Titin-Based Nanoparticle Tension Sensors Map High-Magnitude Integrin Forces within Focal Adhesions

Nano Letters

Volumn 16, Issue 1, 2016, Pages 341-348

  Galior, Kornelia ^a   Liu, Yang ^a   Yehl, Kevin ^a   Vivek, Skanda ^a   Salaita, Khalid ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

biophysics; focal adhesion; Integrins; mechanotransduction

Indexed keywords

BIOPHYSICS; CELL CULTURE; COVALENT BONDS; GLYCOPROTEINS; NANOPARTICLES; PROBES;

EMBRYONIC FIBROBLASTS; FOCAL ADHESIONS; GOLD NANOPARTICLES; INTEGRINS; MECHANICAL UNFOLDING; MECHANICALLY STABLE; MECHANOTRANSDUCTION; TRANSMEMBRANE RECEPTORS;

ADHESION;

CONNECTIN; GOLD; INTEGRIN; NANOPARTICLE;

ANIMAL; CELL ADHESION; CHEMISTRY; DRUG EFFECTS; FIBROBLAST; KINETICS; MECHANICAL STRESS; MECHANICS; RAT;

ANIMALS; CELL ADHESION; CONNECTIN; FIBROBLASTS; GOLD; INTEGRINS; KINETICS; MECHANICAL PHENOMENA; NANOPARTICLES; RATS; STRESS, MECHANICAL;

EID: 84957884135     PISSN: 15306984     EISSN: 15306992     Source Type: Journal    
DOI: 10.1021/acs.nanolett.5b03888     Document Type: Article

References (46)

