RESEARCH PROGRESS OF IN VIVO TWO-PHOTON IMAGING IN SPINAL CORD_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

ZHANGYiling ¹ , LIUXingyu ^2△ , JIXinran ¹ , ZHANGLihai ¹ ,  TANGPeifu ¹

1. Department of Orthopedics, General Hospital of Chinese PLA, Beijing, 100853, P.R.China;
2. Department of Hepatology and Gastroenterology, Beijing YouAn Hospital, Capital Medical University;

Corresponding author：

TANGPeifu, Email: pftang301@126.com

Keywords：

Two-photon microscopy; In vivo imaging; Spinal cord injury; Transgenic mouse

DOI：

10.7507/1002-1892.20160157

Video：

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Objective To review the in vivo imaging research progress of two-photon microscopy (TPM) in spinal cord. Methods The recent literature concerning in vivo two-photon imaging of axon, microglia, and calcium in transgenic mice spinal cord was extensively consulted and reviewed. Results In vivo two-photon imaging of spinal cord provide dynamic information about axonal degeneration and regeneration, microglial accumulation, and calcium influx after spinal cord injury. Conclusion TPM in vivo imaging study on spinal cord will provide theoretical foundation for pathophysiologic process of spinal cord injury.

Citation： ZHANGYiling, LIUXingyu, JIXinran, ZHANGLihai, TANGPeifu. RESEARCH PROGRESS OF IN VIVO TWO-PHOTON IMAGING IN SPINAL CORD. Chinese Journal of Reparative and Reconstructive Surgery, 2016, 30(6): 772-775. doi: 10.7507/1002-1892.20160157 Copy

