SFB 937: Collective Behaviour of Soft and Biological Matter
Biology
Final Report Abstract
Living systems are structurally complex, heterogeneous, and by definition far from thermodynamic equilibrium. In condensed matter physics, the complex behavior of many-particle systems has been very successfully analyzed with the concepts of statistical physics. The strength of a statistical approach is the capability to efficiently describe the collective behavior of large systems with many interacting degrees of freedom. In recent years, non-equilibrium soft-matter systems - short “active matter” -, especially as found in biology, have rapidly moved into the focus of interest. Prominent examples are the materials cells are made from. Understanding how a living cell functions or an organism develops requires a statistical description that goes beyond well-established equilibrium statistical phys- ics. The rapid development of experimental techniques has given unprecedented access to physical properties of molecules, macromolecular aggregates, cells and tissues. Against this background it is timely to ask questions beyond the molecular level of organization in soft and biological matter and to pursue an integrative approach to understand collective non-equilibrium physical phenomena on the microscopic to the mesoscopic or even macroscopic level by applying a broad range of experimental, numerical and theoretical tools. The collaborative research center (CRC) 937 aimed at a quantitative understanding of the physical mechanisms at work when soft and biological matter self-organizes into complex structures to perform dynamic functions such as cell division, cell locomotion or tissue development. With this goal in mind, we analyzed the ways in which macromolecules and cells interact physically, exert forces, respond viscoelastically, move, and self-organize into complex functional patterns on all length scales, ranging from polymers and lipid membranes over cells to tissues. We combined physics, chemistry, biology and medicine, as well as theory, modeling and experiment and em- ployed a two-pronged approach, studying simplified model systems on the one hand, and whole cells, organisms and tissues on the other hand. The major achievements of the CRC 937 are (i) the measurement and theoretical modeling of the viscoelastic and hydrodynamic properties of model systems ranging from polymer brushes and cross-linked passive networks over actively contracting networks to minimal cell cortices, (ii) the assessment of the athermal cell-substrate dynamics during adhesion, growth and migration and (iii) the collective behavior of beating cells, biofilms and developing Drosophila embryos. Apart from these fundamental insights, the research groups identified and developed new model systems to study various aspects of collective phenomena. In parallel, methods and tools comprising new microscopy and simulation techniques were adapted and optimized to examine these systems.
Publications
- (2012) Electrodynamic coupling of electric dipole emitters to a fluctuating mode density within a nanocavity. Phys. Rev. Lett. 108(16):163002
Chizhik A, Gregor I, Schleifenbaum F, Müller CB, Röling C, Meixner AJ, Enderlein, J
(See online at https://doi.org/10.1103/physrevlett.108.163002) - (2012) Force field evolution during human blood platelet activation. J. Cell Sci. 125:3914-3920
Schwarz-Henriques S, Sandmann R, Strate A, Köster S
(See online at https://doi.org/10.1242/jcs.108126) - (2013) Actin cytoskeleton of chemotactic amoebae operates close to the onset of oscillations. Proc. Natl. Acad. Sci. USA 110:3853–3858
Westendorf C, Negrete J, Bae AJ, Sandmann R, Bodenschatz E, Beta C
(See online at https://doi.org/10.1073/pnas.1216629110) - (2013) Nonequilibrium Collective Dynamics in Photoexcited Lipid Multilayers by Time Resolved Diffuse X-Ray Scattering. Phy. Rev. Lett. 111(26):268101
Reusch T, Mai DD, Osterhoff M, Khakhulin D, Wulff M, Salditt T
(See online at https://doi.org/10.1103/physrevlett.111.268101) - (2013) Nonequilibrium Collective Dynamics in Photoexcited Lipid Multilayers by Time Resolved Diffuse X-Ray Scattering. Phy. Rev. Lett. 111(26):268101
Reusch T, Mai DD, Osterhoff M, Khakhulin D, Wulff M, Salditt T
(See online at https://doi.org/10.1103/physrevlett.111.268101) - (2013) Quantum Yield Measurement in a Multicolor Chromophore Solution Using a Nanocavity. Nano Lett. 13:1348
