ER Stress and Effects of DHA as an ER Stress Inhibitor

Larner SF, Hayes RL, Wang KK. Unfolded protein response after neurotrauma. J Neurotrauma. 2006;23:807–29.

Kaufman RJ. Stress signaling from the lumen of the endoplasmic reticulum: coordination of gene transcriptional and translational controls. Genes Dev. 1999;13:1211–33.

Yoshida H. ER stress and diseases. FEBS J. 2007;274:630–58.

Buck TM, Wright CM, Brodsky JL. The activities and function of molecular chaperones in the endoplasmic reticulum. Semin Cell Dev Biol. 2007;18:751–61.

Paschen W. Endoplasmic reticulum: a primary target in various acute disorders and degenerative diseases of the brain. Cell Calcium. 2003;34:365–83.

DeGracia DJ, Montie HL. Cerebral ischemia and the unfolded protein response. J Neurochem. 2004;91:1–8.

Wang S, Kaufman RJ. The impact of the unfolded protein response on human disease. J Cell Biol. 2012;197:857–67.

Shen J, Chen X, Hendershot L, Prywes R. ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev Cell. 2002;3:99–111.

Banhegyi G, Baumeister P, Benedetti A, Dong D, Fu Y, Lee AS, Li J, Mao C, Margittai E, Ni M, Paschen W, Piccirella S, Senesi S, Sitia R, Wang M, Yang W (2007) Endoplasmic reticulum stress. Ann N Y Acad Sci 1113:58-71

Lee AH, Iwakoshi NN, Glimcher LH. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol Cell Biol. 2003;23:7448–59.

Schroder M, Kaufman RJ. The mammalian unfolded protein response. Annu Rev Biochem. 2005;74:739–89.

Berridge MJ. The endoplasmic reticulum: a multifunctional signaling organelle. Cell Calcium. 2002;32:235–49.

Rizzuto R, Pozzan T. Microdomains of intracellular Ca2+: molecular determinants and functional consequences. Physiol Rev. 2006;86:369–408.

Brostrom MA, Brostrom CO. Calcium dynamics and endoplasmic reticular function in the regulation of protein synthesis: implications for cell growth and adaptability. Cell Calcium. 2003;34:345–63.

Michalak M, Robert Parker JM, Opas M. Ca2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium. 2002;32:269–78.

Burdakov D, Petersen OH, Verkhratsky A. Intraluminal calcium as a primary regulator of endoplasmic reticulum function. Cell Calcium. 2005;38:303–10.

Wuytack F, Raeymaekers L, Missiaen L. Molecular physiology of the SERCA and SPCA pumps. Cell Calcium. 2002;32:279–305.

Solovyova N, Veselovsky N, Toescu EC, Verkhratsky A. Ca(2+) dynamics in the lumen of the endoplasmic reticulum in sensory neurons: direct visualization of Ca(2+)-induced Ca(2+) release triggered by physiological Ca(2+) entry. EMBO J. 2002;21:622–30.

Mogami H, Tepikin AV, Petersen OH. Termination of cytosolic Ca2+ signals: Ca2+ reuptake into intracellular stores is regulated by the free Ca2+ concentration in the store lumen. EMBO J. 1998;17:435–42.

Papp S, Dziak E, Michalak M, Opas M. Is all of the endoplasmic reticulum created equal? The effects of the heterogeneous distribution of endoplasmic reticulum Ca2+-handling proteins. J Cell Biol. 2003;160:475–9.

Chen X, Kintner DB, Luo J, Baba A, Matsuda T, Sun D. Endoplasmic reticulum Ca2+ dysregulation and endoplasmic reticulum stress following in vitro neuronal ischemia: role of Na+-K+-Cl- cotransporter. J Neurochem. 2008;106:1563–76.

Gorlach A, Klappa P, Kietzmann T. The endoplasmic reticulum: folding, calcium homeostasis, signaling, and redox control. Antioxid Redox Signal. 2006;8:1391–418.

Missiaen L, Robberecht W, van den Bosch L, Callewaert G, Parys JB, Wuytack F, et al. Abnormal intracellular ca(2+)homeostasis and disease. Cell Calcium. 2000;28:1–21.

Lai E, Teodoro T, Volchuk A. Endoplasmic reticulum stress: signaling the unfolded protein response. Physiology (Bethesda). 2007;22:193–201.

Paschen W, Hotop S, Aufenberg C. Loading neurons with BAPTA-AM activates xbp1 processing indicative of induction of endoplasmic reticulum stress. Cell Calcium. 2003;33:83–9.

