Aquaporin-4 mitigates retrograde degeneration of rubrospinal neurons by facilitating edema clearance and glial scar formation after spinal cord injury in mice

Molecular Neurobiology

Volumn 49, Issue 3, 2014, Pages 1327-1337

  Wu, Qi ^a   Zhang, Yong Jie ^a   Gao, Jun Ying ^a   Li, Xiu Miao ^a   Kong, Hui ^a   Zhang, Yi Ping ^b   Xiao, Ming ^a   Shields, Christopher B ^b   Hu, Gang ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

^b Norton Neuroscience Institute   (United States)

Author keywords

Aquaporin 4; Astrocytes; Edema; Rubrospinal tract; Spinal cord injury

Indexed keywords

AQUAPORIN 4; AQP4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ATROPHY; CELL MIGRATION; CONTROLLED STUDY; DISEASE EXACERBATION; DRUG TARGETING; EDEMA; FEMALE; GLIAL SCAR FORMATION; MOTOR NEURON DISEASE; MOUSE; NERVE CELL DEGENERATION; NERVE FIBER DEGENERATION; NEUROPROTECTION; NONHUMAN; PROTEIN EXPRESSION; RETROGRADE DEGENERATION; RUBROSPINAL TRACT; SCAR FORMATION; SPINAL CORD INJURY; ANIMAL; CERVICAL SPINE; DEFICIENCY; GLIA; KNOCKOUT MOUSE; METABOLISM; NERVE CELL; PATHOLOGY; RED NUCLEUS; SCAR;

ANIMALS; AQUAPORIN 4; CERVICAL VERTEBRAE; CICATRIX; EDEMA; FEMALE; MICE; MICE, KNOCKOUT; NEUROGLIA; NEURONS; RED NUCLEUS; RETROGRADE DEGENERATION; SPINAL CORD INJURIES;

EID: 84902548470     PISSN: 08937648     EISSN: 15591182     Source Type: Journal    
DOI: 10.1007/s12035-013-8607-3     Document Type: Article

References (55)

