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Nano Research 2022, 15(3): 2355-2361 https://doi.org/10.1007/s12274-021-3721-4
Research Article | Issue | Published: 12 August 2021

Infrared nanoimaging of nanoscale sliding dislocation of collagen fibrils

Show Author's Information Zhi Qiao1,2,  Mengfei Xue3,4,5,  Yongqian Zhao4,5,  Yindong Huang2,  Ming Zhang6,  Chao Chang1,2( ),  Jianing Chen4,5,7( )
Key Laboratory for Physical Electronics and Devices of the Ministry of Education, School of Electronic Science and Engineering, Xi'an Jiaotong University, Xi’an 710049, China
Innovation Laboratory of Terahertz Biophysics, National Innovation Institute of Defense Technology, Beijing 100071, China
Wenzhou Institute, University of Chinese Academy of Sciences, Wenzhou 325001, China
Institute of Physics, Chinese Academy of Sciences and Beijing National Laboratory for Condensed Matter Physics, Beijing 100190, China
School of Physical Sciences, University of Chinese Academy of Sciences, Beijing 100049, China
Department of Neurobiology, Collaborative Innovation Center for Brain Science and Shaanxi Key Laboratory of Brain Disorders, School of Basic Medicine, Fourth Military Medical University, Xi’an 710032, China
Songshan Lake Materials Laboratory, Dongguan 523808, China
Keywords:
dislocation, scattering near-field optical microscopy, collagen fibrils, D periodicity
Topics:
Infrared imaging
Cite this article:
Qiao Z, Xue M, Zhao Y, et al. Infrared nanoimaging of nanoscale sliding dislocation of collagen fibrils. Nano Research, 2022, 15(3): 2355-2361. https://doi.org/10.1007/s12274-021-3721-4
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Abstract Full text About this article

Collagen, one of the major components in the mammalian connective tissues, plays an essential role in many vital physiological processes. Many common diseases, such as fibrosis, overuse injuries, and bone fracture, are associated with collagen arrangement defects. However, the underlying mechanism of collagen arrangement defects remains elusive. In this study, we applied infrared scattering-type scanning near-field optical microscopy to study collagen fibrils’ structural properties. Experimentally, we observed two types of collagen fibrils’ arrangement with different periodic characteristics. A crystal sliding model was employed to explain this observation qualitatively. Our results suggest that the collagen dislocation propagates in collagen fibrils, which may shed light on many collagen diseases’ pathogenesis. These findings help to understand the regulation mechanism of hierarchical biological structure.


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About this article

Infrared nanoimaging of nanoscale sliding dislocation of collagen fibrils

Show Author's information Zhi Qiao1,2, Mengfei Xue3,4,5, Yongqian Zhao4,5, Yindong Huang2, Ming Zhang6, Chao Chang1,2( ), Jianing Chen4,5,7( )
Key Laboratory for Physical Electronics and Devices of the Ministry of Education, School of Electronic Science and Engineering, Xi'an Jiaotong University, Xi’an 710049, China
Innovation Laboratory of Terahertz Biophysics, National Innovation Institute of Defense Technology, Beijing 100071, China
Wenzhou Institute, University of Chinese Academy of Sciences, Wenzhou 325001, China
Institute of Physics, Chinese Academy of Sciences and Beijing National Laboratory for Condensed Matter Physics, Beijing 100190, China
School of Physical Sciences, University of Chinese Academy of Sciences, Beijing 100049, China
Department of Neurobiology, Collaborative Innovation Center for Brain Science and Shaanxi Key Laboratory of Brain Disorders, School of Basic Medicine, Fourth Military Medical University, Xi’an 710032, China
Songshan Lake Materials Laboratory, Dongguan 523808, China

Abstract

Collagen, one of the major components in the mammalian connective tissues, plays an essential role in many vital physiological processes. Many common diseases, such as fibrosis, overuse injuries, and bone fracture, are associated with collagen arrangement defects. However, the underlying mechanism of collagen arrangement defects remains elusive. In this study, we applied infrared scattering-type scanning near-field optical microscopy to study collagen fibrils’ structural properties. Experimentally, we observed two types of collagen fibrils’ arrangement with different periodic characteristics. A crystal sliding model was employed to explain this observation qualitatively. Our results suggest that the collagen dislocation propagates in collagen fibrils, which may shed light on many collagen diseases’ pathogenesis. These findings help to understand the regulation mechanism of hierarchical biological structure.