1.	Sorbara CD, Wagmer NE, Ladwig A, et al. Pervasive axonal transport deficits in multiple sclerosis models. Neuron, 2014, 84(6): 1183-1190.
2.	Grutzendler J, Gan WB. Two-photon imaging of synaptic plasticity and pathology in the living mouse brain. NeuroRx, 2006, 3(4): 489-496.
3.	Brennan FH, Cowin GJ, Kurniawan ND, et al. Longitudinal assessment of white matter pathology in the injured mouse spinal cord through ultra-high field (16.4 T) in vivo diffusion tensor imaging. Neuroimage, 2013, 82: 574-585.
4.	Smith AK, Dortch RD, Dethrage LM, et al. Rapid, high-resolution quantitative magnetization transfer MRI of the human spinal cord. Neuroimage, 2014, 95: 106-116.
5.	Haynes SE, Hollopeter G, Yang G, et al. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci, 2006, 9(12): 1512-1519.
6.	Chen X, Leischner U, Rochefort NL, et al. Functional mapping of single spines in cortical neurons in vivo. Nature, 2011, 475(7357): 501-505.
7.	Parkhurst CN, Yang G, Ninan I, et al. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell, 2013, 155(7): 1596-1609.
8.	Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science, 1990, 248(4951): 73-76.
9.	Zhang P, Jiang XF, Nie X, et al. A two-photon fluorescent sensor revealing drug-induced liver injury via tracking gamma-glutamyltranspeptidase (GGT) level in vivo. Biomaterials, 2016, 80: 46-56.
10.	Cooper SR, Emond MR, Duy PQ, et al. Protocadherins control the modular assembly of neuronal columns in the zebrafish optic tectum. J Cell Biol, 2015, 211(4): 807-814.
11.	Sinha S, Liang L, Ho ET, et al. High-speed laser microsurgery of alert fruit flies for fluorescence imaging of neural activity. Proc Natl Acad Sci U S A, 2013, 110(46): 18374-18379.
12.	Greenberg ML, Weinger JG, Matheu MP, et al. Two-photon imaging of remyelination of spinal cord axons by engrafted neural precursor cells in a viral model of multiple sclerosis. Proc Natl Acad Sci U S A, 2014, 111(22): E2349-2355.
13.	Rosenegger DG, Tran CH, Wamsteeker Cusulin JI, et al. Tonic local brain blood flow control by astrocytes independent of phasic neurovascular coupling. J Neurosci, 2015, 35(39): 13463-13474.
14.	Grutzendler J, Kasthuri N, Gan WB. Long-term dendritic spine stability in the adult cortex. Nature, 2002, 420(6917): 812-816.
15.	Yang G, Pan F, Parkhurst CN, et al. Thinned-skull cranial window technique for long-term imaging of the cortex in live mice. Nat Protoc, 2010, 5(2): 201-208.
16.	Kerschensteiner M, Schwab ME, Lichtman JW, et al. In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat Med, 2005, 11(5): 572-577.
17.	Misgeld T, Nikic I, Kerschensteiner M. In vivo imaging of single axons in the mouse spinal cord. Nat Protoc, 2007, 2(2): 263-268.
18.	Davalos D, Lee JK, Smith WB, et al. Stable in vivo imaging of densely populated glia, axons and blood vessels in the mouse spinal cord using two-photon microscopy. J Neurosci Methods, 2008, 169(1): 1-7.
19.	Davalos D, Akassoglou K. In vivo imaging of the mouse spinal cord using two-photon microscopy. J Vis Exp, 2012, 5(59): e2760.
20.	Farrar MJ, Bernstein IM, Schlafer DH, et al. Chronic in vivo imaging in the mouse spinal cord using an implanted chamber. Nat Methods, 2012, 9(3): 297-302.
21.	Fenrich KK, Weber P, Hocine M, et al. Long-term in vivo imaging of normal and pathological mouse spinal cord with subcellular resolution using implanted glass windows. J Physiol, 2012, 590(16): 3665-3675.
22.	Figley SA, Chen Y, Maeda A, et al. A spinal cord window chamber model for in vivo longitudinal multimodal optical and acoustic imaging in a murine model. PLoS One, 2013, 8(3): e58081.
23.	Geoffroy CG, Lorenzana AO, Kwan JP, et al. Effects of PTEN and Nogo codeletion on corticospinal axon sprouting and regeneration in mice. J Neurosci, 2015, 35(16): 6413-6428.
24.	Du K, Zheng S, Zhang Q, et al. Pten deletion promotes regrowth of corticospinal tract axons 1 year after spinal cord injury. J Neurosci, 2015, 35(26): 9754-9763.
25.	Zukor K, Belin S, Wang C, et al. Short hairpin RNA against PTEN enhances regenerative growth of corticospinal tract axons after spinal cord injury. J Neurosci, 2013, 33(39): 15350-15361.
