The protein kinase C activator phorbol myristate acetate decreases brain edema by aquaporin 4 downregulation after middle cerebral artery occlusion in the rat

Journal of Neurotrauma

Volumn 27, Issue 2, 2010, Pages 453-461

  Fazzina, Giovanna ^a   Amorini, Angela M ^a   Marmarou, Christina R ^a   Fukui, Shinji ^a   Okuno, Kenji ^a   Dunbar, Jana G ^a   Glisson, Renee ^a   Marmarou, Anthony ^a   Kleindienst, Andrea ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Aquaporin 4; Brain edema; Middle cerebral artery occlusion; Phorbol 12 myristate 13 acetate; Phorbol ester; Rat

Indexed keywords

AQUAPORIN 4; DIMETHYL SULFOXIDE; PHORBOL 13 ACETATE 12 MYRISTATE; POTASSIUM; PROTEIN KINASE C ACTIVATOR; SODIUM; WATER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN BLOOD FLOW; BRAIN EDEMA; BRAIN INFARCTION; BRAIN ISCHEMIA; BRAIN WATER; CONTROLLED STUDY; DENSITOMETRY; DRUG DOSE INCREASE; DRUG EFFECT; IMMUNOBLOTTING; LASER DOPPLER FLOWMETRY; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; POST HOC ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; REPERFUSION; REPERFUSION INJURY; SHAM PROCEDURE; SPRAGUE DAWLEY RAT; UPREGULATION;

ANIMALS; AQUAPORIN 4; BRAIN EDEMA; BRAIN ISCHEMIA; CEREBROVASCULAR CIRCULATION; DOWN-REGULATION; IMMUNOBLOTTING; INFARCTION, MIDDLE CEREBRAL ARTERY; MALE; NEUROPROTECTIVE AGENTS; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; TETRADECANOYLPHORBOL ACETATE;

EID: 77649097640     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2008.0782     Document Type: Article

References (43)

