Protection by DHA of early hippocampal changes in diabetes: Possible role of CREB and NF-κB

Neurochemical Research

Volumn 37, Issue 1, 2012, Pages 105-115

  Alvarez Nölting, Raquel ^a   Arnal, Emma ^b   Barcia, Jorge M ^c   Miranda, Maria ^a   Romero, Francisco J ^b,c  

^a UNIVERSIDAD CEU CARDENAL HERRERA   (Spain)

^b Unidad de Anatomía Patológica   (Spain)

^c UNIVERSIDAD CATÓLICA DE VALENCIA SAN VICENTE MÁRTIR   (Spain)

Author keywords

Brain; Diabetes; Neurogenesis; Oxidation

Indexed keywords

BROXURIDINE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOCOSAHEXAENOIC ACID; GLUCOSE; GLUTATHIONE; GLUTATHIONE PEROXIDASE; HEMOGLOBIN A1C; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; MALONALDEHYDE; PROTEIN P21; STREPTOZOCIN; TRANSCRIPTION FACTOR NRF2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANTIOXIDANT ACTIVITY; ARTICLE; BODY WEIGHT; BRAIN DISEASE; BRAIN HOMOGENATE; BRAIN NERVE CELL; CELL COUNT; CELL PROLIFERATION; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DENTATE GYRUS; DIABETES MELLITUS; DIABETIC ENCEPHALOPATHY; DISEASE MODEL; GLUCOSE BLOOD LEVEL; HEMOGLOBIN BLOOD LEVEL; HIPPOCAMPUS; INSULIN TREATMENT; LATENT PERIOD; LIPID PEROXIDATION; MALE; MAZE TEST; MONOTHERAPY; MORRIS WATER MAZE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; STREPTOZOCIN DIABETES;

ANIMALS; BLOTTING, WESTERN; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DIABETES MELLITUS, EXPERIMENTAL; DOCOSAHEXAENOIC ACIDS; HIPPOCAMPUS; MALE; MAZE LEARNING; NF-KAPPA B; RATS; RATS, WISTAR;

ANIMALIA; RATTUS; RODENTIA;

EID: 84856283076     PISSN: 03643190     EISSN: 15736903     Source Type: Journal    
DOI: 10.1007/s11064-011-0588-x     Document Type: Article

References (49)

