A novel role for 12/15-lipoxygenase in regulating autophagy

Redox Biology

Volumn 4, Issue , 2015, Pages 40-47

  Morgan, Alwena H ^a   Hammond, Victoria J ^a   Sakoh Nakatogawa, Machiko ^b   Ohsumi, Yoshinori ^b   Thomas, Christopher P ^a   Blanchet, Fabien ^a   Piguet, Vincent ^a   Kiselyov, Kirill ^c   O'Donnell, Valerie B ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Autophagy; Lipid; Lipoxygenase; Mitochondria

Indexed keywords

12 HYDROXYICOSATETRAENOIC ACID PHOSPHATIDYLETHANOLAMINE; ARACHIDONATE 12 LIPOXYGENASE; ARACHIDONATE 15 LIPOXYGENASE; ATG8 PROTEIN; CELL PROTEIN; CHLOROQUINE; LC3 PROTEIN; PHOSPHATIDYLETHANOLAMINE; UNCLASSIFIED DRUG; 12 HYDROXYICOSATETRAENOIC ACID; 12-15-LIPOXYGENASE; ATG8 PROTEIN, S CEREVISIAE; AUTOPHAGY RELATED PROTEIN 8 FAMILY; MICROTUBULE ASSOCIATED PROTEIN; PHOSPHOLIPID; SACCHAROMYCES CEREVISIAE PROTEIN;

ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL ULTRASTRUCTURE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME DEFICIENCY; ENZYME LIPIDATION; ENZYME MODIFICATION; IN VITRO STUDY; INNATE IMMUNITY; LIGHT CHAIN; LIPID OXIDATION; LYSOSOME STORAGE DISEASE; MALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; ANALOGS AND DERIVATIVES; ANIMAL; GENETICS; LIPID METABOLISM; MACROPHAGE; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; SACCHAROMYCES CEREVISIAE;

12-HYDROXY-5,8,10,14-EICOSATETRAENOIC ACID; ANIMALS; ARACHIDONATE 12-LIPOXYGENASE; ARACHIDONATE 15-LIPOXYGENASE; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 8 FAMILY; LIPID METABOLISM; MACROPHAGES; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; OXIDATION-REDUCTION; PHOSPHOLIPIDS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84917706163     PISSN: 22132317     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.redox.2014.11.005     Document Type: Article

References (44)

