Noninvasive two-photon microscopy imaging of mouse retina and retinal pigment epithelium through the pupil of the eye

Nature Medicine

Volumn 20, Issue 7, 2014, Pages 785-789

  Palczewska, Grazyna ^a   Dong, Zhiqian ^a   Golczak, Marcin ^b   Hunter, Jennifer J ^b,d,e   Williams, David R ^c,f   Alexander, Nathan S ^b   Palczewski, Krzysztof ^a,b  

^a Polgenix Inc   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ROCHESTER   (United States)

^d UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^e University of Rochester   (United States)

^f UNIVERSITY OF ROCHESTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGORITHM; ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; IMAGE ANALYSIS; IMAGING SYSTEM; INFORMATION PROCESSING; LIGHT EXPOSURE; MOUSE; NON INVASIVE PROCEDURE; NONHUMAN; OPTICS; PHOTORECEPTOR; PIGMENT EPITHELIUM; PRIORITY JOURNAL; PUPIL; RETINA GANGLION CELL; RETINA IMAGE; RETINA INJURY; TWO PHOTON EXCITATION MICROSCOPY;

MUS;

ANIMALS; MACULAR DEGENERATION; MICE; MICROSCOPY; PUPIL; RETINA; RETINAL PIGMENT EPITHELIUM;

EID: 84904036414     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3590     Document Type: Article

References (47)