Bramlett HM, Dietrich WD. Progressive damage after brain and spinal cord injury: pathomechanisms and treatment strategies. Prog Brain Res. 2007;161:125–41.

Stoica BA, Faden AI. Cell death mechanisms and modulation in traumatic brain injury. Neurotherapeutics. 2010;7:3–12.

Greve MW, Zink BJ. Pathophysiology of traumatic brain injury. Mt Sinai J Med. 2009;76:97–104.

Sande A, West C. Traumatic brain injury: a review of pathophysiology and management. J Vet Emerg Crit Care (San Antonio). 2010;20:177–90.

Thorell WE, Leibrock LG, Agrawal SK. Role of RyRs and IP3 receptors after traumatic injury to spinal cord white matter. J Neurotrauma. 2002;19:335–42.

Sun DA, Deshpande LS, Sombati S, Baranova A, Wilson MS, Hamm RJ, et al. Traumatic brain injury causes a long-lasting calcium (Ca2+)-plateau of elevated intracellular Ca levels and altered Ca2+ homeostatic mechanisms in hippocampal neurons surviving brain injury. Eur J Neurosci. 2008;27:1659–72.

Truettner JS, Hu B, Alonso OF, Bramlett HM, Kokame K, Dietrich WD. Subcellular stress response after traumatic brain injury. J Neurotrauma. 2007;24:599–612.

Larner SF, Hayes RL, McKinsey DM, Pike BR, Wang KK. Increased expression and processing of caspase-12 after traumatic brain injury in rats. J Neurochem. 2004;88:78–90.

Oyadomari S, Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 2004;11:381–9.

Krajewska M, Xu L, Xu W, Krajewski S, Kress CL, Cui J, et al. Endoplasmic reticulum protein BI-1 modulates unfolded protein response signaling and protects against stroke and traumatic brain injury. Brain Res. 2011;1370:227–37.

Yao X, Liu J, McCabe JT. Ubiquitin and ubiquitin-conjugated protein expression in the rat cerebral cortex and hippocampus following traumatic brain injury (TBI). Brain Res. 2007;1182:116–22.

Wang Z, Zhang C, Hong Z, Chen H, Chen W, Chen G. C/EBP homologous protein (CHOP) mediates neuronal apoptosis in rats with spinal cord injury. Exp Ther Med. 2013;5:107–11.

Chiribau CB, Gaccioli F, Huang CC, Yuan CL, Hatzoglou M. Molecular symbiosis of CHOP and C/EBP beta isoform LIP contributes to endoplasmic reticulum stress-induced apoptosis. Mol Cell Biol. 2010;30:3722–31.

Valenzuela V, Collyer E, Armentano D, Parsons GB, Court FA, Hetz C. Activation of the unfolded protein response enhances motor recovery after spinal cord injury. Cell Death Dis. 2012;3:e272.

Mahadevan NR, Rodvold J, Sepulveda H, Rossi S, Drew AF, Zanetti M. Transmission of endoplasmic reticulum stress and pro-inflammation from tumor cells to myeloid cells. Proc Natl Acad Sci U S A. 2011;108:6561–6.

Stillwell W, Wassall SR. Docosahexaenoic acid: membrane properties of a unique fatty acid. Chem Phys Lipids. 2003;126:1–27.

Stillwell W, Shaikh SR, Zerouga M, Siddiqui R, Wassall SR. Docosahexaenoic acid affects cell signaling by altering lipid rafts. Reprod Nutr Dev. 2005;45:559–79.

Singh M. Essential fatty acids, DHA and human brain. Indian J Pediatr. 2005;72:239–42.

Marcheselli VL, Hong S, Lukiw WJ, Tian XH, Gronert K, Musto A, et al. Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression. J Biol Chem. 2003;278:43807–17.

Simopoulos AP. The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med (Maywood). 2008;233:674–88.

Anderson EJ, Taylor DA. Stressing the heart of the matter: re-thinking the mechanisms underlying therapeutic effects of n-3 polyunsaturated fatty acids. F1000 Med Rep. 2012;4:13.

Suzuki H, Park SJ, Tamura M, Ando S. Effect of the long-term feeding of dietary lipids on the learning ability, fatty acid composition of brain stem phospholipids and synaptic membrane fluidity in adult mice: a comparison of sardine oil diet with palm oil diet. Mech Ageing Dev. 1998;101:119–28.

