Differential effects of FK506 on structural and functional axonal deficits after diffuse brain injury in the immature rat

Journal of Neuropathology and Experimental Neurology

Volumn 71, Issue 11, 2012, Pages 959-972

  DiLeonardi, Ann Mae ^a   Huh, Jimmy W ^d   Raghupathi, Ramesh ^a,b,c  

^a Program in Neuroscience   (United States)

^b Department of Neurobiology and Anatomy ^*  (United States)

^c DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^d CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

Axonal injury; Calcineurin; Compound action potential; FK506; Immature rat; Neurofilament; Traumatic brain injury

Indexed keywords

PHOSPHATASE; TACROLIMUS;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INJURY; CONTROLLED STUDY; CORPUS CALLOSUM; DRUG EFFECT; FEMALE; MALE; MYELINATION; NERVE FIBER; NERVE FIBER DEGENERATION; NERVE FUNCTION; NEUROFILAMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

AGING; ANIMALS; AXONS; BRAIN INJURIES; FEMALE; IMMUNOSUPPRESSIVE AGENTS; MALE; RATS; RATS, SPRAGUE-DAWLEY; TACROLIMUS;

EID: 84871207818     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e31826f5876     Document Type: Article

References (61)

1. Langlois JA, Rutland-Brown W, Thomas KE. The incidence of traumatic brain injury among children in the United States: Differences by race. J Head Trauma Rehabil 2005;20:229-38
2. Coronado VG, Xu L, Basavaraju SV, et al. Surveillance for traumatic brain injuryYrelated deathsVUnited States, 1997-2007. MMWR Surveill Summ 2011;60:1-32
3. Tong KA, Ashwal S, Holshouser BA, et al. Diffuse axonal injury in children: Clinical correlation with hemorrhagic lesions. Ann Neurol 2004;56: 36-50
4. Babikian T, Freier MC, Tong KA, et al. Susceptibility weighted imaging: Neuropsychologic outcome and pediatric head injury. Pediatr Neurol 2005;33:184-94
5. Babikian T, Tong KA, Galloway NR, et al. Diffusion-weighted imaging predicts cognition in pediatric brain injury. Pediatr Neurol 2009;41: 406-12
6. Buki A, Siman R, Trojanowski JQ, et al. The role of calpain-mediated spectrin proteolysis in traumatically induced axonal injury. J Neuropathol Exp Neurol 1999;58:365-75
7. Okonkwo DO, Pettus EH, Moroi J, et al. Alteration of the neurofilament sidearm and its relation to neurofilament compaction occurring with traumatic axonal injury. Brain Res 1998;784:1-6
8. Saatman KE, Bozyczko-Coyne D, Marcy V, et al. Prolonged calpainmediated spectrin breakdown occurs regionally following experimental brain injury in the rat. J Neuropathol Exp Neurol 1996;55:850-60
9. Povlishock JT, Becker DP, Cheng CL, et al. Axonal change in minor head injury. J Neuropathol Exp Neurol 1983;42:225-42
10. Stone JR, Singleton RH, Povlishock JT. Intra-axonal neurofilament compaction does not evoke local axonal swelling in all traumatically injured axons. Exp Neurol 2001;172:320-31
11. Pettus EH, Povlishock JT. Characterization of a distinct set of intraaxonal ultrastructural changes associated with traumatically induced alteration in axolemmal permeability. Brain Res 1996;722:1-11
12. Buki A, Povlishock JT. All roads lead to disconnection?VTraumatic axonal injury revisited. Acta Neurochir (Wien) 2006;148:181-93
13. Creed JA, DiLeonardi AM, Fox DP, et al. Concussive brain trauma in the mouse results in acute cognitive deficits and sustained impairment of axonal function. J Neurotrauma 2011;28:547-63
14. Jafari SS, Nielson M, Graham DI, et al. Axonal cytoskeletal changes after nondisruptive axonal injury. II. Intermediate sized axons. J Neurotrauma 1998;15:955-66
15. Saatman KE, Abai B, Grosvenor A, et al. Traumatic axonal injury results in biphasic calpain activation and retrograde transport impairment in mice. J Cereb Blood Flow Metab 2003;23:34-42
16. DiLeonardi AM, Huh JW, Raghupathi R. Impaired axonal transport and neurofilament compaction occur in separate populations of injured axons following diffuse brain injury in the immature rat. Brain Res 2009;1263: 174-82
17. Raghupathi R, Huh JW. Diffuse brain injury in the immature rat: Evidence for an age-at-injury effect on cognitive function and histopathologic damage. J Neurotrauma 2007;24:1596-608
