Synchrotron Radiation-Based Three-Dimensional Visualization of Angioarchitectural Remodeling in Hippocampus of Epileptic Rats

  • Pan Gu
  • Zi-Hao Xu
  • Yu-Ze Cao
  • Sheng-Hui Liao
  • Qian-Fang Deng
  • Xian-Zhen Yin
  • Zhuo-Lu Wang
  • Zhuo-Hui Chen
  • Xin-Hang Hu
  • Hui Wang
  • Li-Zhi Li
  • Shi-Xin Liu
  • Hui Ding
  • Shu-Peng Shi
  • Hong-Lei Li
  • Ti-Qiao Xiao
  • Bo XiaoEmail author
  • Meng-Qi ZhangEmail author
Original Article


Characterizing the three-dimensional (3D) morphological alterations of microvessels under both normal and seizure conditions is crucial for a better understanding of epilepsy. However, conventional imaging techniques cannot detect microvessels on micron/sub-micron scales without angiography. In this study, synchrotron radiation (SR)-based X-ray in-line phase-contrast imaging (ILPCI) and quantitative 3D characterization were used to acquire high-resolution, high-contrast images of rat brain tissue under both normal and seizure conditions. The number of blood microvessels was markedly increased on days 1 and 14, but decreased on day 60 after seizures. The surface area, diameter distribution, mean tortuosity, and number of bifurcations and network segments also showed similar trends. These pathological changes were confirmed by histological tests. Thus, SR-based ILPCI provides systematic and detailed views of cerebrovascular anatomy at the micron level without using contrast-enhancing agents. This holds considerable promise for better diagnosis and understanding of the pathogenesis and development of epilepsy.


Epilepsy Synchrotron radiation 3D Angioarchitecture Blood vessel Remodeling 



This work was completed at the BL13W1 beamline of the Shanghai Synchrotron Radiation Facility (SSRF) in China and was supported by Key Research Project of the Ministry of Science and Technology of China (2016YFC0904400), the National Natural Science Foundation of China (81501025 & 81671299), the Natural Science Foundation of Hunan Province (2016JJ3174), and the Science and Technology Department Funds of Hunan Province Key Project (2016JC2057). We would like to thank Prof. Tiqiao Xiao and other staff at the BL13W1 station of SSRF for their kind assistance during the experiments.


  1. 1.
    Aronica E, Muhlebner A. Neuropathology of epilepsy. Handb Clin Neurol 2017, 145: 193–216.PubMedCrossRefPubMedCentralGoogle Scholar
  2. 2.
    Fisher RS, van Emde Boas W, Blume W, Elger C, Genton P, Lee P, et al. Epileptic seizures and epilepsy: definitions proposed by the International League Against Epilepsy (ILAE) and the International Bureau for Epilepsy (IBE). Epilepsia 2005, 46: 470–472.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Truccolo W, Donoghue JA, Hochberg LR, Eskandar EN, Madsen JR, Anderson WS, et al. Single-neuron dynamics in human focal epilepsy. Nat Neurosci 2011, 14: 635–641.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Schuele SU, Luders HO. Intractable epilepsy: management and therapeutic alternatives. Lancet Neurol 2008, 7: 514–524.PubMedCrossRefPubMedCentralGoogle Scholar
  5. 5.
    Semah F, Picot MC, Adam C, Broglin D, Arzimanoglou A, Bazin B, et al. Is the underlying cause of epilepsy a major prognostic factor for recurrence? Neurology 1998, 51: 1256–1262.PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Xu XX, Luo JH. Mutations of N-methyl-D-aspartate receptor subunits in epilepsy. Neurosci Bull 2018, 34: 549–565.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Wei F, Yan LM, Su T, He N, Lin ZJ, Wang J, et al. Ion channel genes and epilepsy: functional alteration, pathogenic potential, and mechanism of epilepsy. Neurosci Bull 2017, 33: 455–477.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    De Reuck J, Nagy E, Van Maele G. Seizures and epilepsy in patients with lacunar strokes. J Neurol Sci 2007, 263: 75–78.PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Maxwell H, Hanby M, Parkes LM, Gibson LM, Coutinho C, Emsley HC. Prevalence and subtypes of radiological cerebrovascular disease in late-onset isolated seizures and epilepsy. Clin Neurol Neurosurg 2013, 115: 591–596.PubMedCrossRefPubMedCentralGoogle Scholar
  10. 10.