1. Ryan CM, Williams TM, Finegold DN, Orchard TJ (1993) Cognitive dysfunction in adults with type 1 (insulin-dependent) diabetes mellitus of long duration: effects of recurrent hypoglycaemia and other chronic complications. Diabetologia 36:329-334 (Pubitemid 23106017)
2. Flood JF, Mooradian AD, Morley JE (1990) Characteristics of learning and memory in streptozotocin-induced diabetic mice. Diabetes 39:1391-1398 (Pubitemid 20372228)
3. Beauquis J, Saravia F, Coulaud J, Roig P, Dardenne M et al (2008) Prominently decreased hippocampal neurogenesis in a spontaneous model of type 1 diabetes, the nonobese diabetic mouse. Exp Neurol 210:359-367
4. Jackson-Guilford J, Leander J, Nisenbaum L (2000) The effect of streptozotocin induced diabetes on cell proliferation in the rat dentate gyrus. Neurosci Lett 293:91-94
5. Zhang WJ, Tan YF, Yue JT, Vranic M, Wojtowicz JM (2008) Impairment of hippocampal neurogenesis in streptozotocin-treated diabetic rats. Acta Neurol Scand 117:205-210 (Pubitemid 351190151)
6. Puchowicz MA, Xu K, Magnes D, Miller C, Lust WD, Kern TS, LaManna JC (2004) Comparison of glucose influx and blood flow in retina and brain of diabetic rats. J Cereb Blood Flow Metab 24:449-457 (Pubitemid 38452236)
7. Shors TJ, Miesegaes G, Baylin A, Zhao M, Rydel TGE (2001) Neurogenesis in the adult is involved in the formation of trace memories. Nature 410:372-376 (Pubitemid 32246054)
8. Makimattila S, Malmberg-Ceder K, Hakkinen AN, Vuori K, Salonen O, Summanen P, Yki-Jarvinen K, Kaste M, Heikkinen S, Lundbom M, Roine RO (2004) Brain metabolic alterations in patients with type 1 diabetes-hyperglycemia- induced injury. J Cereb Blood Flow Metab 24:1393-1399 (Pubitemid 40019162)
9. Kempermann G, Gage FH (1999) New nerve cells for the adult brain. Sci Am 280:48-53
10. Gould E, Deylin A, Tanapat T, Reeves A, Shors TJ (1999) Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265 (Pubitemid 30491297)
11. Herrera DG, Yagüe AG, Johnsen-Soriano S, Bosch-Morell F, Collado-Morente L, Muriach M, Romero FJ, García-Verdugo JM (2003) Selective impairment of hippocampal neurogenesis by chronic alcoholism: protective effects of an antioxidant. Proc Natl Acad Sci USA 100:7919-7924 (Pubitemid 36760070)
12. Biessels GJ, Kamal A, Ramakers GM, Urban IJ, Spruijt BM et al (1996) Place learning and hippocampal synaptic plasticity in streptozotocin-induced diabetic rats. Diabetes 45:1259-1266 (Pubitemid 26296329)
13. Biessels GJ, Kamal A, Urban IJ, Spruijt BM, Erkelens DW et al (1998) Water maze learning and hippocampal synaptic plasticity in streptozotocin- diabetic rats: effects of insulin treatment. Brain Res 800:125-135 (Pubitemid 28361929)
14. Yamada KA, Rensing N, Izumi Y, Erausquin GAD, Gazit V, Dorsey DA, Herrera DG (2004) The effect of streptozotocin-induced diabetes on cell proliferation in the rat dentate gyrus. Pediatr Res 55:372-379 (Pubitemid 38240812)
15. Li Z, Zhang W, Grunberger G, Sima AF (2002) Hippocampal neuronal apoptosis in type 1 diabetes. Brain Res 946:212-231 (Pubitemid 34876334)
16. Pechnick RN, Zonis S, Wawrowsky K, Pourmorady J, Chesnokova V (2008) p21Cip1 restricts neuronal proliferation in the subgranular zone of the dentate gyrus of the hippocampus. Proc Natl Acad Sci USA 105:1358-1363 (Pubitemid 351397058)
17. Hayden MS, Ghosh S (2008) Shared principles in NF-kappaB signaling. Cell 132:344-362 (Pubitemid 351192002)
18. Piette J, Piret B, Bonizzi G, Schoonbroodt S, Merville MP, Legrand-Poels S, Bours V (1997) Multiple redox regulation in NF-kappaB transcription factor activation. Biol Chem 378:1237-1245 (Pubitemid 27507539)
19. Joyce D, Albanese C, Steer J, Fu M, Bouzahzah B, Pestell RG (2001) NF-kappaB and cell-cycle regulation: the cyclin connection. Cytokine Growth Factor Rev 12:73-90 (Pubitemid 32294588)
20. Seitz CS, Deng H, Hinata K, Lin Q, Khavari PA (2000) Nuclear factor kappaB subunits induce epithelial cell growth arrest. Cancer Res 60:4085-4092 (Pubitemid 30636589)
21. Liu GH, Qu J, Shen X (2008) NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK. Biochim Biophys Acta 1783:713-727
22. He C, Qu X, Cui L, Wang J, Kang JX (2009) Improved spatial learning performance of fat-1 mice is associated with enhanced neurogenesis and neuritogenesis by docosahexaenoic acid. Proc Natl Acad Sci USA 106:11370-11375
23. Bazan NG (2005) Neuroprotectin D1 (NPD1): a DHA-derived mediator that protects brain and retina against cell injury-induced oxidative stress. Brain Pathol 15:159-166 (Pubitemid 40546172)
24. Martin RE, Bazan NG (1992) Changing fatty acid content of growth cone lipids prior to synaptogenesis. J Neurochem 59:318-325
25. Birch EE, Garfield S, Hoffman DR, Uauy R, Birch DG (2000) A randomized controlled trial of early dietary supply of long-chain polyunsaturated fatty acids and mental development in term infants. Dev Med Child Neurol 42:174-181 (Pubitemid 30145332)