26.	Feng G, Mellor RH, Bernstein M, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron, 2000, 28(1): 41-51.
27.	Di Maio A, Skuba A, Himes BT, et al. In vivo imaging of dorsal root regeneration: rapid immobilization and presynaptic differentiation at the CNS/PNS border. J Nurosci, 2011, 31(12): 4569-4582.
28.	Skuba A, Manire MA, Kim H, et al. Time-lapse in vivo imaging of dorsal root nerve regeneration in mice. Methods Mol Biol, 2014, 1162: 219-232.
29.	Zhang Y, Zhang L, Shen J, et al. Two-photon excited fluorescence microscopy as a tool to investigate the efficacy of methylprednisolone in a mouse spinal cord injury model. Spine (Phila Pa 1976), 2014, 39(8): E493-499.
30.	Zhang Y, Zhang L, Ji X, et al. Two-photon microscopy as a tool to investigate the therapeutic time window of methylprednisolone in a mouse spinal cord injury model. Restor Neurol Neurosci, 2015, 33(3): 291-300.
31.	Ellwardt E, Zipp F. Molecular mechanisms linking neuroinflammation and neurodegeneration in MS. Exp Neurol, 2014, 262 Pt A: 8-17.
32.	Micu I, Ridsdale A, Zhang L, et al. Real-time measurement of free Ca2+ changes in CNS myelin by two-photon microscopy. Nat Med, 2007, 13(7): 874-879.
33.	Condie AG, Gerson SL, Miller RH, et al. Two-photon fluorescent imaging of myelination in the spinal cord. Chem Med Chem, 2012, 7(12): 2194-2203.
34.	Wang X, Cao K, Sun X, et al. Macrophages in spinal cord injury: phenotypic and functional change from exposure to myelin debris. Glia, 2015, 63(4): 635-651.
35.	Stirling DP, Cummins K, Mishra M, et al. Toll-like receptor 2-mediated alternative activation of microglia is protective after spinal cord injury. Brain, 2014, 137(Pt 3): 707-723.
36.	Davalos D, Grutzendler J, Yang G, et al. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci, 2005, 8(6): 752-758.
37.	Dibaj P, Nadrigny F, Steffens H, et al. NO mediates microglial response to acute spinal cord injury under ATP control in vivo. Glia, 2010, 58(9): 1133-1144.
38.	Li T, Pang S, Yu Y, et al. Proliferation of parenchymal microglia is the main source of microgliosis after ischaemic stroke. Brain, 2013, 136(Pt 12): 3578-3588.
39.	Evans TA, Barkauskas DS, Myers JT, et al. Intravital imaging of axonal interactions with microglia and macrophages in a mouse dorsal column crush injury. J Vis Exp, 2014, (93): e52228.
40.	Evans TA, Barkauskas DS, Myers JT, et al. High-resolution intravital imaging reveals that blood-derived macrophages but not resident microglia facilitate secondary axonal dieback in traumatic spinal cord injury. Exp Neurol, 2014, 254: 109-120.
41.	Díaz-Ríos M, Dombeck DA, Webb WW, et al. Serotonin modulates dendritic calcium influx in commissural interneurons in the mouse spinal locomotor network. J Neurophysiol, 2007, 98(4): 2157-2167.
42.	Li X, Yu K, Zhang Z, et al. Cholecystokinin from the entorhinal cortex enables neural plasticity in the auditory cortex. Cell Res, 2014, 24(3): 307-330.
43.	Chen Q, Cichon J, Wang W, et al. Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron, 2012, 76(2): 297-308.
44.	Yang G, Lai CS, Cichon J, et al. Sleep promotes branch-specific formation of dendritic spines after learning. Science, 2014, 344(6188): 1173-1178.
45.	Cichon J, Gan WB. Branch-specific dendritic Ca(2+) spikes cause persistent synaptic plasticity. Nature, 2015, 520(7546): 180-185.
46.	Yang G, Pan F, Chang PC, et al. Transcranial two-photon imaging of synaptic structures in the cortex of awake head-restrained mice. Methods Mol Biol, 2013, 1010: 35-43.
47.	Johannssen HC, Helmchen F. In vivo Ca2+ imaging of dorsal horn neuronal populations in mouse spinal cord. J Physiol, 2010, 588(Pt 18): 3397-3402.
48.	Johannssen HC, Helmchen F. Two-photon imaging of spinal cord cellular networks. Exp Neurol, 2013, 242: 18-26.
49.	Nishida K, Matsumura S, Taniguchi W, et al. Three-dimensional distribution of sensory stimulation-evoked neuronal activity of spinal dorsal horn neurons analyzed by in vivo calcium imaging. PLoS One, 2014, 9(8): e103321.
50.	Chen TW, Wardill TJ, Sun Y, et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature, 2013, 499(7458): 295-300.