Keywords: dislocation, scattering near-field optical microscopy, collagen fibrils, D periodicity

References(55)

1

Zitnay, J. L.; Jung, G. S.; Lin, A. H.; Qin, Z.; Li, Y.; Yu, S. M.; Buehler, M. J.; Weiss, J. A. Accumulation of collagen molecular unfolding is the mechanism of cyclic fatigue damage and failure in collagenous tissues. Sci. Adv. 2020, 6, eaba2795.
DOI Google Scholar
2

Henderson, N. C.; Rieder, F.; Wynn, T. A. Fibrosis: From mechanisms to medicines. Nature 2020, 587, 555–566.
DOI Google Scholar
3

Kisseleva, T.; Brenner, D. Molecular and cellular mechanisms of liver fibrosis and its regression. Nat. Rev. Gastroenterol. Hepatol. 2021, 18, 151–166.
DOI Google Scholar
4

Vinson, V. Brittle bones. Science 2009, 323, 1406.
Google Scholar
5

Angele, P.; Abke, J.; Kujat, R.; Faltermeier, H.; Schumann, D.; Nerlich, M.; Kinner, B.; Englert, C.; Ruszczak, Z.; Mehrl, R. et al. Influence of different collagen species on physico-chemical properties of crosslinked collagen matrices. Biomaterials 2004, 25, 2831–2841.
DOI Google Scholar
6

Ivankin, A.; Boldirev, V.; Fadeev, G.; Baburina, M.; Kulikovskii, A.; Vostrikova, N. Denaturation of collagen structures and their transformation under the physical and chemical effects. J. Phys. Conf. Ser. 2017, 918, 012010.
DOI Google Scholar
7

Pashley, D. H.; Tay, F. R.; Yiu, C.; Hashimoto, M.; Breschi, L.; Carvalho, R. M.; Ito, S. Collagen degradation by host-derived enzymes during aging. J. Dent. Res. 2004, 83, 216–221.
DOI Google Scholar
8

Harrington, D. J. Bacterial collagenases and collagen-degrading enzymes and their potential role in human disease. Infect. Immun. 1996, 64, 1885–1891.
DOI Google Scholar
9

Lovell, C. R.; Smolenski, K. A.; Duance, V. C.; Light, N. D.; Young, S.; Dyson, M. Type I and III collagen content and fibre distribution in normal human skin during ageing. Br. J. Dermatol. 1987, 117, 419–428.
DOI Google Scholar
10

Diamant, J.; Keller, A.; Baer, E.; Litt, M.; Arridge, R. G. C. Collagen; ultrastructure and its relation to mechanical properties as a function of ageing. Proc. Roy. Soc.B. 1972, 180, 293–315.
Google Scholar
11

Takano, Y.; Turner, C. H.; Owan, I.; Martin, R. B.; Lau, S. T.; Forwood, M. R.; Burr, D. B. Elastic anisotropy and collagen orientation of osteonal bone are dependent on the mechanical strain distribution. J. Orthop. Res. 1999, 17, 59–66.
DOI Google Scholar
12

Skedros, J. G.; Dayton, M. R.; Sybrowsky, C. L.; Bloebaum, R. D.; Bachus, K. N. The influence of collagen fiber orientation and other histocompositional characteristics on the mechanical properties of equine cortical bone. J. Exp. Biol. 2006, 209, 3025–3042.
DOI Google Scholar
13

