Accurate Characterization of Spatial Orientations of Fiber-Like Structures in Biological Tissues and Its Applications

LIU Zhiyi1 MENG Jia1 QIU Jianrong1 HAN Tao1 WANG Di1 ZHUO Shuangmu2 DING Zhihua1

(1.State Key Laboratory of Modern Optical Instrumentation, College of Optical Science and Engineering, Zhejiang University, Hangzhou, Zhejiang, China 310027)
(2.Key Laboratory of Opto-Electronic Science and Technology for Medicine of Ministry of Education, Fujian Provincial Key Laboratory of Photonics Technology, Fujian Normal University, Fuzhou, Fujian, China 350007)
【Knowledge Link】Fourier transform

【Abstract】Fiber-like structure is one of the basic structures found in biological tissues. The spatial orientations of fiber-like structures change with the initiation and progression of some diseases. In this study, we present a brief overview of quantitative orientation analysis methods for fiber-like structures within biological tissues and main applications of these methods. We especially focus on the research progress of spatial orientation information in important disease models, including wound healing, osteoarthritis, breast cancer, peritoneal metastasis, and brain injury. Additionally, we explore the relations between tissue structure and function via specific engineered tissues. A highly sensitive and highly accurate description of the fiber-like structures within biological tissues serves as a novel method for studying disease initiation and progression, shows potential for early disease diagnosis, and improves our understanding of the mechanisms underlying some disorders. Finally, future potential applications of the orientation analysis methods are explored.

【Keywords】 medical optics; fiber-like structure; spatial orientation; three-dimensional organization; osteoarthritis; cancer; brain-like tissue; multi-photon imaging;

【DOI】

【Funds】 National Key Basic Research Program of China (2017YFA0700501) National Natural Science Foundation of China (11974310, 61905214, 31927801) Zhejiang Provincial Natural Science Foundation (LR20F050001) Fundamental Research Funds for the Central Universities of Ministry of Education of China (2019QNA5004)

Download this article

(Translated by REN XF)

    References

    [1] Geiger B, Bershadsky A, Pankov R, et al. Transmembrane crosstalk between the extracellular matrix and the cytoskeleton [J]. Nature Reviews Molecular Cell Biology, 2001, 2 (11): 793–805.

    [2] Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression [J]. Nature Reviews Cancer, 2002, 2 (3): 161–174.

    [3] Abbott N J, Rönnbäck L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier [J]. Nature Reviews Neuroscience, 2006, 7 (1): 41–53.

    [4] Discher D E, Mooney D J, Zandstra P W. Growth factors, matrices, and forces combine and control stem cells [J]. Science, 2009, 324 (5935): 1673–1677.

    [5] Zamir E, Katz M, Posen Y, et al. Dynamics and segregation of cell-matrix adhesions in cultured fibroblasts [J]. Nature Cell Biology, 2000, 2 (4): 191–196.

    [6] Butcher D T, Alliston T, Weaver V M. A tense situation: forcing tumour progression [J]. Nature Reviews Cancer, 2009, 9 (2): 108–122.

    [7] Lin H X, Zuo N, Zhuo S M, et al. Application of multiphoton microscopy in disease diagnosis [J]. Chinese Journal of Lasers, 2018, 45 (2): 0207014. (in Chinese)

    [8] Li H, Xia X Y, Chen T, et al. Applications of two-photon excitation fluorescence lifetime imaging in tumor diagnosis [J]. Chinese Journal of Lasers, 2018, 45 (2): 0207010. (in Chinese)

    [9] Zipfel W R, Williams R M, Webb W W. Nonlinear magic: multiphoton microscopy in the biosciences [J]. Nature Biotechnology, 2003, 21 (11): 1369–1377.

    [10] Zemel A, Rehfeldt F, Brown A E X, et al. Optimal matrix rigidity for stress-fibre polarization in stem cells [J]. Nature Physics, 2010, 6 (6): 468–473.

    [11] Barnes C, Speroni L, Quinn K P, et al. From single cells to tissues: interactions between the matrix and human breast cells in real time [J]. PLoS One, 2014, 9 (4): e93325.

    [12] Schriefl A J, Zeindlinger G, Pierce D M, et al. Determination of the layer-specific distributed collagen fibre orientations in human thoracic and abdominal aortas and common iliac arteries [J]. Journal of the Royal Society Interface, 2012, 9 (71): 1275–1286.

    [13] Altendorf H, Decencière E, Jeulin D, et al. Imaging and 3D morphological analysis of collagen fibrils [J]. Journal of Microscopy, 2012, 247 (2): 161–175.

    [14] Napadow V J, Chen Q, Mai V, et al. Quantitative analysis of three-dimensional-resolved fiber architecture in heterogeneous skeletal muscle tissue using NMR and optical imaging methods [J]. Biophysical Journal, 2001, 80 (6): 2968–2975.