1. Sekhon LH, Fehlings MG (2001) Epidemiology, demographics, and pathophysiology of acute spinal cord injury. Spine 26:S2-S12 (Pubitemid 34019773)
2. Borgens RB, Liu-Snyder P (2012) Understanding secondary injury. Q Rev Biol 87:89-127
3. Tator CH, Fehlings MG (1991) Review of the secondary injury theory of acute spinal cord trauma with emphasis on vascular mechanisms. J Neurosurg 75:15-26
4. Sharma HS (2011) Early microvascular reactions and blood-spinal cord barrier disruption are instrumental in pathophysiology of spinal cord injury and repair: novel therapeutic strategies including nanowired drug delivery to enhance neuroprotection. J Neural Transm 118:155-176
5. Ge R, Zhu Y, Diao Y, Tao L, Yuan W, Xiong XC (2013) Anti-edema effect of epigallocatechin gallate on spinal cord injury in rats. Brain Res. doi:10.1016/j.brainres.2013.06.009
6. Ning N, Dang X, Bai C, Zhang C, Wang K (2012) Panax notoginsenoside produces neuroprotective effects in rat model of acute spinal cord ischemia-reperfusion injury. J Ethnopharmacol 139:504-512
7. Karimi-Abdolrezaee S, Billakanti R (2012) Reactive astrogliosis after spinal cord injury-beneficial and detrimental effects. Mol Neurobiol 46:251-264
8. Pannu R, Barbosa E, Singh AK, Singh I (2005) Attenuation of acute inflammatory response by atorvastatin after spinal cord injury in rats. J Neurosci Res 79:340-350 (Pubitemid 40278348)
9. Escartin C, Bonvento G (2008) Targeted activation of astrocytes: a potential neuroprotective strategy. Mol Neurobiol 38:231-241
10. Herrmann JE, Imura T, Song B, Qi J, Ao Y, Nguyen TK, Korsak RA, Takeda K, Akira S, Sofroniew MV (2008) STAT3 is a critical regulator of astrogliosis and scar formation after spinal cord injury. J Neurosci 28:7231-7243
11. Kamei N, Kwon SM, Alev C, Ishikawa M, Yokoyama A, Nakanishi K, Yamada K, Horii M, Nishimura H, Takaki S, Kawamoto A, Ii M, Akimaru H, Tanaka N, Nishikawa S, Ochi M, Asahara T (2010) Lnk deletion reinforces the function of bone marrow progenitors in promoting neovascularization and astrogliosis following spinal cord injury. Stem Cells 28:365-375
12. Yuan YM, He C (2013) The glial scar in spinal cord injury and repair. Neurosci Bull 29:421-435
13. Amiry-Moghaddam M, Ottersen OP (2003) The molecular basis of water transport in the brain. Nat Rev Neurosci 4:991-1001 (Pubitemid 37486675)
14. Nesic O, Guest JD, Zivadinovic D, Narayana PA, Herrera JJ, Grill RJ, Mokkapati VU, Gelman BB, Lee J (2010) Aquaporins in spinal cord injury: the janus face of aquaporin 4. Neuroscience 168:1019-1035
15. Nesic O, Lee J, Ye Z, Unabia GC, Rafati D, Hulsebosch CE, Perez-Polo JR (2006) Acute and chronic changes in aquaporin 4 expression after spinal cord injury. Neuroscience 43:779-792 (Pubitemid 44751372)
16. Xu WB, Gu YT, Wang YF, Lu XH, Jia LS, Lv G (2008) Bradykinin preconditioning modulates aquaporin-4 expression after spinal cord ischemic injury in rats. Brain Res 1246:11-18
17. Wang YF, Fan ZK, Cao Y, Yu DS, Zhang YQ, Wang YS (2011) 2-Methoxyestradiol inhibits the up-regulation of AQP4 and AQP1 expression after spinal cord injury. Brain Res 1370:220-226
18. Mao L, Wang HD, Pan H, Qiao L (2011) Sulphoraphane enhances aquaporin-4 expression and decreases spinal cord oedema following spinal cord injury. Brain Inj 25:300-306
19. Saadoun S, Bell BA, Verkman AS, Papadopoulos MC (2008) Greatly improved neurological outcome after spinal cord compression injury in AQP4-deficient mice. Brain 131:1087-1098 (Pubitemid 351499422)
20. Kimura A, Hsu M, Seldin M, Verkman AS, Scharfman HE, Binder DK (2010) Protective role of aquaporin-4 water channels after contusion spinal cord injury. Ann Neurol 67:794-801
21. Suzuki R, Okuda M, Asai J, Nagashima G, Itokawa H, Matsunaga A, Fujimoto T, Suzuki T (2006) Astrocytes co-express aquaporin-1, -4, and vascular endothelial growth factor in brain edema tissue associated with brain contusion. Acta Neurochir Suppl l96:398-401
22. Saadoun S, Papadopoulos MC, Watanabe H, Yan D, Manley GT, Verkman AS (2005) Involvement of aquaporin-4 in astroglial cell migration and glial scar formation. J Cell Sci 118:5691-5698 (Pubitemid 43079263)
23. Auguste KI, Jin S, Uchida K, Yan D, Manley GT, Papadopoulos MC, Verkman AS (2007) Greatly impaired migration of implanted aquaporin-4-deficient astroglial cells in mouse brain toward a site of injury. FASEB J 21:108-116 (Pubitemid 46052550)
24. Lu DC, Zador Z, Yao J, Fazlollahi F, Manley GT (2011) Aquaporin-4 reduces post-traumatic seizure susceptibility by promoting astrocytic glial scar formation in mice. J Neurotrauma
25. Fan Y, Kong H, Shi X, Sun X, Ding J, Wu J, Hu G (2008) Hypersensitivity of aquaporin 4-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine and astrocytic modulation. Neurobiol Aging 29:1226-1236 (Pubitemid 351822407)
26. Liu L, Lu Y, Kong H, Li L, Marshall C, Xiao M, Ding J, Gao J, Hu G (2012) Aquaporin-4 deficiency exacerbates brain oxidative damage and memory deficits induced by long-term ovarian hormone deprivation and D-galactose injection. Int J Neuropsychopharmacol 15:55-68
27. Saji E, Arakawa M, Yanagawa K, Toyoshima Y, Yokoseki A, Okamoto K, Otsuki M, Akazawa K, Kakita A, Takahashi H, Nishizawa M, Kawachi I (2013) Cognitive impairment and cortical degeneration in neuromyelitis optica. Ann Neurol 73:65-76