18. Adelson PD, Jenkins LW, Hamilton RL, et al. Histopathologic response of the immature rat to diffuse traumatic brain injury. J Neurotrauma 2001; 18:967-76
19. Huh JW, Widing AG, Raghupathi R. Midline brain injury in the immature rat induces sustained cognitive deficits, bihemispheric axonal injury and neurodegeneration. Exp Neurol 2008;213:84-92
20. Raghupathi R, Margulies SS. Traumatic axonal injury after closed head injury in the neonatal pig. J Neurotrauma 2002;19:843-53
21. Gennarelli TA. The spectrum of traumatic axonal injury. Neuropathol Appl Neurobiol 1996;22:509-13
22. Maxwell WL, Povlishock JT, Graham DL. A mechanistic analysis of nondisruptive axonal injury: A review. J Neurotrauma 1997;14:419-40
23. Reeves TM, Phillips LL, Povlishock JT. Myelinated and unmyelinated axons of the corpus callosum differ in vulnerability and functional recovery following traumatic brain injury. Exp Neurol 2005;196:126-37
24. Baker AJ, Phan N, Moulton RJ, et al. Attenuation of the electrophysiological function of the corpus callosum after fluid percussion injury in the rat. J Neurotrauma 2002;19:587-99
25. Ai J, Liu E, Park E, et al. Structural and functional alterations of cerebellum following fluid percussion injury in rats. Exp Brain Res 2007; 177:95-112
26. Preston RJ, Waxman SG, Kocsis JD. Effects of 4-aminopyridine on rapidly and slowly conducting axons of rat corpus callosum. Exp Neurol 1983;79: 808-20
27. Ai J, Liu E, Wang J, et al. Calpain inhibitor MDL-28170 reduces the functional and structural deterioration of corpus callosum following fluid percussion injury. J Neurotrauma 2007;24:960-78
28. Maxwell WL, Kosanlavit R, McCreath BJ, et al. Freeze-fracture and cytochemical evidence for structural and functional alteration in the axolemma and myelin sheath of adult guinea pig optic nerve fibers after stretch injury. J Neurotrauma 1999;16:273-84
29. Maxwell WL, McCreath BJ, Graham DI, et al. Cytochemical evidence for redistribution of membrane pump calcium-ATPase and ecto- Ca-ATPase activity, and calcium influx in myelinated nerve fibres of the optic nerve after stretch injury. J Neurocytol 1995;24:925-42
30. Stys PK, Ransom BR, Waxman SG, et al. Role of extracellular calcium in anoxic injury of mammalian central white matter. Proc Natl Acad Sci USA 1990;87:4212-16
31. Fern R, Ransom BR, Waxman SG. Voltage-gated calcium channels in CNS white matter: Role in anoxic injury. J Neurophysiol 1995;74:369-77
32. Colley BS, Phillips LL, Reeves TM. The effects of cyclosporin-A on axonal conduction deficits following traumatic brain injury in adult rats. Exp Neurol 2010;224:241-51
33. Reeves TM, Phillips LL, Lee NN, et al. Preferential neuroprotective effect of tacrolimus (FK506) on unmyelinated axons following traumatic brain injury. Brain Res 2007;1154:225-36
34. Hall GF, Lee VM. Neurofilament sidearm proteolysis is a prominent early effect of axotomy in lamprey giant central neurons. J Comp Neurol 1995; 353:38-49
35. Nixon RA, Paskevich PA, Sihag RK, et al. Phosphorylation on carboxyl terminus domains of neurofilament proteins in retinal ganglion cell neurons in vivo: Influences on regional neurofilament accumulation, interneurofilament spacing, and axon caliber. J Cell Biol 1994;126:1031-46
36. de Waegh SM, Lee VM, Brady ST. Local modulation of neurofilament phosphorylation, axonal caliber, and slow axonal transport by myelinating Schwann cells. Cell 1992;68:451-63
37. Saljo A, Bao F, Haglid KG, et al. Blast exposure causes redistribution of phosphorylated neurofilament subunits in neurons of the adult rat brain. J Neurotrauma 2000;17:719-26
38. Ma M, Matthews BT, Lampe JW, et al. Immediate short-duration hypothermia provides long-term protection in an in vivo model of traumatic axonal injury. Exp Neurol 2009;215:119-27
39. Chung RS, Staal JA, McCormack GH, et al. Mild axonal stretch injury in vitro induces a progressive series of neurofilament alterations ultimately leading to delayed axotomy. J Neurotrauma 2005;22:1081-91
40. Tanaka T, Takeda M, Niigawa H, et al. Phosphorylated neurofilament accumulation in neuronal perikarya by cyclosporine-A injection in rat brain. Method Find Exp Clin 1993;15:77-87