Ying Z, Feng C, Agrawal R, Zhuang Y, Gomez-Pinilla F. Dietary omega-3 deficiency from gestation increases spinal cord vulnerability to traumatic brain injury-induced damage. PLoS One. 2012;7:e52998.

Hasadsri L, Wang BH, Lee JV, Erdman JW, Llano DA, Barbey AK, Wszalek T, Sharrock MF, Wang H (2013) Omega-3 fatty acids as a putative treatment for traumatic brain injury. J Neurotrauma 30:897-906

Salem Jr N, Litman B, Kim HY, Gawrisch K. Mechanisms of action of docosahexaenoic acid in the nervous system. Lipids. 2001;36:945–59.

Chalon S, Delion-Vancassel S, Belzung C, Guilloteau D, Leguisquet AM, Besnard JC, et al. Dietary fish oil affects monoaminergic neurotransmission and behavior in rats. J Nutr. 1998;128:2512–9.

Sergeeva M, Strokin M, Reiser G. Regulation of intracellular calcium levels by polyunsaturated fatty acids, arachidonic acid and docosahexaenoic acid, in astrocytes: possible involvement of phospholipase A2. Reprod Nutr Dev. 2005;45:633–46.

Turner N, Else PL, Hulbert AJ. Docosahexaenoic acid (DHA) content of membranes determines molecular activity of the sodium pump: implications for disease states and metabolism. Naturwissenschaften. 2003;90:521–3.

Bourre JM, Francois M, Youyou A, Dumont O, Piciotti M, Pascal G, et al. The effects of dietary alpha-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J Nutr. 1989;119:1880–92.

Mirnikjoo B, Brown SE, Kim HF, Marangell LB, Sweatt JD, Weeber EJ. Protein kinase inhibition by omega-3 fatty acids. J Biol Chem. 2001;276:10888–96.

Seebungkert B, Lynch JW. Effects of polyunsaturated fatty acids on voltage-gated K+ and Na+ channels in rat olfactory receptor neurons. Eur J Neurosci. 2002;16:2085–94.

Vreugdenhil M, Bruehl C, Voskuyl RA, Kang JX, Leaf A, Wadman WJ. Polyunsaturated fatty acids modulate sodium and calcium currents in CA1 neurons. Proc Natl Acad Sci U S A. 1996;93:12559–63.

Sidhu VK, Huang BX, Kim HY. Effects of docosahexaenoic acid on mouse brain synaptic plasma membrane proteome analyzed by mass spectrometry and (16)O/(18)O labeling. J Proteome Res. 2011;10:5472–80.

Yoshida S, Yasuda A, Kawazato H, Sakai K, Shimada T, Takeshita M, et al. Synaptic vesicle ultrastructural changes in the rat hippocampus induced by a combination of alpha-linolenate deficiency and a learning task. J Neurochem. 1997;68:1261–8.

Moriguchi T, Greiner RS, Salem Jr N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J Neurochem. 2000;75:2563–73.

Catalan J, Moriguchi T, Slotnick B, Murthy M, Greiner RS, Salem Jr N. Cognitive deficits in docosahexaenoic acid-deficient rats. Behav Neurosci. 2002;116:1022–31.

Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol. 2009;7:65–74.

Adibhatla RM, Hatcher JF. Role of lipids in brain injury and diseases. Futur Lipidol. 2007;2:403–22.

Shimazawa M, Nakajima Y, Mashima Y, Hara H. Docosahexaenoic acid (DHA) has neuroprotective effects against oxidative stress in retinal ganglion cells. Brain Res. 2009;1251:269–75.

Morgane PJ, Austin-LaFrance R, Bronzino J, Tonkiss J, Diaz-Cintra S, Cintra L, et al. Prenatal malnutrition and development of the brain. Neurosci Biobehav Rev. 1993;17:91–128.

Fedorova I, Hussein N, Di MC, Moriguchi T, Hoshiba J, Majchrzak S, et al. An n-3 fatty acid deficient diet affects mouse spatial learning in the Barnes circular maze. Prostaglandins Leukot Essent Fat Acids. 2007;77:269–77.

Kaur P, Heggland I, Aschner M, Syversen T. Docosahexaenoic acid may act as a neuroprotector for methylmercury-induced neurotoxicity in primary neural cell cultures. Neurotoxicology. 2008;29:978–87.

Mukherjee PK, Marcheselli VL, Serhan CN, Bazan NG. Neuroprotectin D1: a docosahexaenoic acid-derived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc Natl Acad Sci U S A. 2004;101:8491–6.

