The combination of either tempol or FK506 with delayed hypothermia: Implications for traumatically induced microvascular and axonal protection

Journal of Neurotrauma

Volumn 28, Issue 7, 2011, Pages 1209-1218

  Fujita, Motoki ^a,b   Oda, Yasutaka ^a,b   Wei, Enoch P ^a   Povlishock, John T ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY MEDICAL CENTER   (United States)

^b YAMAGUCHI UNIVERSITY HOSPITAL   (Japan)

Author keywords

axonal injury; pial vessels; traumatic brain injury; vascular reactivity

Indexed keywords

TACROLIMUS; TEMPOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL REACTIVITY; BRAIN BLOOD VESSEL; HYPOTHERMIA; MALE; MICROVASCULARIZATION; NERVE FIBER; NEUROPROTECTION; NONHUMAN; RAT; TRAUMATIC BRAIN INJURY;

ANIMALS; AXONS; BRAIN INJURIES; COMBINED MODALITY THERAPY; CYCLIC N-OXIDES; DISEASE MODELS, ANIMAL; HYPOTHERMIA, INDUCED; IMMUNOSUPPRESSIVE AGENTS; MALE; MICROCIRCULATION; NEUROPROTECTIVE AGENTS; RATS; RATS, SPRAGUE-DAWLEY; SPIN LABELS; TACROLIMUS;

EID: 79960511697     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.1852     Document Type: Article

References (40)