Raspanti, M.; Ottani, V.; Ruggeri, A. Different architectures of the collagen fibril: Morphological aspects and functional implications. Int. J. Biol. Macromol. 1989, 11, 367–371.
DOI Google Scholar
14

Holmes, D. F.; Graham, H. K.; Trotter, J. A.; Kadler, K. E. STEM/TEM studies of collagen fibril assembly. Micron 2001, 32, 273–285.
DOI Google Scholar
15

Yang, R.; Elankumaran, Y.; Hijjawi, N.; Ryan, U. Validation of cell-free culture using scanning electron microscopy (SEM) and gene expression studies. Exp. Parasitol. 2015, 153, 55–62.
DOI Google Scholar
16

Carrière, M.; Gouget, B.; Gallien, J. P.; Avoscan, L.; Gobin, R.; Verbavatz, J. M.; Khodja, H. Cellular distribution of uranium after acute exposure of renal epithelial cells: SEM, TEM and nuclear microscopy analysis. Nucl. Instrum. Methods Phys. Res. Sect. B 2005, 231, 268–273.
Google Scholar
17

Heintzmann, R.; Ficz, G. Breaking the resolution limit in light microscopy. Methods Cell Biol. 2007, 81, 561–580.
Google Scholar
18

Huang, B.; Wang, W. Q.; Bates, M.; Zhuang, X. W. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 2008, 319, 810–813.
DOI Google Scholar
19

Huang, B.; Babcock, H.; Zhuang, X. W. Breaking the diffraction barrier: Super-resolution imaging of cells. Cell 2010, 143, 1047–1058.
DOI Google Scholar
20

Fornasiero, E. F.; Opazo, F. Super-resolution imaging for cell biologists-concepts, applications, current challenges and developments. BioEssays 2015, 37, 436–451.
DOI Google Scholar
21

Cox, S. Super-resolution imaging in live cells. Dev. Biol. 2015, 401, 175–181.
DOI Google Scholar
22

Bozec, L.; van der Heijden, G.; Horton, M. Collagen fibrils: Nanoscale ropes. Biophys. J. 2007, 92, 70–75.
DOI Google Scholar
23

Svensson, R. B.; Hassenkam, T.; Hansen, P.; Magnusson, S. P. Viscoelastic behavior of discrete human collagen fibrils. J. Mech. Behav. Biomed. Mater. 2010, 3, 112–115.
DOI Google Scholar
24

Chen, J. N.; Badioli, M.; Alonso-González, P.; Thongrattanasiri, S.; Huth, F.; Osmond, J.; Spasenović, M.; Centeno, A.; Pesquera, A.; Godignon, P. et al. Optical nano-imaging of gate-tunable graphene plasmons. Nature 2012, 487, 77–81.
DOI Google Scholar
25

Amrania, H.; Drummond, L.; Coombes, R. C.; Shousha, S.; Woodley-Barker, L.; Weir, K.; Hart, W.; Carter, I.; Phillips, C. C. New IR imaging modalities for cancer detection and for intra-cell chemical mapping with a sub-diffraction mid-IR s-SNOM. Faraday Discuss. 2016, 187, 539–553.
DOI Google Scholar
26

Bulat, K.; Rygula, A.; Szafraniec, E.; Ozaki, Y.; Baranska, M. Live endothelial cells imaged by scanning near-field optical microscopy (SNOM): Capabilities and challenges. J. Biophotonics 2017, 10, 928–938.
DOI Google Scholar
27

Andolfi, L.; Trevisan, E.; Troian, B.; Prato, S.; Boscolo, R.; Giolo, E.; Luppi, S.; Martinelli, M.; Ricci, G.; Zweyer, M. The application of scanning near field optical imaging to the study of human sperm morphology. J. Nanobiotechnol. 2015, 13, 2.
DOI Google Scholar
28

Zweyer, M.; Troian, B.; Spreafico, V.; Prato, S. SNOM on cell thin sections: Observation of Jurkat and MDAMB453 cells. J. Microsc. 2008, 229, 440–446.
DOI Google Scholar
29

