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Project Publications: University of California-Davis: Monitoring Endoplasmic Reticulum Stress Caused by Chronic Exposure to Chemicals

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Superfund Research Program

Monitoring Endoplasmic Reticulum Stress Caused by Chronic Exposure to Chemicals

Project Leader: Fawaz G. Haj
Grant Number: P42ES004699
Funding Period: 2017-2023
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Publications

2023

  • Hsu M, Ito Y, Singh JP, Hsu S, Wells A, Jen K, Meng T, Haj FG. 2023. Protein tyrosine phosphatase 1B is a regulator of alpha-actinin4 in the glomerular podocyte. Biochim Biophys Acta 1871(1):119590. doi:10.1016/j.bbamcr.2023.119590 PMID:37730132

2022

  • Hsu M, Ito Y, Afkarian M, Haj FG. 2022. Deficiency of the Src homology phosphatase 2 in podocytes is associated with renoprotective effects in mice under hyperglycemia. Cellular and Molecular Life Sciences 79(10):516. doi:10.1007/s00018-022-04517-6 PMID:36102977

2021

2020

  • An G, Lee K, Yang J, Hammock BD. 2020. Target-Mediated Drug Disposition-A Class Effect of Soluble Epoxide Hydrolase Inhibitors. J Clin Pharmacol doi:10.1002/jcph.1763 PMID:33078430 PMCID:PMC7969377
  • Atone J, Wagner KM, Hashimoto K, Hammock BD. 2020. Cytochrome P450 derived epoxidized fatty acids as a therapeutic tool against neuroinflammatory diseases. Prostaglandins Other Lipid Mediat 147:13. doi:10.1016/j.prostaglandins.2019.106385 PMID:31698143 PMCID:PMC7067627
  • Burmistrov V, Morisseau C, Karlov D, Pitushkin D, Vernigora A, Rasskazova E, Butov GM, Hammock BD. 2020. Bioisosteric substitution of adamantane with bicyclic lipophilic groups improves water solubility of human soluble epoxide hydrolase inhibitors. Bioorg Med Chem Lett 30:127430. doi:10.1016/j.bmcl.2020.127430 PMID:32736212 PMCID:PMC7494652
  • Codony S, Pujol E, Pizarro J, Feixas F, Valverde E, Loza I, Brea J, Saez E, Oyarzabal J, Pineda-Lucena A, Perez B, Perez C, Rodriguez-Franco M, Leiva R, Osuna S, Morisseau C, Hammock BD, Vasquez-Carrera M, Vazquez S. 2020. 2-Oxaadamant-1-yl Ureas as Soluble Epoxide Hydrolase Inhibitors: In Vivo Evaluation in a Murine Model of Acute Pancreatitis. J Med Chem 63:9237-9257. doi:10.1021/acs.jmedchem.0c00310 PMID:32787085 PMCID:PMC7755424
  • Edin ML, Lih FB, Hammock BD, Thomson S, Zeldin DC, Bishop-Bailey D. 2020. Vascular lipidomic profiling of potential endogenous fatty acid PPAR ligands reveals the coronary artery as major producer of CYP450-derived epoxy fatty acids. Cells 9:15. doi:10.3390/cells9051096 PMID:32365470 PMCID:PMC7290345
  • Fishbein A, Wang W, Yang H, Yang J, Hallisey V, Deng J, Verheul S, Hwang SH, Gartung A, Wang Y, Bielenberg DR, Huang S, Kieran MW, Hammock BD, Panigrahy D. 2020. Resolution of eicosanoid/cytokine storm prevents carcinogen and inflammation-initiated hepatocellular cancer progression. Proc Natl Acad Sci U S A 117:21576-21587. doi:10.1073/pnas.2007412117 PMID:32801214 PMCID:PMC7474612
  • Grinan-Ferre C, Codony S, Pujol E, Yang J, Leiva R, Escolano C, Puigoriol-Illamola D, Companys-Alemany J, Corpas R, Sanfeliu C, Perez B, Loza MI, Brea J, Morisseau C, Hammock BD, Vazquez S, Pallas M, Galdeano C. 2020. Pharmacological inhibition of soluble epoxide hydrolase as a new therapy for Alzheimer's Disease. Neurotherapeutics doi:10.1007/s13311-020-00854-1 PMID:32488482
  • Hammock BD, Wang W, Gilligan MM, Panigrahy D. 2020. Eicosanoids The Overlooked Storm in Coronavirus Disease 2019 (COVID-19)?. Am J Pathol 190:1782-1788. doi:10.1016/j.ajpath.2020.06.010 PMID:32650004 PMCID:PMC7340586
  • Hildreth K, Kodani SD, Hammock BD, Zhao L. 2020. Cytochrome P450-derived linoleic acid metabolites EpOMEs and DiHOMEs: a review of recent studies. J Nutr Biochem 86:doi:10.1016/j.jnutbio.2020.108484 PMID:32827665 PMCID:PMC760679
