Administration of progranulin (PGRN) triggers ER stress and impairs insulin sensitivity via PERK-eIF2α-dependent manner

References

• Wu S, Zang W, Li X, Sun H. Proepithelin stimulates growth plate chondrogenesis via nuclear factor-kappaB-p65-dependent mechanisms. J Biol Chem 2011; 286:24057-67; PMID:21566130; http://dx.doi.org/10.1074/jbc.M110.201368
   PubMed Web of Science ®Google Scholar
• Gijselinck I, van der Zee J, Engelborghs S, Goossens D, Peeters K, Mattheijssens M, Corsmit E, Del-Favero J, De Deyn PP, Van Broeckhoven C, et al. Progranulin locus deletion in frontotemporal dementia. Hum Mutat 2008; 29:53-8; PMID:18157829; http://dx.doi.org/10.1002/humu.20651
   PubMed Web of Science ®Google Scholar
• Cenik B, Sephton CF, Kutluk Cenik B, Herz J, Yu G. Progranulin: a proteolytically processed protein at the crossroads of inflammation and neurodegeneration. J Biol Chem 2012; 287:32298-306; PMID:22859297; http://dx.doi.org/10.1074/jbc.R112.399170
   PubMed Web of Science ®Google Scholar
• Nicholson AM, Gass J, Petrucelli L, Rademakers R. Progranulin axis and recent developments in frontotemporal lobar degeneration. Alz Res Ther 2012; 4:4; PMID:22277331; http://dx.doi.org/10.1186/alzrt102
   PubMed Web of Science ®Google Scholar
• He Z, Bateman A. Progranulin (granulin-epithelin precursor, PC-cell-derived growth factor, acrogranin) mediates tissue repair and tumorigenesis. J Mol Med 2003; 81:600-12; PMID:12928786; http://dx.doi.org/10.1007/s00109-003-0474-3
   PubMed Web of Science ®Google Scholar
• Daniel R, Daniels E, He Z, Bateman A. Progranulin (acrogranin/PC cell-derived growth factor/granulin-epithelin precursor) is expressed in the placenta, epidermis, microvasculature, and brain during murine development. Dev Dynam: Off Pub Am Assoc Anatomists 2003; 227:593-9; PMID:12889069; http://dx.doi.org/10.1002/dvdy.10341
   PubMed Web of Science ®Google Scholar
• Matsubara T, Mita A, Minami K, Hosooka T, Kitazawa S, Takahashi K, Tamori Y, Yokoi N, Watanabe M, Matsuo E, et al. PGRN is a key adipokine mediating high fat diet-induced insulin resistance and obesity through IL-6 in adipose tissue. Cell Metab 2012; 15:38-50; PMID:22225875; http://dx.doi.org/10.1016/j.cmet.2011.12.002
   PubMed Web of Science ®Google Scholar
• Bossu P, Salani F, Alberici A, Archetti S, Bellelli G, Galimberti D, Scarpini E, Spalletta G, Caltagirone C, Padovani A, et al. Loss of function mutations in the progranulin gene are related to pro-inflammatory cytokine dysregulation in frontotemporal lobar degeneration patients. J Neuroinflammation 2011; 8:65; PMID:21645364; http://dx.doi.org/10.1186/1742-2094-8-65
   PubMed Web of Science ®Google Scholar
• Qu H, Deng H, Hu Z. Plasma progranulin concentrations are increased in patients with type 2 diabetes and obesity and correlated with insulin resistance. Mediat Inflammat 2013; 2013:360190; PMID:23476101; http://dx.doi.org/10.1155/2013/360190
   PubMed Web of Science ®Google Scholar
• Richter J, Focke D, Ebert T, Kovacs P, Bachmann A, Lossner U, Kralisch S, Kratzsch J, Beige J, Anders M, et al. Serum levels of the adipokine progranulin depend on renal function. Diabetes Care 2013; 36:410-4; PMID:23033238; http://dx.doi.org/10.2337/dc12-0220
   PubMed Web of Science ®Google Scholar
