Curcumin attenuates cerebral edema following traumatic brain injury in mice: A possible role for aquaporin-4?

Journal of Neurochemistry

Volumn 113, Issue 3, 2010, Pages 637-648

  Laird, Melissa D ^a   Sukumari Ramesh, Sangeetha ^a   Swift, Andrew E B ^a   Meiler, Steffen E ^a   Vender, John R ^a   Dhandapani, Krishnan M ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

Cellular edema; Controlled cortical impact; Glia; Intracranial pressure; Neuroinflammation; Neurotrauma

Indexed keywords

AQUAPORIN 4; CURCUMIN; GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; TRANSCRIPTION FACTOR RELA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BRAIN EDEMA; BRAIN WATER; CONTROLLED STUDY; DRUG MECHANISM; MALE; MOUSE; NERVE CELL CULTURE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; TRAUMATIC BRAIN INJURY;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; AQUAPORIN 4; BLOTTING, WESTERN; BRAIN EDEMA; BRAIN INJURIES; CELLS, CULTURED; CURCUMIN; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-1BETA; LEARNING; MALE; MEMORY; MICE; MICROSCOPY, CONFOCAL; NF-KAPPA B; RECOGNITION (PSYCHOLOGY); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

MUS;

EID: 77950634233     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06630.x     Document Type: Article

References (76)