1. Helmchen, F. & Denk, W. Deep tissue two-photon microscopy. Nat. Methods 2, 932-940 (2005).
2. Boettner, E.A. & Wolter, J.R. Transmission of the ocular media. Invest. Ophthalmol. Vis. Sci. 1, 776-783 (1962).
3. Imanishi, Y., Batten, M.L., Piston, D.W., Baehr, W. & Palczewski, K. Noninvasive two-photon imaging reveals retinyl ester storage structures in the eye. J. Cell Biol. 164, 373-383 (2004).
4. Imanishi, Y., Gerke, V. & Palczewski, K. Retinosomes: new insights into intracellular managing of hydrophobic substances in lipid bodies. J. Cell Biol. 166, 447-453 (2004).
5. Palczewska, G. et al. Noninvasive multiphoton fluorescence microscopy resolves retinol and retinal condensation products in mouse eyes. Nat. Med. 16, 1444-1449 (2010).
6. Denk, W., Strickler, J.H. & Webb, W.W. Two-photon laser scanning fluorescence microscopy. Science 248, 73-76 (1990).
7. Hunter, J.J. et al. Images of photoreceptors in living primate eyes using adaptive optics two-photon ophthalmoscopy. Biomed. Opt. Express 2, 139-148 (2010).
8. Godara, P., Dubis, A.M., Roorda, A., Duncan, J.L. & Carroll, J. Adaptive optics retinal imaging: emerging clinical applications. Optom. Vis. Sci. 87, 930-941 (2010).
9. Liang, J., Williams, D.R. & Miller, D.T. Supernormal vision and high-resolution retinal imaging through adaptive optics. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 14, 2884-2892 (1997).
10. Sharma, R. et al. In vivo two-photon imaging of the mouse retina. Biomed. Opt. Express 4, 1285-1293 (2013).
11. Rueckel, M., Mack-Bucher, J.A. & Denk, W. Adaptive wavefront correction in two-photon microscopy using coherence-gated wavefront sensing. Proc. Natl. Acad. Sci. USA 103, 17137-17142 (2006).
12. Huang, S., Heikal, A.A. & Webb, W.W. Two-photon fluorescence spectroscopy and microscopy of NAD(P)H and flavoprotein. Biophys. J. 82, 2811-2825 (2002).
13. Padayatti, P., Palczewska, G., Sun, W., Palczewski, K. & Salom, D. Imaging of protein crystals with two-photon microscopy. Biochemistry 51, 1625-1637 (2012).
14. Kiser, P.D., Golczak, M., Maeda, A. & Palczewski, K. Key enzymes of the retinoid (visual) cycle in vertebrate retina. Biochim. Biophys. Acta 1821, 137-151 (2012).
15. Palczewski, K. Chemistry and biology of vision. J. Biol. Chem. 287, 1612-1619 (2012).
16. von Lintig, J., Kiser, P.D., Golczak, M. & Palczewski, K. The biochemical and structural basis for trans-to-cis isomerization of retinoids in the chemistry of vision. Trends Biochem. Sci. 35, 400-410 (2010).
17. Sparrow, J.R., Wu, Y., Kim, C.Y. & Zhou, J. Phospholipid meets all-trans-retinal: the making of RPE bisretinoids. J. Lipid Res. 51, 247-261 (2010).
18. Maeda, A. et al. Primary amines protect against retinal degeneration in mouse models of retinopathies. Nat. Chem. Biol. 8, 170-178 (2011).
19. Maeda, T. et al. QLT091001, a 9-cis-retinal analog, is well-tolerated by retinas of mice with impaired visual cycles. Invest. Ophthalmol. Vis. Sci. 54, 455-466 (2013).
20. Golczak, M., Kuksa, V., Maeda, T., Moise, A.R. & Palczewski, K. Positively charged retinoids are potent and selective inhibitors of the trans-cis isomerization in the retinoid (visual) cycle. Proc. Natl. Acad. Sci. USA 102, 8162-8167 (2005).
21. Lin, B., Wang, S.W. & Masland, R.H. Retinal ganglion cell type, size, and spacing can be specified independent of homotypic dendritic contacts. Neuron 43, 475-485 (2004).
22. Euler, T. et al. Eyecup scope - optical recordings of light stimulus-evoked fluorescence signals in the retina. Pflugers Arch. 457, 1393-1414 (2009).
23. Bueno, J.M., Gualda, E.J. & Artal, P. Adaptive optics multiphoton microscopy to study ex vivo ocular tissues. J. Biomed. Opt. 15, 066004 (2010).
24. Helmstaedter, M. et al. Connectomic reconstruction of the inner plexiform layer in the mouse retina. Nature 500, 168-174 (2013).
25. Sun, W., Li, N. & He, S. Large-scale morphological survey of mouse retinal ganglion cells. J. Comp. Neurol. 451, 115-126 (2002).
26. Zipfel, W.R., Williams, R.M. & Webb, W.W. Nonlinear magic: multiphoton microscopy in the biosciences. Nat. Biotechnol. 21, 1369-1377 (2003).
27. Chan, F., Bradley, A., Wensel, T.G. & Wilson, J.H. Knock-in human rhodopsin-GFP fusions as mouse models for human disease and targets for gene therapy. Proc. Natl. Acad. Sci. USA 101, 9109-9114 (2004).
28. Spiess, E. et al. Two-photon excitation and emission spectra of the green fluorescent protein variants ECFP, EGFP and EYFP. J. Microsc. 217, 200-204 (2005).
29. Schmucker, C. & Schaeffel, F. A paraxial schematic eye model for the growing C57BL/6 mouse. Vision Res. 44, 1857-1867 (2004).
30. Katz, M.L. & Redmond, T.M. Effect of Rpe65 knockout on accumulation of lipofuscin fluorophores in the retinal pigment epithelium. Invest. Ophthalmol. Vis. Sci. 42, 3023-3030 (2001).
31. Drabent, R., Bryl, K., Smyk, B. & Ulbrych, K. Retinyl palmitate in water environment. J. Photochem. Photobiol. B 37, 254-260 (1997).
32. Chen, C. et al. Reduction of all-trans retinal to all-trans retinol in the outer segments of frog and mouse rod photoreceptors. Biophys. J. 88, 2278-2287 (2005).
33. Moroni, L., Gellini, C., Salvi, P.R. & Schettino, V. Fluorescence of all-trans-retinal as a crystal and in a dense solution phase. J. Phys. Chem. A 104, 11063-11069 (2000).
34. Keilhauer, C.N. & Delori, F.C. Near-infrared autofluorescence imaging of the fundus: visualization of ocular melanin. Invest. Ophthalmol. Vis. Sci. 47, 3556-3564 (2006).
35. London, A., Benhar, I. & Schwartz, M. The retina as a window to the brain-from eye research to CNS disorders. Nat. Rev. Neurol. 9, 44-53 (2013).
36. Kocaoglu, O.P. et al. Imaging cone photoreceptors in three dimensions and in time using ultrahigh resolution optical coherence tomography with adaptive optics. Biomed. Opt. Express 2, 748-763 (2011).
37. Carroll, J. et al. The effect of cone opsin mutations on retinal structure and the integrity of the photoreceptor mosaic. Invest. Ophthalmol. Vis. Sci. 53, 8006-8015 (2012).
38. Delori, F.C., Webb, R.H., Sliney, D.H. & American National Standards, I. Maximum permissible exposures for ocular safety (ANSI 2000), with emphasis on ophthalmic devices. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 24, 1250-1265 (2007).
39. Geng, Y. et al. Adaptive optics retinal imaging in the living mouse eye. Biomed. Opt. Express 3, 715-734 (2012).
40. Xi, P., Andegeko, Y., Pestov, D., Lovozoy, V.V. & Dantus, M. Two-photon imaging using adaptive phase compensated ultrashort laser pulses. J. Biomed. Opt. 14, 014002 (2009).
41. Golczak, M. et al. Lecithin:retinol acyltransferase is responsible for amidation of retinylamine, a potent inhibitor of the retinoid cycle. J. Biol. Chem. 280, 42263-42273 (2005).
42. Maeda, A. et al. Effects of potent inhibitors of the retinoid cycle on visual function and photoreceptor protection from light damage in mice. Mol. Pharmacol. 70, 1220-1229 (2006).
43. Zhang, Y., Poonja, S. & Roorda, A. MEMS-based adaptive optics scanning laser ophthalmoscopy. Opt. Lett. 31, 1268-1270 (2006).
44. Remtulla, S. & Hallett, P.E. A schematic eye for the mouse, and comparisons with the rat. Vision Res. 25, 21-31 (1985).
45. Thibos, L.N. et al. Standards for reporting the optical aberrations of eyes. J. Refract. Surg. 18, S652-S660 (2002).
46. Sun, Y., Duthaler, S. & Nelson, B.J. Autofocusing in computer microscopy: selecting the optimal focus algorithm. Microsc. Res. Tech. 65, 139-149 (2004).
47. Vorontsov, M.A. & Sivokon, V.P. Stochastic parallel-gradient-descent technique for high-resolution wave-front phase-distortion correction. J. Opt. Soc. Am. A Opt. Image Sci. Vis. 15, 2745-2758 (1998).