Wallace Marshall, PhD

Professor
Department of Biochemistry and Biophysics
+1 415 514-4304

Our lab is interested in the engineering design principles that underlie morphogenesis at the cellular level. We want to understand how the three-dimensional geometry of cells can be encoded in a one-dimensional genome and developed into varying cellular architectures under genetic control. We are investigating this question at the level of individual organelles (centrioles, cilia, and mitochondria) as well as through studies of the overall architecture of cells. We are particularly interested in the control of organelle size and copy number, and in the role of biological self-replication processes. Our lab uses a combination of genomic, proteomic, imaging, and mathematical modeling approaches.  Recently we have begun a major new effort to understand pattern formation and regeneration at the single-cell level using the giant ciliate Stentor coeruleus, which is allowing us to take a genomics-based approach to understanding the developmental biology of single cells.

Research Summary: 
Developmental biology of single cells
Mentorship Development: 

2/16/21    Three Truths and Three Tries: Facing and Overcoming Critical Social Justice Challenges at the Micro, Mezzo, and Macro Levels

Websites

Publications: 

Cell motility: Bioelectrical control of behavior without neurons.

Current biology : CB

Larson BT, Marshall WF

Mitochondrial networks through the lens of mathematics.

Physical biology

Lewis GR, Marshall WF

Homologous chromosome recognition via nonspecific interactions.

bioRxiv : the preprint server for biology

Marshall WF, Fung JC

Testing the ion-current model for flagellar length sensing and IFT regulation.

eLife

Ishikawa H, Moore J, Diener DR, Delling M, Marshall WF

Cooperative hydrodynamics accompany multicellular-like colonial organization in the unicellular ciliate Stentor.

bioRxiv : the preprint server for biology

Shekhar S, Guo H, Colin SP, Marshall W, Kanso E, Costello JH

Studying Habituation in Stentor coeruleus.

Journal of visualized experiments : JoVE

Rajan D, Chudinov P, Marshall W

Single-cell analysis of habituation in Stentor coeruleus.

Current biology : CB

Rajan D, Makushok T, Kalish A, Acuna L, Bonville A, Correa Almanza K, Garibay B, Tang E, Voss M, Lin A, Barlow K, Harrigan P, Slabodnick MM, Marshall WF

A unicellular walker controlled by a microtubule-based finite-state machine.

Current biology : CB

Larson BT, Garbus J, Pollack JB, Marshall WF

Modular, cascade-like transcriptional program of regeneration in Stentor.

eLife

Sood P, Lin A, Yan C, McGillivary R, Diaz U, Makushok T, Nadkarni AV, Tang SKY, Marshall WF

Determining protein polarization proteome-wide using physical dissection of individual Stentor coeruleus cells.

Current biology : CB

Lin A, Piehowski PD, Tsai CF, Makushok T, Yi L, Diaz U, Yan C, Summers D, Sood P, Smith RD, Liu T, Marshall WF

Biosynthesis of Linear Protein Nanoarrays Using the Flagellar Axoneme.

ACS synthetic biology

Ishikawa H, Tian JL, Yu JE, Marshall WF, Qin H

A simple method to generate human airway epithelial organoids with externally-oriented apical membranes.

American journal of physiology. Lung cellular and molecular physiology

Boecking CA, Walentek P, Zlock LT, Sun DI, Wolters PJ, Ishikawa H, Jin BJ, Haggie PM, Marshall WF, Verkman AS, Finkbeiner WE

Regeneration in Stentor coeruleus.

Frontiers in cell and developmental biology

Marshall WF

Analysis of Motility Patterns of Stentor During and After Oral Apparatus Regeneration using Cell Tracking.

Journal of visualized experiments : JoVE

Sheung JY, Otsuka M, Seifert G, Lin A, Marshall WF

Deep convolutional and recurrent neural networks for cell motility discrimination and prediction.

IEEE/ACM transactions on computational biology and bioinformatics

Kimmel J, Brack A, Marshall W

Axopodia and the cellular "arms" race.

Cytoskeleton (Hoboken, N.J.)

Marshall WF

Scaling of Subcellular Structures.

Annual review of cell and developmental biology

Marshall WF

Multi-scale spatial heterogeneity enhances particle clearance in airway ciliary arrays.

Nature physics

Juan GRR, Mathijssen AJTM, He M, Jan L, Marshall W, Prakash M

Pattern Formation and Complexity in Single Cells.

