Video-rate multimodal multiphoton imaging and three-dimensional characterization of cellular dynamics in wounded skin

Joanne Li; Madison N. Wilson; Andrew J. Bower; Marina Marjanovic; Eric J. Chaney; Ronit Barkalifa; Stephen A. Boppart

doi:10.1142/s1793545820500078

[1] M. D. Cahalan, I. Parker, "Choreography of cell motility and interaction dynamics imaged by twophoton microscopy in lymphoid organs," Annu. Rev. Immunol. 26, 585–626 (2008).

[2] A. Nimmerjahn, F. Kirchhoff, F. Helmchen, "Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo," Science 308, 1314–1318 (2005).

[3] A. E. Carpenter et al., "CellProfiler: Image analysis software for identifying and quantifying cell phenotypes," Genome Biol. 7, R100 (2006).

[4] E. Meijering, O. Dzyubachyk, I. Smal, Methods for cell and particle tracking, Methods in Enzymology, P. M. Conn, Ed., Vol. 504, pp. 183–200, Academic Press (2012).

[5] D. R. Soil, International Review of Cytology, K. W. Jeon, J. Jarvik, Eds., Vol. 163, pp. 43–104, Academic Press (1995).

[6] G. Rabut, J. Ellenberg, "Automatic real-time threedimensional cell tracking by °uorescence microscopy," J. Microsc. 216, 131–137 (2004).

[7] M. Machacek, G. Danuser, "Morphodynamic pro-filing of protrusion phenotypes," Biophys. J. 90, 1439–1452 (2006).

[8] C. Bakal, J. Aach, G. Church, N. Perrimon, "Quantitative morphological signatures define local signaling networks regulating cell morphology," Science 316, 1753–1756 (2007).

[9] E. Alizadeh, S. M. Lyons, J. M. Castle, A. Prasad, "Measuring systematic changes in invasive cancer cell shape using Zernike moments," Integr. Biol. 8, 1183–1193 (2016).

[10] M. V. Boland, R. F. Murphy, "A neural network classifier capable of recognizing the patterns of all major subcellular structures in °uorescence microscope images of HeLa cells," Bioinformatics 17, 1213–1223 (2001).

[11] L. M. Thurston, P. F. Watson, A. J. Mileham, W. V. Holt, "Morphologically distinct sperm subpopulations defined by fourier shape descriptors in fresh ejaculates correlate with variation in boar semen quality following cryopreservation," J. Androl. 22, 382–394 (2001).

[12] P. J. Campagnola, L. M. Loew, "Second-harmonic imaging microscopy for visualizing biomolecular arrays in cells, tissues and organisms," Nat. Biotechnol. 21, 1356–1360 (2003).

[13] J. S. Bredfeldt, Y. Liu, M. W. Conklin, P. J. Keely, T. R. Mackie, K. W. Eliceiri, "Computational segmentation of collagen fibers from second-harmonic generation images of breast cancer," J. Biomed. Opt. 19, 1–11 (2014).

[14] A. J. Bower, Z. Arp, Y. Zhao, J. Li, E. J. Chaney, M. Marjanovic, A. Hughes-Earle, S. A. Boppart, "Longitudinal in vivo tracking of adverse effects following topical steroid treatment," Exp. Dermatol. 25, 362–367 (2016).

[15] S. Wu, H. Li, H. Yang, X. Zhang, Z. Li, S. Xu, "Quantitative analysis on collagen morphology in aging skin based on multiphoton microscopy," J. Biomed. Opt. 16, 1–4 (2011).

[16] P. D. Dale, J. A. Sherratt, P. K. Maini, "A mathematical model for collagen fibre formation during foetal and adult dermal wound healing," Proc. Royal Soc. B: Biol. Sci. 263, 653–660 (1996).

[17] J. S. Bredfeldt et al., "Automated quantification of aligned collagen for human breast carcinoma prognosis," J. Pathol. Inform. 5, 28 (2014).

