Minocycline improves functional outcomes, memory deficits, and histopathology after endovascular perforation-induced subarachnoid hemorrhage in rats

Journal of Neurotrauma

Volumn 28, Issue 12, 2011, Pages 2503-2512

  Sherchan, Prativa ^a   Lekic, Tim ^a   Suzuki, Hidenori ^a   Hasegawa, Yu ^a   Rolland, William ^a   Duris, Kamil ^a   Zhan, Yan ^a   Tang, Jiping ^a   Zhang, John H ^a  

^a LOMA LINDA UNIVERSITY   (United States)

Author keywords

endovascular perforation; histopathology; long term neurobehavior; minocycline; subarachnoid hemorrhage

Indexed keywords

GELATINASE A; GELATINASE B; MINOCYCLINE;

AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN CORTEX; BRAIN WATER; BRAIN WEIGHT; COGNITION; CONTROLLED STUDY; DRUG MEGADOSE; ENZYME ACTIVITY; HIPPOCAMPUS; HISTOPATHOLOGY; LONG TERM CARE; LOW DRUG DOSE; MALE; MAZE TEST; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; RAT; ROTAROD TEST; SPATIAL MEMORY; SUBARACHNOID HEMORRHAGE; TREATMENT OUTCOME; WATER CONTENT;

ANIMALS; CEREBRAL ARTERIES; ENDOVASCULAR PROCEDURES; INJECTIONS, INTRAPERITONEAL; MALE; MEMORY DISORDERS; MINOCYCLINE; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SUBARACHNOID HEMORRHAGE;

EID: 83455163234     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.1864     Document Type: Article

References (55)