1. Hynes, R. O. Integrins: bidirectional, allosteric signaling machines Cell 2002, 110 (6) 673-87 10.1016/S0092-8674(02)00971-6
2. Redick, S. D.; Settles, D. L.; Briscoe, G.; Erickson, H. P. Defining fibronectin's cell adhesion synergy site by site-directed mutagenesis J. Cell Biol. 2000, 149 (2) 521-527 10.1083/jcb.149.2.521
3. Barczyk, M.; Carracedo, S.; Gullberg, D. Integrins Cell Tissue Res. 2010, 339 (1) 269-80 10.1007/s00441-009-0834-6
4. Humphrey, J. D.; Dufresne, E. R.; Schwartz, M. A. Mechanotransduction and extracellular matrix homeostasis Nat. Rev. Mol. Cell Biol. 2014, 15 (12) 802-12 10.1038/nrm3896
5. Kanchanawong, P.; Shtengel, G.; Pasapera, A. M.; Ramko, E. B.; Davidson, M. W.; Hess, H. F.; Waterman, C. M. Nanoscale architecture of integrin-based cell adhesions Nature 2010, 468 (7323) 580-4 10.1038/nature09621
6. Parsons, J. T.; Horwitz, A. R.; Schwartz, M. A. Cell adhesion: Integrating cytoskeletal dynamics and cellular tension Nat. Rev. Mol. Cell Biol. 2010, 11 (9) 633-43 10.1038/nrm2957
7. Liu, Z.; Liu, Y.; Chang, Y.; Seyf, H. R.; Henry, A.; Mattheyses, A. L.; Yehl, K.; Zhang, Y.; Huang, Z.; Salaita, K. Nat. Meth. 2015, in press.
8. Wang, X.; Ha, T. Defining single molecular forces required to activate integrin and notch signaling Science 2013, 340 (6135) 991-4 10.1126/science.1231041
9. Grashoff, C.; Hoffman, B. D.; Brenner, M. D.; Zhou, R.; Parsons, M.; Yang, M. T.; McLean, M. A.; Sligar, S. G.; Chen, C. S.; Ha, T.; Schwartz, M. A. Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics Nature 2010, 466 (7303) 263-6 10.1038/nature09198
10. Sabass, B.; Gardel, M. L.; Waterman, C. M.; Schwarz, U. S. High resolution traction force microscopy based on experimental and computational advances Biophys. J. 2008, 94 (1) 207-20 10.1529/biophysj.107.113670
11. Tan, J. L.; Tien, J.; Pirone, D. M.; Gray, D. S.; Bhadriraju, K.; Chen, C. S. Cells lying on a bed of microneedles: An approach to isolate mechanical force Proc. Natl. Acad. Sci. U. S. A. 2003, 100 (4) 1484-9 10.1073/pnas.0235407100
12. Wiseman, P. W.; Brown, C. M.; Webb, D. J.; Hebert, B.; Johnson, N. L.; Squier, J. A.; Ellisman, M. H.; Horwitz, A. F. Spatial mapping of integrin interactions and dynamics during cell migration by image correlation microscopy J. Cell Sci. 2004, 117 (23) 5521-5534 10.1242/jcs.01416
13. Engler, A. J.; Sen, S.; Sweeney, H. L.; Discher, D. E. Matrix elasticity directs stem cell lineage specification Cell 2006, 126 (4) 677-89 10.1016/j.cell.2006.06.044
14. Stabley, D. R.; Jurchenko, C.; Marshall, S. S.; Salaita, K. S. Visualizing mechanical tension across membrane receptors with a fluorescent sensor Nat. Methods 2011, 9 (1) 64-67 10.1038/nmeth.1747
15. Jurchenko, C.; Salaita, K. S. Lighting up the Force: Investigating Mechanisms of Mechanotransduction Using Fluorescent Tension Probes Mol. Cell. Biol. 2015, 35, 2570 10.1128/MCB.00195-15
16. Zhang, Y.; Ge, C.; Zhu, C.; Salaita, K. DNA-based digital tension probes reveal integrin forces during early cell adhesion Nat. Commun. 2014, 5, 5167 10.1038/ncomms6167
17. Liu, Y.; Medda, R.; Liu, Z.; Galior, K.; Yehl, K.; Spatz, J. P.; Cavalcanti-Adam, E. A.; Salaita, K. Nanoparticle tension probes patterned at the nanoscale: Impact of integrin clustering on force transmission Nano Lett. 2014, 14 (10) 5539-46 10.1021/nl501912g
18. Liu, Y.; Yehl, K.; Narui, Y.; Salaita, K. Tension sensing nanoparticles for mechano-imaging at the living/nonliving interface J. Am. Chem. Soc. 2013, 135 (14) 5320-3 10.1021/ja401494e
19. Jurchenko, C.; Chang, Y.; Narui, Y.; Zhang, Y.; Salaita, K. S. Integrin-generated forces lead to streptavidin-biotin unbinding in cellular adhesions Biophys. J. 2014, 106 (7) 1436-46 10.1016/j.bpj.2014.01.049
20. Blakely, B. L.; Dumelin, C. E.; Trappmann, B.; McGregor, L. M.; Choi, C. K.; Anthony, P. C.; Duesterberg, V. K.; Baker, B. M.; Block, S. M.; Liu, D. R.; Chen, C. S. A DNA-based molecular probe for optically reporting cellular traction forces Nat. Methods 2014, 11 (12) 1229-32 10.1038/nmeth.3145
21. Morimatsu, M.; Mekhdjian, A. H.; Adhikari, A. S.; Dunn, A. R. Molecular tension sensors report forces generated by single integrin molecules in living cells Nano Lett. 2013, 13 (9) 3985-9 10.1021/nl4005145
22. Morimatsu, M.; Mekhdjian, A. H.; Chang, A. C.; Tan, S. J.; Dunn, A. R. Visualizing the interior architecture of focal adhesions with high-resolution traction maps Nano Lett. 2015, 15 (4) 2220-8 10.1021/nl5047335
23. Botello, E.; Harris, N. C.; Sargent, J.; Chen, W. H.; Lin, K. J.; Kiang, C. H. Temperature and chemical denaturant dependence of forced unfolding of titin I27 J. Phys. Chem. B 2009, 113 (31) 10845-8 10.1021/jp9002356