1. Aggarwal B. B., Sundaram C., Malani N. Ichikawa H. (2007) Curcumin: the Indian solid gold. Adv. Exp. Med. Biol. 595, 1 75.
2. Aldrich E. F., Eisenberg H. M., Saydjari C., Luerssen T. G., Foulkes M. A., Jane J. A., Marshall L. F., Marmarou A. Young H. F. (1992) Diffuse brain swelling in severely head-injured children. A report from the NIH Traumatic Coma Data Bank. J. Neurosurg. 76, 450 454.
3. Anand P., Kunnumakkara A. B., Newman R. A. Aggarwal B. B. (2007) Bioavailability of curcumin: problems and promises. Mol. Pharm. 4, 807 818.
4. Bae M. K., Kim S. R., Lee H. J. et al. (2006) Aspirin-induced blockade of NF-kappaB activity restrains up-regulation of glial fibrillary acidic protein in human astroglial cells. Biochim. Biophys. Acta 1763, 282 289.
5. Biegon A., Fry P. A., Paden C. M., Alexandrovich A., Tsenter J. Shohami E. (2004) Dynamic changes in N-methyl-d-aspartate receptors after closed head injury in mice: Implications for treatment of neurological and cognitive deficits. Proc. Natl Acad. Sci. USA 101, 5117 5122.
6. Bloch O. Manley G. T. (2007) The role of aquaporin-4 in cerebral water transport and edema. Neurosurg. Focus 22, E3.
7. Borgnia M., Nielsen S., Engel A. Agre P. (1999) Cellular and molecular biology of the aquaporin water channels. Annu. Rev. Biochem. 68, 425 458.
8. Cheng A. L., Hsu C. H., Lin J. K. et al. (2001) Phase I clinical trial of curcumin, a chemopreventive agent, in patients with high-risk or pre-malignant lesions. Anticancer Res. 21, 2895 2900.
9. Chiaretti A., Genovese O., Aloe L., Antonelli A., Piastra M., Polidori G. Di Rocco C. (2005) Interleukin 1beta and interleukin 6 relationship with paediatric head trauma severity and outcome. Childs Nerv. Syst. 21, 185 193. discussion 194.
10. Cole G. M., Teter B. Frautschy S. A. (2007) Neuroprotective effects of curcumin. Adv. Exp. Med. Biol. 595, 197 212.
11. Dempsey R. J., Baskaya M. K. Dogan A. (2000) Attenuation of brain edema, blood-brain barrier breakdown, and injury volume by ifenprodil, a polyamine-site N-methyl-d-aspartate receptor antagonist, after experimental traumatic brain injury in rats. Neurosurgery 47, 399 404 discussion 404-396.
12. Dhillon N., Aggarwal B. B., Newman R. A., Wolff R. A., Kunnumakkara A. B., Abbruzzese J. L., Ng C. S., Badmaev V. Kurzrock R. (2008) Phase II trial of curcumin in patients with advanced pancreatic cancer. Clin. Cancer Res. 14, 4491 4499.
13. Di Giorgio A. M., Hou Y., Zhao X., Zhang B., Lyeth B. G. Russell M. J. (2008) Dimethyl sulfoxide provides neuroprotection in a traumatic brain injury model. Restor. Neurol. Neurosci. 26, 501 507.
14. Dietrich W. D., Truettner J., Zhao W., Alonso O. F., Busto R. Ginsberg M. D. (1999) Sequential changes in glial fibrillary acidic protein and gene expression following parasagittal fluid-percussion brain injury in rats. J. Neurotrauma 16, 567 581.
15. Eisenberg H. M., Gary H. E. Jr., Aldrich E. F., Saydjari C., Turner B., Foulkes M. A., Jane J. A., Marmarou A., Marshall L. F. Young H. F. (1990) Initial CT findings in 753 patients with severe head injury. A report from the NIH Traumatic Coma Data Bank. J. Neurosurg. 73, 688 698. (Pubitemid 20364483)
16. Fan L., Young P. R., Barone F. C., Feuerstein G. Z., Smith D. H. McIntosh T. K. (1995) Experimental brain injury induces expression of interleukin-1 beta mRNA in the rat brain. Brain Res. Mol. Brain Res. 30, 125 130.
17. Garodia P., Ichikawa H., Malani N., Sethi G. Aggarwal B. B. (2007) From ancient medicine to modern medicine: ayurvedic concepts of health and their role in inflammation and cancer. J. Soc. Integr. Oncol. 5, 25 37.
18. Griebenow M., Casalis P., Woiciechowsky C., Majetschak M. Thomale U. W. (2007) Ubiquitin reduces contusion volume after controlled cortical impact injury in rats. J. Neurotrauma 24, 1529 1535.