    Naik P, Cucullo L. In vitro blood-brain barrier models: current and perspective technologies. J Pharm Sci 2012, 101: 1337–1354.PubMedCrossRefPubMedCentralGoogle Scholar
  11. 11.
    Camidge DR, Pao W, Sequist LV. Acquired resistance to TKIs in solid tumours: learning from lung cancer. Nat Rev Clin Oncol 2014, 11: 473–481.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Morin-Brureau M, De Bock F, Lerner-Natoli M. Organotypic brain slices: a model to study the neurovascular unit micro-environment in epilepsies. Fluids Barriers CNS 2013, 10: 11.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Fischer S, Wobben M, Marti HH, Renz D, Schaper W. Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1. Microvasc Res 2002, 63: 70–80.PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Rochfort KD, Cummins PM. Cytokine-mediated dysregulation of zonula occludens-1 properties in human brain microvascular endothelium. Microvasc Res 2015, 100: 48–53.PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Marchi N, Lerner-Natoli M. Cerebrovascular remodeling and epilepsy. Neuroscientist 2013, 19: 304–312.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Milesi S, Boussadia B, Plaud C, Catteau M, Rousset MC, De Bock F, et al. Redistribution of PDGFRbeta cells and NG2DsRed pericytes at the cerebrovasculature after status epilepticus. Neurobiol Dis 2014, 71: 151–158.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Klement W, Garbelli R, Zub E, Rossini L, Tassi L, Girard B, et al. Seizure progression and inflammatory mediators promote pericytosis and pericyte-microglia clustering at the cerebrovasculature. Neurobiol Dis 2018, 113: 70–81.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Gales JM, Prayson RA. Chronic inflammation in refractory hippocampal sclerosis-related temporal lobe epilepsy. Ann Diagn Pathol 2017, 30: 12–16.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Li Z, You Z, Li M, Pang L, Cheng J, Wang L. Protective effect of resveratrol on the brain in a rat model of epilepsy. Neurosci Bull 2017, 33: 273–280.PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Ndode-Ekane XE, Hayward N, Grohn O, Pitkanen A. Vascular changes in epilepsy: functional consequences and association with network plasticity in pilocarpine-induced experimental epilepsy. Neuroscience 2010, 166: 312–332.PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Nicoletti JN, Shah SK, McCloskey DP, Goodman JH, Elkady A, Atassi H, et al. Vascular endothelial growth factor is up-regulated after status epilepticus and protects against seizure-induced neuronal loss in hippocampus. Neuroscience 2008, 151: 232–241.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Xu Y, Zhang Y, Guo Z, Yin H, Zeng K, Wang L, et al. Increased placental growth factor in cerebrospinal fluid of patients with epilepsy. Neurochem Res 2012, 37: 665–670.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Rigau V, Morin M, Rousset MC, de Bock F, Lebrun A, Coubes P, et al. Angiogenesis is associated with blood-brain barrier permeability in temporal lobe epilepsy. Brain 2007, 130: 1942–1956.CrossRefGoogle Scholar
  24. 24.
    Benini R, Roth R, Khoja Z, Avoli M, Wintermark P. Does angiogenesis play a role in the establishment of mesial temporal lobe epilepsy? Int J Dev Neurosci 2016, 49: 31–36.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    van Vliet EA, Otte WM, Wadman WJ, Aronica E, Kooij G, de Vries HE, et al. Blood-brain barrier leakage after status epilepticus in rapamycin-treated rats II: Potential mechanisms. Epilepsia 2016, 57: 70–78.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Barnett A, Audrain S, McAndrews MP. Applications of resting-state functional MR imaging to epilepsy. Neuroimaging Clin N Am 2017, 27: 697–708.PubMedCrossRefPubMedCentralGoogle Scholar
  27. 27.
    Russo E, Leo A, Scicchitano F, Donato A, Ferlazzo E, Gasparini S, et al. Cerebral small vessel disease predisposes to temporal lobe epilepsy in spontaneously hypertensive rats. Brain Res Bull 2017, 130: 245–250.PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Zhao W, Zhang J, Song Y, Sun L, Zheng M, Yin H, et al. Irreversible fatal contrast-induced encephalopathy: a case report. BMC Neurol 2019, 19: 46.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Sengupta S, Fritz FJ, Harms RL, Hildebrand S, Tse DHY, Poser BA, et al. High resolution anatomical and quantitative MRI of the entire human occipital lobe ex vivo at 9.4T. Neuroimage 2018, 168: 162–171.Google Scholar
  30. 30.