1. Maskrey B.H., Bermúdez-Fajardo A., Morgan A.H., Stewart-Jones E., Dioszeghy V., Taylor G.W., Baker P.R., Coles B., Coffey M.J., Kühn H., O'Donnell V.B. Activated platelets and monocytes generate four hydroxyphosphatidylethanolamines via lipoxygenase. Journal of Biological Chemistry 2007, 282(28):20151-20163. http://www.ncbi.nlm.nih.gov/pubmed/17519227, 10.1074/jbc.M611776200.
2. Morgan A.H., Dioszeghy V., Maskrey B.H., Thomas C.P., Clark S.R., Mathie S.A., Lloyd C.M., Kühn H., Topley N., Coles B.C., Taylor P.R., Jones S.A., O'Donnell V.B. Phosphatidylethanolamine-esterified eicosanoids in the mouse: tissue localization and inflammation-dependent formation in Th-2 disease. Journal of Biological Chemistry 2009, 284(32):21185-21191. http://www.ncbi.nlm.nih.gov/pubmed/19531470, 10.1074/jbc.M109.021634.
3. Clark S.R., Guy C.J., Scurr M.J., Taylor P.R., Kift-Morgan A.P., Hammond V.J., Thomas C.P., Coles B., Roberts G.W., Eberl M., Jones S.A., Topley N., Kotecha S., O'Donnell V.B. Esterified eicosanoids are acutely generated by 5-lipoxygenase in primary human neutrophils and in human and murine infection. Blood 2011, 117(6):2033-2043. http://www.ncbi.nlm.nih.gov/pubmed/21177434, 10.1182/blood-2010-04-278887.
4. Thomas C.P., Morgan L.T., Maskrey B.H., Murphy R.C., Kühn H., Hazen S.L., Goodall A.H., Hamali H.A., Collins P.W., O'Donnell V.B. Phospholipid-esterified eicosanoids are generated in agonist-activated human platelets and enhance tissue factor-dependent thrombin generation. Journal of Biological Chemistry 2010, 285(10):6891-6903. http://www.ncbi.nlm.nih.gov/pubmed/20061396, 10.1074/jbc.M109.078428.
5. Zhang J. Autophagy and mitophagy in cellular damage control. Redox Biology 2013, 1(1):19-23. http://www.ncbi.nlm.nih.gov/pubmed/23946931, 10.1016/j.redox.2012.11.008.
6. Glick D., Barth S., Macleod K.F. Autophagy: cellular and molecular mechanisms. Journal of Pathology 2010, 221(1):3-12. http://www.ncbi.nlm.nih.gov/pubmed/20225336, 10.1002/path.2697.
7. Lemasters J.J. Variants of mitochondrial autophagy: Types 1 and 2 mitophagy and micromitophagy (Type 3). Redox Biology 2014, 2:749-754. http://www.ncbi.nlm.nih.gov/pubmed/25009776, 10.1016/j.redox.2014.06.004.
8. Giordano S., Darley-Usmar V., Zhang J. Autophagy as an essential cellular antioxidant pathway in neurodegenerative disease. Redox Biology 2014, 2:82-90. http://www.ncbi.nlm.nih.gov/pubmed/24494187, 10.1016/j.redox.2013.12.013.
9. Höhn A., Grune T. Lipofuscin: formation, effects and role of macroautophagy. Redox Biology 2013, 1(1):140-144. http://www.ncbi.nlm.nih.gov/pubmed/24024146, 10.1016/j.redox.2013.01.006.
10. Haberzettl P., Hill B.G. Oxidized lipids activate autophagy in a JNK-dependent manner by stimulating the endoplasmic reticulum stress response. Redox Biology 2013, 1(1):56-64. http://www.ncbi.nlm.nih.gov/pubmed/24024137, 10.1016/j.redox.2012.10.003.
11. Desideri E., Filomeni G., Ciriolo M.R. Glutathione participates in the modulation of starvation-induced autophagy in carcinoma cells. Autophagy 2012, 8(12):1769-1781. http://www.ncbi.nlm.nih.gov/pubmed/22964495, 10.4161/auto.22037.
12. Tanida I., Nishitani T., Nemoto T., Ueno T., Kominami E. Mammalian Apg12p, but not the Apg12p-Apg5p conjugate, facilitates LC3 processing. Biochemical and Biophysical Research Communications 2002, 296(5):1164-1170. http://www.ncbi.nlm.nih.gov/pubmed/12207896, 10.1016/S0006-291X(02)02057-0.
