Label-free 3D computational imaging of spermatozoon locomotion, head spin and flagellum beating over a large volume

Mustafa Ugur Daloglu; Wei Luo; Faizan Shabbir; Francis Lin; Kevin Kim; Inje Lee; Jia-Qi Jiang; Wen-Jun Cai; Vishwajith Ramesh; Meng-Yuan Yu; Aydogan Ozcan

doi:10.1038/lsa.2017.121

Go to Nature Website

Your Location：

Home >

Browse articles >

Label-free 3D computational imaging of spermatozoon locomotion, head spin and flagellum beating over a large volume

Original Articles

- Label-free 3D computational imaging of spermatozoon locomotion, head spin and flagellum beating over a large volume
- Label-free 3D computational imaging of spermatozoon locomotion, head spin and flagellum beating over a large volume
- LSA 2018年7卷第1期
- Affiliations：
  
  1.Electrical and Computer Engineering Department, University of California, Los Angeles, CA 90095, USA
  2.Bioengineering Department, University of California, Los Angeles, CA 90095, USA
  3.California NanoSystems Institute (CNSI), University of California, Los Angeles, CA 90095, USA
  4.Chemistry and Biochemistry Department, University of California, Los Angeles, CA 90095, USA
  5.Department of Physics and Astronomy, University of California, Los Angeles, CA 90095, USA
  6.Department of Mathematics, University of California, Los Angeles, CA 90095, USA
  7.Computer Science Department, University of California, Los Angeles, CA 90095, USA
  8.Department of Surgery, David Geffen School of Medicine, University of California, Los Angeles, CA 90095, USA
- Author bio：
  
  A Ozcan, Email: ozcan@ucla.edu
- Funds：
- DOI：10.1038/lsa.2017.121
  中图分类号：
- 纸质出版日期：2018，
  
  网络出版日期：2018-01-12，
  
  收稿日期：2017-05-27，
  
  修回日期：2017-08-14，
  
  录用日期：2017-08-14
- Accepted：
Scan QR Code
Label-free 3D computational imaging of spermatozoon locomotion, head spin and flagellum beating over a large volume[J]. LSA, 2018,7(1):17121-11.

Ugur, M. et al. Label-free 3D computational imaging of spermatozoon locomotion, head spin and flagellum beating over a large volume. Light: Science & Applications, 7, 17121 (2018).
Label-free 3D computational imaging of spermatozoon locomotion, head spin and flagellum beating over a large volume[J]. LSA, 2018,7(1):17121-11. DOI： 10.1038/lsa.2017.121.

Ugur, M. et al. Label-free 3D computational imaging of spermatozoon locomotion, head spin and flagellum beating over a large volume. Light: Science & Applications, 7, 17121 (2018). DOI： 10.1038/lsa.2017.121.

摘要

Abstract

We report a high-throughput and label-free computational imaging technique that simultaneously measures in three-dimensional (3D) space the locomotion and angular spin of the freely moving heads of microswimmers and the beating patterns of their flagella over a sample volume more than two orders-of-magnitude larger compared to existing optical modalities. Using this platform

we quantified the 3D locomotion of 2133 bovine sperms and determined the spin axis and the angular velocity of the sperm head

providing the perspective of an observer seated at the moving and spinning sperm head. In this constantly transforming perspective

flagellum-beating patterns are decoupled from both the 3D translation and spin of the head

which provides the opportunity to truly investigate the 3D spatio-temporal kinematics of the flagellum. In addition to providing unprecedented information on the 3D locomotion of microswimmers

this computational imaging technique could also be instrumental for micro-robotics and sensing research

enabling the high-throughput quantification of the impact of various stimuli and chemicals on the 3D swimming patterns of sperms

motile bacteria and other micro-organisms

generating new insights into taxis behaviors and the underlying biophysics.