• Youn BS, Bang SI, Kloting N, Park JW, Lee N, Oh JE, Pi KB, Lee TH, Ruschke K, Fasshauer M, et al. Serum progranulin concentrations may be associated with macrophage infiltration into omental adipose tissue. Diabetes 2009; 58:627-36; PMID:19056610; http://dx.doi.org/10.2337/db08-1147
   PubMed Web of Science ®Google Scholar
• Tonjes A, Fasshauer M, Kratzsch J, Stumvoll M, Bluher M. Adipokine pattern in subjects with impaired fasting glucose and impaired glucose tolerance in comparison to normal glucose tolerance and diabetes. PloS One 2010; 5:e13911; PMID:21085476; http://dx.doi.org/10.1371/journal.pone.0013911
   PubMed Web of Science ®Google Scholar
• Kloting N, Fasshauer M, Dietrich A, Kovacs P, Schon MR, Kern M, Stumvoll M, Bluher M. Insulin-sensitive obesity. Am J Physiol Endocrinol Metab 2010; 299:E506-15; PMID:20570822; http://dx.doi.org/10.1152/ajpendo.00586.2009
   PubMed Web of Science ®Google Scholar
• Yoo HJ, Hwang SY, Hong HC, Choi HY, Yang SJ, Choi DS, Baik SH, Bluher M, Youn BS, Choi KM. Implication of progranulin and C1q/TNF-related protein-3 (CTRP3) on inflammation and atherosclerosis in subjects with or without metabolic syndrome. PloS One 2013; 8:e55744; PMID:23409033; http://dx.doi.org/10.1371/journal.pone.0055744
   PubMed Web of Science ®Google Scholar
• Richter J, Ebert T, Stolzenburg JU, Dietel A, Hopf L, Hindricks J, Kralisch S, Kratzsch J, Fasshauer M. Response to comment on: Richter et al. Serum levels of the adipokine progranulin depend on renal function. Diabetes Care 2013;36:410-414. Diabetes care 2013; 36:e84; PMID:23033238; http://dx.doi.org/10.2337/dc12-0220
   PubMed Web of Science ®Google Scholar
• Feng JQ, Guo FJ, Jiang BC, Zhang Y, Frenkel S, Wang DW, Tang W, Xie Y, Liu CJ. Granulin epithelin precursor: a bone morphogenic protein 2-inducible growth factor that activates Erk1/2 signaling and JunB transcription factor in chondrogenesis. FASEB J: Off Pub Federat Am Soc Exp Biol 2010; 24:1879-92; PMID:20124436; http://dx.doi.org/10.1096/fj.09-144659
   PubMed Web of Science ®Google Scholar
• Guo FJ, Liu Y, Zhou J, Luo S, Zhao W, Li X, Liu C. XBP1S protects cells from ER stress-induced apoptosis through Erk1/2 signaling pathway involving CHOP. Histochem Cell Biol 2012; 138:447-60; PMID:22669460; http://dx.doi.org/10.1007/s00418-012-0967-7
   PubMed Web of Science ®Google Scholar
• Masuda M, Miyazaki-Anzai S, Levi M, Ting TC, Miyazaki M. PERK-eIF2alpha-ATF4-CHOP signaling contributes to TNFalpha-induced vascular calcification. J Am Heart Assoc 2013; 2:e000238; PMID:24008080; http://dx.doi.org/10.1161/JAHA.113.000238
   PubMed Web of Science ®Google Scholar
• Hu P, Han Z, Couvillon AD, Kaufman RJ, Exton JH. Autocrine tumor necrosis factor α links endoplasmic reticulum stress to the membrane death receptor pathway through IRE1alpha-mediated NF-kappaB activation and down-regulation of TRAF2 expression. Mol Cell Biol 2006; 26:3071-84; PMID:16581782; http://dx.doi.org/10.1128/MCB.26.8.3071-3084.2006
   PubMed Web of Science ®Google Scholar
• Uysal KT, Wiesbrock SM, Hotamisligil GS. Functional analysis of tumor necrosis factor (TNF) receptors in TNF-α-mediated insulin resistance in genetic obesity. Endocrinology 1998; 139:4832-8; PMID:9832419