    Federau C, Gallichan D. Motion-correction enabled ultra-high resolution in-vivo 7T-MRI of the brain. PLoS One 2016, 11: e0154974.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Jung SC, Kim HS, Choi CG, Kim SJ, Lee DH, Suh DC, et al. Quantitative analysis using high-resolution 3T MRI in acute intracranial artery dissection. J Neuroimaging 2016, 26: 612–617.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Li P, Yu X, Griffin J, Levine JM, Jim J. High-resolution MRI of spinal cords by compressive sensing parallel imaging. Conf Proc IEEE Eng Med Biol Soc 2015, 2015: 4266–4269.Google Scholar
  33. 33.
    Zhang M, Peng G, Sun D, Xie Y, Xia J, Long H, et al. Synchrotron radiation imaging is a powerful tool to image brain microvasculature. Med Phys 2014, 41: 031907.PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Schulz G, Weitkamp T, Zanette I, Pfeiffer F, Beckmann F, David C, et al. High-resolution tomographic imaging of a human cerebellum: comparison of absorption and grating-based phase contrast. J R Soc Interface 2010, 7: 1665–1676.PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Lewis R. Medical applications of synchrotron radiation X-rays. Phys Med Biol 1997, 42: 1213–1243.PubMedCrossRefPubMedCentralGoogle Scholar
  36. 36.
    Eggl E, Schleede S, Bech M, Achterhold K, Loewen R, Ruth RD, et al. X-ray phase-contrast tomography with a compact laser-driven synchrotron source. Proc Natl Acad Sci U S A 2015, 112: 5567–5572.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Hoshino M, Uesugi K, Tsukube T, Yagi N. Quantitative and dynamic measurements of biological fresh samples with X-ray phase contrast tomography. J Synchrotron Radiat 2014, 21: 1347–1357.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Zhou SA, Brahme A. Development of phase-contrast X-ray imaging techniques and potential medical applications. Phys Med 2008, 24: 129–148.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    Endrizzi M. X-ray phase-contrast imaging. Nucl Inst Methods Phys Res A 2018, 878: 88–98.CrossRefGoogle Scholar
  40. 40.
    Snigirev A, Snigireva I, Lyubomirskiy M, Kohn V, Yunkin V, Kuznetsov S. X-ray multilens interferometer based on Si refractive lenses. Opt Express 2014, 22: 25842–25852.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Chapman D, Thomlinson W, Johnston RE, Washburn D, Pisano E, Gmur N, et al. Diffraction enhanced x-ray imaging. Phys Med Biol 1997, 42: 2015–2025.PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Zhang X, Yang XR, Chen Y, Li HQ, Li RM, Yuan QX, et al. Visualising liver fibrosis by phase-contrast X-ray imaging in common bile duct ligated mice. Eur Radiol 2013, 23: 417–423.PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Sztrokay A, Herzen J, Auweter SD, Liebhardt S, Mayr D, Willner M, et al. Assessment of grating-based X-ray phase-contrast CT for differentiation of invasive ductal carcinoma and ductal carcinoma in situ in an experimental ex vivo set-up. Eur Radiol 2013, 23: 381–387.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Lundstrom U, Larsson DH, Burvall A, Scott L, Westermark UK, Wilhelm M, et al. X-ray phase-contrast CO(2) angiography for sub-10 mum vessel imaging. Phys Med Biol 2012, 57: 7431–7441.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Bravin A, Coan P, Suortti P. X-ray phase-contrast imaging: from pre-clinical applications towards clinics. Phys Med Biol 2013, 58: R1–35.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Mayo SC, Stevenson AW, Wilkins SW. In-line phase-contrast X-ray imaging and tomography for materials science. Materials (Basel) 2012, 5: 937–965.CrossRefGoogle Scholar
  47. 47.
