Endoplasmic Reticulum Stress Interacts With Inflammation in Human Diseases

Journal of Cellular Physiology

Volumn 231, Issue 2, 2016, Pages 288-294

  Cao, Stewart Siyan ^a   Luo, Katherine L ^a   Shi, Lynn ^a  

^a Columbia University College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 PHENYLBUTYRIC ACID; ACTIVATING TRANSCRIPTION FACTOR 6; ACTIVATING TRANSCRIPTION FACTOR 6ALPHA; ALKALINE PROTEINASE; BASIC LEUCINE ZIPPER TRANSCRIPTION FACTOR; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALRETICULIN; DEATH RECEPTOR 5; ELASTASE; GLUCOSE REGULATED PROTEIN 78; GLYCOPROTEIN GP 96; INITIATION FACTOR 2ALPHA; INOSITOL REQUIRING KINASE 1ALPHA; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 6; JANUS KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHOLIPID; PROTEIN BCL 2; PROTEIN IRE1; PYOCYANINE; STAT3 PROTEIN; TAUROURSODEOXYCHOLIC ACID; THIOREDOXIN INTERACTING PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; UNCLASSIFIED DRUG; UNINDEXED DRUG; X BOX BINDING PROTEIN 1;

AMYOTROPHIC LATERAL SCLEROSIS; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTHRITIS; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR STRESS RESPONSE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CYSTIC FIBROSIS; CYTOLOGY; DEGENERATIVE DISEASE; DISEASES; ENDOCYTOSIS; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; HUMAN; INFECTION; INFLAMMATION; INTESTINE EPITHELIUM CELL; INTRACELLULAR SIGNALING; LUPUS ERYTHEMATOSUS NEPHRITIS; METABOLIC DISORDER; MOTONEURON; MULTIPLE SCLEROSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OXIDATIVE STRESS; PHOSPHOLIPID SYNTHESIS; PHYSIOLOGICAL PROCESS; PRIMARY BILIARY CIRRHOSIS; PRIORITY JOURNAL; PSEUDOMONAS INFECTION; REVIEW; SALMONELLOSIS; SEDENTARY LIFESTYLE; SYSTEMIC LUPUS ERYTHEMATOSUS; UNFOLDED PROTEIN RESPONSE; VIRUS MYOCARDITIS; AUTOIMMUNITY; NEUROLOGIC DISEASE; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

APOPTOSIS; AUTOIMMUNITY; ENDOPLASMIC RETICULUM STRESS; HOMEOSTASIS; HUMANS; INFECTION; INFLAMMATION; METABOLIC DISEASES; NERVOUS SYSTEM DISEASES; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE;

EID: 84944916392     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25098     Document Type: Review

References (100)

1. Abderrazak A, Syrovets T, Couchie D, El Hadri K, Friguet B, Simmet T, Rouis M. 2015. NLRP3 inflammasome: From a danger signal sensor to a regulatory node of oxidative stress and inflammatory diseases. Redox Biol 4:296-307.
2. Arisato T, Okubo R, Arata H, Abe K, Fukada K, Sakoda S, Shimizu A, Qin XH, Izumo S, Osame M, Nakagawa M. 2003. Clinical and pathological studies of familial amyotrophic lateral sclerosis (FALS) with SOD1 H46R mutation in large Japanese families. Acta Neuropathol 106:561-568.
3. Atkin JD, Farg MA, Walker AK, McLean C, Tomas D, Horne MK. 2008. Endoplasmic reticulum stress and induction of the unfolded protein response in human sporadic amyotrophic lateral sclerosis. Neurobiol Dis 30:400-407.
4. Benner EJ, Banerjee R, Reynolds AD, Sherman S, Pisarev VM, Tsiperson V, Nemachek C, Ciborowski P, Przedborski S, Mosley RL, Gendelman HE. 2008. Nitrated alpha-synuclein immunity accelerates degeneration of nigral dopaminergic neurons. PLos ONE 3:e1376. doi: 10.1371/journal.pone.0001376
5. Bodman-Smith MD, Fife MF, Wythe H, Corrigal VM, Panayi GS, Wedderburn LR, Woo P. 2004. Anti-BiP antibody levels in juvenile idiopathic arthritis (JIA). Rheumatology 43:1305-1306.
