Volume 104, Issue 9, Pages (May 2013)

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Volume 104, Issue 9, Pages 2022-2030 (May 2013) Domain-Domain Interactions in Filamin A (16–23) Impose a Hierarchy of Unfolding Forces  Tianyou Xu, Herbert Lannon, Sébastein Wolf, Fumihiko Nakamura, Jasna Brujic  Biophysical Journal  Volume 104, Issue 9, Pages 2022-2030 (May 2013) DOI: 10.1016/j.bpj.2013.03.034 Copyright © 2013 Biophysical Society Terms and Conditions

Figure 1 A schematic of the dimer of FLNa monomers bound to actin filaments. The actin binding domain anchors the FLNa protein to the actin. Linear repeats 1–15 exhibit strong interactions with actin, whereas FLNa 16–23 bridges the orthogonal actin filaments. Dimerization occurs between domains Ig 24 of two adjacent FLNa proteins. A zoom of the Ig domains 19–21 shows the domain-domain interactions that lead to the propeller-like architecture of the FLNa 16–23 construct. Biophysical Journal 2013 104, 2022-2030DOI: (10.1016/j.bpj.2013.03.034) Copyright © 2013 Biophysical Society Terms and Conditions

Figure 2 (A) Typical force-extension trace at a constant velocity of 400 nm/s and (B) force-clamp trace at a constant force of 100 pN for the linear construct FLNa 1–8. Sawtooth patterns are fit with the worm-like chain (WLC) model (red line) to give the contour length ΔLFX given out between consecutive peaks. The regular staircase in force-clamp is indicative of individual Ig domain unfolding, as seen in tandem proteins, such as I27 (10,33). Biophysical Journal 2013 104, 2022-2030DOI: (10.1016/j.bpj.2013.03.034) Copyright © 2013 Biophysical Society Terms and Conditions

Figure 3 Distinct mechanical behaviors of FLNa 16–23: (A) Diversity in the lengths unraveled, fit by the WLC model. (B) Trajectory of length over time at a constant force of 100 pN, similarly revealing the release of diverse end-to-end lengths. (C) Other traces under the same conditions reveal strong rupture events occurring before weak ones. (Inset) Decrease in the frequency of the number of consecutive weak events after a strong rupture. (D) Observation of small after large peaks in force-extension measurements manifests itself as a separation of timescales in constant force experiments. In this case, the slow events occur before the fast ones. Biophysical Journal 2013 104, 2022-2030DOI: (10.1016/j.bpj.2013.03.034) Copyright © 2013 Biophysical Society Terms and Conditions

Figure 4 Examples of refolding trajectories in FLNa 16–23. The protein is first pulled under a constant velocity of 400 nm/s (top black) and then relaxed to ∼70% of the initial extension (top blue) to keep the AFM tip off the surface for a waiting time of tw = 7 s. The protein is then extended again (bottom black), followed by a final return of the AFM tip to the surface (bottom blue). (Red curves) Fits to the WLC model. (A) Example where the original and refolded proteins unfold with a very similar linear pattern of unfolding events. (Inset) Experimental protocol. (B) Trajectories with a diversity in the unfolded lengths also refold successfully, but the order of events can be reversed due to their similar rupture force. (C) Example where weaker intermediates unfold after stronger rupture forces, but refolding the molecule recovers the same mechanical hierarchy imposed by the folding structure. (D) Example of a trajectory in which a much stronger rupture event occurs before weaker events. Upon relaxation, the mechanical stability of the strong rupture event is lost and is not seen when the protein is extended a second time. Biophysical Journal 2013 104, 2022-2030DOI: (10.1016/j.bpj.2013.03.034) Copyright © 2013 Biophysical Society Terms and Conditions

Figure 5 (A) Histogram of rupture forces for FLNa 16–23 under a constant velocity of 400 nm/s. (Shaded histogram) Ig domain rupture in FLNa 1–8 for comparison. Native FLNa 16–23 gives a much broader distribution than that of the Ig domains alone, which could be due to domain-domain interactions or other higher-order structures. (Inset) Power law decay captures the breadth of the distribution. (B) Histogram of contour lengths released between consecutive peaks for FLNa 16–23 is compared with the shaded histogram of Ig domains in FLNa 1–8. (Inset) Probability map of the histograms from Fig. 3, A and B. The map shows a high probability to observe ΔLFx ∼20–30 nm, in the range of Ig domain unfolding, but a significant chance to originate from another mechanism. (C) A histogram of contour lengths released after the rupture of strong events also reveals a broad distribution. (Inset) Probability map of rupture force and ΔLFx that isolates a peak at ΔLFx at ∼25–30 nm, which may indicate Ig domain rupture. (D) Histogram of step sizes for FLNa 16–23 under a constant force of 100 pN reveals a broad distribution with a peak at 20 nm, indicative of Ig domain rupture. (Inset) Uniform step-size distribution for FLNa 1–8, which is peaked near the size of the Ig domains in the chain. Biophysical Journal 2013 104, 2022-2030DOI: (10.1016/j.bpj.2013.03.034) Copyright © 2013 Biophysical Society Terms and Conditions

Figure 6 Empirical CDFs for the dwell times and the normalized end-to-end length of FLNa 1–8 and 16–23 at a pulling force of 100 pN. Data are fit with a biexponential function in Eq. 2. (FLNa 1–8: a1 = 0.11 ± 0.03 s−1, a2 = 1.9 ± 0.5 s−1, A = 0.8 ± 0.1; and FLNa 16–23: a1 = 0.30 ± 0.08 s−1, a2 = 3.1 ± 0.7 s−1, A = 0.7 ± 0.1). The normalized length and CDF are almost identical in both constructs, which indicates no correlation between the step size and time of the rupture event. Biophysical Journal 2013 104, 2022-2030DOI: (10.1016/j.bpj.2013.03.034) Copyright © 2013 Biophysical Society Terms and Conditions

Figure 7 Examples of hypothetical arrangements of Ig domains 16–23. (A) Arrangement of the domains in a linear polyprotein chain. (B) The known interactions in FLNa 16–23 are incorporated into a globular configuration. Biophysical Journal 2013 104, 2022-2030DOI: (10.1016/j.bpj.2013.03.034) Copyright © 2013 Biophysical Society Terms and Conditions