关键词

Keywords

flagellar motionholographyon-chip microscopysperm head spinsperm tracking

references

Battle C, Broedersz CP, Fakhri N, Geyer VF, Howard Jet al. Broken detailed balance at mesoscopicscales in active biological systems.Science2016;352: 604–607..

Acott TS, Katz DF, Hoskins DD. Movement characteristics of bovine epididymal spermatozoa: effects of forward motility protein and epididymal maturation.Biol Reprod1983;29: 389–399..

Keller JB, Rubinow SI. Swimming of flagellated microorganisms.Biophys J1976;16: 151–170..

Gray J. The movement of the spermatozoa of the bull.J Exp Biol1958;35: 96–108..

Rikmenspoel R. The tail movement of bull spermatozoa: observations and model calculations.Biophys J1965;5: 365–392..

Ishijima S, Hamaguchi MS, Naruse M, Ishijima SA, Hamaguchi Y. Rotational movement of a spermatozoon around its long axis.J Exp Biol1992;163: 15–31..

Mortimer ST. CASA—practical aspects.J Androl2000;21: 515–524..

Mortimer ST, van der Horst G, Mortimer D. The future of computer-aided sperm analysis.Asian J Androl2015;17: 545–553..

Amann RP, Waberski D. Computer-assisted sperm analysis (CASA): Capabilities and potential developments.Theriogenology2014;81: 5–17..

Su TW, Xue L, Ozcan A. High-throughput lensfree 3D tracking of human sperms reveals rare statistics of helical trajectories.Proc Natl Acad Sci USA2012;109: 16018–16022..

DRM-600 CELL-VU®sperm counting chamber. Available athttp://cellvu.com/products/drm-600-cell-vu-sperm-counting-chamber/http://cellvu.com/products/drm-600-cell-vu-sperm-counting-chamber/(accessed on September 2016)..

Liu J, Leung C, Lu Z, Sun Y Human sperm tracking, analysis, and manipulation. In: Rakotondrabe M editors.Smart Materials-Based Actuators at the Micro/Nano-Scale. Springer: New York, NY, USA. 2013, pp251–264.

Smith DJ, Gaffney EA, Blake JR, Kirkman-Brown JC. Human sperm accumulation near surfaces: a simulation study.J Fluid Mech2009;621: 289–320..

Bahr GF, Zeitler E. Study of bull spermatozoa. Quantitative electron microscopy.J Cell Biol1964;21: 175–189..

Pesch S, Bergmann M. Structure of mammalian spermatozoa in respect to viability, fertility and cryopreservation.Micron2006;37: 597–612..

Krzyzosiak J, Molan P, Vishwanath R. Measurements of bovine sperm velocities under true anaerobic and aerobic conditions.Anim Reprod Sci1999;55: 163–173..

Minsky M. Memoir on inventing the confocal scanning microscope.Scanning1988;10: 128–138..

Huisken J, Swoger J, Del Bene F, Wittbrodt J, Stelzer EHK. Optical sectioning deep inside live embryos by selective plane illumination microscopy.Science2004;305: 1007–1009..

Planchon TA, Gao L, Milkie DE, Davidson MW, Galbraith JAet al. Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination.Nat Methods2011;8: 417–423..

Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WGet al. Optical coherence tomography.Science1991;254: 1178–1181..

Tearney GJ, Brezinski ME, Bouma BE, Boppart SA, Pitris Cet al.In vivoendoscopic optical biopsy with optical coherence tomography.Science1997;276: 2037–2039..

de Boer JF, Cense B, Park BH, Pierce MC, Tearney GJet al. Improved signal-to-noise ratio in spectral-domain compared with time-domain optical coherence tomography.Opt Lett2003;28: 2067–2069..

Drescher K, Leptos KC, Goldstein RE. How to track protists in three dimensions.Rev Sci Instrum2009;80: 014301..

Silva-Villalobos F, Pimentel JA, Darszon A, Corkidi G (eds). Imaging of the 3D dynamics of flagellar beating in human sperm. InProceedings of the 36th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC); 26–30 August 2014; Chicago, IL, USA. IEEE: Chicago, IL, USA, 2014, pp190–193.