1. Anderson, S.W., Todd, M.M., Hindman, B.J., Clarke, W.R., Torner, J.C., Tranel, D., Yoo, B., Weeks, J., Manzel, K.W., and Samra, S. (2006). Effects of intraoperative hypothermia on neuropsychological outcomes after intracranial aneurysm surgery. Ann. Neurol. 60, 518-527. (Pubitemid 44871794)
2. Bar-Haim, S., Harries, N., Nammaourah, I., Oraibi, S., Malhees, W., Loeppky, J., Perkins, N.J., Belokopytov, M., Kaplanski, J., Lahat, E., and MERC project. (2010). Effectiveness of motor learning coaching in children with cerebral palsy: a randomized controlled trial. Clin. Rehabil. 24, 1009-1020.
3. Bederson, J.B., Germano, I.M., and Guarino, L. (1995). Cortical blood flow and cerebral perfusion pressure in a new non-craniotomy model of subarachnoid hemorrhage in the rat. Stroke 26, 1086-1091.
4. Cahill, J., Calvert, J.W., and Zhang, J.H. (2006). Mechanisms of early brain injury after subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 26, 1341-1353. (Pubitemid 44629883)
5. Cheng, O., Ostrowski, R.P., Wu, B., Liu, W., Chen, C., and Zhang, J.H. (2011). Cyclooxygenase-2 mediates hyperbaric oxygen preconditioning in the rat model of transient global cerebral ischemia. Stroke 42, 484-490.
6. Chen, W., Hartman, R., Ayer, R., Marcantonio, S., Kamper, J., Tang, J., and Zhang, J.H. (2009). Matrixmetalloproteinases inhibition provides neuroprotection against hypoxia-ischemia in developing brain. J. Neurochem. 111, 726-736.
7. Domercq, M., and Matute, C. (2004). Neuroprotection by tetra-cyclines. Trends Pharmacol. Sci. 25, 609-612.
8. Fathali, N., Ostrowski, R.P., Lekic, T., Jadhav, V., Tong, W., Tang, J., and Zhang, J.H. (2010). Cyclooxygenase-2 inhibition provides lasting protection against neonatal hypoxic-ischemic brain injury. Crit. Care. Med. 38, 572-578.
9. Garcia J.H., Wagner, S., Liu, K.F., and Hu, X.J. (1995). Neurological deficit and extent of neuronal necrosis attributable to middle cerebral artery occlusion in rats: statistical validation. Stroke 26, 627-634.
10. Guo, Z.D., Wu, H.T., Sun, X.C., Zhang, X.D., and Zhang, J.H. (2011). Protection of minocycline on early brain injury after subarachnoid hemorrhage in rats. Acta Neurochir. Suppl. 110, 71-74.
11. Hackett, M.L., and Anderson, C.S. (2000). Health outcomes 1 year after subarachnoid hemorrhage: An international population-based study. The Australian Cooperative Research on sub-arachnoid hemorrhage study group. Neurology 55, 658-662.
12. Hansen-Schwartz, J., Vajkoczy, P., Macdonald, R.L., Pluta, R.M., and Zhang, J.H. (2007). Cerebral vasospasm: looking beyond vasoconstriction. Trends Pharmacol. Sci. 28, 252-256. (Pubitemid 46818461)
13. Hartman, R., Lekic, T., Rojas, H., Tang, J., and Zhang, J.H. (2009). Assessing functional outcomes following intracerebral hemorrhage in rats. Brain Res. 1280, 148-157.
14. Homsi, S., Federico, F., Croci, N., Palmier, B., Plotkine, M., Leroux, C.M., and Tehrani, M.J. (2009). Minocycline effects on cerebral edema: Relations with inflammatory and oxidative stress markers following traumatic brain injury in mice. Brain Res. 1291, 122-132.
15. Jeon, H., Ai, J., Sabri, M., Tariq, A., and Macdonald, R.L. (2010). Learning deficits after experimental subarachnoid hemorrhage in rats. Neuroscience 169, 1805-1814.
16. Kreiter, K.T., Copeland, D., Bernardini, G.L., Bates, J.E., Peery, S., Claassen, J., Du, Y.E., Stern, Y., Connolly, E.S., and Mayer, S.A. (2002). Predictors of cognitive dysfunction after sub-arachnoid hemorrhage. Stroke 33, 200-209.
17. Lampl, Y., Boaz, M., Gilad, R., Lorberboym, M., Dabby, R., Rapoport, A., Anca-Hershkowitz, M., and Sadeh, M. (2007). Minocycline treatment in acute stroke: an open-label, evalua-tor-blinded study. Neurology 69, 1404-1410. (Pubitemid 47511461)
18. Lee, C.Z., Xue, Z., Zhu, Y., Yang, G.Y., and Young, W.L. (2007). Matrix metalloproteinase-9 inhibition attenuates vascular en-dothelial growth factor-induced intracerebral hemorrhage. Stroke 38, 2563-2568. (Pubitemid 47329638)