28. Fan Y, Zhang J, Sun XL, Gao L, Zeng XN, Ding JH, Cao C, Niu L, Hu G (2005) Sex-and region-specific alterations of basal amino acid and monoamine metabolism in the brain of aquaporin-4 knockout mice. J Neurosci Res 82:458-464 (Pubitemid 41579345)
29. Hill RL, Zhang YP, Burke DA, Devries WH, Zhang Y, Magnuson DS, Whittemore SR, Shields CB (2009) Anatomical and functional outcomes following a precise, graded, dorsal laceration spinal cord injury in C57BL/6 mice. J Neurotrauma 26:1-15
30. Kozlowski DA, James DC, Schallert T (1996) Use-dependent exaggeration of neuronal injury following unilateral sensorimotor cortex lesions. J Neurosci 16:4776-4786 (Pubitemid 26251072)
31. Liu Y, Kim D, Himes BT, Chow SY, Schallert T, Murray M, Tessler A, Fischer I (1999) Transplants of fibroblasts genetically modified to express BDNF promote regeneration of adult rat rubrospinal axons and recovery of forelimb function. J Neurosci 19:4370-4387 (Pubitemid 29241090)
32. Li X, Kong H, Wu W, Xiao M, Sun X, Hu G (2009) Aquaporin-4 maintains ependymal integrity in adult mice. Neuroscience 162:67-77
33. Brown LT (1974) Rubrospinal projections in the rat. J Comp Neurol 154:169-188
34. Mori F, Himes BT, Kowada M, Murray M, Tessler A (1997) Fetal spinal cord transplants rescue some axotomized rubrospinal neurons from retrograde cell death in adult rats. Exp Neurol 143:45-60 (Pubitemid 27049131)
35. Monzón Mayor M, Yánes Méndez CM, Trujillo Trujillo CM (1986) A Nissl, Golgi-Kopsch and ultrastructural study of the Gallotia galloti red nucleus. J Hirnforsch 27:61-78 (Pubitemid 16079496)
36. García-Amado M, Prensa L (2012) Stereological analysis of neuron, glial and endothelial cell numbers in the human amygdaloid complex. PLoS One 7:e38692
37. Liang H, Paxinos G, Watson C (2012) The red nucleus and the rubrospinal projection in the mouse. Brain Struct Funct 217:221-232
38. Holtz A, Levi R (2010) Spinal cord injury. Oxford University Press, New York
39. Papadopoulos MC, Manley GT, Krishna S, Verkman AS (2004) Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J 18:1291-1293 (Pubitemid 39561580)
40. Geisert EE Jr, Frankfurter A (1989) The neuronal response to injury as visualized by immunostaining of class III beta-tubulin in the rat. Neurosci Lett 102:137-141
41. Wong DY, Leveque JC, Brumblay H, Krebsbach PH, Hollister SJ, Lamarca F (2008) Macro-architectures in spinal cord scaffold implants influence regeneration. J Neurotrauma 25:1027-1037
42. Tanaka T, Ueno M, Yamashita T (2009) Engulfment of axon debris by microglia requires p38 MAPK activity. J Biol Chem 284:21626-21636
43. Rosenzweig ES, McDonald JW (2004) Rodent models for treatment of spinal cord injury: research trends and progress toward useful repair. Curr Opin Neurol 17:121-131 (Pubitemid 38446452)
44. Bunge RP, Puckett WR, Becerra JL, Marcillo A, Quencer RM (1993) Observations on the pathology of human spinal cord injury. A review and classification of 22 new cases with details from a case of chronic cord compression with extensive focal demyelination. Adv Neurol 59:75-89
45. Ruff CA, Wilcox JT, Fehlings MG (2012) Cell-based transplantation strategies to promote plasticity following spinal cord injury. Exp Neurol 235:78-90
46. Onose G, Anghelescu A, Muresanu DF, Padure L, Haras MA, Chendreanu CO, Onose LV, Mirea A, Ciurea AV, El Masri WS, von Wild KR (2009) A review of published reports on neuroprotection in spinal cord injury. Spinal Cord 47:716-726
47. Egan DA, Flumerfelt BA, Gwyn DG (1977) Axon reaction in the red nucleus of the rat. Perikaryal volume changes and the time course of chromatolysis following cervical and thoracic lesions. Acta Neuropathol 37:13-19 (Pubitemid 8032711)
48. Hagg T, Oudega M (2006) Degenerative and spontaneous regenerative processes after spinal cord injury. J Neurotrauma 23:264-280 (Pubitemid 43726309)
49. Moon L, Bunge MB (2005) From animal models to humans: strategies for promoting CNS axon regeneration and recovery of limb function after spinal cord injury. J Neurol Phys Ther 29:55-69
50. Saadoun S, Papadopoulos MC (2010) Aquaporin-4 in brain and spinal cord oedema. Neuroscience 168:1036-1046
51. Menet V, Prieto M, Privat A, Giménez y Ribotta M (2003) Axonal plasticity and functional recovery after spinal cord injury in mice deficient in both glial fibrillary acidic protein and vimentingenes. Proc Natl Acad Sci U S A 100:8999-9004 (Pubitemid 36899212)
52. Deng LX, Hu J, Liu N, Wang X, Smith GM, Wen X, Xu XM (2011) GDNF modifies reactive astrogliosis allowing robust axonal regeneration through Schwann cell-seeded guidance channels after spinal cord injury. Exp Neurol 229:238-250
53. Flanders AE, Spettell CM, Friedman DP, Marino RJ, Herbison GJ (1999) The relationship between the functional abilities of patients with cervical spinal cord injury and the severity of damage revealed by MR imaging. AJNR Am J Neuroradiol 20:926-934 (Pubitemid 29536273)
54. Zeng XN, Sun XL, Gao L, Fan Y, Ding JH, Hu G (2007) Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes. Mol Cell Neurosci 34:34-39 (Pubitemid 46026927)
55. Strohschein S, Hüttmann K, Gabriel S, Binder DK, Heinemann U, Steinhäuser C (2011) Impact of aquaporin-4 channels on K+ buffering and gap junction coupling in the hippocampus. Glia 59:973-980