   PubMed Web of Science ®Google Scholar
• Greene MW, Ruhoff MS, Burrington CM, Garofalo RS, Orena SJ. TNFalpha activation of PKCdelta, mediated by NFkappaB and ER stress, cross-talks with the insulin signaling cascade. Cell Signalling 2010; 22:274-84; PMID:19782747; http://dx.doi.org/10.1016/j.cellsig.2009.09.029
   PubMed Web of Science ®Google Scholar
• Peraldi P, Hotamisligil GS, Buurman WA, White MF, Spiegelman BM. Tumor necrosis factor (TNF)-α inhibits insulin signaling through stimulation of the p55 TNF receptor and activation of sphingomyelinase. J Biol Chem 1996; 271:13018-22; PMID:8662983; http://dx.doi.org/10.1074/jbc.271.22.13018
   PubMed Web of Science ®Google Scholar
• Ito D, Yagi T, Ikawa M, Suzuki N. Characterization of inclusion bodies with cytoprotective properties formed by seipinopathy-linked mutant seipin. Hum Mol Genet 2012; 21:635-46; PMID:22045697; http://dx.doi.org/10.1093/hmg/ddr497
   PubMed Web of Science ®Google Scholar
• Judy ME, Nakamura A, Huang A, Grant H, McCurdy H, Weiberth KF, Gao F, Coppola G, Kenyon C, Kao AW. A shift to organismal stress resistance in programmed cell death mutants. PLoS Genet 2013; 9:e1003714; PMID:24068943; http://dx.doi.org/10.1371/journal.pgen.1003714
   PubMed Web of Science ®Google Scholar
• Ozcan U, Yilmaz E, Ozcan L, Furuhashi M, Vaillancourt E, Smith RO, Gorgun CZ, Hotamisligil GS. Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 2006; 313:1137-40; PMID:16931765; http://dx.doi.org/10.1126/science.1128294
   PubMed Web of Science ®Google Scholar
• Mayer CM, Belsham DD. Palmitate attenuates insulin signaling and induces endoplasmic reticulum stress and apoptosis in hypothalamic neurons: rescue of resistance and apoptosis through adenosine 5' monophosphate-activated protein kinase activation. Endocrinology 2010; 151:576-85; PMID:19952270; http://dx.doi.org/10.1210/en.2009-1122
   PubMed Web of Science ®Google Scholar
• Peng G, Li L, Liu Y, Pu J, Zhang S, Yu J, Zhao J, Liu P. Oleate blocks palmitate-induced abnormal lipid distribution, endoplasmic reticulum expansion and stress, and insulin resistance in skeletal muscle. Endocrinology 2011; 152:2206-18; PMID:21505048; http://dx.doi.org/10.1210/en.2010-1369
   PubMed Web of Science ®Google Scholar
• Guo W, Wong S, Xie W, Lei T, Luo Z. Palmitate modulates intracellular signaling, induces endoplasmic reticulum stress, and causes apoptosis in mouse 3T3-L1 and rat primary preadipocytes. Am J Physiol Endocrinol Metab 2007; 293:E576-86; PMID:17519282; http://dx.doi.org/10.1152/ajpendo.00523.2006
   PubMed Web of Science ®Google Scholar
• Tang W, Lu Y, Tian QY, Zhang Y, Guo FJ, Liu GY, Syed NM, Lai Y, Lin EA, Kong L, et al. The growth factor progranulin binds to TNF receptors and is therapeutic against inflammatory arthritis in mice. Science 2011; 332:478-84; PMID:21393509; http://dx.doi.org/10.1126/science.1199214
   PubMed Web of Science ®Google Scholar
• Dupuis L, Petersen A, Weydt P. Progranulin bridges energy homeostasis and fronto-temporal dementia. Cell Metab 2012; 15:269-70; author reply 70; PMID:22405061; http://dx.doi.org/10.1016/j.cmet.2012.02.003
   PubMed Web of Science ®Google Scholar