19. Griffiths M., Neal J. W. Gasque P. (2007) Innate immunity and protective neuroinflammation: new emphasis on the role of neuroimmune regulatory proteins. Int. Rev. Neurobiol. 82, 29 55.
20. Guo Q., Sayeed I., Baronne L. M., Hoffman S. W., Guennoun R. Stein D. G. (2006) Progesterone administration modulates AQP4 expression and edema after traumatic brain injury in male rats. Exp. Neurol. 198, 469 478.
21. Hayakata T., Shiozaki T., Tasaki O. et al. (2004) Changes in CSF S100B and cytokine concentrations in early-phase severe traumatic brain injury. Shock 22, 102 107.
22. Hewett S. J., Silakova J. M. Hewett J. A. (2006) Oral treatment with rofecoxib reduces hippocampal excitotoxic neurodegeneration. J. Pharmacol. Exp. Ther. 319, 1219 1224.
23. Hinkle D. A., Baldwin S. A., Scheff S. W. Wise P. M. (1997) GFAP and S100beta expression in the cortex and hippocampus in response to mild cortical contusion. J. Neurotrauma 14, 729 738.
24. Hu H., Yao H. T., Zhang W. P., Zhang L., Ding W., Zhang S. H., Chen Z. 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.
25. Hutchinson P. J., O'Connell M. T., Rothwell N. J., Hopkins S. J., Nortje J., Carpenter K. L., Timofeev I., Al-Rawi P. G., Menon D. K. Pickard J. D. (2007) Inflammation in human brain injury: intracerebral concentrations of IL-1alpha, IL-1beta, and their endogenous inhibitor IL-1ra. J. Neurotrauma 24, 1545 1557.
26. Ito J., Marmarou A., Barzo P., Fatouros P. Corwin F. (1996) Characterization of edema by diffusion-weighted imaging in experimental traumatic brain injury. J. Neurosurg. 84, 97 103. (Pubitemid 26007003)
27. Ito H., Yamamoto N., Arima H., Hirate H., Morishima T., Umenishi F., Tada T., Asai K., Katsuya H. Sobue K. (2006) Interleukin-1beta induces the expression of aquaporin-4 through a nuclear factor-kappaB pathway in rat astrocytes. J. Neurochem. 99, 107 118.
28. Katayama Y., Tsubokawa T., Miyazaki S., Kawamata T. Yoshino A. (1990) Oedema fluid formation within contused brain tissue as a cause of medically uncontrollable elevation of intracranial pressure: the role of surgical therapy. Acta Neurochir. Suppl. (Wien) 51, 308 310.
29. Khan M. M., Hadman M., Wakade C., De Sevilla L. M., Dhandapani K. M., Mahesh V. B., Vadlamudi R. K. Brann D. W. (2005) Cloning, expression, and localization of MNAR/PELP1 in rodent brain: colocalization in estrogen receptor-alpha- but not in gonadotropin-releasing hormone-positive neurons. Endocrinology 146, 5215 5227.
30. Kiening K. L., van Landeghem F. K., Schreiber S., Thomale U. W., von Deimling A., Unterberg A. W. 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.
31. Kimelberg H. K. (1992) Astrocytic edema in CNS trauma. J. Neurotrauma 9 (Suppl. 1 S71 S81.
32. Kimelberg H. K., Rutledge E., Goderie S. 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.
33. Kleindienst A., Fazzina G., Amorini A. M., Dunbar J. G., Glisson R. Marmarou A. (2006) Modulation of AQP4 expression by the protein kinase C activator, phorbol myristate acetate, decreases ischemia-induced brain edema. Acta Neurochir. Suppl. 96, 393 397.
34. Koch J. D., Miles D. K., Gilley J. A., Yang C. P. Kernie S. G. (2008) Brief exposure to hyperoxia depletes the glial progenitor pool and impairs functional recovery after hypoxic-ischemic brain injury. J. Cereb. Blood Flow Metab. 28, 1294 1306.
35. Laird M. D., Vender J. R. Dhandapani K. M. (2008) Opposing roles for reactive astrocytes following traumatic brain injury. Neurosignals 16, 154 164.
36. Lam A. G., Koppal T., Akama K. T., Guo L., Craft J. M., Samy B., Schavocky J. P., Watterson D. M. Van Eldik L. J. (2001) Mechanism of glial activation by S100B: involvement of the transcription factor NFkappaB. Neurobiol. Aging 22, 765 772.
37. Lazovic J., Basu A., Lin H. W., Rothstein R. P., Krady J. K., Smith M. B. Levison S. W. (2005) Neuroinflammation and both cytotoxic and vasogenic edema are reduced in interleukin-1 type 1 receptor-deficient mice conferring neuroprotection. Stroke 36, 2226 2231.
