AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
Article Link
Collect
Submit Manuscript
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article

Infrared nanoimaging of nanoscale sliding dislocation of collagen fibrils

Zhi Qiao1,2Mengfei Xue3,4,5Yongqian Zhao4,5Yindong Huang2Ming Zhang6Chao 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
Show Author Information

Graphical Abstract

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.

References

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.

2

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

3

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

4

Vinson, V. Brittle bones. Science 2009, 323, 1406.

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.

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.

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.

8

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

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.

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.

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.

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.

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.

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.

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.

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.

17

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

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.

19

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

20

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

21

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

22

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

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.

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.

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.

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.

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.

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.

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.

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.

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.

32

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

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.

34

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

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.

36

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

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.

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.

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.

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.

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.

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.

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.

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.

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.

46

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

47

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

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.

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.

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.

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.

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.

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.

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.

55

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

Nano Research
Pages 2355-2361
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
Topics:

971

Views

16

Crossref

8

Web of Science

15

Scopus

2

CSCD

Altmetrics

Received: 08 May 2021
Revised: 24 June 2021
Accepted: 28 June 2021
Published: 12 August 2021
© Tsinghua University Press and Springer-Verlag GmbH Germany, part of Springer Nature 2021
Return