Li, P. N.; Lewin, M.; Kretinin, A. V.; Caldwell, J. D.; Novoselov, K. S.; Taniguchi, T.; Watanabe, K.; Gaussmann, F.; Taubner, T. Hyperbolic phonon-polaritons in boron nitride for near-field optical imaging and focusing. Nat. Commun. 2015, 6, 7507.
DOI Google Scholar
30

Li, P.; Dolado, I.; Alfaro-Mozaz, F. J.; Nikitin, A. Y.; Casanova, F.; Hueso, L. E.; Vélez, S.; Hillenbrand, R. Optical nanoimaging of hyperbolic surface polaritons at the edges of van der Waals materials. Nano Lett. 2017, 17, 228–235.
DOI Google Scholar
31

Alonso-González, P.; Albella, P.; Schnell, M.; Chen, J.; Huth, F.; García-Etxarri, A.; Casanova, F.; Golmar, F.; Arzubiaga, L.; Hueso, L. E. et al. Resolving the electromagnetic mechanism of surface-enhanced light scattering at single hot spots. Nat. Commun. 2012, 3, 684.
DOI Google Scholar
32

Carney, P. S.; Deutsch, B.; Govyadinov, A. A.; Hillenbrand, R. Phase in nanooptics. ACS Nano 2012, 6, 8–12.
DOI Google Scholar
33

Mouw, J. K.; Ou, G. Q.; Weaver, V. M. Extracellular matrix assembly: A multiscale deconstruction. Nat. Rev. Mol. Cell Biol. 2014, 15, 771–785.
Google Scholar
34

Petruska, J. A.; Hodge, A. J. A subunit model for the tropocollagen macromolecule. Proc. Natl. Acad. Sci. USA 1964, 51, 871–876.
DOI Google Scholar
35

Erickson, B.; Fang, M.; Wallace, J. M.; Orr, B. G.; Les, C. M.; Holl, M. M. B. Nanoscale structure of type I collagen fibrils: Quantitative measurement of d-spacing. Biotechnol. J. 2013, 8, 117–126.
DOI Google Scholar
36

Jung, G. S.; Buehler, M. J. Multiscale modeling of muscular-skeletal systems. Annu. Rev. Biomed. Eng. 2017, 19, 435–457.
DOI Google Scholar
37

Gautieri, A.; Vesentini, S.; Redaelli, A.; Buehler, M. J. Hierarchical structure and nanomechanics of collagen microfibrils from the atomistic scale up. Nano Lett. 2011, 11, 757–766.
DOI Google Scholar
38

Depalle, B.; Qin, Z.; Shefelbine, S. J.; Buehler, M. J. Influence of cross-link structure, density and mechanical properties in the mesoscale deformation mechanisms of collagen fibrils. J. Mech. Behav. Biomed. Mater. 2015, 52, 1–13.
DOI Google Scholar
39

Siegmund, T.; Allen, M. R.; Burr, D. B. Failure of mineralized collagen fibrils: Modeling the role of collagen cross-linking. J. Biomech. 2008, 41, 1427–1435.
DOI Google Scholar
40

Buehler, M. J. Atomistic and continuum modeling of mechanical properties of collagen: Elasticity, fracture, and self-assembly. J. Mater. Res. 2006, 21, 1947–1961.
DOI Google Scholar
41

Goldenfeld, N.; Woese, C. Life is physics: Evolution as a collective phenomenon far from equilibrium. Annu. Rev. Condens. Matter Phys. 2011, 2, 375–399.
DOI Google Scholar
42

Govyadinov, A. A.; Amenabar, I.; Huth, F.; Carney, P. S.; Hillenbrand, R. Quantitative measurement of local infrared absorption and dielectric function with tip-enhanced near-field microscopy. J. Phys. Chem. Lett. 2013, 4, 1526–1531.
DOI Google Scholar
43