41. Eyer J, Leterrier JF. Influence of the phosphorylation state of neurofilament proteins on the interactions between purified filaments in vitro. Biochem J 1988;252:655-60
42. Kurz JE, Parsons JT, Rana A, et al. A significant increase in both basal and maximal calcineurin activity following fluid percussion injury in the rat. J Neurotrauma 2005;22:476-90
43. Kurz JE, Hamm RJ, Singleton RH, et al. A persistent change in subcellular distribution of calcineurin following fluid percussion injury in the rat. Brain Res 2005;1048:153-60
44. Bales JW, Ma X, Yan HQ, et al. Regional calcineurin subunit B isoform expression in rat hippocampus following a traumatic brain injury. Brain Res 2010;1358:211-20
45. Bales JW, Ma X, Yan HQ, et al. Expression of protein phosphatase 2B (calcineurin) subunit A isoforms in rat hippocampus after traumatic brain injury. J Neurotrauma 2010;27:109-20
46. Marmarou CR, Povlishock JT. Administration of the immunophilin ligand FK506 differentially attenuates neurofilament compaction and impaired axonal transport in injured axons following diffuse traumatic brain injury. Exp Neurol 2006;197:353-62
47. Singleton RH, Stone JR, Okonkwo DO, et al. The immunophilin ligand FK506 attenuates axonal injury in an impact-acceleration model of traumatic brain injury. J Neurotrauma 2001;18:607-14
48. Buki A, Okonkwo DO, Povlishock JT. Postinjury cyclosporin A administration limits axonal damage and disconnection in traumatic brain injury. J Neurotrauma 1999;16:511-21
49. Okonkwo DO, Buki A, Siman R, et al. Cyclosporin A limits calcium-induced axonal damage following traumatic brain injury. Neuroreport 1999;10: 353-58
50. Staal JA, Dickson TC, Gasperini R, et al. Initial calcium release from intracellular stores followed by calcium dysregulation is linked to secondary axotomy following transient axonal stretch injury. J Neurochem 2010;112: 1147-55
51. Setkowicz Z, Ciarach M, Guzik R, et al. Different effects of neuroprotectants FK-506 and cyclosporin A on susceptibility to pilocarpine-induced seizures in rats with brain injured at different developmental stages. Epilepsy Res 2004;61:63-72
52. Schumacher PA, Eubanks JH, Fehlings MG. Increased calpain IYmediated proteolysis and preferential loss of dephosphorylated NF200 following traumatic spinal cord injury. Neuroscience 1999;91:733-44
53. Guandalini P, Franchi G, Semenza P, et al. The functional development of input-output relationships in the rostral portion of the corpus callosum in the kitten. Exp Brain Res 1989;74:453-62
54. Iwata A, Stys PK, Wolf JA, et al. Traumatic axonal injury induces proteolytic cleavage of the voltage-gated sodium channels modulated by tetrodotoxin and protease inhibitors. J Neurosci 2004;24: 4605-13
55. von Reyn CR, Spaethling JM, Mesfin MN, et al. Calpain mediates proteolysis of the voltage-gated sodium channel alpha-subunit. J Neurosci 2009;29:10350-56
56. Reeves TM, Smith TL, Williamson JC, et al. Unmyelinated axons show selective rostrocaudal pathology in the corpus callosum after traumatic brain injury. J Neuropathol Exp Neurol 2012;71:198-210
57. Jafari SS, Maxwell WL, Neilson M, et al. Axonal cytoskeletal changes after non-disruptive axonal injury. J Neurocytol 1997;26:207-21
58. Stone JR, Walker SA, Povlishock JT. The visualization of a new class of traumatically injured axons through the use of a modified method of microwave antigen retrieval. Acta Neuropathol 1999;97: 335-45
59. Stone JR, Okonkwo DO, Dialo AO, et al. Impaired axonal transport and altered axolemmal permeability occur in distinct populations of damaged axons following traumatic brain injury. Exp Neurol 2004;190: 59-69
60. Nottingham S, Knapp P, Springer J. FK506 treatment inhibits caspase-3 activation and promotes oligodendroglial survival following traumatic spinal cord injury. Exp Neurol 2002;177:242-51
61. Wakita H, Tomimoto H, Akiguchi I, et al. Dose-dependent, protective effect of FK506 against white matter changes in the rat brain after chronic cerebral ischemia. Brain Res 1998;792:105-13