    Debatin JF, Spritzer CE, Grist TM, Beam C, Svetkey LP, Newman GE, et al. Imaging of the renal arteries: value of MR angiography. AJR Am J Roentgenol 1991, 157: 981–990.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Cao Y, Liao S, Zeng H, Ni S, Tintani F, Hao Y, et al. 3D characterization of morphological changes in the intervertebral disc and endplate during aging: A propagation phase contrast synchrotron micro-tomography study. Sci Rep 2017, 7: 43094.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Zhang MQ, Zhou L, Deng QF, Xie YY, Xiao TQ, Cao YZ, et al. Ultra-high-resolution 3D digitalized imaging of the cerebral angioarchitecture in rats using synchrotron radiation. Sci Rep 2015, 5: 14982.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Zhang MQ, Sun DN, Xie YY, Peng GY, Xia J, Long HY, et al. Three-dimensional visualization of rat brain microvasculature following permanent focal ischaemia by synchrotron radiation. Br J Radiol 2014, 87: 20130670.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Li B, Zhang Y, Wu W, Du G, Cai L, Shi H, et al. Neovascularization of hepatocellular carcinoma in a nude mouse orthotopic liver cancer model: a morphological study using X-ray in-line phase-contrast imaging. BMC Cancer 2017, 17: 73.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Hu J, Li P, Yin X, Wu T, Cao Y, Yang Z, et al. Nondestructive imaging of the internal microstructure of vessels and nerve fibers in rat spinal cord using phase-contrast synchrotron radiation microtomography. J Synchrotron Radiat 2017, 24: 482–489.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Fratini M, Bukreeva I, Campi G, Brun F, Tromba G, Modregger P, et al. Simultaneous submicrometric 3D imaging of the micro-vascular network and the neuronal system in a mouse spinal cord. Sci Rep 2015, 5: 8514.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Studer F, Serduc R, Pouyatos B, Chabrol T, Brauer-Krisch E, Donzelli M, et al. Synchrotron X-ray microbeams: A promising tool for drug-resistant epilepsy treatment. Phys Med 2015, 31: 607–614.PubMedCrossRefPubMedCentralGoogle Scholar
  55. 55.
    Pouyatos B, Nemoz C, Chabrol T, Potez M, Brauer E, Renaud L, et al. Synchrotron X-ray microtransections: a non invasive approach for epileptic seizures arising from eloquent cortical areas. Sci Rep 2016, 6: 27250.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Pacile S, Baran P, Dullin C, Dimmock M, Lockie D, Missbach-Guntner J, et al. Advantages of breast cancer visualization and characterization using synchrotron radiation phase-contrast tomography. J Synchrotron Radiat 2018, 25(Pt 5): 1460–1466.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Tavakoli Taba S, Baran P, Lewis S, Heard R, Pacile S, Nesterets YI, et al. Toward improving breast cancer imaging: radiological assessment of propagation-based phase-contrast CT technology. Acad Radiol 2019, 26: e79–e89.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Honchar MP, Olney JW, Sherman WR. Systemic cholinergic agents induce seizures and brain damage in lithium-treated rats. Science 1983, 220: 323–325.PubMedCrossRefPubMedCentralGoogle Scholar
  59. 59.
    Eslami SM, Ghasemi M, Bahremand T, Momeny M, Gholami M, Sharifzadeh M, et al. Involvement of nitrergic system in anticonvulsant effect of zolpidem in lithium-pilocarpine induced status epilepticus: Evaluation of iNOS and COX-2 genes expression. Eur J Pharmacol 2017, 815: 454–461.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Racine RJ. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972, 32: 281–294.CrossRefGoogle Scholar
  61. 61.
    Wu T, Ido K, Osada Y, Kotani S, Tamaoka A, Hanada T. The neuroprotective effect of perampanel in lithium-pilocarpine rat seizure model. Epilepsy Res 2017, 137: 152–158.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Wu Q, Li Y, Shu Y, Feng L, Zhou L, Yue ZW, et al. NDEL1 was decreased in the CA3 region but increased in the hippocampal blood vessel network during the spontaneous seizure period after pilocarpine-induced status epilepticus. Neuroscience 2014, 268: 276–283.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Chen RC, Dreossi D, Mancini L, Menk R, Rigon L, Xiao TQ, et al. PITRE: software for phase-sensitive X-ray image processing and tomography reconstruction. J Synchrotron Radiat 2012, 19: 836–845.PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Luo Y, Yin X, Shi S, Ren X, Zhang H, Wang Z, et al. Non-destructive 3D microtomography of cerebral angioarchitecture changes following ischemic stroke in rats using synchrotron radiation. Front Neuroanat 2019, 13: 5.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Yang G, Kitslaar P, Frenay M, Broersen A, Boogers MJ, Bax JJ, et al. Automatic centerline extraction of coronary arteries in coronary computed tomographic angiography. Int J Cardiovasc Imaging 2012, 28: 921–933.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Chatzikonstantinou A. Epilepsy and the hippocampus. Front Neurol Neurosci 2014, 34: 121–142.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Romariz SA, Garcia Kde O, Paiva Dde S, Bittencourt S, Covolan L, Mello LE, et al. Participation of bone marrow-derived cells in hippocampal vascularization after status epilepticus. Seizure 2014, 23: 386–389.PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Yamamoto H, Iku S, Adachi Y, Imsumran A, Taniguchi H, Nosho K, et al. Association of trypsin expression with tumour progression and matrilysin expression in human colorectal cancer. J Pathol 2003, 199: 176–184.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Hu JZ, Wu TD, Zeng L, Liu HQ, He Y, Du GH, et al. Visualization of microvasculature by x-ray in-line phase contrast imaging in rat spinal cord. Phys Med Biol 2012, 57: N55–63.PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Figueiredo G, Brockmann C, Boll H, Heilmann M, Schambach SJ, Fiebig T, et al. Comparison of digital subtraction angiography, micro-computed tomography angiography and magnetic resonance angiography in the assessment of the cerebrovascular system in live mice. Clin Neuroradiol 2012, 22: 21–28.PubMedCrossRefPubMedCentralGoogle Scholar
  71. 71.