Corkidi G, Taboada B, Wood CD, Guerrero A, Darszon A. Tracking sperm in three-dimensions.Biochem Biophys Res Commun2008;373: 125–129..

Frauel Y, Naughton TJ, Matoba O, Tajahuerce E, Javidi B. Three-dimensional imaging and processing using computational holographic imaging.Proc IEEE2006;94: 636–653..

Rosen J, Brooker G. Non-scanning motionless fluorescence three-dimensional holographic microscopy.Nat Photon2008;2: 190–195..

Rivenson Y, Stern A, Javidi B. Overview of compressive sensing techniques applied in holography [Invited].Appl Opt2013;52: A423–A432..

Gorocs Z, Ozcan A. On-chip biomedical imaging.IEEE Rev Biomed Eng2013;6: 29–46..

Shan MG, Kandel ME, Popescu G. Refractive index variance of cells and tissues measured by quantitative phase imaging.Opt Express2017;25: 1573–1581..

Kandel ME, Teng KW, Selvin PR, Popescu G. Label-free imaging of single microtubule dynamics using spatial light interference microscopy.ACS Nano2017;11: 647–655..

Indebetouw G, Tada Y, Rosen J, Brooker G. Scanning holographic microscopy with resolution exceeding the Rayleigh limit of the objective by superposition of off-axis holograms.Appl Opt2007;46: 993–1000..

Moon I, Javidi B. Three-dimensional identification of stem cells by computational holographic imaging.J Roy Soc Interface2007;4: 305–313..

Xu WB, Jericho MH, Meinertzhagen IA, Kreuzer HJ. Digital in-line holography for biological applications.Proc Natl Acad Sci USA2001;98: 11301–11305..

Matrecano M, Paturzo M, Ferraro P. Extended focus imaging in digital holographic microscopy: a review.Opt Eng2014;53: 112317..

Colomb T, Pavillon N, Kühn J, Cuche E, Depeursinge Cet al. Extended depth-of-focus by digital holographic microscopy.Opt Lett2010;35: 1840–1842..

Di Caprio G, Gioffrè MA, Saffioti N, Grilli S, Ferraro Pet al. Quantitative label-free animal sperm imaging by means of digital holographic microscopy.IEEE J Sel Top Quantum Electron2010;16: 833–840..

Memmolo P, Di Caprio G, Distante C, Paturzo M, Puglisi Ret al. Identification of bovine sperm head for morphometry analysis in quantitative phase-contrast holographic microscopy.Opt Express2011;19: 23215–23226..

Merola F, Miccio L, Memmolo P, Di Caprio G, Galli Aet al. Digital holography as a method for 3D imaging and estimating the biovolume of motile cells.Lab Chip2013;13: 4512–4516..

Di Caprio G, El Mallahi A, Ferraro P, Dale R, Coppola Get al. 4D tracking of clinical seminal samples for quantitative characterization of motility parameters.Biomed Opt Express2014;5: 690–700..

Jikeli JF, Alvarez L, Friedrich BM, Wilson LG, Pascal Ret al. Sperm navigation along helicalpaths in 3D chemoattractant landscapes.Nat Commun2015;6: 7985..

Wilson LG, Carter LM, Reece SE. High-speed holographic microscopy of malaria parasites reveals ambidextrous flagellar waveforms.Proc Natl Acad Sci USA2013;110: 18769–18774..

Su TW, Erlinger A, Tseng D, Ozcan A. Compact and light-weight automated semen analysis platform using lensfree on-chip microscopy.Anal Chem2010;82: 8307–8312..

Su TW, Choi I, Feng JW, Huang K, McLeod Eet al. Sperm trajectories form chiral ribbons.Sci Rep2013;3: 1664..