24. Lu, H.; Isralewitz, B.; Krammer, A.; Vogel, V.; Schulten, K. Unfolding of titin immunoglobulin domains by steered molecular dynamics simulation Biophys. J. 1998, 75 (2) 662-71 10.1016/S0006-3495(98)77556-3
25. Rief, M.; Gautel, M.; Oesterhelt, F.; Fernandez, J. M.; Gaub, H. E. Reversible unfolding of individual titin immunoglobulin domains by AFM Science 1997, 276 (5315) 1109-12 10.1126/science.276.5315.1109
26. Li, H.; Carrion-Vazquez, M.; Oberhauser, A. F.; Marszalek, P. E.; Fernandez, J. M. Point mutations alter the mechanical stability of immunoglobulin modules Nat. Struct. Biol. 2000, 7 (12) 1117-1120 10.1038/81964
27. Szoszkiewicz, R.; Ainavarapu, S. R.; Wiita, A. P.; Perez-Jimenez, R.; Sanchez-Ruiz, J. M.; Fernandez, J. M. Dwell time analysis of a single-molecule mechanochemical reaction Langmuir 2008, 24 (4) 1356-64 10.1021/la702368b
28. Zhou, Z.; Cironi, P.; Lin, A. J.; Xu, Y.; Hrvatin, S.; Golan, D. E.; Silver, P. A.; Walsh, C. T.; Yin, J. Genetically encoded short peptide tags for orthogonal protein labeling by Sfp and AcpS phosphopantetheinyl transferases ACS Chem. Biol. 2007, 2 (5) 337-46 10.1021/cb700054k
29. Aubin-Tam, M. E. Conjugation of nanoparticles to proteins Methods Mol. Biol. 2013, 1025, 19-27 10.1007/978-1-62703-462-3-3
30. Yehl, K.; Joshi, J. P.; Greene, B. L.; Dyer, R. B.; Nahta, R.; Salaita, K. Catalytic deoxyribozyme-modified nanoparticles for RNAi-independent gene regulation ACS Nano 2012, 6 (10) 9150-7 10.1021/nn3034265
31. Yehl, K.; Mugler, A.; Vivek, S.; Liu, Y.; Zhang, Y.; Fan, M.; Weeks, E. R.; Salaita, K. High-speed DNA-based rolling motors powered by RNase H. Nat. Nanotechnol. 2015, in press.
32. Dietz, H.; Rief, M. Exploring the energy landscape of GFP by single-molecule mechanical experiments Proc. Natl. Acad. Sci. U. S. A. 2004, 101 (46) 16192-7 10.1073/pnas.0404549101
33. Otten, M.; Ott, W.; Jobst, M. A.; Milles, L. F.; Verdorfer, T.; Pippig, D. A.; Nash, M. A.; Gaub, H. E. From genes to protein mechanics on a chip Nat. Methods 2014, 11 (11) 1127-30 10.1038/nmeth.3099
34. Pedelacq, J. D.; Cabantous, S.; Tran, T.; Terwilliger, T. C.; Waldo, G. S. Engineering and characterization of a superfolder green fluorescent protein Nat. Biotechnol. 2006, 24 (1) 79-88 10.1038/nbt1172
35. Pankov, R.; Yamada, K. M. Fibronectin at a glance J. Cell Sci. 2002, 115 (20) 3861-3863 10.1242/jcs.00059
36. Ainavarapu, S. R.; Brujic, J.; Huang, H. H.; Wiita, A. P.; Lu, H.; Li, L.; Walther, K. A.; Carrion-Vazquez, M.; Li, H.; Fernandez, J. M. Contour length and refolding rate of a small protein controlled by engineered disulfide bonds Biophys. J. 2007, 92 (1) 225-33 10.1529/biophysj.106.091561
37. Wiita, A. P.; Ainavarapu, S. R.; Huang, H. H.; Fernandez, J. M. Force-dependent chemical kinetics of disulfide bond reduction observed with single-molecule techniques Proc. Natl. Acad. Sci. U. S. A. 2006, 103 (19) 7222-7 10.1073/pnas.0511035103
38. Ainavarapu, S. R.; Wiita, A. P.; Huang, H. H.; Fernandez, J. M. A single-molecule assay to directly identify solvent-accessible disulfide bonds and probe their effect on protein folding J. Am. Chem. Soc. 2008, 130 (2) 436-7 10.1021/ja077851s
39. Wiita, A. P.; Perez-Jimenez, R.; Walther, K. A.; Grater, F.; Berne, B. J.; Holmgren, A.; Sanchez-Ruiz, J. M.; Fernandez, J. M. Probing the chemistry of thioredoxin catalysis with force Nature 2007, 450 (7166) 124-7 10.1038/nature06231
40. Liang, J.; Fernandez, J. M. Kinetic measurements on single-molecule disulfide bond cleavage J. Am. Chem. Soc. 2011, 133 (10) 3528-34 10.1021/ja109684q
41. Koti Ainavarapu, S. R.; Wiita, A. P.; Dougan, L.; Uggerud, E.; Fernandez, J. M. Single-molecule force spectroscopy measurements of bond elongation during a bimolecular reaction J. Am. Chem. Soc. 2008, 130 (20) 6479-87 10.1021/ja800180u
42. Pani, G.; Colavitti, R.; Bedogni, B.; Anzevino, R.; Borrello, S.; Galeotti, T. A redox signaling mechanism for density-dependent inhibition of cell growth J. Biol. Chem. 2000, 275 (49) 38891-9
43. Aroush, D.; Zaidel-Bar, R.; Bershadsky, A. D.; Wagner, H. D. Temporal evolution of cell focal adhesions: Experimental observations and shear stress profiles Soft Matter 2008, 4 (12) 2410-2417 10.1039/b804643n
44. Roca-Cusachs, P.; Gauthier, N. C.; Del Rio, A.; Sheetz, M. P. Clustering of alpha(5)beta(1) integrins determines adhesion strength whereas alpha(v)beta(3) and talin enable mechanotransduction Proc. Natl. Acad. Sci. U. S. A. 2009, 106 (38) 16245-50 10.1073/pnas.0902818106
45. Saeger, J.; Hytonen, V. P.; Klotzsch, E.; Vogel, V. GFPs mechanical intermediate states PLoS One 2012, 7 (10) e46962 10.1371/journal.pone.0046962
46. White, D. P.; Caswell, P. T.; Norman, J. C. alpha v beta3 and alpha5beta1 integrin recycling pathways dictate downstream Rho kinase signaling to regulate persistent cell migration J. Cell Biol. 2007, 177 (3) 515-25 10.1083/jcb.200609004