6. Borchelt DR, Lee MK, Slunt HS, Guarnieri M, Xu ZS, Wong PC, Brown RH, Jr., Price DL, Sisodia SS, Cleveland DW. 1994. Superoxide dismutase 1 with mutations linked to familial amyotrophic lateral sclerosis possesses significant activity. Proc Natl Acad Sci USA 91:8292-8296.
7. Byrne S, Walsh C, Lynch C, Bede P, Elamin M, Kenna K, McLaughlin R, Hardiman O. 2011. Rate of familial amyotrophic lateral sclerosis: A systematic review and meta-analysis. J Neurol Neurosurg Psychiatry 82:623-627.
8. Cao SS, Kaufman RJ. 2012. Unfolded protein response. Curr Biol 22:R622-R626.
9. Cao SS, Kaufman RJ. 2013a. PKR in DSS-induced colitis: A matter of genetic background and maternal microflora? Inflamm Bowel Dis 19:E49-E50.
10. Cao SS, Kaufman RJ. 2013b. Targeting endoplasmic reticulum stress in metabolic disease. Expert Opin Ther Targets 17:437-448.
11. Cao SS, Kaufman RJ. 2014. Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid Redox Signal 21:396-413.
12. Cao SS, Wang M, Harrington JC, Chuang BM, Eckmann L, Kaufman RJ. 2014. Phosphorylation of eIF2a is dispensable for differentiation but required at a posttranscriptional level for paneth cell function and intestinal homeostasis in mice. Inflamm Bowel Dis 20:712-722.
13. Cao SS, Zimmermann EM, Chuang BM, Song B, Nwokoye A, Wilkinson JE, Eaton KA, Kaufman RJ. 2013. The unfolded protein response and chemical chaperones reduce protein misfolding and colitis in mice. Gastroenterology 144:989-1000 e1006.
14. Castano A, Herrera AJ, Cano J, Machado A. 1998. Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J Neurochem 70:1584-1592.
15. Chan C-P, Siu K-L, Chin K-T, Yuen K-Y, Zheng B, Jin D-Y. 2006. Modulation of the unfolded protein response by the severe acute respiratory syndrome coronavirus spike protein. J Virol 80:9279-9287.
16. Conn KJ, Gao WW, McKee A, Lan MS, Ullman MD, Eisenhauer PB, Fine RE, Wells JM. 2004. Identification of the protein disulfide isomerase family member PDIp in experimental Parkinson's disease and Lewy body pathology. Brain Res 1022:164-172.
17. Cooper AA, Gitler AD, Cashikar A, Haynes CM, Hill KJ, Bhullar B, Liu KN, Xu KX, Strathearn KE, Liu F, Cao SS, Caldwell KA, Caldwell GA, Marsischky G, Kolodner RD, LaBaer J, Rochet JC, Bonini NM, Lindquist S. 2006. Alpha-synuclein blocks ER-Golgi traffic and Rab1 rescues neuron loss in Parkinson's models. Science 313:324-328.
18. de L'Etang AF, Maharjan N, Brana MC, Ruegsegger C, Rehmann R, Goswami A, Roos A, Troost D, Schneider BL, Weis J, Saxena S. 2015. Marinesco-Sjogren syndrome protein SIL1 regulates motor neuron subtype-selective ER stress in ALS. Nat Neurosci 18:227-238.
19. Deng HX, Hentati A, Tainer JA, Iqbal Z, Cayabyab A, Hung WY, Getzoff ED, Hu P, Herzfeldt B, Roos RP, Warner C, Deng G, Soriano E, Smyth C, Parge HE, Ahmed A, Roses AD, Hallewell RA, Pericak-Vance MA, Siddique T. 1993. Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase. Science 261:1047-1051.