  • Hsu M, Koike S, Mello A, Nagy LE, Haj FG. 2020. Hepatic protein-tyrosine phosphatase 1B disruption and pharmacological inhibition attenuate ethanol-induced oxidative stress and ameliorate alcoholic liver disease in mice. Redox Biol 36:doi:10.1016/j.redox.2020.101658 PMID:32769011 PMCID:PMC7408361
  • Knuth M, Mahapatra D, Jima DD, Wan D, Hammock BD, Law M, Kullman SW. 2020. Vitamin D deficiency serves as a precursor to stunted growth and central adiposity in zebrafish. Sci Rep 10:doi:10.1038/s41598-020-72622-2 PMID:32994480 PMCID:PMC7524799
  • Matin N, Fisher C, Lansdell TA, Hammock BD, Yang J, Jackson WF, Dorrance AM. 2020. Soluble epoxide hydrolase inhibition improves cognitive function and parenchymal artery dilation in a hypertensive model of chronic cerebral hypoperfusion. Microcirculation 11:doi:10.1111/micc.12653 PMID:32767848 PMCID:PMC7990111
  • Overby HB, Yang Y, Xu X, Graham K, Hildreth K, Choi S, Wan D, Morisseau C, Zeldin DC, Hammock BD, Wang S, Bettaieb A, Zhao L. 2020. Soluble Epoxide Hydrolase Inhibition by t-TUCB Promotes Brown Adipogenesis and Reduces Serum Triglycerides in Diet-Induced Obesity. Int J Mol Sci 21:doi:10.3390/ijms21197039 PMID:32987880 PMCID:PMC7582898
  • Panigrahy D, Gilligan MM, Gartung A, Cortes-Puch I, Sime PJ, Phipps RP, Serhan CN, Hammock BD. 2020. Inflammation resolution: a dual-pronged approach to averting cytokine storms in COVID-19?. Cancer Metastasis Rev 4:doi:10.1007/s10555-020-09889-4 PMID:32385712 PMCID:PMC7207990
  • Pu Y, Yang J, Chang L, Qu Y, Wang S, Zhang K, Xiong Z, Zhang J, Tan Y, Wang X, Fujita Y, Ishima T, Wan D, Hee-Hwang S, Hammock BD, Hashimoto K. 2020. Maternal glyphosate exposure causes autism-like behaviors in offspring through increased expression of soluble epoxide hydrolase. Proc Natl Acad Sci U S A 117:11753-11759. doi:10.1073/pnas.1922287117 PMID:32398374 PMCID:PMC7260984
  • Shihadih DS, Harris TR, Kodani SD, Hwang SH, Lee KS, Mavangira V, Hamamoto B, Guedes AP, Hammock BD, Morisseau C. 2020. Selection of Potent Inhibitors of Soluble Epoxide Hydrolase for Usage in Veterinary Medicine. Front Vet Sci 7:doi:10.3389/fvets.2020.00580 PMID:33005645 PMCID:PMC7479175
  • Sirish P, Thai PN, Lee JH, Yang J, Zhang X, Ren L, Li N, Timofeyev V, Lee KS, Nader CE, Rowland DJ, Yechikov S, Ganaga S, Young JN, Lieu DK, Yamoah EN, Hammock BD, Chiamvimonvat N. 2020. Suppression of inflammation and fibrosis using soluble epoxide hydrolase inhibitors enhances cardiac stem cell-based therapy. Stem Cells Transl Med doi:10.1002/sctm.20-0143 PMID:32790136
  • Tu M, Wang W, Zhang G, Hammock BD. 2020. omega-3 polyunsaturated fatty acids on colonic inflammation and colon cancer: roles of lipid-metabolizing enzymes involved. Nutrients 12(11):3301. doi:10.3390/nu12113301 PMID:33126566 PMCID:PMC7693568
  • Wagner KM, Atone J, Hammock BD. 2020. Soluble epoxide hydrolase inhibitor mediated analgesia lacks tolerance in rat models. Brain Res 1728:doi:10.1016/j.brainres.2019.146573 PMID:31790682 PMCID:PMC6996511
  • Wagner KM, Gomes AV, McReynolds C, Hammock BD. 2020. Soluble Epoxide Hydrolase Regulation of Lipid Mediators Limits Pain. Neurotherapeutics doi:10.1007/s13311-020-00916-4 PMID:32875445
  • Wang Y, Yang J, Wang W, Sanidad KZ, Cinelli MA, Wan D, Hee-Hwang S, Kim D, Lee KS, Xiao H, Hammock BD, Zhang G. 2020. Soluble epoxide hydrolase is an endogenous regulator of obesity-induced intestinal barrier dysfunction and bacterial translocation. Proc Natl Acad Sci U S A 117:8431-8436. doi:10.1073/pnas.1916189117 PMID:32220957 PMCID:PMC7165420
  • Wilt S, Kodani SD, Le TN, Nguyen L, Vo N, Ly T, Rodriguez M, Hudson PK, Morrisseau C, Hammock BD, Pecic S. 2020. Development of multitarget inhibitors for the treatment of pain: Design, synthesis, biological evaluation and molecular modeling studies. Bioorg Chem 103:17. doi:10.1016/j.bioorg.2020.104165 PMID:32891856 PMCID:PMC7723751