    Liu X, Zhao J, Sun J, Gu X, Xiao T, Liu P, et al. Lung cancer and angiogenesis imaging using synchrotron radiation. Phys Med Biol 2010, 55: 2399–2409.PubMedCrossRefPubMedCentralGoogle Scholar
  72. 72.
    Margaritondo G, Meuli R. Synchrotron radiation in radiology: novel X-ray sources. Eur Radiol 2003, 13: 2633–2641.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Alonso-Nanclares L, DeFelipe J. Alterations of the microvascular network in the sclerotic hippocampus of patients with temporal lobe epilepsy. Epilepsy Behav 2014, 38: 48–52.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    Shi S, Tang M, Li H, Ding H, Lu Y, Gao L, et al. X-box binding protein l splicing attenuates brain microvascular endothelial cell damage induced by oxygen-glucose deprivation through the activation of phosphoinositide 3-kinase/protein kinase B, extracellular signal-regulated kinases, and hypoxia-inducible factor-1alpha/vascular endothelial growth factor signaling pathways. J Cell Physiol 2019, 234: 9316–9327.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Sakurai M, Morita T, Takeuchi T, Shimada A. Relationship of angiogenesis and microglial activation to seizure-induced neuronal death in the cerebral cortex of Shetland Sheepdogs with familial epilepsy. Am J Vet Res 2013, 74: 763–770.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Myczek K, Yeung ST, Castello N, Baglietto-Vargas D, LaFerla FM. Hippocampal adaptive response following extensive neuronal loss in an inducible transgenic mouse model. PLoS One 2014, 9: e106009.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Morin-Brureau M, Rigau V, Lerner-Natoli M. Why and how to target angiogenesis in focal epilepsies. Epilepsia 2012, 53 Suppl 6: 64–68.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Winkler EA, Bell RD, Zlokovic BV. Central nervous system pericytes in health and disease. Nat Neurosci 2011, 14: 1398–1405.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Shanghai Institutes for Biological Sciences, CAS 2019

Authors and Affiliations

  • Pan Gu
    • 1
  • Zi-Hao Xu
    • 1
  • Yu-Ze Cao
    • 1
  • Sheng-Hui Liao
    • 2
  • Qian-Fang Deng
    • 1
  • Xian-Zhen Yin
    • 3
  • Zhuo-Lu Wang
    • 4
  • Zhuo-Hui Chen
    • 1
  • Xin-Hang Hu
    • 1
  • Hui Wang
    • 1
  • Li-Zhi Li
    • 1
  • Shi-Xin Liu
    • 1
  • Hui Ding
    • 1
  • Shu-Peng Shi
    • 1
  • Hong-Lei Li
    • 1
  • Ti-Qiao Xiao
    • 5
  • Bo Xiao
    • 1
    Email author
  • Meng-Qi Zhang
    • 1
    Email author
  1. 1.Department of Neurology, Xiangya HospitalCentral South UniversityChangshaChina
  2. 2.School of Information Science and EngineeringCentral South UniversityChangshaChina
  3. 3.State Key Laboratory of Drug Research, CAS Key Laboratory of Receptor Research, Shanghai Institute of Materia MedicaChinese Academy of SciencesShanghaiChina
  4. 4.Department of Breast SurgeryHunan Provincial Maternal and Child Health Care HospitalChangshaChina
  5. 5.Shanghai Synchrotron Radiation Facility, Shanghai Advanced Research InstituteChinese Academy of SciencesShanghaiChina

Personalised recommendations