20. Donath MY, Ehses JA, Maedler K, Schumann DM, Ellingsgaard H, Eppler E, Reinecke M. 2005. Mechanisms of beta-cell death in type 2 diabetes. Diabetes 54:S108-S113.
21. Drachman DB, Frank K, Dykes-Hoberg M, Teismann P, Almer G, Przedborski S, Rothstein JD. 2002. Cyclooxygenase 2 inhibition protects motor neurons and prolongs survival in a transgenic mouse model of ALS. Ann Neurol 52:771-778.
22. Drori A, Messerle M, Brune W, Tirosh B. 2014. Lack of XBP-1 impedes murine cytomegalovirus gene expression. PLos ONE 9: e110942. doi: 10.1371/journal.pone.0110942
23. Dumont AO, Goursaud S, Desmet N, Hermans E. 2014. Differential regulation of glutamate transporter subtypes by pro-inflammatory cytokine TNF-alpha in cortical astrocytes from a rat model of amyotrophic lateral sclerosis. PLos ONE 9:8.
24. Eggleton P, Ward FJ, Johnson S, Khamashta MA, Hughes GRV, Hajela VA, Michalak M, Corbett EF, Staines NA, Reid KBM. 2000. Fine specificity of autoantibodies to calreticulin: Epitope mapping and characterization. Clin Exp Immunol 120:384-391.
25. Fung TS, Liao Y, Liu DX. 2014. The endoplasmic reticulum stress sensor IRE1 alpha protects cells from apoptosis induced by the coronavirus infectious bronchitis virus. J Virol 88:12752-12764.
26. Goeb V, Thomas-L'Otellier M, Daveau R, Charlionet R, Fardellone P, Le Loet X, Tron F, Gilbert D, Vittecoq O. 2009. Candidate autoantigens identified by mass spectrometry in early rheumatoid arthritis are chaperones and citrullinated glycolytic enzymes. Arthritis Res Ther 11:R38. doi: 10.1186/ar2644
27. Goldknopf IL, Sheta EA, Bryson J, Folsom B, Wilson C, Duty J, Yen AA, Appel SH. 2006. Complement C3c and related protein biomarkers in amyotrophic lateral sclerosis and Parkinson's disease. Biochem Biophys Res Commun 342:1034-1039.
28. Guegn C, Vila M, Rosoklija G, Hays AP, Przedborski S. 2001. Recruitment of the mitochondrial-dependent apoptotic pathway in amyotrophic lateral sclerosis. J Neurosci 21:6569-6576.
29. Hasnain SZ, Borg DJ, Harcourt BE, Tong H, Sheng YHH, Ng CP, Das I, Wang R, Chen ACH, Loudovaris T, Kay TW, Thomas HE, Whitehead JP, Forbes JM, Prins JB, McGuckin MA. 2014. Glycemic control in diabetes is restored by therapeutic manipulation of cytokines that regulate beta cell stress. Nat Med 20:1417-1426.
30. Hetz C. 2012. The unfolded protein response: Controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13:89-102.
31. Hetz C, Thielen P, Matus S, Nassif M, Court F, Kiffin R, Martinez G, Cuervo AM, Brown RH, Glimcher LH. 2009. XBP-1 deficiency in the nervous system protects against amyotrophic lateral sclerosis by increasing autophagy. Genes Dev 23:2294-2306.
32. Hirabayashi Y, Oka Y, Ikeda T, Fujii H, Ishii T, Sasaki T, Harigae H. 2010. The endoplasmic reticulum stress-inducible protein, Herp, is a potential triggering antigen for anti-DNA response. J Immunol 184:3276-3283.
33. Hirsch EC, Vyas S, Hunot S. 2012. Neuroinflammation in Parkinson's disease. Parkinsonism Relat Disord 18:S210-S212.
34. Hunter RL, Dragicevic N, Seifert K, Choi DY, Liu M, Kim HC, Cass WA, Sullivan PG, Bing GY. 2007. Inflammation induces mitochondrial dysfunction and dopaminergic neurodegeneration in the nigrostriatal system. J Neurochem 100:1375-1386.