13. Sou Y.S., Tanida I., Komatsu M., Ueno T., Kominami E. Phosphatidylserine in addition to phosphatidylethanolamine is an in vitro target of the mammalian Atg8 modifiers, LC3, GABARAP, and GATE-16. Journal of Biological Chemistry 2006, 281(6):3017-3024. http://www.ncbi.nlm.nih.gov/pubmed/16303767, 10.1074/jbc.M505888200.
14. Grüllich C., Duvoisin R.M., Wiedmann M., van Leyen K. Inhibition of 15-lipoxygenase leads to delayed organelle degradation in the reticulocyte. FEBS Letters 2001, 489(1):51-54. http://www.ncbi.nlm.nih.gov/pubmed/11231012, 10.1016/S0014-5793(01)02080-4.
15. Van Leyen K., Duvoisin R.M., Engelhardt H., Wiedmann M. A function for lipoxygenase in programmed organelle degradation. Nature 1998, 395(6700):392-395. http://www.ncbi.nlm.nih.gov/pubmed/9759730, 10.1038/26500.
16. Miller Y.I., Chang M.K., Funk C.D., Feramisco J.R., Witztum J.L. 12/15-Lipoxygenase translocation enhances site-specific actin polymerization in macrophages phagocytosing apoptotic cells. Journal of Biological Chemistry 2001, 276(22):19431-19439. http://www.ncbi.nlm.nih.gov/pubmed/11278875, 10.1074/jbc.M011276200.
17. Ferreira A.M., Ferrari M.I., Trostchansky A., Batthyany C., Souza J.M., Alvarez M.N., López G.V., Baker P.R., Schopfer F.J., O'Donnell V., Freeman B.A., Rubbo H. Macrophage activation induces formation of the anti-inflammatory lipid cholesteryl-nitrolinoleate. Biochemical Journal 2009, 417(1):223-234. http://www.ncbi.nlm.nih.gov/pubmed/18671672, 10.1042/BJ20080701.
18. Ichimura Y., Imamura Y., Emoto K., Umeda M., Noda T., Ohsumi Y. In vivo and in vitro reconstitution of Atg8 conjugation essential for autophagy. Journal of Biological Chemistry 2004, 279(39):40584-40592. http://www.ncbi.nlm.nih.gov/pubmed/15277523, 10.1074/jbc.M405860200.
19. Bassnett S., Beebe D.C. Coincident loss of mitochondria and nuclei during lens fiber cell differentiation. Developmental Dynamics 1992, 194(2):85-93. http://www.ncbi.nlm.nih.gov/pubmed/1421526, 10.1002/aja.1001940202.
20. Bassnett S., Mataic D. Chromatin degradation in differentiating fiber cells of the eye lens. Journal of Cell Biology 1997, 137(1):37-49. http://www.ncbi.nlm.nih.gov/pubmed/9105035, 10.1083/jcb.137.1.37.
21. Dahm R., Gribbon C., Quinlan R.A., Prescott A.R. Lens cell organelle loss during differentiation versus stress-induced apoptotic changes. Biochemical Society Transactions 1997, 25(4):S584. http://www.ncbi.nlm.nih.gov/pubmed/9450012.
22. Schewe T., Halangk W., Hiebsch C., Rapoport S.M. A lipoxygenase in rabbit reticulocytes which attacks phospholipids and intact mitochondria. FEBS Letters 1975, 60(1):149-152. http://www.ncbi.nlm.nih.gov/pubmed/6318, 10.1016/0014-5793(75)80439-X.
23. Schewe T., Halangk W., Hiebsch C., Rapoport S. Degradation of mitochondria by cytosolic factors in reticulocytes. Acta Biologica et Medica Germanica 1977, 36(3-4):563-572. http://www.ncbi.nlm.nih.gov/pubmed/202126.
24. Sun D., Funk C.D. Disruption of 12/15-lipoxygenase expression in peritoneal macrophages. Enhanced utilization of the 5-lipoxygenase pathway and diminished oxidation of low density lipoprotein. Journal of Biological Chemistry 1996, 271(39):24055-24062. http://www.ncbi.nlm.nih.gov/pubmed/8798642, 10.1074/jbc.271.39.24055.
