Actin depolymerization under force is governed by lysine 113:glutamic acid 195-mediated catch-slip bonds

Lee, Cho-yin; Lou, Jizhong; Wen, Kuo‐Kuang; McKane, Melissa; Eskin, Suzanne G.; Ono, Shoichiro; Chien, Shu; Rubenstein, Peter A.; Zhu, Cheng; McIntire, Larry V.

doi:10.1073/pnas.1218407110

Cited by 68 publications

(105 citation statements)

References 48 publications

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“…In general, the lifetime of the receptor-ligand bond exponentially decreases with an increase of the mechanical force (3). However, there is growing evidence demonstrating that the lifetimes of some receptorligand bonds increase when moderate levels of force are applied (4)(5)(6)(7)(8)(9). However, the underlying mechanism of this phenomenon is still elusive and in some cases controversial.…”

Section: E7304-e7305mentioning

confidence: 99%

“…This model proposes that force tilts the binding interface to make it parallel to the direction of force, allowing the selectin ligand to slide on the selectin and to form new contacts. The sliding-rebinding model has also been used to explain the force-induced activation of von Willebrand factor-mediated adhesion and actin depolymerization (6,8).…”

Section: E7304-e7305mentioning

confidence: 99%

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Mechanical force effect on the two-state equilibrium of the hyaluronan-binding domain of CD44 in cell rolling

Suzuki

Ogino

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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The authors note that Fig. 4 and Fig. S4 appeared incorrectly. The corrected figures and their legends appear below. The SI has been corrected online.The authors also note that on page 1 of the supporting information, right column, second full paragraph, lines 5-13, "The starting structure was solvated in a 62 × 129 × 69-Å TIP3 water box (6) with 54 chloride ions to neutralize the system, resulting in 53,872 atoms. The system was minimized for three consecutive 500-conjugate gradient steps, during which the protein was first held fixed; next, only the heavy atoms of the protein were held fixed, and finally, all atoms were allowed to move. After the energy minimizations, the system was heated gradually from 0 K to 310 K over 52 ps, and the temperature was maintained using Langevin dynamics" should instead appear as "The starting structure was solvated in a 68 × 116 × 79-Å TIP3 water box (6) with 53 chloride ions to neutralize the system, resulting in 59,606 atoms. The system was minimized for two consecutive 500-conjugate gradient steps, during which the protein was first held fixed; next, only the heavy atoms of the protein were held fixed. After the energy minimizations, the system was heated gradually from 0 K to 310 K over 9.3 ps, and the temperature was maintained using Langevin dynamics. Subsequently, the system was equilibrated by 4 rounds, first the heavy atoms were held fixed, then only backbone atoms, then only Cα atoms, and finally all atoms were allowed to move." These errors do not affect the conclusions of the article.A B C Fig. 4. Steered molecular dynamics (SMD) simulation of CD44 HABD by pulling force. (A) Snapshots of the HABD-HA8 complex at 0 ns (Left) and 3.5 ns (Right) during the SMD simulation. In the SMD simulation, the Cα carbon of the C-terminal residue Ile173 (gray sphere) was pulled at 10 Å/ns in the indicated direction (arrow), whereas the C2 atom of the N-acetylglucosamine residue (green sphere) was kept fixed. In the snapshot after 3.5 ns in the SMD simulation, the C-terminal mechanosensitive latch was completely separated from the α1 helix. (B) The time course of the hydrogen bond donor-acceptor distances between HA NAG1177 and I100 (red) and E52 and Y166 (blue). (C) Schematic depiction of the mechanosensitive latch in the force-induced conformational change of CD44 HABD.

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Section: E7304-e7305mentioning

confidence: 99%

Section: E7304-e7305mentioning

confidence: 99%

Mechanical force effect on the two-state equilibrium of the hyaluronan-binding domain of CD44 in cell rolling

Suzuki

Ogino

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…Since the initial demonstration of the P-selectin complex binding to PSGL-1 as a catch bond (35), these bonds have been demonstrated for integrins (27,36), actomyosin (37), bacterial adhesion FimH (38), platelet glycoprotein Ibα (39), kinetochore protein (40), cadherin (41), and actin (42). Here we provide a definitive physiologic demonstration of catch bond regulation by a semaphorin signaling through a plexin.…”