35. Hussien Y, Cavener DR, Popko B. 2014. Genetic inactivation of PERK signaling in mouse oligodendrocytes: Normal developmental myelination with increased susceptibility to inflammatory demyelination. Glia 62:680-691.
36. Imai Y, Soda M, Takahashi R. 2000. Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J Biol Chem 275:35661-35664.
37. Inacio P, Zuzarte-Luis V, Ruivo MT, Falkard B, Nagaraj N, Rooijers K, Mann M, Mair G, Fidock DA, Mota MM. 2015. Parasite-induced ER stress response in hepatocytes facilitates Plasmodium liver stage infection. EMBO Rep pii: e201439979. [Epub ahead of print].
38. Inoue H, Tsukita K, Iwasato T, Suzuki Y, Tomioka M, Tateno M, Nagao M, Kawata A, Saido TC, Miura M, Misawa H, Itohara S, Takahashi R. 2003. The crucial role of caspase-9 in the disease progression of a transgenic ALS mouse model. EMBO J 22:6665-6674.
39. Italiani P, Carlesi C, Giungato P, Puxeddu I, Borroni B, Bossu P, Migliorini P, Siciliano G, Boraschi D. 2014. Evaluating the levels of interleukin-1 family cytokines in sporadic amyotrophic lateral sclerosis. J Neuroinflammation 11:94. doi: 10.1186/1742-2094-11-94
40. Kaser A, Lee A-H, Franke A, Glickman JN, Zeissig S, Tilg H, Nieuwenhuis EES, Higgins DE, Schreiber S, Glimcher LH, Blumberg RS. 2008. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease. Cell 134:743-756.
41. Kaser A, Martinez-Naves E, Blumberg RS. 2010. Endoplasmic reticulum stress: Implications for inflammatory bowel disease pathogenesis. Curr Opin Gastroenterol 26:318-326.
42. Kieran D, Woods I, Villunger A, Strasser A, Prehn JHM. 2007. Deletion of the BH3-only protein puma protects motoneurons from ER stress-induced apoptosis and delays motoneuron loss in ALS mice. Proc Natl Acad Sci USA 104:20606-20611.
43. Kikuchi H, Almer G, Yamashita S, Guegan C, Nagai M, Xu ZS, Sosunov AA, McKhann GM, Przedborski S. 2006. Spinal cord endoplasmic reticulum stress associated with a microsomal accumulation of mutant superoxide dismutase-1 in an ALS model. Proc Natl Acad Sci USA 103:6025-6030.
44. Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS. 2000. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: Role of microglia. J Neurosci 20:6309-6316.
45. Kohl S, Zobor D, Chiang WC, Weisschuh N, Staller J, Menendez IG, Chang S, Beck SC, Garcia Garrido M, Sothilingam V, Seeliger MW, Stanzial F, Benedicenti F, Inzana F, Heon E, Vincent A, Beis J, Strom TM, Rudolph G, Roosing S, Hollander AI, Cremers FP, Lopez I, Ren H, Moore AT, Webster AR, Michaelides M, Koenekoop RK, Zrenner E, Kaufman RJ, Tsang SH, Wissinger B, Lin JH. 2015. Mutations in the unfolded protein response regulator ATF6 cause the cone dysfunction disorder achromatopsia. Nat Genet 47:757-765.
46. Komurasaki R, Imaoka S, Tada N, Okada K, Nishiguchi S, Funae Y. 2010. LKM-1 sera from autoimmune hepatitis patients that recognize ERp57, carboxylesterase 1 and CYP2 D6. Drug Metab Pharmacokinet 25:84-92.
47. Kostic V, Jackson-Lewis V, de Bilbao F, Dubois-Dauphin M, Przedborski S. 1997. Bcl-2: Prolonging life in a transgenic mouse model of familial amyotrophic lateral sclerosis. Science 277:559-562.