1. Bales, J.W., Ma, X., Yan, H.Q., Jenkins, L.W., and Dixon, C.E. (2010). Expression of protein phosphatase 2B (calcineurin) subunit A isoforms in rat hippocampus after traumatic brain injury. J. Neurotrauma 27, 109-120.
2. Baranova, A.I., Wei, E.P., Ueda, Y., Sholley, M.M., Kontos, H.A., and Povlishock, J.T. (2008). Cerebral vascular responsiveness after experimental traumatic brain injury: the beneficial effects of delayed hypothermia combined with superoxide dismutase administration. J. Neurosurg 109, 502-509.
3. Behringer, W., Safar, P., Kentner, R., Wu, X., Kagan, V.E., Radovsky, A., Clark, R.S., Kochanek, P.M., Subramanian, M., Tyurin, V.A., Tyurina, Y.Y., and Tisherman, S.A. (2002). Antioxidant Tempol enhances hypothermic cerebral preservation during prolonged cardiac arrest in dogs. J. Cereb. Blood Flow Metab. 22, 105-117. (Pubitemid 34038389) (Pubitemid 34038389)
4. Büki, A., and Povlishock, J.T. (2006). All roads lead to disconnection?- Traumatic axonal injury revisited. Acta Neurochir. 148, 181-194.
5. Carroll, R.T., Galatsis, P., Borosky, S., Kopec, K.K., Kumar, V., Althaus, J.S., and Hall, E.D. (2000). 4-Hydroxy-2,2,6,6-tetramethylpiperidine- 1-oxyl (Tempol) inhibits peroxynitritemediated phenol nitration. Chem. Res. Toxicol. 13, 294-300.
6. Clifton, G.L., Miller, E.R., Choi, S.C., Levin, H.S., McCauley, S., Smith, K.R. Jr., Muizelaar, J.P., Wagner, F.C. Jr., Marion, D.W., Luerssen, T.G., Chesnut, R.M., and Schwartz, M. (2001). Lack of effect of induction of hypothermia after acute brain injury. N. Engl. J. Med. 344, 556-563. (Pubitemid 32167869) (Pubitemid 32167869)
7. Deng-Bryant, Y., Singh, I.N., Carrico, K.M., and Hall, E.D. (2008). Neuroprotective effects of Tempol, a catalytic scavenger of peroxynitrite- derived free radicals, in a mouse traumatic brain injury model. J. Cereb Blood Flow Metab. 28, 1114-1126. (Pubitemid 351733341) (Pubitemid 351733341)
8. Deng, Y., Thompson, B.M., Gao, X., and Hall, E.D. (2007). Temporal relationship of peroxynitrite-induced oxidative damage, calpain-mediated cytoskeletal degradation and neurodegeneration after traumatic brain injury. Exp. Neurol. 205, 154-165. (Pubitemid 46621175) (Pubitemid 46621175)
9. Ellis, E.F., Wei, E.P., Cockrell, C.S., Choi, S., and Kontos, H.A. (1983). The effect of PGF2 alpha on in vivo cerebral arteriolar diameter in cats and rats. Prostaglandins 26, 917-923. (Pubitemid 14165831) (Pubitemid 14165831)
10. Gao, G., Oda, Y., Wei, E.P., and Povlishock, J.T. (2010). The adverse pial arteriolar and axonal consequences of traumatic brain injury complicated by hypoxia and their therapeutic modulation with hypothermia in rat. J. Cereb Blood Flow Metab, 30, 628-637.
11. Globus, M.Y., Alonso, O., Dietrich, W.D., Busto, R., and Ginsberg, M.D. (1995). Glutamate release and free radical production following brain injury: effects of posttraumatic hypothermia. J. Neurochem. 65, 1704-1711.
12. Hall, E.D., Vaishnav, R.A., and Mustafa, A.G. (2010). Antioxidant therapies for traumatic brain injury. Neurotherapeutics 7, 51-61.
13. Jiang, J.Y., Lyeth, B.G., Clifton, G.L., Jenkins, L.W., Hamm, R.J., and Hayes, R.L. (1991). Relationship between body and brain temperature in traumatically brain-injured rodents. J. Neurosurg 74, 492-496.
14. Kato, N., Yanaka, K., Hyodo, K., Homma, K., Nagase, S., and Nose, T. (2003). Stable nitroxide Tempol ameliorates brain injury by inhibiting lipid peroxidation in a rat model of transient focal cerebral ischemia. Brain Res. 979, 188-193. (Pubitemid 36792169) (Pubitemid 36792169)
15. Koda, Y., Tsuruta, R., Fujita, M., Miyauchi, T., Kaneda, K., Todani, M., Aoki, T., Shitara, M., Izumi, T., Kasaoka, S., Yuasa, M., and Maekawa, T. (2010). Moderate hypothermia suppresses jugular venous superoxide anion radical, oxidative stress, early inflammation, and endothelial injury in forebrain ischemia/reperfusion rats. Brain Res. 1311, 197-205.
16. Koizumi, H., and Povlishock, J.T. (1998). Posttraumatic hypothermia in the treatment of axonal damage in an animal model of traumatic axonal injury. J. Neurosurg, 89, 303-309. (Pubitemid 28346151) (Pubitemid 28346151)
17. Kontos, H.A., and Hess, M.L. (1983). Oxygen radicals and vascular damage. Adv. Exp. Med. Biol. 161, 365-375.
18. Kontos, H.A., and Povlishock, J.T. (1986). Oxygen radicals in brain injury. Cent. Nerv. Syst. Trauma 3, 257-263. (Pubitemid 17055007) (Pubitemid 17055007)
19. Kontos, H.A., Wei, E.P., and Marshall, J.J. (1988). In vivo bioassay of endothelium-derived relaxing factor. Am. J. Physiol. 255, 1259-1262.
20. Kontos, H.A., and Wei, E.P. (1986). Superoxide production in experimental brain injury. J. Neurosurg. 64, 803-807. (Pubitemid 16115360) (Pubitemid 16115360)
21. Krishna, M.C., Russo, A., Mitchell, J.B., Goldstein, S., Dafni, H., and Samuni, A. (1996). Do nitroxide antioxidants act as scavengers of O2- or as SOD mimics? J. Biol. Chem. 271, 26026-26031. (Pubitemid 26347441) (Pubitemid 26347441)