• Hossein-Nezhad A, Mirzaei K, Ansar H, Emam-Gholipour S, Tootee A, Keshavarz SA. Obesity, inflammation and resting energy expenditure: possible mechanism of progranulin in this pathway. Minerva Endocrinologica 2012; 37:255-66; PMID:22766892
   PubMedGoogle Scholar
• Kim HK, Shin MS, Youn BS, Namkoong C, Gil SY, Kang GM, Yu JH, Kim MS. Involvement of progranulin in hypothalamic glucose sensing and feeding regulation. Endocrinology 2011; 152:4672-82; PMID:21933869; http://dx.doi.org/10.1210/en.2011-1221
   PubMed Web of Science ®Google Scholar
• Guilherme A, Virbasius JV, Puri V, Czech MP. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 2008; 9:367-77; PMID:18401346; http://dx.doi.org/10.1038/nrm2391
   PubMed Web of Science ®Google Scholar
• Bateman A, Belcourt D, Bennett H, Lazure C, Solomon S. Granulins, a novel class of peptide from leukocytes. Biochem Biophy Res Commun 1990; 173:1161-8; PMID:2268320; http://dx.doi.org/10.1016/S0006-291X(05)80908-8
   PubMed Web of Science ®Google Scholar
• Kawasaki N, Asada R, Saito A, Kanemoto S, Imaizumi K. Obesity-induced endoplasmic reticulum stress causes chronic inflammation in adipose tissue. Sci Rep 2012; 2:799; PMID:23150771; http://dx.doi.org/10.1038/srep00799
   PubMed Web of Science ®Google Scholar
• Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, Ozdelen E, Tuncman G, Gorgun C, Glimcher LH, Hotamisligil GS. Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 2004; 306:457-61; PMID:15486293; http://dx.doi.org/10.1126/science.1103160
   PubMed Web of Science ®Google Scholar
• Park B, Buti L, Lee S, Matsuwaki T, Spooner E, Brinkmann MM, Nishihara M, Ploegh HL. Granulin is a soluble cofactor for toll-like receptor 9 signaling. Immunity 2011; 34:505-13; PMID:21497117; http://dx.doi.org/10.1016/j.immuni.2011.01.018
   PubMed Web of Science ®Google Scholar
• Zhu J, Nathan C, Jin W, Sim D, Ashcroft GS, Wahl SM, Lacomis L, Erdjument-Bromage H, Tempst P, Wright CD, et al. Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell 2002; 111:867-78; PMID:12526812; http://dx.doi.org/10.1016/S0092-8674(02)01141-8
   PubMed Web of Science ®Google Scholar
• Tanaka A, Tsukamoto H, Mitoma H, Kiyohara C, Ueda N, Ayano M, Ohta S, Inoue Y, Arinobu Y, Niiro H, et al. Serum progranulin levels are elevated in patients with systemic lupus erythematosus, reflecting disease activity. Arthrit Res Ther 2012; 14:R244; PMID:23140401; http://dx.doi.org/10.1186/ar4087
   PubMed Web of Science ®Google Scholar
• Li H, Zhou B, Xu L, Liu J, Zang W, Wu S, Sun H. Circulating PGRN is significantly associated with systemic insulin sensitivity and autophagic activity in metabolic syndrome. Endocrinology 2014; 155:3493-507; PMID:24971611; http://dx.doi.org/10.1210/en.2014-1058
   PubMed Web of Science ®Google Scholar
• Yang L, Li P, Fu S, Calay ES, Hotamisligil GS. Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab 2010; 11:467-78; PMID:20519119; http://dx.doi.org/10.1016/j.cmet.2010.04.005
   PubMed Web of Science ®Google Scholar
• Qin L, Wang Z, Tao L, Wang Y. ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy 2010; 6:239-47; PMID:20104019; http://dx.doi.org/10.4161/auto.6.2.11062
   PubMed Web of Science ®Google Scholar
• Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D, Yin XM. Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 2007; 171:513-24; PMID:17620365; http://dx.doi.org/10.2353/ajpath.2007.070188