48. Kreisel W, Siegel A, Bahler A, Spamer C, Schiltz E, Kist M, Seilnacht G, Klein R, Berg PA, Heilmann C. 1999. High prevalence of antibodies to calreticulin of the IgA class in primary biliary cirrhosis: A possible role of gut-derived bacterial antigens in its aetiology? Scand J Gastroenterol 34:623-628.
49. Lee W-S, Sung M-S, Lee E-G, Yoo H-G, Cheon Y-H, Chae H-J, Yoo W-H. 2015. A pathogenic role for ER stress-induced autophagy and ER chaperone GRP78/BiP in T lymphocyte systemic lupus erythematosus. J Leukoc Biol 97:425-433.
50. Lencer WI, DeLuca H, Grey MJ, Cho JA. 2015. Innate immunity at mucosal surfaces: The IRE1-RIDD-RIG-I pathway. Trends Immunol 36:401-409.
51. Lenna S, Farina AG, Martyanov V, Christmann RB, Wood TA, Farber HW, Scorza R, Whitfield ML, Lafyatis R, Trojanowska M. 2013. Increased expression of endoplasmic reticulum stress and unfolded protein response genes in peripheral blood mononuclear cells from patients with limited cutaneous systemic sclerosis and pulmonary arterial hypertension. Arthritis Rheum 65:1357-1366.
52. Lin WS, Lin YF, Li J, Fenstermaker AG, Way SW, Clayton B, Jamison S, Harding HP, Ron D, Popko B. 2013. Oligodendrocyte-specific activation of PERK signaling protects mice against experimental autoimmune encephalomyelitis. J Neurosci 33:5980-5991.
53. Ling S, Cline EN, Haug TS, Fox DA, Holoshitz J. 2013. Citrullinated calreticulin potentiates rheumatoid arthritis shared epitope signaling. Arthritis Rheum 65:618-626.
54. Ling S, Lai A, Borschukova O, Pumpens P, Holoshitz J. 2006. Activation of nitric oxide signaling by the rheumatoid arthritis shared epitope. Arthritis Rheum 54:3423-3432.
55. Liu YC, Fallon L, Lashuel HA, Liu ZH, Lansbury PT. 2002. The UCH-L1 gene encodes two opposing enzymatic activities that affect alpha-synuclein degradation and Parkinson's disease susceptibility. Cell 111:209-218.
56. Lu M, Lawrence DA, Marsters S, Acosta-Alvear D, Kimmig P, Mendez AS, Paton AW, Paton JC, Walter P, Ashkenazi A. 2014. Cell death. Opposing unfolded-protein-response signals converge on death receptor 5 to control apoptosis. Science 345:98-101.
57. Luo K, Cao SS. 2015. Endoplasmic reticulum stress in intestinal epithelial cell function and inflammatory bowel disease. Gastroenterol Res Pract 2015:328791.
58. Meares GP, Liu Y, Rajbhandari R, Qin H, Nozell SE, Mobley JA, Corbett JA, Benveniste EN. 2014. PERK-dependent activation of JAK1 and STAT3 contributes to endoplasmic reticulum stress-induced inflammation. Mol Cell Biol 34:3911-3925.
59. Montane J, Cadavez L, Novials A. 2014. Stress and the inflammatory process: A major cause of pancreatic cell death in type 2 diabetes. Diabetes Metab Syndr Obes 7:25-34.
60. Nagayama S, Yokoi T, Tanaka H, Kawaguchi Y, Shirasaka T, Kamataki T. 1994. Occurrence of autoantibody to protein disulfide isomerase in patients with hepatic disorder. J Toxicol Sci 19:163-169.
61. Nishitoh H, Kadowaki H, Nagai A, Maruyama T, Yokota T, Fukutomi H, Noguchi T, Matsuzawa A, Takeda K, Ichijo H. 2008. ALS-linked mutant SOD1 induces ER stress- and ASK1-dependent motor neuron death by targeting Derlin-1. Genes Dev 22:1451-1464.