Chizhik AI, Gregor I, Enderlein J
(See online at https://doi.org/10.1021/nl400313z) - (2014) A lipid bound actin meshwork organizes liquid phase separation in model membranes. eLife 3:e01671
Honigmann A, Sadeghi S, Keller J. Hell SW, Eggeling C, Vink R
(See online at https://doi.org/10.7554/elife.01671) - (2014) High-resolution mapping of intracellular fluctuations using carbon nanotubes. Science 344(6187):1031 – 1035
Fakhri N, Wessel AD, Willms C, Pasquali M, Klopfenstein DR, MacKintosh FC, Schmidt CF
(See online at https://doi.org/10.1126/science.1250170) - (2014) Metal-induced energy transfer for live cell nanoscopy. Nat. Photonics 8:124-127
Chizhik AI, Rother J, Gregor I, Janshoff A, Enderlein, J
(See online at https://doi.org/10.1038/nphoton.2013.345) - (2014) Scale-Dependent Nonaffine Elasticity of Semiflexible Polymer Networks: Phys. Rev. Lett. 112:088101
Atakhorrami M, Koenderink GH, Palierne JF, MacKintosh F, Schmidt CF
(See online at https://doi.org/10.1103/PhysRevLett.112.088101) - (2015) Alignment of copolymer morphology by planar step elongation during spinodal self-assembly. Phys. Rev. Lett. 115:228301
Müller M, Tang J
(See online at https://doi.org/10.1103/physrevlett.115.228301) - (2015) Fluctuation Analysis of Centrosomes Reveals a Cortical Function of Kinesin-1. Biophys J. 109:856:868
Winkler F, Gummalla M, Künneke L, Lv Z, Zippelius A, Aspelmeier T, Grosshans J
(See online at https://doi.org/10.1016/j.bpj.2015.07.044) - (2015) Intracellular and extracellular forces drive primary cilia movement: Proc. Natl. Acad. Sci. USA 112(5):1410-1415
Battle C, Ott CM, Burnette DT, Lippincott-Schwartz J, Schmidt CF
(See online at https://doi.org/10.1073/pnas.1421845112) - (2016) Broken detailed balance at mesoscopic scales in active biological systems. Science 352(6285):604-607
Battle C, Broedersz CP, Fakhri N, Geyer VF, Howard J, Schmidt CF, MacKintosh FC
(See online at https://doi.org/10.1126/science.aac8167) - (2016) Noisy Oscillations in the Actin Cytoskeleton of Chemotactic Amoeba. Phys. Rev. Lett. 117(14):148102
Negrete J, Pumir A, Hsu HF, Westendorf C, Tarantola M, Beta C, Bodenschatz E
(See online at https://doi.org/10.1103/physrevlett.117.148102) - (2016) Photoactivation of Luminescent Centers in Single SiO2 Nanoparticles. Nano Lett. 16(7):4312-4316
Tarpani L, Ruhlandt D, Latterini L, Haehnel D, Gregor I, Enderlein J, Chizhik AI
(See online at https://doi.org/10.1021/acs.nanolett.6b01361) - (2016) Self-driven jamming in growing microbial populations. Nat. Phys. 12(8):762–766
Delarue M, Hartung J, Schreck C, Gniewek P, Hu L, Herminghaus S, Hallatschek O
(See online at https://doi.org/10.1038/nphys3741) - (2016) Super-Resolution Optical Fluctuation Bio-Imaging with Dual-Color Carbon Nanodots Nano Lett. 16:237-242
Chizhik AM, Stein S, Dekaliuk MO, Battle C, Li W, Huss A, Platen M, Schaap IAT, Gregor I, Demchenko A, Schmidt CF, Enderlein J, Chizhik AI
(See online at https://doi.org/10.1021/acs.nanolett.5b03609) - (2016) Transition from a Linear to a Harmonic Potential in Collective Dynamics of a Multifilament Actin Bundle. Phys. Rev. Lett. 116:108102
Schnauß J, Golde T, Schuldt C, Schmidt BUS, Glaser M, Strehle D, Händler T, Heussinger C, Käs JA
(See online at https://doi.org/10.1103/physrevlett.116.108102) - (2017) Cell-Substrate Dynamics of the Epithelial-to- Mesenchymal Transition. Nano Lett. 17:3320-3326
Baronsky T, Ruhlandt D, Brückner BR, Schäfer J, Karedla N, Isbaner S, Hähnel H, Gregor I, Enderlein J, Janshoff A, Chizhik IA
(See online at https://doi.org/10.1021/acs.nanolett.7b01558) - (2017) Envelope glycoprotein mobility on HIV-1 particles depends on the virus maturation state. Nature Comm. 8:545
Chojnacki J, Waithe D, Carravilla P, Huarte N, Galiani S, Enderlein J, Eggeling C
(See online at https://doi.org/10.1038/s41467-017-00515-6) - (2017) Fast propagation regions cause self-sustained reentry in excitable media. Proc. Natl. Acad. Sci. USA 114:1281-1286
Zykov V, Krekhov A, Bodenschatz E
(See online at https://doi.org/10.1073/pnas.1611475114) - (2017) Features of Chaotic Transients in Excitable Media Governed by Spiral and Scroll Waves. Phys. Rev. Lett. 119:054101
Lilienkamp T, Christoph J, Parlitz U
(See online at https://doi.org/10.1103/physrevlett.119.054101) - (2017) Feedback-tracking microrheology in living cells Sci.Adv. 3:e1700318