38. Lee S. C., Dickson D. W. Brosnan C. F. (1995) Interleukin-1, nitric oxide and reactive astrocytes. Brain Behav. Immun. 9, 345 354.
39. Lenzlinger P. M., Morganti-Kossmann M. C., Laurer H. L. McIntosh T. K. (2001) The duality of the inflammatory response to traumatic brain injury. Mol. Neurobiol. 24, 169 181.
40. Levin H. S., Eisenberg H. M., Gary H. E., Marmarou A., Foulkes M. A., Jane J. A., Marshall L. F. Portman S. M. (1991) Intracranial hypertension in relation to memory functioning during the first year after severe head injury. Neurosurgery 28, 196 199 discussion 200.
41. Lim G. P., Chu T., Yang F., Beech W., Frautschy S. A. Cole G. M. (2001) The curry spice curcumin reduces oxidative damage and amyloid pathology in an Alzheimer transgenic mouse. J. Neurosci. 21, 8370 8377.
42. Lin H. W., Basu A., Druckman C., Cicchese M., Krady J. K. Levison S. W. (2006) Astrogliosis is delayed in type 1 interleukin-1 receptor-null mice following a penetrating brain injury. J. Neuroinflamm. 3, 15.
43. Mason J. L., Suzuki K., Chaplin D. D. Matsushima G. K. (2001) Interleukin-1beta promotes repair of the CNS. J. Neurosci. 21, 7046 7052.
44. Miller J. D., Becker D. P., Ward J. D., Sullivan H. G., Adams W. E. Rosner M. J. (1977) Significance of intracranial hypertension in severe head injury. J. Neurosurg. 47, 503 516.
45. Morganti-Kossmann M. C., Rancan M., Stahel P. F. Kossmann T. (2002) Inflammatory response in acute traumatic brain injury: a double-edged sword. Curr. Opin. Crit. Care 8, 101 105.
46. Moynagh P. N. (2005) The interleukin-1 signalling pathway in astrocytes: a key contributor to inflammation in the brain. J. Anat. 207, 265 269.
47. Myer D. J., Gurkoff G. G., Lee S. M., Hovda D. A. Sofroniew M. V. (2006) Essential protective roles of reactive astrocytes in traumatic brain injury. Brain 129, 2761 2772.
48. Nadjar A., Combe C., Laye S., Tridon V., Dantzer R., Amedee T. Parnet P. (2003) Nuclear factor kappaB nuclear translocation as a crucial marker of brain response to interleukin-1. A study in rat and interleukin-1 type I deficient mouse. J. Neurochem. 87, 1024 1036.
49. Nicchia G. P., Nico B., Camassa L. M., Mola M. G., Loh N., Dermietzel R., Spray D. C., Svelto M. Frigeri A. (2004) The role of aquaporin-4 in the blood-brain barrier development and integrity: studies in animal and cell culture models. Neuroscience 129, 935 945.
50. Nielsen S., Nagelhus E. A., Amiry-Moghaddam M., Bourque C., Agre P. Ottersen O. P. (1997) Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 17, 171 180.
51. Nieto-Sampedro M. Berman M. A. (1987) Interleukin-1-like activity in rat brain: sources, targets, and effect of injury. J. Neurosci. Res. 17, 214 219.
52. Nilsson P., Hillered L., Olsson Y., Sheardown M. J. Hansen A. J. (1993) Regional changes in interstitial K+ and Ca2 + levels following cortical compression contusion trauma in rats. J. Cereb. Blood Flow Metab. 13, 183 192.
53. Nonaka M., Chen X. H., Pierce J. E., Leoni M. J., McIntosh T. K., Wolf J. A. Smith D. H. (1999) Prolonged activation of NF-kappaB following traumatic brain injury in rats. J. Neurotrauma 16, 1023 1034.
54. Nortje J. Menon D. K. (2004) Traumatic brain injury: physiology, mechanisms, and outcome. Curr. Opin. Neurol. 17, 711 718.
55. Pan M. H., Huang T. M. Lin J. K. (1999) Biotransformation of curcumin through reduction and glucuronidation in mice. Drug Metab. Dispos. 27, 486 494.
56. Pelinka L. E., Kroepfl A., Leixnering M., Buchinger W., Raabe A. Redl H. (2004a) GFAP versus S100B in serum after traumatic brain injury: relationship to brain damage and outcome. J. Neurotrauma 21, 1553 1561.
57. Pelinka L. E., Kroepfl A., Schmidhammer R., Krenn M., Buchinger W., Redl H. Raabe A. (2004b) Glial fibrillary acidic protein in serum after traumatic brain injury and multiple trauma. J. Trauma 57, 1006 1012.
