Use of artificial neural networks to identify and analyze polymerized actin-based cytoskeletal structures in 3D confocal images

Doyoung Park

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Quant. Biol. ›› 2023, Vol. 11 ›› Issue (3) : 306-319. DOI: 10.15302/J-QB-022-0325
RESEARCH ARTICLE
RESEARCH ARTICLE

Use of artificial neural networks to identify and analyze polymerized actin-based cytoskeletal structures in 3D confocal images

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Abstract

Background: Living cells need to undergo subtle shape adaptations in response to the topography of their substrates. These shape changes are mainly determined by reorganization of their internal cytoskeleton, with a major contribution from filamentous (F) actin. Bundles of F-actin play a major role in determining cell shape and their interaction with substrates, either as “stress fibers,” or as our newly discovered “Concave Actin Bundles” (CABs), which mainly occur while endothelial cells wrap micro-fibers in culture.

Methods: To better understand the morphology and functions of these CABs, it is necessary to recognize and analyze as many of them as possible in complex cellular ensembles, which is a demanding and time-consuming task. In this study, we present a novel algorithm to automatically recognize CABs without further human intervention. We developed and employed a multilayer perceptron artificial neural network (“the recognizer”), which was trained to identify CABs.

Results: The recognizer demonstrated high overall recognition rate and reliability in both randomized training, and in subsequent testing experiments.

Conclusion: It would be an effective replacement for validation by visual detection which is both tedious and inherently prone to errors.

Author summary

We propose an artificial neural network (ANN) as a kernel function of the recognizer of legitimate CABs from candidate CABs, that does not need human interventions. The performance of the recognizer shows noticeable recognition accuracy and addresses shortcomings of previous methods, including the need for human visual validation to recognize CABs from candidate CABs. Further, it helps to find and reduce errors resulting from human visual validation, which in turn would provide biologists/biophysicists a more comprehensive. understanding of a CAB.

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Keywords

Concave Actin Bundles / artificial neural network recognizer / planar actin distribution / 3D probability density estimation / cytoskeletal structures

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Doyoung Park. Use of artificial neural networks to identify and analyze polymerized actin-based cytoskeletal structures in 3D confocal images. Quant. Biol., 2023, 11(3): 306‒319 https://doi.org/10.15302/J-QB-022-0325