1. Sorbara CD, Wagmer NE, Ladwig A, et al. Pervasive axonal transport deficits in multiple sclerosis models. Neuron, 2014, 84(6): 1183-1190.
2. Grutzendler J, Gan WB. Two-photon imaging of synaptic plasticity and pathology in the living mouse brain. NeuroRx, 2006, 3(4): 489-496.
3. Brennan FH, Cowin GJ, Kurniawan ND, et al. Longitudinal assessment of white matter pathology in the injured mouse spinal cord through ultra-high field (16.4 T) in vivo diffusion tensor imaging. Neuroimage, 2013, 82: 574-585.
4. Smith AK, Dortch RD, Dethrage LM, et al. Rapid, high-resolution quantitative magnetization transfer MRI of the human spinal cord. Neuroimage, 2014, 95: 106-116.
5. Haynes SE, Hollopeter G, Yang G, et al. The P2Y12 receptor regulates microglial activation by extracellular nucleotides. Nat Neurosci, 2006, 9(12): 1512-1519.
6. Chen X, Leischner U, Rochefort NL, et al. Functional mapping of single spines in cortical neurons in vivo. Nature, 2011, 475(7357): 501-505.
7. Parkhurst CN, Yang G, Ninan I, et al. Microglia promote learning-dependent synapse formation through brain-derived neurotrophic factor. Cell, 2013, 155(7): 1596-1609.
8. Denk W, Strickler JH, Webb WW. Two-photon laser scanning fluorescence microscopy. Science, 1990, 248(4951): 73-76.
9. Zhang P, Jiang XF, Nie X, et al. A two-photon fluorescent sensor revealing drug-induced liver injury via tracking gamma-glutamyltranspeptidase (GGT) level in vivo. Biomaterials, 2016, 80: 46-56.
10. Cooper SR, Emond MR, Duy PQ, et al. Protocadherins control the modular assembly of neuronal columns in the zebrafish optic tectum. J Cell Biol, 2015, 211(4): 807-814.
11. Sinha S, Liang L, Ho ET, et al. High-speed laser microsurgery of alert fruit flies for fluorescence imaging of neural activity. Proc Natl Acad Sci U S A, 2013, 110(46): 18374-18379.
12. Greenberg ML, Weinger JG, Matheu MP, et al. Two-photon imaging of remyelination of spinal cord axons by engrafted neural precursor cells in a viral model of multiple sclerosis. Proc Natl Acad Sci U S A, 2014, 111(22): E2349-2355.
13. Rosenegger DG, Tran CH, Wamsteeker Cusulin JI, et al. Tonic local brain blood flow control by astrocytes independent of phasic neurovascular coupling. J Neurosci, 2015, 35(39): 13463-13474.
14. Grutzendler J, Kasthuri N, Gan WB. Long-term dendritic spine stability in the adult cortex. Nature, 2002, 420(6917): 812-816.
15. Yang G, Pan F, Parkhurst CN, et al. Thinned-skull cranial window technique for long-term imaging of the cortex in live mice. Nat Protoc, 2010, 5(2): 201-208.
16. Kerschensteiner M, Schwab ME, Lichtman JW, et al. In vivo imaging of axonal degeneration and regeneration in the injured spinal cord. Nat Med, 2005, 11(5): 572-577.
17. Misgeld T, Nikic I, Kerschensteiner M. In vivo imaging of single axons in the mouse spinal cord. Nat Protoc, 2007, 2(2): 263-268.
18. Davalos D, Lee JK, Smith WB, et al. Stable in vivo imaging of densely populated glia, axons and blood vessels in the mouse spinal cord using two-photon microscopy. J Neurosci Methods, 2008, 169(1): 1-7.
19. Davalos D, Akassoglou K. In vivo imaging of the mouse spinal cord using two-photon microscopy. J Vis Exp, 2012, 5(59): e2760.
20. Farrar MJ, Bernstein IM, Schlafer DH, et al. Chronic in vivo imaging in the mouse spinal cord using an implanted chamber. Nat Methods, 2012, 9(3): 297-302.
21. Fenrich KK, Weber P, Hocine M, et al. Long-term in vivo imaging of normal and pathological mouse spinal cord with subcellular resolution using implanted glass windows. J Physiol, 2012, 590(16): 3665-3675.
22. Figley SA, Chen Y, Maeda A, et al. A spinal cord window chamber model for in vivo longitudinal multimodal optical and acoustic imaging in a murine model. PLoS One, 2013, 8(3): e58081.
23. Geoffroy CG, Lorenzana AO, Kwan JP, et al. Effects of PTEN and Nogo codeletion on corticospinal axon sprouting and regeneration in mice. J Neurosci, 2015, 35(16): 6413-6428.
24. Du K, Zheng S, Zhang Q, et al. Pten deletion promotes regrowth of corticospinal tract axons 1 year after spinal cord injury. J Neurosci, 2015, 35(26): 9754-9763.
25. Zukor K, Belin S, Wang C, et al. Short hairpin RNA against PTEN enhances regenerative growth of corticospinal tract axons after spinal cord injury. J Neurosci, 2013, 33(39): 15350-15361.