2019

  • Bailey KA, Moreno E, Haj FG, Simon SI, Passerini AG. 2019. Mechanoregulation of p38 activity enhances endoplasmic reticulum stress-mediated inflammation by arterial endothelium. FASEB J 33:12888-12899. doi:10.1096/fj.201900236R PMID:31499005 PMCID:PMC6902662
  • Hrdlicka J, Neckar J, Papousek F, Huskova Z, Kikerlova S, Vanourkova Z, Vernerova Z, Akat F, Vasinova J, Hammock BD, Hwang SH, Imig JD, Falck JR, Cervenka L, Kolar F. 2019. Epoxyeicosatrienoic acid-based therapy attenuates the progression of postischemic heart failure in normotensive Sprague-Dawley but not in hypertensive Ren-2 transgenic rats. Front Pharmacol 10:12. doi:10.3389/fphar.2019.00159 PMID:30881303 PMCID:PMC6406051
  • Klocke J, Ulu A, Wu K, Rudolph B, Dragun D, Gollasch M, Schunck W, Hammock BD, Riemekasten G, Enghard P. 2019. Prophylactic inhibition of soluble epoxide hydrolase delays onset of nephritis and ameliorates kidney damage in NZB/W F1 mice. Sci Rep 9(1):8993. doi:10.1038/s41598-019-45299-5 PMID:31222024 PMCID:PMC6586931
  • Kodani SD, Morisseau C. 2019. Role of epoxy-fatty acids and epoxide hydrolases in the pathology of neuro-inflammation. Biochimie 159:59-65. doi:10.1016/j.biochi.2019.01.020 PMID:30716359 PMCID:PMC6431267
  • Li Q, Kailemia M, Merleev A, Xu G, Serie D, Danan L, Haj FG, Maverakis E, Lebrilla CB. 2019. Site-Specific Glycosylation Quantitation of 50 Serum Glycoproteins Enhanced by Predictive Glycopeptidomics for Improved Disease Biomarker Discovery. Anal Chem 91:5433-5445. doi:10.1021/acs.analchem.9b00776
  • Liang Z, Zhang B, Xu M, Morisseau C, Hwang SH, Hammock BD, Li QX. 2019. 1-Trifluoromethoxyphenyl-3-(1-propionylpiperidin-4-yl) urea, a selective and potent dual inhibitor of soluble epoxide hydrolase and p38 kinase intervenes in Alzheimer's signaling in human nerve cells. ACS Chem Neurosci 10:4018-4030. doi:10.1021/acschemneuro.9b00271 PMID:31378059 PMCID:PMC7028313
  • Luo Y, Wu M, Deng B, Huang J, Hwang SH, Li M, Zhou C, Zhang Q, Yu H, Zhao D, Zhang G, Qin L, Peng A, Hammock BD, Liu J. 2019. Inhibition of soluble epoxide hydrolase attenuates a high-fat diet-mediated renal injury by activating PAX2 and AMPK. Proc Natl Acad Sci U S A 116(11):5154-5159. doi:10.1073/pnas.1815746116 PMID:30804206 PMCID:PMC6421466