Su TW, Choi I, Feng JW, Huang K, Ozcan A. High-throughput analysis of horse sperms' 3D swimming patterns using computational on-chip imaging.Anim Reprod Sci2016;169: 45–55..

Yu X, Hong J, Liu CG, Kim MK. Review of digital holographic microscopy for three-dimensional profiling and tracking.Opt Eng2014;53: 112306..

Memmolo P, Miccio L, Paturzo M, Di Caprio G, Coppola Get al. Recent advances in holographic 3D particle tracking.Adv Opt Photon2015;7: 713–755..

Greenbaum A, Luo W, Su TW, Göröcs Z, Xue Let al. Imaging without lenses: achievements and remaining challenges of wide-field on-chip microscopy.Nat Methods2012;9: 889–895..

Greenbaum A, Luo W, Khademhosseinieh B, Su TW, Coskun AFet al. Increased space-bandwidth product in pixel super-resolved lensfree on-chip microscopy.Sci Rep2013;3: 1717..

Gurtner M, Zemánek J. Twin-beam real-time position estimation of micro-objects in 3D.Meas Sci Technol2016;27: 127003..

Memmolo P, Finizio A, Paturzo M, Miccio L, Ferraro P. Twin-beams digital holography for 3D tracking and quantitative phase-contrast microscopy in microfluidics.Opt Express2011;19: 25833–25842..

Merola F, Miccio L, Paturzo M, Finizio A, Grilli Set al. Driving and analysis of micro-objects by digital holographic microscope in microfluidics.Opt Lett2011;36: 3079–3081..

Goodman JW.Introduction to Fourier Optics. New York: Roberts&Company Publishers; 2005.

Mudanyali O, Tseng D, Oh C, Isikman SO, Sencan Iet al. Compact, light-weight and cost-effective microscope based on lensless incoherent holography for telemedicine applications.Lab Chip2010;10: 1417–1428..

Wei QS, Luo W, Chiang S, Kappel T, Mejia Cet al. Imaging and sizing of single DNA molecules on a mobile phone.ACS Nano2014;8: 12725–12733..

Penfold LM, Holt C, Holt WV, Welch GR, Cran DGet al. Comparative motility of X and Y chromosome-bearing bovine sperm separated on the basis of DNA content by flow sorting.Mol Reprod Dev1998;50: 323–327..

Leung C, Lu Z, Esfandiari N, Casper RF, Sun Y. Detection and tracking of low contrast human sperm tail. In:Proceedings of the 2010 IEEE Conference on Automation Science and Engineering (CASE); 21–24 August 2010; Toronto, ON, USA. IEEE: Toronto, ON, USA, 2010, pp 263–268.

Yang HF, Descombes X, Prigent S, Malandain G, Druart Xet al. Head tracking and flagellum tracing for sperm motility analysis. InProceedings of the 11th International Symposium on Biomedical Imaging (ISBI); 29 April–2 May 2014; Beijing, China. IEEE: Beijing, China, 2014, pp 310–313..

Babcock DF, Wandernoth PM, Wennemuth G. Episodic rolling and transient attachments create diversity in sperm swimming behavior.BMC Biol2014;12: 67..

Afzelius B. Electron microscopy of the sperm tail results obtained with a new fixative.J Cell Biol1959;5: 269–278..

Gibbons IR. Structural asymmetry in cilia and flagella.Nature1961;190: 1128–1129..

Woolley DM Interpretations of the pattern of sperm tail movements. In: Fawcett DW, Bedford JM (eds).The Spermatozoon. Urban&Schwarzenburg: Baltimore-Munich. 1979, pp 69–79.

Nosrati R, Driouchi A, Yip CM, Sinton D. Two-dimensional slither swimming of sperm within a micrometre of a surface.Nat Commun2015;6: 8703..

浏览量

Downloads

CSCD

文章被引用时，请邮件提醒。

Submit

工具集

关联资源

Phase recovery and holographic image reconstruction using deep learning in neural networks