Current biology : CB

Marshall WF

Aging induces aberrant state transition kinetics in murine muscle stem cells.

Development (Cambridge, England)

Kimmel JC, Hwang AB, Scaramozza A, Marshall WF, Brack AS

Aurora kinase inhibitors delay regeneration in Stentor coeruleus at an intermediate step.

Matters select

Lin A, Summers D, Reiff SB, Tipton AR, Tang SK, Marshall WF

Towards computer aided design of cellular structure.

Physical biology

Bianco S, Chan YM, Marshall WF

Reorganization of complex ciliary flows around regenerating Stentor coeruleus.

Philosophical transactions of the Royal Society of London. Series B, Biological sciences

Wan KY, Hürlimann SK, Fenix AM, McGillivary RM, Makushok T, Burns E, Sheung JY, Marshall WF

Testing the role of intraflagellar transport in flagellar length control using length-altering mutants of Chlamydomonas.

Philosophical transactions of the Royal Society of London. Series B, Biological sciences

Wemmer K, Ludington W, Marshall WF

Microtubules are necessary for proper Reticulon localization during mitosis.

PloS one

Diaz U, Bergman ZJ, Johnson BM, Edington AR, de Cruz MA, Marshall WF, Riggs B

Dynamics of living cells in a cytomorphological state space.

Proceedings of the National Academy of Sciences of the United States of America

Chang AY, Marshall WF

Simple Rules Determine Distinct Patterns of Branching Morphogenesis.

Cell systems

Yu W, Marshall WF, Metzger RJ, Brakeman PR, Morsut L, Lim W, Mostov KE

Cell learning.

Current biology : CB

Tang SKY, Marshall WF

A Dilution Model for Embryonic Scaling.

Developmental cell

Marshall WF

Methods for the Study of Regeneration in Stentor.

Journal of visualized experiments : JoVE

Lin A, Makushok T, Diaz U, Marshall WF

Mechanical Forces Program the Orientation of Cell Division during Airway Tube Morphogenesis.

Developmental cell

Tang Z, Hu Y, Wang Z, Jiang K, Zhan C, Marshall WF, Tang N

Testing the time-of-flight model for flagellar length sensing.

Molecular biology of the cell

Ishikawa H, Marshall WF

Non-model model organisms.

BMC biology

Russell JJ, Theriot JA, Sood P, Marshall WF, Landweber LF, Fritz-Laylin L, Polka JK, Oliferenko S, Gerbich T, Gladfelter A, Umen J, Bezanilla M, Lancaster MA, He S, Gibson MC, Goldstein B, Tanaka EM, Hu CK, Brunet A

Microfluidic guillotine for single-cell wound repair studies.

Proceedings of the National Academy of Sciences of the United States of America

Blauch LR, Gai Y, Khor JW, Sood P, Marshall WF, Tang SKY

Intraflagellar Transport and Ciliary Dynamics.

Cold Spring Harbor perspectives in biology

Ishikawa H, Marshall WF

The Macronuclear Genome of Stentor coeruleus Reveals Tiny Introns in a Giant Cell.

Current biology : CB

Slabodnick MM, Ruby JG, Reiff SB, Swart EC, Gosai S, Prabakaran S, Witkowska E, Larue GE, Fisher S, Freeman RM, Gunawardena J, Chu W, Stover NA, Gregory BD, Nowacki M, Derisi J, Roy SW, Marshall WF, Sood P

Cell Geometry: How Cells Count and Measure Size.

Annual review of biophysics

Marshall WF

Organelle Size Scaling of the Budding Yeast Vacuole by Relative Growth and Inheritance.

Current biology : CB

Chan YH, Reyes L, Sohail SM, Tran NK, Marshall WF

Versatile protein tagging in cells with split fluorescent protein.

Nature communications

Kamiyama D, Sekine S, Barsi-Rhyne B, Hu J, Chen B, Gilbert LA, Ishikawa H, Leonetti MD, Marshall WF, Weissman JS, Huang B

How Cells Measure Length on Subcellular Scales.

Trends in cell biology

Marshall WF

Subcellular size.

Cold Spring Harbor perspectives in biology

Marshall WF

A systematic comparison of mathematical models for inherent measurement of ciliary length: how a cell can measure length and volume.