62. Oslowski CM, Hara T, O'Sullivan-Murphy B, Kanekura K, Lu SM, Hara M, Ishigaki S, Zhu LHJ, Hayashi E, Hui ST, Greiner D, Kaufman RJ, Bortell R, Urano F. 2012. Thioredoxin-interacting protein mediates ER stress-induced beta cell death through initiation of the inflammasome. Cell Metab 16:265-273.
63. Pasinelli P, Houseweart MK, Brown RH, Jr., Cleveland DW. 2000. Caspase-1 and -3 are sequentially activated in motor neuron death in Cu, Zn superoxide dismutase-mediated familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 97:13901-13906.
64. Petrova PS, Raibekas A, Pevsner J, Vigo N, Anafi M, Moore MK, Peaire AE, Shridhar V, Smith DI, Kelly J, Durocher Y, Commissiong JW. 2003. MANF-A new mesencephalic, astrocyte-derived neurotrophic factor with selectivity for dopaminergic neurons. J Mol Neurosci 20:173-187.
65. Reed M, Morris SH, Owczarczyk AB, Lukacs NW. 2015. Deficiency of autophagy protein Map1-LC3b mediates IL-17-dependent lung pathology during respiratory viral infection via ER stress-associated IL-1. Mucosal Immunol. doi: 10.1038/mi.2015.3. [Epub ahead of print].
66. Reynolds AD, Kadiu I, Garg SK, Glanzer JG, Nordgren T, Ciborowski P, Banerjee R, Gendelman HE. 2008. Nitrated alpha-synuclein and microglial neuroregulatory activities. J Neuroimmune Pharmacol 3:59-74.
67. Ropelle ER, Flores MB, Cintra DE, Rocha GZ, Pauli JR, Morari J, de Souza CT, Moraes JC, Prada PO, Guadagnini D, Marin RM, Oliveira AG, Augusto TM, Carvalho HF, Velloso LA, Saad MJA, Carvalheira JBC. 2010. IL-6 and IL-10 anti-inflammatory activity links exercise to hypothalamic insulin and leptin sensitivity through IKK beta and ER stress inhibition. PLoS Biol 8:e1000465. doi: 10.1371/journal.pbio.1000465
68. Salvado L, Barroso E, Gomez-Foix AM, Palomer X, Michalik L, Wahli W, Vazquez-Carrera M. 2014. PPAR beta/delta prevents endoplasmic reticulum stress-associated inflammation and insulin resistance in skeletal muscle cells through an AMPK-dependent mechanism. Diabetologia 57:2126-2135.
69. Sasaki M, Miyakoshi M, Sato Y, Nakanuma Y. 2014. A possible involvement of endoplasmic reticulum stress in the process of biliary epithelial autophagy and senescence in primary biliary cirrhosis. Hepatology 60:350A-350A.
70. Saxena S, Cabuy E, Caroni P. 2009. A role for motoneuron subtype-selective ER stress in disease manifestations of FALS mice. Nat Neurosci 12:627-636.
71. Schaffler A, Scholmerich J. 2010. Innate immunity and adipose tissue biology. Trends Immunol 31:228-235.
72. Simpson EP, Henry YK, Henkel JS, Smith RG, Appel SH. 2004. Increased lipid peroxidation in sera of ALS patients-A potential biomarker of disease burden. Neurology 62:1758-1765.
73. Siyan S, Song BB, Kaufman RJ. 2012. PKR protects colonic epithelium against colitis through the unfolded protein response and prosurvival signaling. Inflamm Bowel Dis 18:1735-1742.
74. Srivastava P. 2002. Interaction of heat shock proteins with peptides and antigen presenting cells: Chaperoning of the innate and adaptive immune responses. Ann Rev Immunol 20:395-425.
75. Tabas I, Ron D. 2011. Integrating the mechanisms of apoptosis induced by endoplasmic reticulum stress. Nat Cell Biol 13:184-190.