References

[1]
Karp,J. M. (2007). Development and therapeutic applications of advanced biomaterials. Curr. Opin. Biotechnol., 18: 454–459
CrossRef Google scholar
[2]
Langer,R. Tirrell,D. (2004). Designing materials for biology and medicine. Nature, 428: 487–492
CrossRef Google scholar
[3]
ParkD. Y.,Jones D.,MoldovanN. I.,MachirajuR.. (2013) Robust detection and visualization of cytoskeletal structures in fibrillar scaffolds from 3-dimensional confocal images, In: IEEE symposium on biological data visualization, Atlanta, GA, pp. 25–32
[4]
Jones,D., Park,D., Anghelina,M., cot,T., Machiraju,R., Xue,R., Lannutti,J. J., Thomas,J., Cole,S. L., Moldovan,L. . (2015). Actin grips: circular actin-rich cytoskeletal structures that mediate the wrapping of polymeric microfibers by endothelial cells. Biomaterials, 52: 395–406
CrossRef Google scholar
[5]
Boykov,Y., Veksler,O. (2001). Fast approximate energy minimization via graph cuts. IEEE Trans. Pattern Anal. Mach. Intell., 23: 1222–1239
CrossRef Google scholar
[6]
Friman,O., Hindennach,M., hnel,C. Peitgen,H. (2010). Multiple hypothesis template tracking of small 3D vessel structures. Med. Image Anal., 14: 160–171
CrossRef Google scholar
[7]
Petroll,W. M., Cavanagh,H. D., Barry,P., Andrews,P. Jester,J. (1993). Quantitative analysis of stress fiber orientation during corneal wound contraction. J. Cell Sci., 104: 353–363
CrossRef Google scholar
[8]
Thomason,D. B., Anderson,O. (1996). Fractal analysis of cytoskeleton rearrangement in cardiac muscle during head-down tilt. J. Appl. Physiol., 81: 1522–1527
CrossRef Google scholar
[9]
Weichsel,J., Herold,N., Lehmann,M. J., usslich,H. Schwarz,U. (2010). A quantitative measure for alterations in the actin cytoskeleton investigated with automated high-throughput microscopy. Cytometry A, 77: 52–63
CrossRef Google scholar
[10]
Lichtenstein,N., Geiger,B. (2003). Quantitative analysis of cytoskeletal organization by digital fluorescent microscopy. Cytometry A, 54: 8–18
CrossRef Google scholar
[11]
Shariff,A., Murphy,R. F. Rohde,G. (2010). A generative model of microtubule distributions, and indirect estimation of its parameters from fluorescence microscopy images. Cytometry A, 77: 457–466
CrossRef Google scholar
[12]
Fleischer,F., Ananthakrishnan,R., Eckel,S., Schmidt,H., Kas,J., Svitkina,T., Schmidt,V. (2010). Actin network architecture and elasticity in lamellipodia of melanoma cells. New J. Phys., 9: 1–14
[13]
LiH.,Shen T.,ShenT.. (2011) Actin filament segmentation using dynamic programming. In: International Conference on Information Processing in Medical Imaging (IPMI), pp. 411–423
[14]
LiH.,Shen T.,VavylonisD.. (2010) Actin filament segmentation using spatiotemporal active-surface and active-contour models. In: International Conference on Medical Image Computing and Computer Assisted Intervention (MICCAI), pp. 96–94
[15]
LiH.,Shen T.,VavylonisD.. (2009) Actin filament tracking based on particle filters and stretching open active contour models. In: International Conference on Medical Image Computing and Computer Assisted Intervention (MICCAI), pp. 673–681
[16]
LiH.,Shen T.,SmithM. B.,FujiwaraI.,Vavylonis D.. (2009) Automated actin filament segmentation, tracking, and tip elongation measurements based on open active contour models. In: IEEE International Symposium Biomedical Imaging: From Nano to Macro (ISBI), pp. 1302–1305
[17]
Fujiwara,I., Vavylonis,D. Pollard,T. (2007). Polymerization kinetics of ADP- and ADP-Pi-actin determined by fluorescence microscopy. Proc. Natl. Acad. Sci. USA, 104: 8827–8832
CrossRef Google scholar
[18]
Can,A., Shen,H., Turner,J. N., Tanenbaum,H. L. (1999). Rapid automated tracing and feature extraction from retinal fundus images using direct exploratory algorithms. IEEE Trans. Inf. Technol. Biomed., 3: 125–138
CrossRef Google scholar
[19]
Tupin,F., Maitre,H., Mangin,J. F., Nicolas,J. M. (1998). Detection of linear features in SAR images: application to road network extraction. IEEE Trans. Geosci. Remote Sens., 36: 434–453
CrossRef Google scholar
[20]
Stoica,R., Descombes,X. (2004). A Gibbs point process for road extraction from remotely sensed images. Int. J. Comput. Vis., 57: 121–136
CrossRef Google scholar
[21]
AguetF.,Jacob M.. (2005) Three-dimensional feature detection using optimal steerable filters. In: IEEE International Conference on Image Processing, pp. 1158–1161
[22]
Wu,J., Rajwa,B., Filmer,D. L., Hoffmann,C. M., Yuan,B., Chiang,C., Sturgis,J. Robinson,J. (2003). Automated quantification and reconstruction of collagen matrix from 3D confocal datasets. J. Microsc., 210: 158–165
CrossRef Google scholar
[23]
SteinA.Vader D.JawerthL.WeitzD.SanderL., (2009) An algorithm for extracting the network geometry of three-dimensional collagen gels. J. Microsc., 232, 463–475
[24]
Guy,G. (1997). Inference of surfaces, 3D curves, and junctions from sparse, noisy 3D data. IEEE Trans. Pattern Anal. Mach. Intell., 19: 1265–1277
CrossRef Google scholar
[25]
MedioniG.,Lee M. S.TangC.. (2000) Computational Framework for Segmentation and Grouping. New York: Elsevier Science Inc
[26]
NemhauserG. L.WolseyL.. (1988) Integer and Combinatorial Optimization. New York: John Wiley & Sons
[27]
KingG.. (1998) Unifying Political Methodology: The Likelihood Theory of Statistical Inference. New York: Cambridge University Press
[28]
Otsu,N. (1979). A threshold selection method from gray-level histograms, IEEE Trans. Sys. IEEE Trans. Syst. Man Cybern., 9: 62–66
CrossRef Google scholar
[29]
MitchellT.. (1997) Machine Learning. New York: WCB–McGraw–Hill

COMPLIANCE WITH ETHICS GUIDELINES

Conflicts of interest The author Doyoung Park declares that he has no conflict of interest or financial conflicts to disclose.
This article does not contain any studies with human or animal materials performed by any of the authors

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2023 The Author(s). Published by Higher Education Press.
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