Biophysical journal

Ludington WB, Ishikawa H, Serebrenik YV, Ritter A, Hernandez-Lopez RA, Gunzenhauser J, Kannegaard E, Marshall WF

Methods in cilia & flagella. Preface.

Methods in cell biology

Basto R, Marshall WF

Preface. Building a cell from its component parts.

Methods in cell biology

Ross J, Marshall WF

Mechanobiology of Ciliogenesis.

Bioscience

Ishikawa H, Marshall WF

Stentor coeruleus.

Current biology : CB

Slabodnick MM, Marshall WF

Actin is required for IFT regulation in Chlamydomonas reinhardtii.

Current biology : CB

Avasthi P, Onishi M, Karpiak J, Yamamoto R, Mackinder L, Jonikas MC, Sale WS, Shoichet B, Pringle JR, Marshall WF

Quantitative analysis and modeling of katanin function in flagellar length control.

Molecular biology of the cell

Kannegaard E, Rego EH, Schuck S, Feldman JL, Marshall WF

The kinase regulator mob1 acts as a patterning protein for stentor morphogenesis.

PLoS biology

Slabodnick MM, Ruby JG, Dunn JG, Feldman JL, DeRisi JL, Marshall WF

The Golgi is a measuring cup.

Developmental cell

Marshall WF

Correction: TTC26/DYF13 is an intraflagellar transport protein required for transport of motility-related proteins into flagella.

eLife

Ishikawa H, Ide T, Yagi T, Jiang X, Hirono M, Sasaki H, Yanagisawa H, Wemmer KA, Stainier DY, Qin H, Kamiya R, Marshall WF

FAP20 is an inner junction protein of doublet microtubules essential for both the planar asymmetrical waveform and stability of flagella in Chlamydomonas.

Molecular biology of the cell

Yanagisawa HA, Mathis G, Oda T, Hirono M, Richey EA, Ishikawa H, Marshall WF, Kikkawa M, Qin H

TTC26/DYF13 is an intraflagellar transport protein required for transport of motility-related proteins into flagella.

eLife

Ishikawa H, Ide T, Yagi T, Jiang X, Hirono M, Sasaki H, Yanagisawa H, Wemmer KA, Stainier DY, Qin H, Kamiya R, Marshall WF

Visualizing cytoplasmic flow during single-cell wound healing in Stentor coeruleus.

Journal of visualized experiments : JoVE

Slabodnick M, Prevo B, Gross P, Sheung J, Marshall W

Ciliary regulation: disassembly takes the spotlight.

Current biology : CB

Avasthi P, Marshall WF

Intraflagellar transport drives flagellar surface motility.

eLife

Shih SM, Engel BD, Kocabas F, Bilyard T, Gennerich A, Marshall WF, Yildiz A

Ciliary secretion: switching the cellular antenna to 'transmit'.

Current biology : CB

Avasthi P, Marshall W

Avalanche-like behavior in ciliary import.

Proceedings of the National Academy of Sciences of the United States of America

Ludington WB, Wemmer KA, Lechtreck KF, Witman GB, Marshall WF

Analysis of ciliary assembly and function in planaria.

Methods in enzymology

Rompolas P, Azimzadeh J, Marshall WF, King SM

Chemical screening methods for flagellar phenotypes in Chlamydomonas.

Methods in enzymology

Avasthi P, Marshall WF

Isolation of mammalian primary cilia.

Methods in enzymology

Ishikawa H, Marshall WF

Methods in Enzymology. Cilia, part A. Preface.

Methods in enzymology

Marshall WF

Methods in Enzymology. Cilia, part B. Preface.

Methods in enzymology

Marshall WF

What determines cell size?

BMC biology

Marshall WF, Young KD, Swaffer M, Wood E, Nurse P, Kimura A, Frankel J, Wallingford J, Walbot V, Qu X, Roeder AH

Statistical method for comparing the level of intracellular organization between cells.

Proceedings of the National Academy of Sciences of the United States of America

Apte ZS, Marshall WF

Mitochondrial network size scaling in budding yeast.

Science (New York, N.Y.)

Rafelski SM, Viana MP, Zhang Y, Chan YH, Thorn KS, Yam P, Fung JC, Li H, Costa Lda F, Marshall WF

Cell biology 2.0.

Trends in cell biology

Lim WA, Alvania R, Marshall WF

Centrosome positioning in vertebrate development.

Journal of cell science

Tang N, Marshall WF

Organelle size equalization by a constitutive process.