1. Belayev, L., Alonso, O.F., Busto, R., Zhao, W., and Ginsberg, M.D. (1996). Middle cerebral artery occlusion in the rat by intraluminal suture. Neurological and pathological evaluation of an improved model. Stroke 27, 1616-1622; discussion 1623.
2. Chen, Y., and Swanson, R.A. (2003). Astrocytes and brain injury. J. Cereb. Blood Flow Metab. 23, 137-149.
3. Chesnut, R.M., Marshall, L.F., Klauber, M.R., Blunt, B.A., Baldwin, N., Eisenberg, H.M., Jane, J.A., Marmarou, A., and Foulkes, M.A. (1993). The role of secondary brain injury in determining outcome from severe head injury. J. Trauma 34, 216-222. (Pubitemid 23111023)
4. Dijkhuizen, R.M., de Graaf, R.A., Tulleken, K.A., and Nicolay, K. (1999). Changes in the diffusion of water and intracellular metabolites after excitotoxic injury and global ischemia in neonatal rat brain. J. Cereb Blood Flow Metab. 19, 341-349.
5. Fu, X., Li, Q., Feng, Z., and Mu, D. (2007). The roles of aquaporin-4 in brain edema following neonatal hypoxia ischemia and reoxygenation in a cultured rat astrocyte model. Glia 55, 935-941.
6. Gotoh, O., Asano, T., Koide, T., and Takakura, K. (1985). Ischemic brain edema following occlusion of the middle cerebral artery in the rat. I: The time courses of the brain water, sodium and potassium contents and blood-brain barrier permeability to 125I-albumin. Stroke 16, 101-109.
7. Han, Z., Wax, M.B., and Patil, R.V. (1998). Regulation of aquaporin-4 water channels by phorbol ester-dependent protein phosphorylation. J. Biol. Chem. 273, 6001-6004.
8. Han, Z.T., Tong, Y.K., He, L.M., Zhang, Y., Sun, J.Z., Wang, T.Y., Zhang, H., Cui, Y.L., Newmark, H.L., Conney, A.H., and Chang, R.L. (1998). 12-O-Tetradecanoylphorbol-13-acetate (TPA)-induced increase in depressed white blood cell counts in patients treated with cytotoxic cancer chemotherapeutic drugs. Proc. Natl. Acad. Sci. U.S.A. 95, 5362-5365.
9. Hatashita, S., Hoff, J.T., and Salamat, S.M. (1988). Ischemic brain edema and the osmotic gradient between blood and brain. J. Cereb. Blood Flow Metab. 8, 552-559.
10. Hourez, R., Azdad, K., Vanwalleghem, G., Roussel, C., Gall, D., and Schiffmann, S.N. (2005). Activation of protein kinase C and inositol 1,4,5-triphosphate receptors antagonistically modulate voltage-gated sodium channels in striatal neurons. Brain Res. 1059, 189-196.
11. Hu, H., Yao, H.T., Zhang, W.P., Zhang, L., Ding, W., Zhang, S.H., Chen, Z., and Wei, E.Q. (2005). Increased expression of aquaporin-4 in human traumatic brain injury and brain tumors. J. Zhejiang Univ. Sci. B. 6, 33-37.
12. Hussaini, I.M., Karns, L.R., Vinton, G., Carpenter, J.E., Redpath, G.T., Sando, J.J., and VandenBerg, S.R. (2000). Phorbol 12-myristate 13-acetate induces protein kinase ceta-specific proliferative response in astrocytic tumor cells. J. Biol. Chem. 275, 22348-22354.
13. Iannotti, F., and Hoff, J. (1983). Ischemic brain edema with and without reperfusion: an experimental study in gerbils. Stroke 14, 562-567.
14. Ke, C., Poon, W.S., Ng, H.K., Pang, J.C., and Chan, Y. (2001). Heterogeneous responses of aquaporin-4 in oedema formation in a replicated severe traumatic brain injury model in rats. Neurosci. Lett. 301, 21-24.
15. Kiening, K.L., van Landeghem, F.K., Schreiber, S., Thomale, U.W., von Deimling, A., Unterberg, A.W., and Stover, J.F. (2002). Decreased hemispheric aquaporin-4 is linked to evolving brain edema following controlled cortical impact injury in rats. Neurosci. Lett. 324, 105-108.
16. Kimelberg, H.K., Rutledge, E., Goderie, S., and Charniga, C. (1995). Astrocytic swelling due to hypotonic or high K+ medium causes inhibition of glutamate and aspartate uptake and increases their release. J. Cereb. Blood Flow Metab. 15, 409-416.
17. Kleindienst, A., Dunbar, J.G., Glisson, R., Okuno, K., and Marmarou, A. (2006). Effect of dimethyl sulfoxide on blood-brain barrier integrity following middle cerebral artery occlusion in the rat. Acta Neurochir. Suppl. 96, 258-262.
18. Lafuze, J.E., Baker, M.D., Oakes, A.L., and Baehner, R.L. (1987). Comparison of in vivo effects of intravenous infusion of Nformyl-methionyl- leucyl-phenylalanine and phorbol myristate acetate in rabbits. Inflammation 11, 481-488.
19. Loo, D.D., Zeuthen, T., Chandy, G., and Wright, E.M. (1996). Cotransport of water by the Na+=glucose cotransporter. Proc. Natl. Acad. Sci. U.S.A. 93, 13367-13370.
20. Loubinoux, I., Volk, A., Borredon, J., Guirimand, S., Tiffon, B., Seylaz, J., and Meric, P. (1997). Spreading of vasogenic edema and cytotoxic edema assessed by quantitative diffusion and T2 magnetic resonance imaging. Stroke 28, 419-426; discussion 426-1417
21. Lu, H., and Sun, S.Q. (2003). A correlative study between AQP4 expression and the manifestation of DWI after the acute ischemic brain edema in rats. Chin. Med. J. (Engl.) 116, 1063-1069.
22. Madrid, R., Le Maout, S., Barrault, M.B., Janvier, K., Benichou, S., and Merot, J. (2001). Polarized trafficking and surface expression of the AQP4 water channel are coordinated by serial and regulated interactions with different clathrin-adaptor complexes. EMBO J. 20, 7008-7021.