76. Tamura Y, Hirohashi Y, Kutomi G, Nakanishi K, Kamiguchi K, Torigoe T, Sato N. 2011. Tumor-produced secreted form of binding of immunoglobulin protein elicits antigen-specific tumor immunity. J Immunol 186:4325-4330.
77. Tarr JM, Winyard PG, Ryan B, Harries LW, Haigh R, Viner N, Eggleton P. 2010. Extracellular calreticulin is present in the joints of patients with rheumatoid arthritis and inhibits FasL (CD95L)-mediated apoptosis of T cells. Arthritis Rheum 62:2919-2929.
78. Timmins JM, Ozcan L, Seimon TA, Li G, Malagelada C, Backs J, Backs T, Bassel-Duby R, Olson EN, Anderson ME, Tabas I. 2009. Calcium/calmodulin-dependent protein kinase II links ER stress with Fas and mitochondrial apoptosis pathways. J Clin Invest 119:2925-2941.
79. Tobisawa S, Hozumi Y, Arawaka S, Koyama S, Wada M, Nagai M, Aoki M, Itoyama Y, Goto K, Kato T. 2003a. Mutant SOD1 linked to familial amyotrophic lateral sclerosis, but not wild-type SOD1, induces ER stress in COS7 cells and transgenic mice. Biochem Biophys Res Commun 303:496-503.
80. Tobisawa S, Hozumi Y, Arawaka S, Koyama S, Wada M, Nagai M, Aoki M, Itoyama Y, Goto K, Kato T. 2003b. Mutant SOD1 linked to familial amyotrophic lateral sclerosis, but not wild-type SOD1, induces ER stress in COS7 cells and transgenic mice. Biochem Biophys Res Commun 303:496-503.
81. Udono H, Levey DL, Srivastava PK. 1994. Cellular-requirements for tumor-specific immunity elicited by heat-shock proteins-Tumor rejection antigen-GP96 primes CD8+ t-cells in-vivo. Proc Natl Acad Sci USA 91:3077-3081.
82. Urushitani M, Sik A, Sakurai T, Nukina N, Takahashi R, Julien JP. 2006. Chromogranin-mediated secretion of mutant superoxide dismutase proteins linked to amyotrophic lateral sclerosis. Nat Neurosci 9:108-118.
83. van 't Wout EF, van Schadewijk A, van Boxtel R, Dalton LE, Clarke HJ, Tommassen J, Marciniak SJ, Hiemstra PS. 2015. Virulence factors of pseudomonas aeruginosa induce both the unfolded protein and integrated stress responses in airway epithelial cells. PLoS Pathog 11:e1004946.
84. Walter P, Ron D. 2011. The unfolded protein response: From stress pathway to homeostatic regulation. Science 334:1081-1086.
85. Wang JJ, Cheng QY, Wang X, Zu BB, Xu JH, Xu YH, Zuo XB, Shen YJ, Wang J, Shen YX. 2014. Deficiency of IRE1 and PERK signal pathways in systemic lupus erythematosus. Am J Med Sci 348:465-473.
86. Wang Y, Vera L, Fischer WH, Montminy M. 2009. The CREB coactivator CRTC2 links hepatic ER stress and fasting gluconeogenesis. Nature 460:534-537.
87. Watanabe K, Ohira H, Orikasa H, Saito K, Kanno K, Shioya Y, Obara K, Sato Y. 2006. Anti-calreticulin antibodies in patients with inflammatory bowel disease. Fukushima J Med Sci 52:1-11.
88. Watkin LB, Jessen B, Wiszniewski W, Vecel TJ, Jan M, Sha Y, Thamsen M, Santos-Cortez RLP, Lee K, Gambint T, Forbes LR, Law CS, Stray-Pedersenzt A, Cheng MH, Mace EM, Anderson MS, Liu D, Tang LF, Nicholas SK, Nahmod K, Makedonas G, Canter DL, Kwok P-Y, Hicks J, Jones KD, Penney S, Jhangiani SN, Rosenblum MD, Dell SD, Waterfield MR, Papa FR, Muzny DM, Zaitlen N, Leal SM, Gonzaga-Jaureguit C, Boerwinkle E, Eissa NT, Gibbs RA, Lupski JR, Orange JS, Shum AK, Baylor-Hopkins Ctr Mendelian G. 2015. COPA mutations impair ER-Golgi transport and cause hereditary autoimmune-mediated lung disease and arthritis. Nat Genet 47:654-660.