Bazan NG. The onset of brain injury and neurodegeneration triggers the synthesis of docosanoid neuroprotective signaling. Cell Mol Neurobiol. 2006;26:901–13.

Bazan NG. Omega-3 fatty acids, pro-inflammatory signaling and neuroprotection. Curr Opin Clin Nutr Metab Care. 2007;10:136–41.

King VR, Huang WL, Dyall SC, Curran OE, Priestley JV, Michael-Titus AT. Omega-3 fatty acids improve recovery, whereas omega-6 fatty acids worsen outcome, after spinal cord injury in the adult rat. J Neurosci. 2006;26:4672–80.

Eady TN, Belayev L, Khoutorova L, Atkins KD, Zhang C, Bazan NG. Docosahexaenoic acid signaling modulates cell survival in experimental ischemic stroke penumbra and initiates long-term repair in young and aged rats. PLoS One. 2012;7:e46151.

Eady TN, Khoutorova L, Atkins KD, Bazan NG, Belayev L. Docosahexaenoic acid complexed to human albumin in experimental stroke: neuroprotective efficacy with a wide therapeutic window. Exp Transl Stroke Med. 2012;4:19.

Belayev L, Khoutorova L, Atkins KD, Eady TN, Hong S, Lu Y, et al. Docosahexaenoic acid therapy of experimental ischemic stroke. Transl Stroke Res. 2011;2:33–41.

Serhan CN, Chiang N. Endogenous pro-resolving and anti-inflammatory lipid mediators: a new pharmacologic genus. Br J Pharmacol. 2008;153 Suppl 1:S200–15.

Lukiw WJ, Cui JG, Marcheselli VL, Bodker M, Botkjaer A, Gotlinger K, et al. A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. J Clin Invest. 2005;115:2774–83.

Serhan CN. Lipoxins and aspirin-triggered 15-epi-lipoxin biosynthesis: an update and role in anti-inflammation and pro-resolution. Prostaglandins Other Lipid Mediat. 2002;68–69:433–55.

Arita M, Bianchini F, Aliberti J, Sher A, Chiang N, Hong S, et al. Stereochemical assignment, antiinflammatory properties, and receptor for the omega-3 lipid mediator resolvin E1. J Exp Med. 2005;201:713–22.

Hasturk H, Kantarci A, Ohira T, Arita M, Ebrahimi N, Chiang N, et al. RvE1 protects from local inflammation and osteoclast- mediated bone destruction in periodontitis. FASEB J. 2006;20:401–3.

Hong S, Gronert K, Devchand PR, Moussignac RL, Serhan CN. Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation. J Biol Chem. 2003;278:14677–87.

Litman BJ, Niu SL, Polozova A, Mitchell DC. The role of docosahexaenoic acid containing phospholipids in modulating G protein-coupled signaling pathways: visual transduction. J Mol Neurosci. 2001;16:237–42.

Michalik L, Auwerx J, Berger JP, Chatterjee VK, Glass CK, Gonzalez FJ, et al. International Union of Pharmacology. LXI. Peroxisome proliferator-activated receptors. Pharmacol Rev. 2006;58:726–41.

Zhao G, Etherton TD, Martin KR, Vanden Heuvel JP, Gillies PJ, West SG, et al. Anti-inflammatory effects of polyunsaturated fatty acids in THP-1 cells. Biochem Biophys Res Commun. 2005;336:909–17.

Deckelbaum RJ, Worgall TS, Seo T. n-3 fatty acids and gene expression. Am J Clin Nutr. 2006;83:1520S–5.

Calder PC. Omega-3 fatty acids and inflammatory processes. Nutrients. 2010;2:355–74.

Begum G, Kintner D, Liu Y, Cramer SW, Sun D. DHA inhibits ER Ca2+ release and ER stress in astrocytes following in vitro ischemia. J Neurochem. 2012;120:622–30.

Begum G, Yan HQ, Shi Y, Zhu W, Dixon CE, Sun D (2012) Docosahexaenoic acid reduces ER stress response after traumatic brain injury in rats. Program No. 769.10. 2012 Neuroscience Meeting Planner. New Orleans, LA; Society for Neuroscience. Online.

Begum G, Yan HQ, Li LL, Singh A, Dixon CE, Sun D (2013) DHA reduces ER stress and abnormal protein accumulation and improves neuronal function following traumatic brain injury. To be submitted.