19. Lekic, T., Hartman, H., Rojas, H., Manaenko, A., Chen, W., Ayer, R., Tang, J., and Zhang, J.H. (2010a). Protective effect of mel-atonin upon neuropathology, striatal function, and memory ability after intracerebral hemorrhage in rats. J. Neurotrauma 27, 627-637.
20. Lekic, T., Rolland, W., Hartman, R., Kamper, J., Suzuki, H., Tang, J., and Zhang, J.H. (2010b). Characterization of brain injury, neurobehavioral profiles, and histopathology in a rat model of cerebellar hemorrhage. Exp. Neurol. 227, 96-103.
21. Macdonald, R.L., Pluta, R.M., and Zhang, J.H. (2007). Cerebral vasospasm after subarachnoid hemorrhage: the emerging revolution. Nat. Clin. Pract. Neurol. 3, 256-263. (Pubitemid 46745473)
22. MacLellan, C.L., Silasi, G., Poon, C.C., Edmundson, C.L., Buist, R., Peeling, J., and Colbourne, F. (2008). Intracerebral hemorrhage models in rat: comparing collagenase to blood infusion. J. Cereb. Blood Flow Metab. 28, 516-525. (Pubitemid 351304262)
23. Mayer, S.A., Kreiter, K.T., Copeland, D., Bernardini, G.L., Bates, J.E., Peery, S., Classen, J., Du, Y.E., and Connolly, E.S., Jr. (2002). Global and domain-specific cognitive impairment and outcome after subarachnoid hemorrhage. Neurology 59, 1750-1758. (Pubitemid 35424458)
24. Morimoto, N., Shimazawa, M., Yamashima, T., Nagai, H., and Hara, H. (2005). Minocycline inhibits oxidative stress and decreases in vitro and in vivo ischemic neuronal damage. Brain Res. 1044, 8-15. (Pubitemid 40616047)
25. Murata, Y., Rosell, A., Scannevin, R.H., Rhodes, K.J., Wang, X., and Lo, E.H. (2008). Extension of the thrombolytic time window with minocycline in experimental stroke. Stroke 39, 3372-3377.
26. Niemeier, J.P., Kreutzer, J.S., Marwitz, J.H., Gary, K.W., and Ketchum, J.M. (2011). Efficacy of a brief acute neurobeha-vioural intervention following traumatic brain injury: a preliminary investigation. Brain Inj. 25, 680-690.
27. Ogden, J.A., Mee, E.W., and Henning, M. (1993). A prospective study of impairment of cognition and memory and recovery after subarachnoid hemorrhage. Neurosurgery 33, 572-587. (Pubitemid 23292748)
28. Ostrowski, R.P., Colohan, A.R., and Zhang, J.H. (2006). Molecular mechanisms of early brain injury after subarachnoid hemorrhage. Neurol. Res. 28, 399-414. (Pubitemid 43967787)
29. Ostrowski, R.P., Colohan, A.R.T., and Zhang, J.H. (2005). Mechanisms of hyperbaric oxygen-induced neuroprotection in a rat model of subarachnoid hemorrhage. J. Cereb. Blood Flow Metab. 25, 554-571. (Pubitemid 40562929)
30. Paxinos, G., and Watson, C. (1998). The Rat Brain in Sterotaxic Coordinates. Academic Press: Sydney.
31. Piron, L., Turolla, A., Agostini, M., Zucconi, C.S., Ventura, L., Tonin, P., and Dam, M. (2010). Motor learning principles for rehabilitation: a pilot randomized controlled study in post-stroke patients. Neurorehabil. Neural Repair 24, 501-508.
32. Prunell, G.F., Svendgaard, N.A., Alkass, K., and Mathiesen, T. (2005). Delayed cell death related to acute cerebral blood flow changes following subarachnoid hemorrhage in the rat brain. J. Neurosurg. 102, 1046-1054. (Pubitemid 43193974)
33. Schwartz, A.Y., Masago, A., Sehba, F.A., and Bederson, J.B. (2000). Experimental models of subarachnoid hemorrhage in the rat: a refinement of the endovascular filament model. J. Neurosci. Methods 96, 161-167. (Pubitemid 30138061)
34. Sehba, F.A., Mostafa, G., Knopman, J., Friedrich, V. Jr., and Benderson, J.B. (2004). Acute alterations in microvascular basal lamina after subarachnoid hemorrhage. J. Neurosurg. 101, 633-640. (Pubitemid 43186422)
35. Sehba, F.A., Pluta, R.M., and Zhang, J.H. (2011). Metamorphosis of subarachnoid hemorrhage research: from delayed vaso-spasm to early brain injury. Mol. Neurobiol. 43, 27-40.
36. Silasi, G., and Colbourne, F. (2009). Long-term assessment of motor and cognitive behaviours in the intraluminal perforation model of subarachnoid hemorrhage in rats. Behav. Brain Res. 198, 380-387.
37. Sozen, T., Tsuchiyama, R., Hasegawa, Y., Suzuki, H., Jadhav, V., Nishizawa, S., and Zhang, J.H. (2009). Role of interleukin-1beta in early brain injury after subarachnoid hemorrhage in mice. Stroke 40, 2519-2525.
