Multimodal coherent anti-Stokes Raman scattering microscopy reveals microglia-associated myelin and axonal dysfunction in multiple sclerosis-like lesions in mice

Journal of Biomedical Optics

Volumn 16, Issue 2, 2011, Pages

  Imitola, Jaime ^a,b   Côté, Daniel ^b,c,d,e   Rasmussen, Stine ^a,b   Sunney Xie, X ^b,c   Liu, Yingru ^a,b   Chitnis, Tanuja ^a,b   Sidman, Richard L ^b   Lin, Charles P ^b,c   Khoury, Samia J ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d CENTRE DE RECHERCHE DE L INSTITUT UNIVERSITAIRE EN SANTÉ MENTALE DE QUÉBEC   (Canada)

^e CENTRE D OPTIQUE   (Canada)

Author keywords

Coherent anti Stokes Raman scattering; Confocal; CX 3CR1 green fluorescence protein; Live imaging; Microglia; Neurodegeneration; Reflectance

Indexed keywords

COHERENT ANTI-STOKES RAMAN SCATTERING; CONFOCAL; GREEN FLUORESCENCE PROTEINS; LIVE IMAGING; MICROGLIA; NEURODEGENERATION;

COHERENT SCATTERING; FLUORESCENCE; MAMMALS; RADIOLOGY; RAMAN SPECTROSCOPY; REFLECTION; SIGNAL TO NOISE RATIO; TISSUE;

RAMAN SCATTERING;

ANIMALIA; MUS;

ANIMAL; ARTICLE; METHODOLOGY; MICROSCOPY; MOUSE; MULTIPLE SCLEROSIS; MYELINATED NERVE; NERVE FIBER; PATHOLOGY; RAMAN SPECTROMETRY;

ANIMALS; AXONS; MICE; MICROSCOPY; MULTIPLE SCLEROSIS; NERVE FIBERS, MYELINATED; SPECTRUM ANALYSIS, RAMAN;

EID: 79957811598     PISSN: 10833668     EISSN: 15602281     Source Type: Journal    
DOI: 10.1117/1.3533312     Document Type: Article

References (31)