    [15] Bancelin S, Nazac A, Ibrahim B H, et al. Determination of collagen fiber orientation in histological slides using Mueller microscopy and validation by second harmonic generation imaging [J]. Optics Express, 2014, 22 (19): 22561.

    16] Sivaguru M, Durgam S, Ambekar R, et al. Quantitative analysis of collagen fiber organization in injured tendons using Fourier transform-second harmonic generation imaging [J]. Optics Express, 2010, 18 (24): 24983.

    [17] Quinn K P, Georgakoudi I. Rapid quantification of pixel-wise fiber orientation data in micrographs [J]. Journal of Biomedical Optics, 2013, 18 (4): 046003.

    [18] Lau T Y, Ambekar R, Toussaint K C. Quantification of collagen fiber organization using three-dimensional Fourier transform-second-harmonic generation imaging [J]. Optics Express, 2012, 20 (19): 21821–21832.

    [19] Liu Z Y, Pouli D, Sood D, et al. Automated quantification of three-dimensional organization of fiber-like structures in biological tissues [J]. Biomaterials, 2017, 116: 34–47.

    [20] Liu Z Y, Quinn K P, Speroni L, et al. Rapid three-dimensional quantification of voxel-wise collagen fiber orientation [J]. Biomedical Optics Express, 2015, 6 (7): 2294–2310.

    [21] Quinn K P, Golberg A, Broelsch G F, et al. An automated image processing method to quantify collagen fibre organization within cutaneous scar tissue [J]. Experimental Dermatology, 2015, 24 (1): 78–80.

    [22] Quinn K P, Sullivan K E, Liu Z Y, et al. Optical metrics of the extracellular matrix predict compositional and mechanical changes after myocardial infarction [J]. Scientific Reports, 2016, 6: 35823.

    [23] Loeser R F, Goldring S R, Scanzello C R, et al. Osteoarthritis: a disease of the joint as an organ [J]. Arthritis & Rheumatism, 2012, 64 (6): 1697–1707.

    24] Mingalone C K, Liu Z Y, Hollander J M, et al. Bioluminescence and second harmonic generation imaging reveal dynamic changes in the inflammatory and collagen landscape in early osteoarthritis [J]. Laboratory Investigation, 2018, 98 (5): 656–669.

    [25] Nieminen M T, Rieppo J, Töyräs J, et al. T2 relaxation reveals spatial collagen architecture in articular cartilage: a comparative quantitative MRI and polarized light microscopic study [J]. Magnetic Resonance in Medicine, 2001, 46 (3): 487–493.

    [26] Ambekar R, Lau T Y, Walsh M, et al. Quantifying collagen structure in breast biopsies using second-harmonic generation imaging [J]. Biomedical Optics Express, 2012, 3 (9): 2021–2035.

    [27] Schnelldorfer T, Ware A L, Sarr M G, et al. Long-term survival after pancreatoduodenectomy for pancreatic adenocarcinoma [J]. Annals of Surgery, 2008, 247 (3): 456–462.

    28] Whatcott C J, Diep C H, Jiang P, et al. Desmoplasia in primary tumors and metastatic lesions of pancreatic cancer [J]. Clinical Cancer Research, 2015, 21 (15): 3561–3568.

    [29] Tang-Schomer M D, White J D, Tien L W, et al. Bioengineered functional brain-like cortical tissue [J]. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111 (38): 13811–13816.

    [30] Hirokawa N, Niwa S, Tanaka Y. Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease [J]. Neuron, 2010, 68 (4): 610–638.

    [31] Sundarakrishnan A, Zukas H, Coburn J, et al. Bioengineered in vitro tissue model of fibroblast activation for modeling pulmonary fibrosis [J]. ACS Biomaterials Science & Engineering, 2019, 5 (5): 2417–2429.

    [32] Liu Z Y, Speroni L, Quinn K P, et al. 3D organizational mapping of collagen fibers elucidates matrix remodeling in a hormone-sensitive 3D breast tissue model [J]. Biomaterials, 2018, 179: 96–108.

    [33] Dhimolea E, Maffini M V, Soto A M, et al. The role of collagen reorganization on mammary epithelial morphogenesis in a 3D culture model [J]. Biomaterials, 2010, 31 (13): 3622–3630.

    [34] Birk J W, Tadros M, Moezardalan K, et al. Second harmonic generation imaging distinguishes both high-grade dysplasia and cancer from normal colonic mucosa [J]. Digestive Diseases and Sciences, 2014, 59 (7): 1529–1534.

This Article

ISSN:0258-7025

CN: 31-1339/TN

Vol 47, No. 02, Pages 22-35

February 2020

Downloads:2

Share
Article Outline

Knowledge

Abstract

  • 1 Introduction
  • 2 Quantitative characterization method of spatial orientation of fiber-like structures
  • 3 Application of spatial orientation information in biomedicine
  • 4 Conclusion
  • References