89. Watowich SS, Morimoto RI, Lamb RA. 1991. Flux of the paramyxovirus hemagglutinin-neuraminidase glycoprotein through the endoplasmic-reticulum activates transcription of the GRP78-BIP gene. J Virol 65:3590-3597.
90. Weber CK, Haslbeck M, Englbrecht M, Sehnert B, Mielenz D, Graef D, Distler JH, Mueller RB, Burkhardt H, Schett G, Voll RE, Furnrohr BG. 2010. Antibodies to the endoplasmic reticulum-resident chaperones calnexin, BiP and Grp94 in patients with rheumatoid arthritis and systemic lupus erythematosus. Rheumatology 49:2255-2263.
91. West M, Mhatre M, Ceballos A, Floyd RA, Grammas P, Gabbita SP, Hamdheydari L, Mai T, Mou S, Pye QN, Stewart C, West S, Williamson KS, Zemlan F, Hensley K. 2004. The arachidonic acid 5-lipoxygenase inhibitor nordihydroguaiaretic acid inhibits tumor necrosis factor alpha activation of microglia and extends survival of G93A-SOD1 transgenic mice. J Neurochem 91:133-143.
92. Williams LM. 2012. Hypothalamic dysfunction in obesity. Proc Nutr Soc 71:521-533.
93. Wootz H, Hansson I, Korhonen L, Napankangas U, Lindholm D. 2004. Caspase-12 cleavage and increased oxidative stress during motoneuron degeneration in transgenic mouse model of ALS. Biochem Biophys Res Commun 322:281-286.
94. Yasojima K, Tourtellotte WW, McGeer EG, McGeer PL. 2001. Marked increase in cyclooxygenase-2 in ALS spinal cord-Implications for therapy. Neurology 57:952-956.
95. Ye RS, Holland WL, Gordillo R, Wang M, Wang QA, Shao ML, Morley TS, Gupta RK, Stahl A, Scherer PE. 2014. Adiponectin is essential for lipid homeostasis and survival under insulin deficiency and promotes beta-cell regeneration. eLife 3:e03851. doi: 10.7554/eLife.03851
96. Yiangou Y, Facer P, Durrenberger P, Chessell IP, Naylor A, Bountra C, Banati RR, Anand P. 2006. COX-2, CB2 and P2×7-immunoreactivities are increased in activated microglial cells/macrophages of multiple sclerosis and amyotrophic lateral sclerosis spinal cord. BMC Neurol 6:12. doi: 10.1186/1471-2377-6-12
97. Zeng LX, Tao J, Liu HL, Tan SW, Yang YD, Peng XJ, Liu ZH, Jiang J, Wu B. 2015. Beta-Arrestin2 encourages inflammation-induced epithelial apoptosis through ER stress/PUMA in colitis. Mucosal Immunol 8:683-695.
98. Zha X, Yue Y, Dong N, Xiong S. 2015. Endoplasmic reticulum stress aggravates viral myocarditis by raising inflammation through the IRE1-associated NF-kappaB pathway. Can J Cardiol pii: S0828-282X(15)00178-6. doi: 10.1016/j.cjca.2015.03.003. [Epub ahead of print].
99. Zhang W, Wang TG, Pei Z, Miller DS, Wu XF, Block ML, Wilson B, Zhang WQ, Zhou Y, Hong JS, Zhang J. 2005. Aggregated alpha-synuclein activates microglia: A process leading to disease progression in Parkinson's disease. FASEB J 19:533-542.
100. Zhou Y, Rui L. 2013. Leptin signaling and leptin resistance. Front Med 7:207-222.