Nishizawa K, Bremerich M, Ayade H, Schmidt CF, Ariga T, Mizuno D
(See online at https://doi.org/10.1126/sciadv.1700318) - (2017) Nonlinear Loading-Rate-Dependent Force Response of Individual Vimentin Intermediate Filaments to Applied Strain. Phys. Rev. Lett. 118:048101
Block J, Witt H, Candelli A, Peterman EJG, Wuite GJL, Janshoff A, Köster S
(See online at https://doi.org/10.1103/physrevlett.118.048101) - (2017) Shear force-based genetic screen reveals negative regulators of cell adhesion and protrusive activity. Proc. Natl. Acad. Sci. USA 114(37):E7727-E7736
Lampert TJ, Kamprad N, Edwards M, Borleis J, Watson AJ, Tarantola M, Devreotes PN
(See online at https://doi.org/10.1073/pnas.1616600114) - (2017) Size and mobility of lipid domains tuned by geometrical constraints. Proc. Natl. Acad. Sci. USA 114(30): E6064- E6071
Schütte MO, Mey I, Enderlein J, Savic F, Geil B, Janshoff A, Steinem C
(See online at https://doi.org/10.1073/pnas.1704199114) - (2017) Three-Dimensional Reconstruction of Nuclear Envelope Architecture Using Dual-Color Metal-Induced Energy Transfer Imaging. ACS Nano. 11(12):11839-11846
Chizhik AM, Ruhlandt D, Pfaff J, Karedla N, Chizhik AI, Gregor I, Kehlenbach RH, Enderlein J
(See online at https://doi.org/10.1021/acsnano.7b04671) - (2017) Variability and Order in Cytoskeletal Dynamics of Motile Amoeboid Cells. Phys. Rev. Lett. 119:148101
Hsu HF, Bodenschatz E, Westendorf C, Gholami A, Pumir A, Tarantola M, Beta C
(See online at https://doi.org/10.1103/physrevlett.119.148101) - (2018) A ‘molecular guillotine’ reveals the interphase function of Kinesin-5. J. Cell Sci. 131:210583
Lv Z, Rosenbaum J, Aspelmeier T, Großhans J
(See online at https://doi.org/10.1242/jcs.210583) - (2018) Adhesion forces and cortical tension couple cell proliferation and differentiation to drive epidermal stratification. Nat. Cell Biol. 20:69-80
Miroshnikova YA, Le HQ, Schneider D, Thalheim T, Rübsam M, Bremicker N, Polleux J, Kamprad Tarantola M, Wang I, Balland M, Niessen CM, Galle J, Wickström SA
(See online at https://doi.org/10.1038/s41556-017-0005-z) - (2018) Axial Colocalization of Single Molecules with Nanometer Accuracy Using Metal-Induced Energy Transfer. Nano Lett. 18:2516-2622
Isbaner S, Karedla N, Kaminska I, Ruhlandt D, Raab M, Bohlen J, Chizhik A, Gregor I, Tinnefeld P, Enderlein J, Tsukanov R
(See online at https://doi.org/10.1021/acs.nanolett.8b00425) - (2018) Correlative microscopy approach for biology using x-ray holography, xray scanning diffraction and STED microscopy. Nat.Commun 9:3641
Marten B, Nicolas JD, Osterhoff M, Mittelstädt H, Reuss M, Harke B, Wittmeier A, Sprung M, Köster S, Salditt T
(See online at https://doi.org/10.1038/s41467-018-05885-z) - (2018) Curvature-Guided Motility of Microalgae in Geometric Confinement. Phys. Rev. Lett. 120:068002
Ostapenko T, Schwarzendahl FJ, Böddeker TJ, Kreis CT, Cammann J, Mazza MG, Bäumchen O
(See online at https://doi.org/10.1103/physrevlett.120.068002) - (2018) Dynamics of force generation by spreading platelets. Soft Matter 14:6571
Hanke J, Probs D, Zemel A, Schwarz US, Köster S
(See online at https://doi.org/10.1039/c8sm00895g) - (2018) Electromechanical vortex filaments during cardiac fibrillation. Nature 555:667-672
Christoph J, M. Chebbok M, Richter C, Schröder-Schetelig J, Bittih P, Stein S, Uzelac I, Fenton F, Hasenfuß G, Gilmour RF Jr, Luther S
(See online at https://doi.org/10.1038/nature26001) - (2018) Metastable Prepores in Tension-Free Lipid Bilayers. Phys. Rev. Lett. 120:128103
Ting CL, Awasthi N, Müller M, Hub JS
(See online at https://doi.org/10.1103/physrevlett.120.128103) - (2018) Self-organization of stress patterns drives state transitions in actin cortices. Sci. Adv. 4:eaar2847
Tan TH, Garbi M, Abu-Shah E, Li J, Sharma A, MacKintosh Fc, Keren K, Schmidt Cf, Fakhri N
(See online at https://doi.org/10.1126/sciadv.aar2847) - (2018) Terminal Transient Phase of Chaotic Transients. Phys. Rev. Lett. 120:94101
Lilienkamp T, Parlitz U
(See online at https://doi.org/10.1103/physrevlett.120.094101) - (2018) Viscoelastic properties of vimentin originate from non-equilibrium conformational changes Sci. Adv. 4:eaat1161
Block J, Witt H, Candelli A, Danes JC, Peterman E, Wuite GJL, Janshoff A, Köster S
(See online at https://doi.org/10.1126/sciadv.aat1161)