Current biology : CB

Ludington WB, Shi LZ, Zhu Q, Berns MW, Marshall WF

The role of retrograde intraflagellar transport in flagellar assembly, maintenance, and function.

The Journal of cell biology

Engel BD, Ishikawa H, Wemmer KA, Geimer S, Wakabayashi K, Hirono M, Craige B, Pazour GJ, Witman GB, Kamiya R, Marshall WF

Centriole asymmetry determines algal cell geometry.

Current opinion in plant biology

Marshall WF

How cells know the size of their organelles.

Science (New York, N.Y.)

Chan YH, Marshall WF

Organelle size control systems: from cell geometry to organelle-directed medicine.

BioEssays : news and reviews in molecular, cellular and developmental biology

Marshall WF

A chemical screen identifies class a g-protein coupled receptors as regulators of cilia.

ACS chemical biology

Avasthi P, Marley A, Lin H, Gregori-Puigjane E, Shoichet BK, von Zastrow M, Marshall WF

Proteomic analysis of mammalian primary cilia.

Current biology : CB

Ishikawa H, Thompson J, Yates JR, Marshall WF

Centrosome loss in the evolution of planarians.

Science (New York, N.Y.)

Azimzadeh J, Wong ML, Downhour DM, Sánchez Alvarado A, Marshall WF

Stages of ciliogenesis and regulation of ciliary length.

Differentiation; research in biological diversity

Avasthi P, Marshall WF

Three-dimensional structure of basal body triplet revealed by electron cryo-tomography.

The EMBO journal

Li S, Fernandez JJ, Marshall WF, Agard DA

CLUMPED CHLOROPLASTS 1 is required for plastid separation in Arabidopsis.

Proceedings of the National Academy of Sciences of the United States of America

Yang Y, Sage TL, Liu Y, Ahmad TR, Marshall WF, Shiu SH, Froehlich JE, Imre KM, Osteryoung KW

Origins of cellular geometry.

BMC biology

Marshall WF

Centrosome size: scaling without measuring.

Current biology : CB

Marshall WF

Control of mitotic spindle angle by the RAS-regulated ERK1/2 pathway determines lung tube shape.

Science (New York, N.Y.)

Tang N, Marshall WF, McMahon M, Metzger RJ, Martin GR

Ciliogenesis: building the cell's antenna.

Nature reviews. Molecular cell biology

Ishikawa H, Marshall WF

A cell-based screen for inhibitors of flagella-driven motility in Chlamydomonas reveals a novel modulator of ciliary length and retrograde actin flow.

Cytoskeleton (Hoboken, N.J.)

Engel BD, Ishikawa H, Feldman JL, Wilson CW, Chuang PT, Snedecor J, Williams J, Sun Z, Marshall WF

Regulation of flagellar motility by the conserved flagellar protein CG34110/Ccdc135/FAP50.

Molecular biology of the cell

Yang Y, Cochran DA, Gargano MD, King I, Samhat NK, Burger BP, Sabourin KR, Hou Y, Awata J, Parry DA, Marshall WF, Witman GB, Lu X

Building the centriole.

Current biology : CB

Azimzadeh J, Marshall WF

Influence of centriole number on mitotic spindle length and symmetry.

Cytoskeleton (Hoboken, N.J.)

Keller LC, Wemmer KA, Marshall WF

Scaling properties of cell and organelle size.

Organogenesis

Chan YH, Marshall WF

Total internal reflection fluorescence (TIRF) microscopy of Chlamydomonas flagella.

Methods in cell biology

Engel BD, Lechtreck KF, Sakai T, Ikebe M, Witman GB, Marshall WF

Centriole evolution.

Current opinion in cell biology

Marshall WF

Katanin knockdown supports a role for microtubule severing in release of basal bodies before mitosis in Chlamydomonas.

Molecular biology of the cell

Rasi MQ, Parker JD, Feldman JL, Marshall WF, Quarmby LM

Modeling recursive RNA interference.

PLoS computational biology

Marshall WF

Controlling size within cells.

Seminars in cell & developmental biology

Marshall WF

Building the cell: design principles of cellular architecture.

Nature reviews. Molecular cell biology

Rafelski SM, Marshall WF

Engineering design principles for organelle size control systems.

Seminars in cell & developmental biology

Marshall WF

Cilia orientation and the fluid mechanics of development.