1. H. S. David M, and B. Altevogt, Neuroscience Biomarkers and BIosignatures: Covering Technologies, Emerging Partnerships-Workshop Summary, National Academies Press, Washington, D.C. (2008).
2. D. Davalos, J. Grutzendler, G. Yang, J. V. Kim, Y. Zuo, S. Jung, D. R. Littman, M. L. Dustin, and W. B. Gan, "ATP mediates rapid microglial response to local brain injury in vivo," Nat. Neurosci. 8(6), 752-758 (2005).
3. A. Nimmerjahn, F. Kirchhoff, and F. Helmchen, "Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo," Science 308(5726), 1314-1318 (2005).
4. M. Nuriya, J. Jiang, B. Nemet, K. B. Eisenthal, and R. Yuste, "Imaging membrane potential in dendritic spines," Proc. Natl. Acad. Sci. USA 103(3), 786-790 (2006).
5. R. D. Roorda, T. M. Hohl, R. Toledo-Crow, and G. Miesenbock, "Video-rate nonlinear microscopy of neuronal membrane dynamics with genetically encoded probes," J. Neurophysiol. 92(1), 609-621 (2004).
6. H. Wang, Y. Fu, P. Zickmund, R. Shi, and J. X. Cheng, "Coherent anti-stokes Raman scattering imaging of axonal myelin in live spinal tissues," Biophys. J. 89(1), 581-591 (2005).
7. Y. Fu, H. Wang, T. B. Huff, R. Shi, and J. X. Cheng, "Coherent anti-Stokes Raman scattering imaging of myelin degradation reveals a calcium-dependent pathway in lyso-PtdCho-induced demyelination," J. Neurosci. Res. 85(13), 2870-2881 (2007).
8. X. R. Huang, R. W. Knighton, and L. N. Cavuoto, "Microtubule contribution to the reflectance of the retinal nerve fiber layer," Invest. Ophthalmol. Vis. Sci. 47(12), 5363-5367 (2006).
9. R. W. Knighton, X. Huang, and Q. Zhou, "Microtubule contribution to the reflectance of the retinal nerve fiber layer," Invest. Ophthalmol. Vis. Sci. 39(1), 189-193 (1998).
10. M. A. Middelkamp-Hup, H. Y. Park, J. Lee, B. A. Gilchrest, and S. Gonzalez, "Detection of UV-induced pigmentary and epidermal changes over time using in vivo reflectance confocal microscopy," J. Invest. Dermatol. 126(2), 402-407 (2006).
11. J. Imitola, T. Chitnis, and S. J. Khoury, "Insights into the molecular pathogenesis of progression in multiple sclerosis: potential implications for future therapies," Arch. Neurol. 63(1), 25-33 (2006).
12. B. Zhu, I. Guleria, A. Khosroshahi, T. Chitnis, J. Imitola, M. Azuma, H. Yagita, M. H. Sayegh, and S. J. Khoury, "Differential role of programmed death-ligand 1 [corrected] and programmed death-ligand 2 [corrected] in regulating the susceptibility and chronic progression of experimental autoimmune encephalomyelitis," J. Immunol. 176(6), 3480-3489 (2006).
13. S. Rasmussen, Y. Wang, P. Kivisakk, R. T. Bronson, M. Meyer, J. Imitola, and S. J. Khoury, "Persistent activation of microglia is associated with neuronal dysfunction of callosal projecting pathways and multiple sclerosis-like lesions in relapsing - remitting experimental autoimmune encephalomyelitis, " Brain 130(Pt 11), 2816-2829 (2007).
14. S. J. Veilleux I, D. Biss, D. Cote, and C. P. Lin, "In vivo cell tracking with multimodal video rate microscopy," Biophotonics 14(1), 10-18 (2008).
15. C. L. Evans, E. O. Potma, M. Puoris'haag, D. Cote, C. P. Lin, and X. S. Xie, "Chemical imaging of tissue in vivo with video-rate coherent anti-Stokes Raman scattering microscopy," Proc. Natl. Acad. Sci. USA 102(46), 16807-16812 (2005).
16. B. Kornek, M. K. Storch, J. Bauer, A. Djamshidian, R. Weissert, E. Wallstroem, A. Stefferl, F. Zimprich, T. Olsson, C. Linington, M. Schmidbauer, and H. Lassmann, "Distribution of a calcium channel subunit in dystrophic axons in multiple sclerosis and experimental autoimmune encephalomyelitis," Brain 124(Pt 6), 1114-1124 (2001).
17. R. J. Reynolds and J. W. Heath, "Patterns of morphological variation within myelin internodes of normal peripheral nerve: quantitative analysis by confocal microscopy," J. Anat. 187(Pt 2), 369-378 (1995).