[18] A. Keikhosravi, J. S. Bredfeldt, A. K. Sagar, K. W. Eliceiri, Methods in Cell Biology, J. C. Waters, T. Wittman, Eds., Vol. 123, pp. 531–546, Academic Press (2014).

[19] X. Chen, X. Zhou, S. T. C. Wong, "Automated segmentation, classification, and tracking of cancer cell nuclei in time-lapse microscopy," IEEE Trans. Biomed. Eng. 53, 762–766 (2006).

[20] D. G. Spiller, C. D. Wood, D. A. Rand, M. R. H. White, "Measurement of single-cell dynamics," Nature 465, 736–745 (2010).

[21] M. Esseling, B. Kemper, M. Antkowiak, D. J. Stevenson, L. Chaudet, M. A. Neil, P. W. French, G. von Bally, K. Dholakia, C. Denz, "Multimodal biophotonic workstation for live cell analysis," J. Biophoton. 5, 9–13 (2012).

[22] B. W. Graf, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, S. A. Boppart, "Long-term time-lapse multimodal intravital imaging of regeneration and bone-marrow-derived cell dynamics in skin," Technology 1, 8–19 (2013).

[23] M. C. Skala, K. M. Riching, A. Gendron- Fitzpatrick, J. Eickhoff, K. W. Eliceiri, J. G. White, N. Ramanujam, "In vivo multiphoton microscopy of NADH and FAD redox states, °uorescence lifetimes, and cellular morphology in precancerous epithelia," Proc. Natl. Acad. Sci. 104, 19494–19499 (2007).

[24] A. J. Bower, J. Li, E. J. Chaney, M. Marjanovic, D. R. Spillman, S. A. Boppart, "High-speed imaging of transient metabolic dynamics using two-photon °uorescence lifetime imaging microscopy," Optica 5, 1290–1296 (2018).

[25] B. W. Graf, A. J. Bower, E. J. Chaney, M. Marjanovic, S. G. Adie, M. De Lisio, M. C. Valero, M. D. Boppart, S. A. Boppart, "In vivo multimodal microscopy for detecting bone-marrow-derived cell contribution to skin regeneration," J. Biophoton. 7, 96–102 (2014).

[26] Y. Zhao, A. J. Bower, B. W. Graf, M. D. Boppart, S. A. Boppart, Imaging and Tracking Stem Cells: Methods and Protocols, K. Turksen, Ed., pp. 57–76, Humana Press, Totowa, NJ (2013).

[27] A. J. Bower, J. E. Sorrells, J. Li, M. Marjanovic, R. Barkalifa, S. A. Boppart, "Tracking metabolic dynamics of apoptosis with high-speed two-photon °uorescence lifetime imaging microscopy," Biomed. Opt. Exp. 10, 6408–6421 (2019).

[28] J. Li, A. J. Bower, V. Vainstein, Z. Gluzman- Poltorak, E. J. Chaney, M. Marjanovic, L. A. Basile, S. A. Boppart, "Effect of recombinant interleukin-12 on murine skin regeneration and cell dynamics using in vivo multimodal microscopy," Biomed. Opt. Exp. 6, 4277–4287 (2015).

[29] A. J. Walsh, A. T. Shah, J. T. Sharick, M. C. Skala, Advanced Time-Correlated Single Photon Counting Applications, W. Becker, Ed., pp. 435–456, Springer International Publishing, Cham (2015).

[30] J. D. Jones, H. E. Ramser, A. E. Woessner, K. P. Quinn, "In vivo multiphoton microscopy detects longitudinal metabolic changes associated with delayed skin wound healing," Commun. Biol. 1, 198 (2018).

[31] D. K. Bird, L. Yan, K. M. Vrotsos, K. W. Eliceiri, E. M. Vaughan, P. J. Keely, J. G. White, N. Ramanujam, "Metabolic mapping of MCF10A human breast cells via multiphoton °uorescence lifetime imaging of the coenzyme NADH," Cancer Res. 65, 8766–8773 (2005).