  • Minaz N, Razdan R, Hammock BD, Mujwar S, Goswami SK. 2019. Impact of diabetes on male sexual function in streptozotocin-induced diabetic rats: Protective role of soluble epoxide hydrolase inhibitor. Biomed Pharmacother 115:108897. doi:10.1016/j.biopha.2019.108897 PMID:31102913 PMCID:PMC6893866
  • Pardeshi R, Bolshette N, Gadhave K, Arfeen M, Ahmed S, Jamwal R, Hammock BD, Lahkar M, Goswami SK. 2019. Docosahexaenoic Acid Increases the Potency of Soluble Epoxide Hydrolase Inhibitor in Alleviating Streptozotocin-Induced Alzheimers Disease-Like Complications of Diabetes. Front Pharmacol 10:288. doi:10.3389/fphar.2019.00288 PMID:31068802 PMCID:PMC6491817
  • Perez S, Finamor I, Marti-Andres P, Pereda J, Campos A, Domingues R, Haj FG, Sabater L, de-Madaria E, Sastre J. 2019. Role of obesity in the release of extracellular nucleosomes in acute pancreatitis: a clinical and experimental study. Int J Obes 43:158-168. doi:10.1038/s41366-018-0073-6 PMID:29717278
  • Rand AA, Rajamani A, Kodani SD, Harris TR, Schlatt L, Barnych B, Passerini AG, Hammock BD. 2019. Epoxyeicosatrienoic acid (EET)-stimulated angiogenesis is mediated by epoxy hydroxyeicosatrienoic acids (EHETs) formed from COX-2. J Lipid Res 60:1996-2005. doi:10.1194/jlr.M094219 PMID:31641036 PMCID:PMC6889709
  • Zarriello S, Tuazon JP, Corey S, Schimmel S, Rajani M, Gorsky A, Incontri D, Hammock BD, Borlongan CV. 2019. Humble beginnings with big goals: small molecule soluble epoxide hydrolase inhibitors for treating CNS disorders. Prog Neurobiol 172:23-39. doi:10.1016/j.pneurobio.2018.11.001 PMID:30447256 PMCID:PMC6993804
  • Zhang C, Duan J, Yang H, Sun C, Zhong W, Tao J, Guan X, Jiang H, Hammock BD, Hee-Hwang S, Zhou Y, Guan C. 2019. COX-2/sEH dual inhibitor PTUPB alleviates bleomycin-induced pulmonary fibrosis in mice via inhibiting senescence. FEBS Lett 287(8):doi:10.1111/febs.15105 (ahead of print)

2018

  • Červenka L, Huskova Z, Kopkan L, Kikerlova S, Sedlakova L, Vanourkova Z, Alanova P, Kolar F, Hammock BD, Hee-Hwang S, Imig JD, Falck JR, Sadowski J, Kompanowska-Jezierska E, Neckar J. 2018. Two pharmacological epoxyeicosatrienoic acid-enhancing therapies are effectively antihypertensive and reduce the severity of ischemic arrhythmias in rats with angiotensin II-dependent hypertension. J Hypertens 36:doi:10.1097/hjh.0000000000001708 PMID:29570510 PMCID:PMC7375140 (accepted for publication)