18. A. Erturk, F. Hellal, J. Enes, and F. Bradke, "Disorganized microtubules underlie the formation of retraction bulbs and the failure of axonal regeneration," J. Neurosci. 27(34), 9169-9180 (2007).
19. B. Kornek, M. K. Storch, R. Weissert, E. Wallstroem, A. Stefferl, T. Olsson, C. Linington, M. Schmidbauer, and H. Lassmann, "Multiple sclerosis and chronic autoimmune encephalomyelitis: a comparative quantitative study of axonal injury in active, inactive, and remyelinated lesions," Am. J. Pathol. 157(1), 267-276 (2000).
20. S. Menon, H. Chi, H. Zhang, X. W. Deng, R. A. Flavell, and N. Wei, "COP9 signalosome subunit 8 is essential for peripheral T cell homeostasis and antigen receptor-induced entry into the cell cycle from quiescence," Nat. Immunol. 8(11), 1236-1245 (2007).
21. L. P. Shriver and B. N. Dittel, "T-cell-mediated disruption of the neuronal microtubule network: correlation with early reversible axonal dysfunction in acute experimental autoimmune encephalomyelitis," Am. J. Pathol. 169(3), 999-1011 (2006).
22. H. Takeuchi, T. Mizuno, G. Zhang, J. Wang, J. Kawanokuchi, R. Kuno, and A. Suzumura, "Neuritic beading induced by activated microglia is an early feature of neuronal dysfunction toward neuronal death by inhibition of mitochondrial respiration and axonal transport," J. Biol. Chem. 280(11), 10444-10454 (2005).
23. P. G. Bannerman, A. Hahn, S. Ramirez, M. Morley, C. Bonnemann, S. Yu, G. X. Zhang, A. Rostami, and D. Pleasure, "Motor neuron pathology in experimental autoimmune encephalomyelitis: studies in THY1-YFP transgenic mice," Brain 128(Pt 8), 1877-1886 (2005).
24. N. Kawakami, U. V. Nagerl, F. Odoardi, T. Bonhoeffer, H. Wekerle, and A. Flugel, "Live imaging of effector cell trafficking and autoantigen recognition within the unfolding autoimmune encephalomyelitis lesion," J. Exp. Med. 201(11), 1805-1814 (2005).
25. F. P. Henry, D. Cote, M. A. Randolph, E. A. Rust, R. W. Redmond, I. E. Kochevar, C. P. Lin, and J. M. Winograd, "Real-time in vivo assessment of the nerve microenvironment with coherent anti-Stokes Raman scattering microscopy," Plast. Reconstr. Surg. 123(2 Suppl), 123S-130S (2009).
26. A. Kutzelnigg, C. F. Lucchinetti, C. Stadelmann, W. Bruck, H. Rauschka, M. Bergmann, M. Schmidbauer, J. E. Parisi, and H. Lassmann, "Cortical demyelination and diffuse white matter injury in multiple sclerosis," Brain 128(Pt 11), 2705-2712 (2005).
27. A. D. Salama, T. Chitnis, J. Imitola, M. J. Ansari, H. Akiba, F. Tushima, M. Azuma, H. Yagita, M. H. Sayegh, and S. J. Khoury, "Critical role of the programmed death-1 (PD-1) pathway in regulation of experimental autoimmune encephalomyelitis," J. Exp. Med. 198(1), 71-78 (2003).
28. J. Imitola, K. Raddassi, K. I. Park, F. J. Mueller, M. Nieto, Y. D. Teng, D. Frenkel, J. Li, R. L. Sidman, C. A. Walsh, E. Y. Snyder, and S. J. Khoury, "Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway," Proc. Natl. Acad. Sci. USA 101(52), 18117-18122 (2004).
29. A. Monsonego, J. Imitola, S. Petrovic, V. Zota, A. Nemirovsky, R. Baron, Y. Fisher, T. Owens, and H. L. Weiner, "Abeta-induced meningoencephalitis is IFN-gamma-dependent and is associated with T cell-dependent clearance of Abeta in a mouse model of Alzheimer's disease," Proc. Natl. Acad. Sci. USA 103(13), 5048-5053 (2006).
30. S. Xiao, N. Najafian, J. Reddy, M. Albin, C. Zhu, E. Jensen, J. Imitola, T. Korn, A. C. Anderson, Z. Zhang, C. Gutierrez, T. Moll, R. A. Sobel, D. T. Umetsu, H. Yagita, H. Akiba, T. Strom, M. H. Sayegh, R. H. DeKruyff, S. J. Khoury, and V. K. Kuchroo, "Differential engagement of Tim-1 during activation can positively or negatively costimulate T cell expansion and effector function," J. Exp. Med. 204(7), 1691-1702 (2007).
31. C. Zhu, A. C. Anderson, A. Schubart, H. Xiong, J. Imitola, S. J. Khoury, X. X. Zheng, T. B. Strom, and V. K. Kuchroo, "The Tim-3 ligand galectin-9 negatively regulates T helper type 1 immunity," Nat. Immunol. 6(12), 1245-1252 (2005).