38. Stirling, D.P., Koochesfahani, K.M., Steeves, J.D., and Tetzlaff, W. (2005). Minocycline as a neuroprotective agent. Neu-roscientist 11, 308-322. (Pubitemid 41040860)
39. Stroke Therapy Academic Industry Roundtable (STAIR). (1999). Recommendations for standards regarding preclinical neuro-protective and restorative drug development. Stroke 30, 2752-2758.
40. Sugawara, T., Ayer, R., Jadhav, V., and Zhang, J.H. (2008). A new grading system evaluating bleeding scale in filament perforation subarachnoid hemorrhage rat model. J. Neurosci. Methods 167, 327-334. (Pubitemid 350235625)
41. Suzuki, H., Ayer, R., Sugawara, T., Chen, W., Sozen, T., Hase-gawa, Y., Kanamaru, K., and Zhang, J.H. (2010a). Protective effects of recombinant osteopontin on early brain injury after subarachnoid hemorrhage in rats. Crit. Care Med. 38, 612-618.
42. Suzuki, H., Hasegawa, Y., Kanamaru, K., and Zhang, J.H. (2010b). Mechanisms of osteopontin-induced stabilization of blood-brain barrier disruption after subarachnoid hemorrhage in rats. Stroke 41, 1783-1790.
43. Takata, K., Sheng, H., Borel, C.O., Laskowitz, D.T., Warner, D.S., and Lombard, F.W. (2008). Long-term cognitive dysfunction following experimental subarachnoid hemorrhage: new perspectives. Exp. Neurol. 213, 336-344.
44. Thal, S.C., Mebmer, K., Elsaesser, R.S., and Zausinger, S. (2008). Neurological impairment in rats after subarachnoid hemorrhage-A comparison of functional tests. J. Neurol. Sci. 268, 150-159.
45. Tikka, T., Fiebich, B.L., Goldsteins, G., Keinanen, R., and Kois-tinaho, J. (2001). Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J. Neurosci. 21, 2580-2588. (Pubitemid 32298200)
46. Titova, E., Ostrowski, R.P., Zhang, J.H., and Tang, J. (2009). Experimental models of subarachnoid hemorrhage for studies of cerebral vasospasm. Neurol. Res. 31, 568-581.
47. Tsubokawa, T., Solaroglu, I., Yatsushige, H., Cahill, J., and Yata, K. (2006). Cathepsin and calpain inhibitor E64d attenuates matrix metalloproteinase-9 activity after focal cerebral ischemia in rats. Stroke 37, 1888-1894. (Pubitemid 44297747)
48. Vann, S.D., and Aggleton, H.P. (2003). Evidence of a spatial encoding deficit in rats with lesions of the mammillary bodies or mammillothalamic tract. J. Neurosci. 23, 3506-3514. (Pubitemid 36531994)
49. Vann, S.D. (2009). Gudden's ventral tegmental nucleus is vital for memory: re-evaluating diencephalic inputs for amnesia. Brain 132, 2372-2384.
50. Wagner, A.P., Stöcker, K., Balseanu, A.T., Rogalewski, A., Die-derich, K., Minnerup, J., Margaritescu, C., and Schäbitz, W.F. (2010). Effects of granulocyte-colony stimulating factor after stroke in aged rats. Stroke 41, 1027-1031.
51. Wu, B., Ma, Q., Khatibi, N., Chen, W., Sozen, T., Cheng, O., and Tang, J. (2010). Ac-YVAD-CMK decreases blood brain barrier degradation by inhibiting caspase-1 activation of interleukin-1b in intracerebral hemorrhage mouse model. Trans. Stroke Res. 1, 57-64.
52. Xu, L., Fagan, S.C., Waller, J.L., Edwards, D., Borlongan, C.V., Zheng, J., Hill, W.D., Feuerstein, G., and Hess, D.C. (2004). Low dose intravenous minocycline is neuroprotective after middle cerebral artery occlusion- reperfusion in rat. BMC Neurol. 26, 1-7.
53. Yrjanheikki, J., Keinanen, R., Pellikka, M., Hokfelt, T., and Koistinaho, J. (1998). Tetracyclines inhibit microglial activation and are neuroprotective in global brain ischemia. Proc. Natl. Acad. Sci. 95, 15769-15774. (Pubitemid 29018775)
54. Zhou, Y., Lekic, T., Fathali, N., Ostrowski, R.P., Martin, R.D., Tang, J., and Zhang, J.H. (2010). Isoflurane posttreatment reduces neonatal hypoxic-ischemic brain injury in rats by the sphingosine-1-phosphate/ phosphatidylinositol-3-kinase/Akt pathway. Stroke 4, 1521-1527.
55. Zongduo, G., Xiaochuan, S., Zhaohui, H., Yong, J., Xiaodong, Z., and Zhang, J.H. (2010). Matrix metalloproteinase-9 potentiates early brain injury after subarachnoid hemorrhage. Neurol. Res. 32, 715-720.