23. Manabe, S., Lin, Y.C., Takaoka, M., Yamoto, T., Yanai, T., Yamashita, K., Tarumi, C., Matsunuma, N., and Masuda, H. (1992). Species difference in susceptibility to phorbol myristate acetate-induced leukopenia and lung injury: rat vs. dog. J. Toxicol. Sci. 17, 211-223.
24. Manley, G.T., Fujimura, M., Ma, T., Noshita, N., Filiz, F., Bollen, A.W., Chan, P., and Verkman, A.S. (2000). Aquaporin-4 deletion in mice reduces brain edema after acute water intoxication and ischemic stroke. Nat. Med. 6, 159-163.
25. Marmarou, A., Fatouros, P.P., Barzo, P., Portella, G., Yoshihara, M., Tsuji, O., Yamamoto, T., Laine, F., Signoretti, S., Ward, J.D., Bullock, M.R., and Young, H.F. (2000). Contribution of edema and cerebral blood volume to traumatic brain swelling in head-injured patients. J. Neurosurg. 93, 183-193.
26. Meng, S., Qiao, M., Lin, L., Del Bigio, M.R., Tomanek, B., and Tuor, U.I. (2004). Correspondence of AQP4 expression and hypoxic-ischaemic brain oedema monitored by magnetic resonance imaging in the immature and juvenile rat. Eur. J. Neurosci. 19, 2261-2269.
27. Mosior, M., and Newton, A.C. (1995). Mechanism of interaction of protein kinase C with phorbol esters. Reversibility and nature of membrane association. J. Biol. Chem. 270, 25526-25533.
28. Nakahama, K., Nagano, M., Fujioka, A., Shinoda, K., and Sasaki, H. (1999). Effect of TPA on aquaporin 4 mRNA expression in cultured rat astrocytes. Glia 25, 240-246.
29. Neely, J.D., Christensen, B.M., Nielsen, S., and Agre, P. (1999). Heterotetrameric composition of aquaporin-4 water channels. Biochemistry 38, 11156-11163.
30. Neumann-Haefelin, T., Kastrup, A., de Crespigny, A., Yenari, M.A., Ringer, T., Sun, G.H., and Moseley, M.E. (2000). Serial MRI after transient focal cerebral ischemia in rats: dynamics of tissue injury, blood-brain barrier damage, and edema formation. Stroke 31, 1965-1972; discussion 1972-11963
31. O'Flaherty, J.T., Cousart, S., Lineberger, A.S., Bond, E., Bass, D.A., DeChatelet, L.R., Leake, E.S., and McCallm, C.E. (1980). Phorbol myristate acetate: in vivo effects upon neutrophils, platelets, and lung. Am. J. Pathol. 101, 79-92.
32. Ribeiro Mde, C., Hirt, L., Bogousslavsky, J., Regli, L., and Badaut, J. (2006). Time course of aquaporin expression after transient focal cerebral ischemia in mice. J. Neurosci. Res. 83, 1231-1240.
33. Sato, S., Umenishi, F., Inamasu, G., Sato, M., Ishikawa, M., Nishizawa, M., and Oizumi, T. (2000). Expression of water channel mRNA following cerebral ischemia. Acta Neurochir. Suppl. 76, 239-241.
34. Strair, R.K., Schaar, D., Goodell, L., Aisner, J., Chin, K.V., Eid, J., Senzon, R., Cui, X.X., Han, Z.T., Knox, B., Rabson, A.B., Chang, R., and Conney, A. (2002). Administration of a phorbol ester to patients with hematological malignancies: preliminary results from a phase I clinical trial of 12-O-tetradecanoylphorbol-13-acetate. Clin. Cancer Res. 8, 2512-2518.
35. Sun, M.C., Honey, C.R., Berk, C., Wong, N.L., and Tsui, J.K. (2003). Regulation of aquaporin-4 in a traumatic brain injury model in rats. J. Neurosurg. 98, 565-569.
36. Taniguchi, M., Yamashita, T., Kumura, E., Tamatani, M., Kobayashi, A., Yokawa, T., Maruno, M., Kato, A., Ohnishi, T., Kohmura, E., Tohyama, M., and Yoshimine, T. (2000). Induction of aquaporin-4 water channel mRNA after focal cerebral ischemia in rat. Brain Res. Mol. Brain Res. 78, 131-137.
37. Taylor, R.G., McCall, C.E., Thrall, R.S., Woodruff, R.D., and O'Flaherty, J.T. (1985). Histopathologic features of phorbol myristate acetate-induced lung injury. Lab. Invest. 52, 61-70.
38. Venero, J.L., Vizuete, M.L., Ilundain, A.A., Machado, A., Echevarria, M., and Cano, J. (1999). Detailed localization of aquaporin-4 messenger RNA in the CNS: preferential expression in periventricular organs. Neuroscience 94, 239-250.
39. Vizuete, M.L., Venero, J.L., Vargas, C., Ilundain, A.A., Echevarria, M., Machado, A., and Cano, J. (1999). Differential upregulation of aquaporin-4 mRNA expression in reactive astrocytes after brain injury: potential role in brain edema. Neurobiol. Dis. 6, 245-258.
40. Won, J.S., Song, D.K., Kim, Y.H., Huh, S.O., and Suh, H.W. (1998). The stimulation of rat astrocytes with phorbol-12-myristate-13-acetate increases the proenkephalin mRNA: involvement of proto-oncogenes. Brain Res. Mol. Brain Res. 54, 288-297.
41. Wright, E.M., and Loo, D.D. (2000). Coupling between Na+, sugar, and water transport across the intestine. Ann. N.Y. Acad. Sci. 915, 54-66.
42. Yamamoto, N., Sobue, K., Miyachi, T., Inagaki, M., Miura, Y., Katsuya, H., and Asai, K. (2001). Differential regulation of aquaporin expression in astrocytes by protein kinase C. Brain Res. Mol. Brain Res. 95, 110-116.
43. Yang, G.Y., and Betz, A.L. (1994). Reperfusion-induced injury to the blood-brain barrier after middle cerebral artery occlusion in rats. Stroke 25, 1658-1664; discussion 1664-11655