26. Gamoh S, Hashimoto M, Hossain S, Masumura S (2001) Chronic administration of docosahexaenoic acid improves the performance of radial arm maze task in aged rats. Clin Exp Pharmacol Physiol 28:266-270 (Pubitemid 32250711)
27. Fedorova I, Hussein N, Di Martino C, Moriguchi T, Hoshiba J, Majchrzak S, Salem N Jr. (2007) An n-3 fatty acid deficient diet affects mouse spatial learning in the Barnes circular maze. Prostaglandins Leukot Essent Fatty Acids 77:269-277 (Pubitemid 350198859)
28. Wang TM, Chen CJ, Lee TS, Chao HY, Wu WH, Hsieh SC, Sheu HH, Chiang AN (2011) Docosahexaenoic acid attenuates VCAM-1 expression and NF-κB activation in TNF-α-treated human aortic endothelial cells. Nutr Biochem 22(2):187-194
29. Bazan NG (2006) Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors. Trends Neurosci 29:263-271
30. Mukherjee PK, Marcheselli VL, Serhan CN, Bazan NG (2004) Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc Natl Acad Sci USA 101:8491-8496 (Pubitemid 38736602)
31. Marcheselli VL, Hong S, Lukiw WJ, Tian XH, Gronert K, Musto A, Hardy M, Gimenez JM, Chiang N, Serhan CN, Bazan NG (2003) Novel docosanoids inhibit brain ischemia-reperfusion mediated leukocyte infiltration and pro-inflammatory gene expression. J Biol Chem 278:43807-43817 (Pubitemid 37346009)
32. Richard MJ, Guiraud P, Meo J, Favier A (1992) High performance liquid chromatography separation of malondialdehyde thiobarbituric acid adduct in biological materials (plasma and human cell) using a commercially available reagent. J Chromatogr 577:9-18
33. Romero MJ, Bosch-Morell F, Romero B, Rodrigo JM, Serra MA, Romero FJ (1998) Serum malondialdehyde: possible use for the clinical management of chronic hepatitis C patients. Free Radical Biol Med 25:993-997 (Pubitemid 28558324)
34. Lawrence RA, Parkhill LK, Burk RF (1978) Hepatic cytosolic non-selenium dependent glutathione peroxidase activity: its nature and the effect of selenium deficiency. J Nutr 108:981-987 (Pubitemid 9204050)
35. Reed DJ, Babson JR, Beatty PW, Brodie AE, Ellis WW, Potter DW (1980) High-performance liquid chromatography analysis of nanomole levels of glutathione, glutathione disulfide, and related disulfides. Anal Biochem 106:55-62 (Pubitemid 11246564)
36. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
37. Messier C (2005) Impact of impaired glucose tolerance and type 2 diabetes on cognitive aging. Neurobiol Aging 26:26-30 (Pubitemid 41739421)
38. Stranahan AM, Arumugam TV, Cutler RG, Lee K, Egan JM, Mattson MP (2008) Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons. Nat Neurosci 11:309-317 (Pubitemid 351311802)
39. O'Neill LA, Kaltschmidt C (1997) NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 20:252-258 (Pubitemid 27261456)
40. Mattson MP, Camandola S (2001) NF-kappaB in neuronal plasticity and neurodegenerative disorders. J Clin Invest 107:247-254 (Pubitemid 32162153)
41. Tergaonkar V (2006) NFkappaB pathway: a good signaling paradigm and therapeutic target. Int J Biochem Cell Biol 38:1647-1653 (Pubitemid 43947652)
42. Grilli M, Memo M (1999) Possible role of NF-kappaB and p53 in the glutamate-induced pro-apoptotic neuronal pathway. Cell Div Differ 6:22-27 (Pubitemid 29051851)
43. Packer MA, Stasiv Y, Benraiss A, Chmielnicki E, Grinberg A, Westphal H, Goldman SA, Enikolopov G (2003) Nitric oxide negatively regulates mammalian adult neurogenesis. Proc Natl Acad Sci USA 100:9566-9571 (Pubitemid 37033968)
44. Fujioka T, Fujioka A, Duman RS (2004) Activation of cAMP signaling facilitates the morphological maturation of newborn neurons in adult hippocampus. J Neurosci 24:319-328 (Pubitemid 38112363)
45. Nakagawa S, Kim JE, Lee R, Chen J, Fujioka T, Malberg J, Tsuji S, Duman RS (2002) Localization of phosphorylated cAMP response element-binding protein in immature neurons of adult hippocampus. J Neurosci 22:9868-9876 (Pubitemid 35332871)
46. Nakagawa S, Kim JE, Lee R, Malberg JE, Chen J, Steffen C, Zhang YJ, Nestler EJ, Duman RS (2002) Regulation of neurogenesis in adult mouse hippocampus by cAMP and the cAMP response element-binding protein. J Neurosci 22:3673-3682 (Pubitemid 37465772)
47. Zou J, Crews F (2006) CREB and NF-κB transcription factors regulate densitivity to excitotoxic and oxidative stress induced neuronal cell death. Cell Mol Neurobiol 26:4-6
48. Shenkar R, Yum HK, Arcaroli J, Kupfner J, Abraham E (2001) Interactions between CBP, NF-kappaB, and CREB in the lungs after hemorrhage and endotoxemia. Am J Physiol Lung Cell Mol Physiol 281:L418-L426
49. Wang W, Shinto L, Connor WE, Quinn JF (2008) Biomarkers in Alzheimer's disease: the association between carotenoids, n-3 fatty acids, and dementia severity. J Alzheimer's Dis 13:31-38 (Pubitemid 351365625)