Current opinion in cell biology

Marshall WF, Kintner C

The cell biological basis of ciliary disease.

The Journal of cell biology

Marshall WF

Basal bodies platforms for building cilia.

Current topics in developmental biology

Marshall WF

Isolation and proteomic analysis of Chlamydomonas centrioles.

Methods in molecular biology (Clifton, N.J.)

Keller LC, Marshall WF

Use of transcriptomic data to support organelle proteomic analysis.

Methods in molecular biology (Clifton, N.J.)

Marshall WF

Centriole assembly: the origin of nine-ness.

Current biology : CB

Marshall WF

The Chlamydomonas genome reveals the evolution of key animal and plant functions.

Science (New York, N.Y.)

Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Maréchal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren Q, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernández E, Fukuzawa H, González-Ballester D, González-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meier I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riaño-Pachón DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan J, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang P, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P, Dubchak I, Goodstein D, Hornick L, Huang YW, Jhaveri J, Luo Y, Martínez D, Ngau WC, Otillar B, Poliakov A, Porter A, Szajkowski L, Werner G, Zhou K, Grigoriev IV, Rokhsar DS, Grossman AR

What is the function of centrioles?

Journal of cellular biochemistry

Marshall WF

Flagellar length control in chlamydomonas--paradigm for organelle size regulation.

International review of cytology

Wemmer KA, Marshall WF

Quantitative modeling in cell biology: what is it good for?

Developmental cell

Mogilner A, Wollman R, Marshall WF

Axon guidance by diffusible chemoattractants: a gradient of netrin protein in the developing spinal cord.

The Journal of neuroscience : the official journal of the Society for Neuroscience

Kennedy TE, Wang H, Marshall W, Tessier-Lavigne M

Cilia: tuning in to the cell's antenna.

Current biology : CB

Marshall WF, Nonaka S

De novo formation of left-right asymmetry by posterior tilt of nodal cilia.

PLoS biology

Nonaka S, Yoshiba S, Watanabe D, Ikeuchi S, Goto T, Marshall WF, Hamada H

Proteomic analysis of isolated chlamydomonas centrioles reveals orthologs of ciliary-disease genes.

Current biology : CB

Keller LC, Romijn EP, Zamora I, Yates JR, Marshall WF

Genome-wide transcriptional analysis of flagellar regeneration in Chlamydomonas reinhardtii identifies orthologs of ciliary disease genes.

Proceedings of the National Academy of Sciences of the United States of America

Stolc V, Samanta MP, Tongprasit W, Marshall WF

Flagellar motility: all pull together.

Current biology : CB

Wemmer KA, Marshall WF

Flagellar length control system: testing a simple model based on intraflagellar transport and turnover.

Molecular biology of the cell

Marshall WF, Qin H, Rodrigo Brenni M, Rosenbaum JL

PCR-based assay for mating type and diploidy in Chlamydomonas.

BioTechniques

Zamora I, Feldman JL, Marshall WF

Centrioles: bad to be bald?

Current biology : CB

Feldman JL, Marshall WF

Cellular length control systems.

Annual review of cell and developmental biology

Marshall WF

Tubulin superfamily: giving birth to triplets.

Current biology : CB

Marshall WF, Rosenbaum JL

Size control in dynamic organelles.

Trends in cell biology

Marshall W

Order and disorder in the nucleus.

Current biology : CB

Marshall WF

Polar wind left flapping in the breeze?

Trends in cell biology

Marshall WF

Homologous chromosome pairing in Drosophila melanogaster proceeds through multiple independent initiations.

The Journal of cell biology

Fung JC, Marshall WF, Dernburg A, Agard DA, Sedat JW

Interphase chromosomes undergo constrained diffusional motion in living cells.

Current biology : CB

Marshall WF, Straight A, Marko JF, Swedlow J, Dernburg A, Belmont A, Murray AW, Agard DA, Sedat JW

Mitosis in living budding yeast: anaphase A but no metaphase plate.

Science (New York, N.Y.)

Straight AF, Marshall WF, Sedat JW, Murray AW

Deconstructing the nucleus: global architecture from local interactions.

Current opinion in genetics & development

Marshall WF, Fung JC, Sedat JW

Perturbation of nuclear architecture by long-distance chromosome interactions.

Cell

Dernburg AF, Broman KW, Fung JC, Marshall WF, Philips J, Agard DA, Sedat JW