Section: Discussionmentioning

confidence: 64%

Dynamic control of β1 integrin adhesion by the plexinD1-sema3E axis

Choi

Duke‐Cohan

Chen

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Plexins and semaphorins comprise a large family of receptorligand pairs controlling cell guidance in nervous, immune, and vascular systems. How plexin regulation of neurite outgrowth, lymphoid trafficking, and vascular endothelial cell branching is linked to integrin function, central to most directed movement, remains unclear. Here we show that on developing thymocytes, plexinD1 controls surface topology of nanometer-scaled β1 integrin adhesion domains in cis, whereas its ligation by sema3E in trans regulates individual β1 integrin catch bonds. Loss of plexinD1 expression reduces β1 integrin clustering, thereby diminishing avidity, whereas sema3E ligation shortens individual integrin bond lifetimes under force to reduce stability. Consequently, both decreased expression of plexinD1 during developmental progression and a thymic medulla-emanating sema3E gradient enhance thymocyte movement toward the medulla, thus enforcing the orchestrated lymphoid trafficking required for effective immune repertoire selection. Our results demonstrate plexin-tunable molecular features of integrin adhesion with broad implications for many cellular processes.thymocyte development | mechanobiology | integrin activation | autoimmunity | central tolerance I t is well established that plexins and their semaphorin ligands regulate biological processes in multiple physiological domains including axon pathfinding (1, 2), angiogenesis (3), and immunity (4). Although plexins harbor potential for regulating small GTPases that mediate cytoskeletal remodeling, either through a direct cytoplasmic GTPase-activating protein (GAP) domain and Rac/Rho-GTPase binding domain or through sequestration of guanidine nucleotide exchange factor (GEF) proteins to the membrane-proximal cytoplasmic face, there is little consensus on plexin signaling pathways in a complex physiological context (5).While studying the molecular interactions controlling mouse thymocyte development, we identified plexinD1 as a critical mediator for thymocytes destined to mature into T lymphocytes populating the mammalian immune system (6). Plxnd1 encoding plexinD1 is transcriptionally regulated at a key intermediate stage of thymocyte development. Double-negative (DN) thymocytes lacking expression of CD4 and CD8 as well as plexinD1 differentiate in the thymic cortex into largely nondividing CD4 + CD8 + double-positive (DP) thymocytes that display surface αβ T-cell receptors (TCRs) and express plexinD1 (6). Despite being highly mobile (7), DP thymocytes remain sequestered in the cortex in frequent physical association with thymic epithelial cells (TECs), moving toward the thymic medulla via chemokine guidance only subsequent to TCR stimulation by self-derived peptide/MHC complexes (pMHC) that induce CD69 expression and support cell survival, i.e., positive selection (8, 9). CD69 + DP cells differentiate further into CD4 + CD8 − or CD4 − CD8 + singlepositive (SP) thymocytes, translocating to the thymic medulla to complete their maturation (10, 11). While traversing the thymus, immatu...

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“…Surprisingly, we find a complex mechanical regulation of adhesive bonds at the single-molecule level: tensile force prolongs the bond lifetime (that is, catch bonds). In contrast to the well-known catch bonds of bimolecular systems, such as cell adhesion receptors (integrins 28,38,39 , selectins 40,41 , glycoprotein Iba 30,42 , E-cadherin 43 and FimH 44 ), the T-cell receptor 31 and cytoskeletal linkages 45,46 , the Thy-1 catch bond is strongly correlated with a bond-stiffening phenotype, termed 'dynamic catch', which partially shifts force to the already engaged but unstretched coreceptor Syn4. Thus, the data reveal a unique, previously unreported class of receptor-ligand bonds whereby force tightens co-receptor engagement that is required for forcemediated adhesion signalling.…”

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confidence: 99%

Dynamic catch of a Thy-1–α5β1+syndecan-4 trimolecular complex

Fiore

Chen

et al. 2014

Nat Commun

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Cancer cell adhesion to the vascular endothelium is a critical step of tumour metastasis. Endothelial surface molecule Thy-1 (CD90) is implicated in the metastatic process through its interactions with integrins and syndecans. However, how Thy-1 supports cell-cell adhesion in a dynamic mechanical environment is not known. Here we show that Thy-1 supports b 1 integrin-and syndecan-4 (Syn4)-mediated contractility-dependent mechanosignalling of melanoma cells. At the single-molecule level, Thy-1 is capable of independently binding a 5 b 1 integrin and syndecan-4 (Syn4) receptors. However, in the presence of both a 5 b 1 and Syn4, the two receptors bind cooperatively to Thy-1, to form a trimolecular complex. This trimolecular complex displays a unique phenomenon we coin 'dynamic catch', characterized by abrupt bond stiffening followed by the formation of catch bonds, where force prolongs the bond lifetime. Thus, we reveal a new class of trimolecular interactions where force strengthens the synergistic binding of two co-receptors and modulates downstream mechanosignalling.

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Actin depolymerization under force is governed by lysine 113:glutamic acid 195-mediated catch-slip bonds

Cited by 68 publications

References 48 publications

Mechanical force effect on the two-state equilibrium of the hyaluronan-binding domain of CD44 in cell rolling

Mechanical force effect on the two-state equilibrium of the hyaluronan-binding domain of CD44 in cell rolling

Dynamic control of β1 integrin adhesion by the plexinD1-sema3E axis

Dynamic catch of a Thy-1–α5β1+syndecan-4 trimolecular complex

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