Biophysical Analysis of Membrane Functions by Laser Tweezers
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1 Biophysical Analysis of Membrane Functions by Laser Tweezers Plasma Membrane Functions (Control by PIP2 Levels in Plasma Membrane) Cell Motility Endocytosis (Cell Volume regulation) Membrane resealing Modified Model of Membrane Structure
2 Evidence for the Bilayer Couple hypothesis from membrane mechanics O Inner Mono O Outer Mono O Expansion Expansion I I I Lim et al., (2003) PNAS. 99:
3 Tether Formation on Fibroblasts
4
5 Apparent Membrane T Tension m CELL Tether Force γ T m B γ: membrane-cytoskeleton adhesion T m : in-plane tension B: membrane bending stiffness Apparent tension (T) = T m + γ
6 Tether Force vs. Length Indicates Membrane Reservoir is Present Force (pn) Tether length (µm) Plateau Exponential Frame Raucher and Sheetz, Biophys J 77:1992 (1999).
7 a) Reservoir Increases With Each Tether Pull Relative Tether Length control Pull Number b) Tether length (µm) 15 Force (pn) pull 1 pull 3 pull Frame
8 Reservoir Increase Is Sensed 8 7 Over Whole Cell 1 Tether Length ( µm) before multiple pulls after multiple pulls control Raucher & Sheetz (1999) Biophys. J. 77:1992.
9 Summary In-plane tension is small and is continuous over the whole cell surface Membrane-cytoskeleton interaction is the major component of the apparent membrane tension
10 Cell Biophysics: Analysis of Physical Basis of Cell Functions Physical and chemical analysis of cell functions is critical Tension in Membrane is Critical for Membrane Functions (Global Control) Cell Forces Generated and Sensed by Cytoskeleton
11 Functions Controlled by Plasma Membrane Tension Motility Endocytosis Rate Cell Volume regulation Bleb resistance (Membrane-cytoskeleton adhesion) Membrane resealing
12 RBL Secretion Correlates with Drop in Tether Force and Rise in Endocytosis Rate Dai et al. (1997) J. Gen. Physiol. 11:1
13 RBL Tether Force Decreases Faster Than Granule Secretion
14 Endocytosis Inhibited Dramatically in Mitosis Endocytosis (% of interphase) Relative Number of Vesicles Relative Fluorescence Intensity Interphase Prometaphase Metaphase Anaphase Cytokinesis
15 Titration of Membrane Tension with Deoxycholic Acid Tether Force (pn) interphase metaphase Endocytosis Rate (% of interphase) interphase metaphase Deoxycholic Acid Concentration (mm) Deoxycholic Acid Concentration (mm) When membrane tension in metaphase cells is adjusted to the interphase level with detergent addition, the endocytosis rate reaches the interphase level. Raucher & Sheetz (1999) J. Cell Biol. 144: 497
16 Correlation of Relative Endocytosis Rate and Membrane Tension Relative Endocytosis (% of interphase) vinblastine DMSO ethanol interphase metaphase taxol 20 R 2 = Relative Tether Force (% of interphase)
17 Model for Regulation of Endocytosis during Mitosis interphase mitosis mitosis membrane tension membrane tension reducing reagents endocytosis
18 Bleb Formation Involves Separation of membrane from cytoskeleton Sheetz, MP. Nature Rev.CMB. 2:392-8(2001)
19 A tether from a bleb on a M2 cell
20 Tether Force over Cytoskeleton versus Blebs in Epithelial Cells Dai & Sheetz (1999) Biophys. J. 77:3363
21 Biophysical Analysis of Membrane Functions by Laser Tweezers Plasma Membrane Functions (Control by PIP2 Levels in Plasma Membrane) Endocytosis (Cell Volume regulation) Cell Motility Membrane resealing Modified Model of Membrane Structure
22 MARCKS (Myristilated Alanine Rich C Kinase Substrate) Concentration present in cell at 10µM Binds 3 to 4 molecules PIP(4,5)2 with a K D of 10-8 M Effector domain (AA ) has +13 charge Competes w/ PLCδ PH for PIP(4,5)2 Other functions: actin crosslinking protein and as a scaffolding protein between the PM and the cytoskeleton Effector Domain =PIP(4,5)2 =PC or cholesterol =mystirlation sequence
23 MARCKS, PLCδ-PH, Are Equally Effective in Reducing Tether Force E6 molecules of EGFP-PIP2 binding proteins MAR G2A MAR FL MAR ED PLC PH PI5K+PH AktPH w/lyn Akt PH Spectrin PH GRP1 PH PI5K+pEGFP pegfp control 0 F (pn)
24 PI5 Kinase & PKC Restore Normal Adhesion F (pn) MAR FL MAR FL +PI5K PLC PH PI5K+PH PI5K+pEGFP control F (pn) Control control+pma MAR FL (control) PRE MAR FL +PMA 2min MAR FL +PMA 4min MAR FL +PMA 6min
25 Protein Kinase C Activation Reverses PH Domain Blebs Pre + PMA 1 min
26 MARCKS Causes Small Blebs Reversed by PMA MARCKS MARCKS + PMA Enlarged Region
27 MARCKS & PH Domains Move Oppositely with PKC MAR FL GFP PLC PH RFP Merge A Pre +PMA B MAR FL GFP PLC PH GFP Pre +PMA 1 +PMA 3
28 MARCKS Sequesters PIP2 Released by PKC A IP(4)P + PI5K 1. Local Synthesis of PI(4,5)P2 2. Sequestration of PI(4,5)P2 via MARCKS Scaffolding Complex B 1. MARCKS Translocation to Perinuclear Region 2. Increased Actin Polymerization at the Plasma Membrane PI(4,5)P2 MARCKS PH Domain PKC PI5K (Iα) F-Actin
29 Cholesterol Depletion Increases Recoils and Decreases Diffusion Control MCD treated Kwik et al., PNAS 100: (2003).
30 GFP-PLC-PH Leaves PM in 20 of MCD Before After 20 10mM MCD Intensity GFP-PH
31 Surface Potential of PS(20%) or PIP2 (1%) with MARCKS ED (0.1 M NaCl) PS (20%) PS + MARCKS ED PIP2 (1%) PIP2 + MARCKS ED Wang et al., JBC 277:34401 (2002).
32 Model of Membrane Structure From Sheetz, Nature Rev CMB 2:392-8(2001)
33 Apparent Membrane Tension Resists Extension by Actin and Tension α [PIP2] Extension Tension Reviewed: Sheetz, Nature Rev. MCB. 2:392 (2001)
34
35
36 Membrane Load Alters Activation and Rate of Actin Assembly Raucher & Sheetz (2000) J. Cell Biol. 147:1313
37 Membrane Tension: Physical Control of Cell Functions Adhesion of membrane to the cytoskeleton develops tension that provides general regulation of endocytosis rate (surface-area/volume ratio), motility, and resealing Model of lipid-dependent membrane-cytoskeleton adhesion PIP2 is major lipid controlling membranecytoskeleton adhesion Tension is too low to activate stretch channels
38 Acknowledgements Sheetz Lab Drazen Raucher Catherine Galbraith Dan Felsenfeld Daniel Choquet Ben Dubin-Thaler Yasuharo Sawada Jianwu Dai Goetz Wichert Julia Sable Guoying Jiang Adam Meshel Masako Tamada Duke University Dr. Robert Hochmuth Stuart McLaughlin (SUNY Stonybrook) Michael Edidin North Carolina State University Dr. Paul Franzon David Nackashi
39
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