22. Kwon, T.H., Chao, D.L., Malloy, K., Sun, D., Alessandri, B., and Bullock, M.R. (2003). Tempol, a novel stable nitroxide, reduces brain damage and free radical production, after acute subdural hematoma in the rat. J. Neurotrauma 20, 337-345. (Pubitemid 36529880) (Pubitemid 36529880)
23. Leker, R.R., Teichner, A., Lavie, G., Shohami, E., Lamensdorf, I., and Ovadia, H. (2002). The nitroxide antioxidant Tempol is cerebroprotective against focal cerebral ischemia in spontaneously hypertensive rats. Exp. Neurol. 176, 355-363. (Pubitemid 35193352) (Pubitemid 35193352)
24. Levasseur, J.E., Wei, E.P., Raper, A.J., Kontos, A.A., and Patterson, J.L. (1975). Detailed description of a cranial window technique for acute and chronic experiments. Stroke 6, 308-317.
25. Marmarou, A., Foda, M.A., van den Brink, W., Campbell, J., Kita, H., and Demetriadou, K. (1994). A new model of diffuse brain injury in rats. Part I: Pathophysiology and biomechanics. J. Neurosurg. 80, 291-300. (Pubitemid 24036501) (Pubitemid 24036501)
26. Marmarou, C.R., and Povlishock, J.T. (2006). Administration of the immunophilin ligand FK506 differentially attenuates neurofilament compaction and impaired axonal transport in injured axons following diffuse traumatic brain injury. Exp. Neurol. 2, 353-362. (Pubitemid 43077143) (Pubitemid 43077143)
27. Oda, Y., Gao, G., Wei, E.P., and Povlishock, J.T. (2011). Combinational therapy using hypothermia and the immunophilin ligand FK506 to target altered pial arteriolar reactivity, axonal damage, and blood-brain barrier dysfunction after traumatic brain injury in rat. J. Cereb. Blood Flow Metab. 31, 1143-1154.
28. Povlishock, J.T. (2000). Pathophysiology of neural injury: therapeutic opportunities and challenges. Clin. Neurosurg. 46, 113-126.
29. Povlishock, J.T., Marmarou, A., McIntosh, T., Trojanowski, J.Q., and Moroi, J. (1997). Impact acceleration injury in the rat: evidence for focal axolemmal change and related neurofilament sidearm alteration. J. Neuropathol. Exp. Neurol. 56, 347-359. (Pubitemid 27465017) (Pubitemid 27465017)
30. Rak, R., Chao, D.L., Pluta, R.M., Mitchell, J.B., Oldfield, E.H., and Watson, J.C. (2000). Neuroprotection by the stable nitroxide Tempol during reperfusion in a rat model of transient focal ischemia. J. Neurosurg. 92, 646-651. (Pubitemid 30180671) (Pubitemid 30180671)
31. Reeves, T.M., Phillips, L.L., Lee, N.N., and Povlishock, J.T. (2007). Preferential neuroprotective effect of tacrolimus (FK506) on unmyelinated axons following traumatic brain injury. Brain Res. 1154, 225-236. (Pubitemid 46860352) (Pubitemid 46860352)
32. Singleton, R.H., Stone, J.R., Okonkwo, D.O., Pellicane, A.J., and Povlishock, J.T. (2001). The immunophilin ligand FK506 attenuates axonal injury in an impact-acceleration model of traumatic brain injury. J. Neurotrauma 18, 607-614. (Pubitemid 32568178) (Pubitemid 32568178)
33. Stone, J.R., Singleton, R.H., and Povlishock, J.T. (2000). Antibodies to the C-terminus of the beta-amyloid precursor protein (APP): a site specific marker for the detection of traumatic axonal injury. Brain Res. 871, 288-302. (Pubitemid 30433880) (Pubitemid 30433880)
34. Stone, J.R., Walker, S.A., and Povlishock, J.T. (1999). The visualization of a new class of traumatically injured axons through the use of a modified method of microwave antigen retrieval. Acta Neuropathol. 97, 335-345. (Pubitemid 29134513) (Pubitemid 29134513)
35. Suehiro, E., and Povlishock, J.T. (2001). Exacerbation of traumatically induced axonal injury by rapid posthypothermic rewarming and attenuation of axonal change by cyclosporin A. J. Neurosurg. 94, 493-498. (Pubitemid 32786031) (Pubitemid 32786031)
36. Suehiro, E., Ueda, Y., Wei, E.P., Kontos, H.A., and Povlishock, J.T. (2003). Posttraumatic hypothermia followed by slow rewarming protects the cerebral microcirculation. J. Neurotrauma 20, 381-390. (Pubitemid 36529884) (Pubitemid 36529884)
37. Tortorici, M.A., Kochanek, P.M., and Poloyac, S.M. (2007). Effects of hypothermia on drug disposition, metabolism, and response: A focus of hypothermia-mediated alterations on the cytochrome P450 enzyme system. Crit. Care Med. 35, 2196-2204. (Pubitemid 47326460) (Pubitemid 47326460)
38. Ueda, Y., Wei, E.P., Kontos, H.A., Suehiro, E., and Povlishock, J.T. (2003). Effects of delayed, prolonged hypothermia on the pial vascular response after traumatic brain injury in rats. J. Neurosurg. 99, 899-906. (Pubitemid 37314927) (Pubitemid 37314927)
39. Wei, E.P., Hamm, R.J., Baranova, A.I., and Povlishock, J.T. (2009). The long-term microvascular and behavioral consequences of experimental traumatic brain injury after hypothermic intervention. J. Neurotrauma 26, 527-537.
40. Wei, E.P., Kukreja, R., and Kontos, H.A. (1992). Effects in cats of inhibition of nitric oxide synthesis on cerebral vasodilation and endothelium-derived relaxing factor from acetylcholine. Stroke 23, 1623-1628.