26. Feng G, Mellor RH, Bernstein M, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron, 2000, 28(1): 41-51.
27. Di Maio A, Skuba A, Himes BT, et al. In vivo imaging of dorsal root regeneration: rapid immobilization and presynaptic differentiation at the CNS/PNS border. J Nurosci, 2011, 31(12): 4569-4582.
28. Skuba A, Manire MA, Kim H, et al. Time-lapse in vivo imaging of dorsal root nerve regeneration in mice. Methods Mol Biol, 2014, 1162: 219-232.
29. Zhang Y, Zhang L, Shen J, et al. Two-photon excited fluorescence microscopy as a tool to investigate the efficacy of methylprednisolone in a mouse spinal cord injury model. Spine (Phila Pa 1976), 2014, 39(8): E493-499.
30. Zhang Y, Zhang L, Ji X, et al. Two-photon microscopy as a tool to investigate the therapeutic time window of methylprednisolone in a mouse spinal cord injury model. Restor Neurol Neurosci, 2015, 33(3): 291-300.
31. Ellwardt E, Zipp F. Molecular mechanisms linking neuroinflammation and neurodegeneration in MS. Exp Neurol, 2014, 262 Pt A: 8-17.
32. Micu I, Ridsdale A, Zhang L, et al. Real-time measurement of free Ca2+ changes in CNS myelin by two-photon microscopy. Nat Med, 2007, 13(7): 874-879.
33. Condie AG, Gerson SL, Miller RH, et al. Two-photon fluorescent imaging of myelination in the spinal cord. Chem Med Chem, 2012, 7(12): 2194-2203.
34. Wang X, Cao K, Sun X, et al. Macrophages in spinal cord injury: phenotypic and functional change from exposure to myelin debris. Glia, 2015, 63(4): 635-651.
35. Stirling DP, Cummins K, Mishra M, et al. Toll-like receptor 2-mediated alternative activation of microglia is protective after spinal cord injury. Brain, 2014, 137(Pt 3): 707-723.
36. Davalos D, Grutzendler J, Yang G, et al. ATP mediates rapid microglial response to local brain injury in vivo. Nat Neurosci, 2005, 8(6): 752-758.
37. Dibaj P, Nadrigny F, Steffens H, et al. NO mediates microglial response to acute spinal cord injury under ATP control in vivo. Glia, 2010, 58(9): 1133-1144.
38. Li T, Pang S, Yu Y, et al. Proliferation of parenchymal microglia is the main source of microgliosis after ischaemic stroke. Brain, 2013, 136(Pt 12): 3578-3588.
39. Evans TA, Barkauskas DS, Myers JT, et al. Intravital imaging of axonal interactions with microglia and macrophages in a mouse dorsal column crush injury. J Vis Exp, 2014, (93): e52228.
40. Evans TA, Barkauskas DS, Myers JT, et al. High-resolution intravital imaging reveals that blood-derived macrophages but not resident microglia facilitate secondary axonal dieback in traumatic spinal cord injury. Exp Neurol, 2014, 254: 109-120.
41. Díaz-Ríos M, Dombeck DA, Webb WW, et al. Serotonin modulates dendritic calcium influx in commissural interneurons in the mouse spinal locomotor network. J Neurophysiol, 2007, 98(4): 2157-2167.
42. Li X, Yu K, Zhang Z, et al. Cholecystokinin from the entorhinal cortex enables neural plasticity in the auditory cortex. Cell Res, 2014, 24(3): 307-330.
43. Chen Q, Cichon J, Wang W, et al. Imaging neural activity using Thy1-GCaMP transgenic mice. Neuron, 2012, 76(2): 297-308.
44. Yang G, Lai CS, Cichon J, et al. Sleep promotes branch-specific formation of dendritic spines after learning. Science, 2014, 344(6188): 1173-1178.
45. Cichon J, Gan WB. Branch-specific dendritic Ca(2+) spikes cause persistent synaptic plasticity. Nature, 2015, 520(7546): 180-185.
46. Yang G, Pan F, Chang PC, et al. Transcranial two-photon imaging of synaptic structures in the cortex of awake head-restrained mice. Methods Mol Biol, 2013, 1010: 35-43.
47. Johannssen HC, Helmchen F. In vivo Ca2+ imaging of dorsal horn neuronal populations in mouse spinal cord. J Physiol, 2010, 588(Pt 18): 3397-3402.
48. Johannssen HC, Helmchen F. Two-photon imaging of spinal cord cellular networks. Exp Neurol, 2013, 242: 18-26.
49. Nishida K, Matsumura S, Taniguchi W, et al. Three-dimensional distribution of sensory stimulation-evoked neuronal activity of spinal dorsal horn neurons analyzed by in vivo calcium imaging. PLoS One, 2014, 9(8): e103321.
50. Chen TW, Wardill TJ, Sun Y, et al. Ultrasensitive fluorescent proteins for imaging neuronal activity. Nature, 2013, 499(7458): 295-300.

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