2017

  • Bettaieb A, Koike S, Chahed S, Bachaalany S, Hashoush N, Graham J, Fatima H, Havel PJ, Gruzdev A, Zeldin DC, Hammock BD, Haj FG, Zhao Y. 2017. Podocyte-specific soluble exposide hydrolase deficiency in mice attenuates acute kidney injury. FEBS J 284(13):1970-1986. doi:10.1111/febs.14100 PMID:28485854 PMCID:PMC5515292
  • Bettaieb A, Koike S, Hsu M, Ito Y, Chahed S, Bachaalany S, Gruzdev A, Calvo-Rubio M, Lee KS, Inceoglu B, Imig JD, Villalba JM, Zeldin DC, Hammock BD, Haj FG. 2017. Soluble epoxide hydrolase in podocytes is a significant contributor to renal function under hyperglycemia. Biochim Biophys Acta 1861:2758-2765. doi:10.1016/j.bbagen.2017.07.021 PMID:28757338
  • Flitter B, Hvorecny KL, Ono E, Eddens TJ, Yang J, Kwak D, Bahl CD, Hampton TH, Morisseau C, Hammock BD, Liu X, Lee JS, Kolls J, Levy BD, Madden DR, Bomberger JM. 2017. Pseudomonas aeruginosa sabotages the generation of host proresolving lipid mediators. Proc Natl Acad Sci U S A 114(1):136-141. doi:10.1073/pnas.1610242114 PMID:27980032 PMCID:PMC5224368
  • Goswami SK, Rand A, Wan DB, Yang J, Inceoglu B, Thomas M, Morisseau C, Yang G, Hammock BD. 2017. Pharmacological inhibition of soluble epoxide hydrolase or genetic deletion reduces diclofenac-induced gastric ulcers. Life Sciences 180:114-122. doi:10.1016/j.lfs.2017.05.018 PMID:28522175 PMCID:PMC5659729
  • Guedes AP, Galuppo L, Hood D, Hwang SH, Morisseau C, Hammock BD. 2017. Soluble epoxide hydrolase activity and pharmacologic inhibition in horses with chronic severe laminitis. Equine Vet J 49(3):345-351. doi:10.1111/evj.12603 PMID:27338788
  • Hwang SH, Wagner KM, Xu J, Yang J, Li X, Cao Z, Morisseau C, Lee K, Hammock BD. 2017. Chemical synthesis and biological evaluation of ω-hydroxy polyunsaturated fatty acids. Bioorg Med Chem Lett 27(3):620-625. doi:10.1016/j.bmcl.2016.12.002 PMID:28025003
  • Inceoglu B, Bettaieb A, Haj FG, Gomes AV, Hammock BD. 2017. Modulation of mitochondrial dysfunction and endoplasmic reticulum stress are key mechanisms for the wide-ranging actions of epoxy fatty acids and soluble epoxide hydrolase inhibitors. Prostaglandins Other Lipid Mediat 133:68-78. doi:10.1016/j.prostaglandins.2017.08.003 PMID:28847566 PMCID:PMC5584617
  • Kitamura S, Morisseau C, Harris TR, Inceoglu B, Hammock BD. 2017. Occurrence of urea-based soluble epoxide hydrolase inhibitors from the plants in the order Brassicales. PLoS One 12(5):e0176571. doi:10.1371/journal.pone.0176571 PMID:28472063 PMCID:PMC5417501
  • Kodani SD, Barthelemy M, Kamita SG, Hammock BD, Morisseau C. 2017. Development of amide-based fluorescent probes for selective measurement of carboxylesterase 1 activity in tissue extracts. Anal Biochem 539:81-89. doi:10.1016/j.ab.2017.10.014 PMID:29054529 PMCID:PMC5696082
  • Lee KS, Henriksen NM, Ng CJ, Yang J, Jia W, Morisseau C, Andaya A, Gilson MK, Hammock BD. 2017. Probing the orientation of inhibitor and epoxy-eicosatrienoic acid binding in the active site of soluble epoxide hydrolase. Arch Biochem Biophys 613:1-11. doi:10.1016/j.abb.2016.10.017 PMID:27983948 PMCID:PMC5172606
  • Orcholski ME, Khurshudyan A, Shamskhou EA, Yuan K, Chen IY, Kodani SD, Morisseau C, Hammock BD, Hong EM, Alexandrova L, Alastalo T, Berry G, Zamanian RT, de Jesus Perez VA. 2017. Reduced carboxylesterase 1 is associated with endothelial injury in methamphetamine-induced pulmonary arterial hypertension. Am J Physiol Lung Cell Mol Physiol 313:L252-L266. doi:10.1152/ajplung.00453.2016 PMID:28473326
  • Rand A, Barnych B, Morisseau C, Cajka T, Lee KS, Panigrahy D, Hammock BD. 2017. Cyclooxygenase-derived proangiogenic metabolites of epoxyeicosatrienoic acids. Proc Natl Acad Sci U S A 114:4370-4375. doi:10.1073/pnas.1616893114 PMID:28396419 PMCID:PMC5410821
  • Trindade-da-Silva C, Bettaieb A, Napimoga M, Stephen Lee KS, Inceoglu B, Ueira-Vieira C, Bruun DA, Goswami SK, Haj FG, Hammock BD. 2017. Soluble epoxide hydrolase pharmacological inhibition decreases alveolar bone loss by modulating host inflammatory response, RANK-related signaling, endoplasmic reticulum stress, and apoptosis. J Pharmacol Exp Ther 361(3):408-416. doi:10.1124/jpet.116.238113 PMID:28356494 PMCID:PMC5443319
  • Wagner KM, Gilda JE, Yang J, Wan D, Morisseau C, Gomes AV, Hammock BD. 2017. Soluble epoxide hydrolase inhibition alleviates neuropathy in Akita (Ins2 Akita) mice. Behav Brain Res 326:69-76. doi:10.1016/j.bbr.2017.02.048 PMID:28259677 PMCID:PMC5409858