Cvitkovic, A.; Ocelic, N.; Hillenbrand, R. Analytical model for quantitative prediction of material contrasts in scattering-type near-field optical microscopy. Opt. Express 2007, 15, 8550–8565.
DOI Google Scholar
44

McLeod, A. S.; Kelly, P.; Goldflam, M. D.; Gainsforth, Z.; Westphal, A. J.; Dominguez, G.; Thiemens, M. H.; Fogler, M. M.; Basov, D. N. Model for quantitative tip-enhanced spectroscopy and the extraction of nanoscale-resolved optical constants. Phys. Rev. B 2014, 90, 085136.
DOI Google Scholar
45

Veres, S. P.; Harrison, J. M.; Lee, J. M. Mechanically overloading collagen fibrils uncoils collagen molecules, placing them in a stable, denatured state. Matrix Biol. 2014, 33, 54–59.
DOI Google Scholar
46

Hulmes, D. J. S. Building collagen molecules, fibrils, and suprafibrillar structures. J. Struct. Biol. 2002, 137, 2–10.
DOI Google Scholar
47

Hulmes, D. J. S.; Miller, A. Quasi-hexagonal molecular packing in collagen fibrils. Nature 1979, 282, 878–880.
DOI Google Scholar
48

Lee, J. L.; Scheraga, H. A.; Rackovsky, S. Computational study of packing a collagen-like molecule: Quasi-hexagonal vs “Smith” collagen microfibril model. Pept. Sci. 1996, 40, 595–607.
DOI
49

Eekhoff, J. D.; Fang, F.; Lake, S. P. Multiscale mechanical effects of native collagen cross-linking in tendon. Connect. Tissue Res. 2018, 59, 410–422.
DOI Google Scholar
50

Minary-Jolandan, M.; Yu, M. F. Nanomechanical heterogeneity in the gap and overlap regions of type I collagen fibrils with implications for bone heterogeneity. Biomacromolecules 2009, 10, 2565–2570.
DOI Google Scholar
51

Bose, K.; Lech, C. J.; Heddi, B.; Phan, A. T. High-resolution AFM structure of DNA G-wires in aqueous solution. Nat. Commun. 2018, 9, 1959.
DOI Google Scholar
52

Depalle, B.; Qin, Z.; Shefelbine, S. J.; Buehler, M. J. Large deformation mechanisms, plasticity, and failure of an individual collagen fibril with different mineral content. J. Bone Miner. Res. 2016, 31, 380–390.
DOI Google Scholar
53

Marino, M. Molecular and intermolecular effects in collagen fibril mechanics: A multiscale analytical model compared with atomistic and experimental studies. Biomech. Model. Mechanobiol. 2016, 15, 133–154.
DOI Google Scholar
54

Leikina, E.; Mertts, M. V.; Kuznetsova, N.; Leikin, S. Type I collagen is thermally unstable at body temperature. Proc. Natl. Acad. Sci. USA 2002, 99, 1314–1318.
DOI Google Scholar
55

Hansen, N.; Kuhlmann-Wilsdorf, D. Low energy dislocation structures due to unidirectional deformation at low temperatures. Mater. Sci. Eng. 1986, 81, 141–161.
DOI Google Scholar
Publication history
Copyright
Acknowledgements

Publication history

Received: 08 May 2021
Revised: 24 June 2021
Accepted: 28 June 2021
Published: 12 August 2021
Issue date: March 2022

Copyright

© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2021

Acknowledgements

Acknowledgements

This work was supported by the National Key Research and Development Program of China (No. 2016YFA0203500), the National Natural Science Foundation of China (No. 11874407), and Strategic Priority Research Program of the Chinese Academy of Sciences (No. XDB 30000000). C. C. acknowledges the support from the XPLORER PRIZE. We thank the staff from BL01B beamline of the National Facility for Protein Science in Shanghai (NFPS) at Shanghai Synchrotron Radiation Facility for assistance during data collection.

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