   PubMed Web of Science ®Google Scholar
• Zhou B, Li H, Xu L, Zang W, Wu S, Sun H. Osteocalcin reverses endoplasmic reticulum stress and improves impaired insulin sensitivity secondary to diet-induced obesity through nuclear factor-kappaB signaling pathway. Endocrinology 2013; 154:1055-68; PMID:23407450; http://dx.doi.org/10.1210/en.2012-2144
   PubMed Web of Science ®Google Scholar
• Deng J, Lu PD, Zhang Y, Scheuner D, Kaufman RJ, Sonenberg N, Harding HP, Ron D. Translational repression mediates activation of nuclear factor kappa B by phosphorylated translation initiation factor 2. Mol Cell Biol 2004; 24:10161-8; PMID:15542827; http://dx.doi.org/10.1128/MCB.24.23.10161-10168.2004
   PubMed Web of Science ®Google Scholar
• Yamazaki H, Hiramatsu N, Hayakawa K, Tagawa Y, Okamura M, Ogata R, Huang T, Nakajima S, Yao J, Paton AW, et al. Activation of the Akt-NF-kappaB pathway by subtilase cytotoxin through the ATF6 branch of the unfolded protein response. J Immunol 2009; 183:1480-7; PMID:19561103; http://dx.doi.org/10.4049/jimmunol.0900017
   PubMed Web of Science ®Google Scholar
• Shoelson SE, Lee J, Goldfine AB. Inflammation and insulin resistance. J Clin Invest 2006; 116:1793-801; PMID:16823477; http://dx.doi.org/10.1172/JCI29069
   PubMed Web of Science ®Google Scholar
• Senn JJ, Klover PJ, Nowak IA, Mooney RA. Interleukin-6 induces cellular insulin resistance in hepatocytes. Diabetes 2002; 51:3391-9; PMID:12453891; http://dx.doi.org/10.2337/diabetes.51.12.3391
   PubMed Web of Science ®Google Scholar
• Chen X, Chang J, Deng Q, Xu J, Nguyen TA, Martens LH, Cenik B, Taylor G, Hudson KF, Chung J, et al. Progranulin does not bind tumor necrosis factor (TNF) receptors and is not a direct regulator of TNF-dependent signaling or bioactivity in immune or neuronal cells. J Neurosci: Off J Soc Neurosci 2013; 33:9202-13; PMID:23699531; http://dx.doi.org/10.1523/JNEUROSCI.5336-12.2013
   PubMed Web of Science ®Google Scholar
• Etemadi N, Webb A, Bankovacki A, Silke J, Nachbur U. Progranulin does not inhibit TNF and lymphotoxin-α signalling through TNF receptor 1. Immunol Cell Biol 2013; 91:661-4; PMID:24100384; http://dx.doi.org/10.1038/icb.2013.53
   PubMed Web of Science ®Google Scholar
• Liu CJ, Bosch X. Progranulin: a growth factor, a novel TNFR ligand and a drug target. Pharmacol Therap 2012; 133:124-32; PMID:22008260; http://dx.doi.org/10.1016/j.pharmthera.2011.10.003
   PubMed Web of Science ®Google Scholar
• Liang H, Yin B, Zhang H, Zhang S, Zeng Q, Wang J, Jiang X, Yuan L, Wang CY, Li Z. Blockade of tumor necrosis factor (TNF) receptor type 1-mediated TNF-α signaling protected Wistar rats from diet-induced obesity and insulin resistance. Endocrinology 2008; 149:2943-51; PMID:18339717; http://dx.doi.org/10.1210/en.2007-0978
   PubMed Web of Science ®Google Scholar
• Li M, Liu Y, Xia F, Wu Z, Deng L, Jiang R, Guo FJ. Progranulin is required for proper ER stress response and inhibits ER stress-mediated apoptosis through TNFR2. Cell Signalling 2014; 26:1539-48; PMID:24703938; http://dx.doi.org/10.1016/j.cellsig.2014.03.026
   PubMed Web of Science ®Google Scholar