2016

  • Goswami SK, Wan D, Yang J, Trindade da Silva CA, Morisseau C, Kodani SD, Yang G, Inceoglu B, Hammock BD. 2016. Anti-ulcer efficacy of soluble epoxide hydrolase inhibitor TPPU on diclofenac-induced intestinal ulcers. J Pharmacol Exp Ther 357(3):529-536. doi:10.1124/jpet.116.232108 PMID:26989141 PMCID:PMC4885505
  • Harris TR, Kodani SD, Yang J, Imai DM, Hammock BD. 2016. An ω-3-enriched diet alone does not attenuate CCl4-induced hepatic fibrosis. J Nutr Biochem 38:93-101. doi:10.1016/j.jnutbio.2016.08.010 PMID:27732914 PMCID:PMC5102762
  • Kodani SD, Overby HB, Morisseau C, Chen J, Zhao L, Hammock BD. 2016. Parabens inhibit fatty acid amide hydrolase: a potential role in paraben-enhanced 3T3-L1 adipocyte differentiation. Toxicol Lett 262:92-99. doi:10.1016/j.toxlet.2016.09.011 PMID:27659731 PMCID:PMC5096949
  • Liu J, Morisseau C, Huang H, Hammock BD. 2016. Screening of soluble epoxide hydrolase inhibitory ingredients from traditional Chinese medicines for anti-inflammatory use. J Ethnopharmacol 194:475-482. doi:10.1016/j.jep.2016.09.044 PMID:27702689
  • Ren Q, Ma M, Ishima T, Morisseau C, Yang J, Wagner KM, Zhang J, Yao W, Dong C, Han M, Hammock BD, Hashimoto K. 2016. Gene deficiency and pharmacological inhibition of soluble epoxide hydrolase confers resilience to repeated social defeat stress. Proc Natl Acad Sci U S A 113(13):E1944-E1952. doi:10.1073/pnas.1601532113 PMID:26976569 PMCID:PMC4822604
  • Shih P, Yang J, Morisseau C, German JB, Zeeland AA, Armando AM, Quehenberger O, Bergen AW, Magistretti P, Berrettini W, Halmi KA, Schork N, Hammock BD, Kaye W. 2016. Dysregulation of soluble epoxide hydrolase and lipidomic profiles in anorexia nervosa. Mol Psychiatry 21(4):537-546. doi:10.1038/mp.2015.26 PMID:25824304 PMCID:PMC4591075
  • Wu X, Yang J, Morisseau C, Robertson LW, Hammock BD, Lehmler H. 2016. 3,3',4,4',5-Pentachlorobiphenyl (PCB 126) decreases hepatic and systemic ratios of epoxide to diol metabolites of unsaturated fatty acids in male rats. Toxicol Sci 152(2):309-322. doi:10.1093/toxsci/kfw084 PMID:27208083 PMCID:PMC4960907
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