58. Rajeevan M. S., Ranamukhaarachchi D. G., Vernon S. D. Unger E. R. (2001) Use of real-time quantitative PCR to validate the results of cDNA array and differential display PCR technologies. Methods 25, 443 451.
59. Richardson R. M., Singh A., Sun D., Fillmore H. L., Dietrich D. W. Bullock M. R. (2009) Stem cell biology in traumatic brain injury: effects of injury and strategies for repair. J. Neurosurg. [Epub ahead of print] PMID:19499984.
60. Sanz O., Acarin L., Gonzalez B. Castellano B. (2002) NF-kappaB and IkappaBalpha expression following traumatic brain injury to the immature rat brain. J. Neurosci. Res. 67, 772 780.
61. Sarabia R., Lobato R. D., Rivas J. J., Cordobes F., Rubio J., Cabrera A., Gomez P., Munoz M. J. Madera A. (1988) Cerebral hemisphere swelling in severe head injury patients. Acta Neurochir. Suppl. (Wien) 42, 40 46.
62. Saul T. G. Ducker T. B. (1982) Effect of intracranial pressure monitoring and aggressive treatment on mortality in severe head injury. J. Neurosurg. 56, 498 503.
63. Singh S. Aggarwal B. B. (1995) Activation of transcription factor NF-kappa B is suppressed by curcumin (diferuloylmethane) [corrected]. J. Biol. Chem. 270, 24995 25000.
64. Sinke A. P., Jayakumar A. R., Panickar K. S., Moriyama M., Reddy P. V. Norenberg M. D. (2008) NFkappaB in the mechanism of ammonia-induced astrocyte swelling in culture. J. Neurochem. 106, 2302 2311.
65. Taupin V., Toulmond S., Serrano A., Benavides J. Zavala F. (1993) Increase in IL-6, IL-1 and TNF levels in rat brain following traumatic lesion. Influence of pre- and post-traumatic treatment with Ro5 4864, a peripheral-type (p site) benzodiazepine ligand. J. Neuroimmunol. 42, 177 185.
66. Tehranian R., Andell-Jonsson S., Beni S. M., Yatsiv I., Shohami E., Bartfai T., Lundkvist J. Iverfeldt K. (2002) Improved recovery and delayed cytokine induction after closed head injury in mice with central overexpression of the secreted isoform of the interleukin-1 receptor antagonist. J. Neurotrauma 19, 939 951.
67. Thiyagarajan M. Sharma S. S. (2004) Neuroprotective effect of curcumin in middle cerebral artery occlusion induced focal cerebral ischemia in rats. Life Sci. 74, 969 985.
68. Unterberg A. W., Stover J., Kress B. Kiening K. L. (2004) Edema and brain trauma. Neuroscience 129, 1021 1029.
69. Vallee M., Mayo W., Dellu F., Le Moal M., Simon H. Maccari S. (1997) Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion. J. Neurosci. 17, 2626 2636.
70. Vizuete M. L., Venero J. L., Vargas C., Ilundain A. A., Echevarria M., Machado A. 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.
71. Wakade C., King M. D., Laird M. D., Alleyne Jr. C. H. Dhandapani K. M. (2009) Curcumin Attenuates Vascular Inflammation and Cerebral Vasospasm After Subarachnoid Hemorrhage in Mice. Antioxid. Redox Signal. 11, 35 45.
72. Wakade C., King M. D., Laird M. D., Alleyne C. H. Jr. Dhandapani K. M. (2009) Curcumin attenuates vascular inflammation and cerebral vasospasm after subarachnoid hemorrhage in mice. Antioxid. Redox Signal. 11, 35 45.
73. Wu A., Ying Z. Gomez-Pinilla F. (2006) Dietary curcumin counteracts the outcome of traumatic brain injury on oxidative stress, synaptic plasticity, and cognition. Exp. Neurol. 197, 309 317.
74. Yang B., Zador Z. Verkman A. S. (2008) Glial cell aquaporin-4 overexpression in transgenic mice accelerates cytotoxic brain swelling. J. Biol. Chem. 283, 15280 15286.
75. Zhao J., Zhao Y., Zheng W., Lu Y., Feng G. Yu S. (2008) Neuroprotective effect of curcumin on transient focal cerebral ischemia in rats. Brain Res. 1229, 224 232.
76. Zweckberger K., Eros C., Zimmermann R., Kim S. W., Engel D. Plesnila N. (2006) Effect of early and delayed decompressive craniectomy on secondary brain damage after controlled cortical impact in mice. J. Neurotrauma 23, 1083 1093.