• Hu Y, Xiao H, Shi T, Oppenheim JJ, Chen X. Progranulin promotes tumour necrosis factor-induced proliferation of suppressive mouse CD4(+) Foxp3(+) regulatory T cells. Immunology 2014; 142:193-201; PMID:24383743; http://dx.doi.org/10.1111/imm.12241
   PubMed Web of Science ®Google Scholar
• Jian J, Zhao S, Tian Q, Gonzalez-Gugel E, Mundra JJ, Uddin SM, Liu B, Richbourgh B, Brunetti R, Liu CJ. Progranulin directly binds to the CRD2 and CRD3 of TNFR extracellular domains. FEBS Lett 2013; 587:3428-36; PMID:24070898; http://dx.doi.org/10.1016/j.febslet.2013.09.024
   PubMed Web of Science ®Google Scholar
• Liu C, Li XX, Gao W, Liu W, Liu DS. Progranulin-derived Atsttrin directly binds to TNFRSF25 (DR3) and inhibits TNF-like ligand 1A (TL1A) activity. PloS One 2014; 9:e92743
   PubMed Web of Science ®Google Scholar
• Bluml S, Binder NB, Niederreiter B, Polzer K, Hayer S, Tauber S, Schett G, Scheinecker C, Kollias G, Selzer E, et al. Antiinflammatory effects of tumor necrosis factor on hematopoietic cells in a murine model of erosive arthritis. Arthritis Rheum 2010; 62:1608-19; PMID:20155834; http://dx.doi.org/10.1002/art.27399
   PubMed Web of Science ®Google Scholar
• Faustman D, Davis M. TNF receptor 2 pathway: drug target for autoimmune diseases. Nat Rev Drug Discov 2010; 9:482-93; PMID:20489699; http://dx.doi.org/10.1038/nrd3030
   PubMed Web of Science ®Google Scholar
• Kessenbrock K, Frohlich L, Sixt M, Lammermann T, Pfister H, Bateman A, Belaaouaj A, Ring J, Ollert M, Fassler R, et al. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J Clin Invest 2008; 118:2438-47; PMID:18568075
   PubMed Web of Science ®Google Scholar
• Wu H, Siegel RM. Medicine. Progranulin resolves inflammation. Science 2011; 332:427-8; PMID:21512023; http://dx.doi.org/10.1126/science.1205992
   PubMed Web of Science ®Google Scholar
• Tian Q, Zhao S, Liu C. A solid-phase assay for studying direct binding of progranulin to TNFR and progranulin antagonism of TNF/TNFR interactions. Methods Mol Biol 2014; 1155:163-72; PMID:24788181; http://dx.doi.org/10.1007/978-1-4939-0669-7_14
   PubMedGoogle Scholar
• Tian QY, Zhao YP, Liu CJ. Modified yeast-two-hybrid system to identify proteins interacting with the growth factor progranulin. J Visualized Exp: JoVE 2012; pii:3562; PMID:22297851; http://dx.doi.org/10.3791/3562
   PubMed Web of Science ®Google Scholar
• Cha SH, Hu Z, Chohnan S, Lane MD. Inhibition of hypothalamic fatty acid synthase triggers rapid activation of fatty acid oxidation in skeletal muscle. Proc Natl Acad Sci U S A 2005; 102:14557-62; PMID:16203972; http://dx.doi.org/10.1073/pnas.0507300102
   PubMed Web of Science ®Google Scholar
• Kim KH, Jeong YT, Oh H, Kim SH, Cho JM, Kim YN, Kim SS, Kim do H, Hur KY, Kim HK, et al. Autophagy deficiency leads to protection from obesity and insulin resistance by inducing Fgf21 as a mitokine. Nat Med 2013; 19:83-92; PMID:23202295; http://dx.doi.org/10.1038/nm.3014
   PubMed Web of Science ®Google Scholar
• Zhou B, Li H, Liu J, Xu L, Zang W, Wu S, Sun H. Intermittent injections of osteocalcin reverse autophagic dysfunction and endoplasmic reticulum stress resulting from diet-induced obesity in the vascular tissue via the NFkappaB-p65-dependent mechanism. Cell Cycle 2013; 12:1901-13; PMID:23708521; http://dx.doi.org/10.4161/cc.24929
   PubMed Web of Science ®Google Scholar