule-microfibril go- diverged from animals as are plants, this
plexes, likewise depletes CSI-positive between.These results imply thatas faras studystandsasaparadigmforhowthecell
material. These results leave little doubt the movement of the CESA complex is controls the growth of external, miner-
as to the close association between CSI1 concerned, the loss of microtubules and alized structures.
and CESA. the loss of CSI1 are equivalent, making a For aligning protein-rich matrices in
But a putative linker between CESA powerful case for the function of CSI1 vertebrates, actin isknowntobeinvolved.
complexes and microtubules needs also to being to inform the cellulose synthase Actin helps build collagen-rich tendons,
interact with microtubules; such an inter- complex about the disposition of the partly through actin-rich structures (fibri-
action is substantiated in several ways by microtubules. positors) in the cell cortex that guide the
the new work.14-16 First, CSI1 binds Why does depolymerizing the micro- formationoffibrils21butalsobygivingrise
microtubules in vitro, with a dissociation tubules require 10 to 16 h to slow down to forces that condition the developing
constant, ~1 mM, that is similar to that of the CESA complexes but just 1 h or so to tendon.22 That actin guides collagen
canonical microtubule-associated proteins, remove microtubules? This discrepancy assembly (and maybe biomineralization)
such as MAP2.15 Microtubule binding is impliesthatCSI1affectsCESAmovement but microtubules guide cellulose assembly
plausible,insofarasCSI1containsmultiple indirectly. Why does the loss of a micro- shouldnotdevaluethiscomparison.Inthe
armadillorepeats,motifsknowntobestow tubule binding protein slow down the evolution of plants and animals, micro-
microtubule-binding activity on several CESA complex? Naïvely, we might tubules and actin have, to a large extent,
proteins. Second, CSI1 moves along the suppose microtubule-binding activity to switched places. In animals, microtubules
plasma membrane in trajectories that act as a brake and the removal thereof are the mainline tracks for organelles,
closely overlay microtubules (Fig.2B). would accelerate the movement even as it while actin presides over the cell cortex
Third, when microtubules are depolymer- lost directional control. Finally, is the and regulates whole-cell motility; conver-
ized, CSI1 spots at the plasma membrane purview of CSI1 solely guidance or does sely in plants, actin filaments are the
are reduced in number and intensity, it extend to synthesis? That is, do micro- organelle tracks, while microtubules dom-
although they do not disappear alto- fibrils built in the absence of CSI1 have inate the cortex and regulate cell expan-
gether.14,15Finally,undersomeconditions, assembly defects? It would be useful to sion. But in both kingdoms, information
www.landesbioscience.com CellAdhesion&Migration 407
flows from a set of organized cytoplasmic many kinds of cell and to many kinds of US Department of Energy through Grant
filaments, across the membrane, to regu- matrixtounderstandhoworganisms draw DE-FG-03ER15421. Work in the Gu
late the structure and activity of the parallel lines, even if they never meet. laboratory is supported by grants from
extracellular matrix. National Science Foundation (1121375),
Therefore, the growing understanding Acknowledgments and The Center for LignoCellulose
of how cortical microtubules align cel- WorkintheBaskinlaboratoryoncellulose Structure and Formation, an Energy
lulose microfibrils has valuable lessons for and the control of growth anisotropy is Frontier Research Center funded by the
us all. As exemplified by the studies supported by the Division of Chemical US Department of Energy, Office of
reviewed here on CSI1, we need to Sciences, Geosciences, and Biosciences, Science under Award Number DE-
intercept information flowing out from Office of Basic Energy Sciences of the SC0001090.
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