25. Uderhardt S., Herrmann M., Oskolkova O.V., Aschermann S., Bicker W., Ipseiz N., Sarter K., Frey B., Rothe T., Voll R., Nimmerjahn F., Bochkov V.N., Schett G., Krönke G. 12/15-lipoxygenase orchestrates the clearance of apoptotic cells and maintains immunologic tolerance. Immunity 2012, 36(5):834-846. http://www.ncbi.nlm.nih.gov/pubmed/22503541, 10.1016/j.immuni.2012.03.010.
26. Osellame L.D., Duchen M.R. Quality control gone wrong: mitochondria, lysosomal storage disorders and neurodegeneration. British Journal of Pharmacology 2014, 171(8):1958-1972. http://www.ncbi.nlm.nih.gov/pubmed/24116849, 10.1111/bph.12453.
27. Osellame L.D., Duchen M.R. Defective quality control mechanisms and accumulation of damaged mitochondria link Gaucher and Parkinson diseases. Autophagy 2013, 9(10):1633-1635. http://www.ncbi.nlm.nih.gov/pubmed/23989665, 10.4161/auto.25878.
28. Osellame L.D., Rahim A.A., Hargreaves I.P., Gegg M.E., Richard-Londt A., Brandner S., Waddington S.N., Schapira A.H., Duchen M.R. Mitochondria and quality control defects in a mouse model of Gaucher disease-links to Parkinson's disease. Cell Metabolism 2013, 17(6):941-953. http://www.ncbi.nlm.nih.gov/pubmed/23707074, 10.1016/j.cmet.2013.04.014.
29. Raben N., Wong A., Ralston E., Myerowitz R. Autophagy and mitochondria in Pompe disease: nothing is so new as what has long been forgotten. American Journal of Medical Genetics Part C: Seminars in Medical Genetics 2012, 160C(1):13-21. http://www.ncbi.nlm.nih.gov/pubmed/22253254, 10.1002/ajmg.c.31317.
30. Kiselyov K., Soyombo A., Muallem S. TRPpathies. Journal of Physiology 2007, 578(3):641-653. http://www.ncbi.nlm.nih.gov/pubmed/17138610, 10.1113/jphysiol.2006.119024.
31. Mullock B.M., Bright N.A., Fearon C.W., Gray S.R., Luzio J.P. Fusion of lysosomes with late endosomes produces a hybrid organelle of intermediate density and is NSF dependent. Journal of Cell Biology 1998, 140(3):591-601. http://www.ncbi.nlm.nih.gov/pubmed/9456319, 10.1083/jcb.140.3.591.
32. Bright N.A., Reaves B.J., Mullock B.M., Luzio J.P. Dense core lysosomes can fuse with late endosomes and are re-formed from the resultant hybrid organelles. Journal of Cell Science 1997, 110(17):2027-2040. http://www.ncbi.nlm.nih.gov/pubmed/9378754.
33. Ponder K.P., Haskins M.E. Gene therapy for mucopolysaccharidosis. Expert Opinion on Biological Therapy 2007, 7(9):1333-1345. http://www.ncbi.nlm.nih.gov/pubmed/17727324, 10.1517/14712598.7.9.1333.
34. Gozuacik D., Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004, 23(16):2891-2906. http://www.ncbi.nlm.nih.gov/pubmed/15077152, 10.1038/sj.onc.1207521.
35. Scherz-Shouval R., Elazar Z. ROS, mitochondria and the regulation of autophagy. Trends in Cell Biology 2007, 17(9):422-427. http://www.ncbi.nlm.nih.gov/pubmed/17804237, 10.1016/j.tcb.2007.07.009.
36. Aflaki E., Stubblefield B.K., Maniwang E., Lopez G., Moaven N., Goldin E., Marugan J., Patnaik S., Dutra A., Southall N., Zheng W., Tayebi N., Sidransky E. Macrophage models of Gaucher disease for evaluating disease pathogenesis and candidate drugs. Science Translational Medicine 2014, 6(240):240ra273. http://www.ncbi.nlm.nih.gov/pubmed/24920659, 10.1126/scitranslmed.3008659.
37. Taylor P.R., Heydeck D., Jones G.W., Krönke G., Funk C.D., Knapper S., Adams D., Kühn H., O'Donnell V.B. Development of myeloproliferative disease in 12/15-lipoxygenase deficiency. Blood 2012, 119(25):6174-6175. http://www.ncbi.nlm.nih.gov/pubmed/22730527, 10.1182/blood-2012-02-410928.
38. Giorgio M., Migliaccio E., Orsini F., Paolucci D., Moroni M., Contursi C., Pelliccia G., Luzi L., Minucci S., Marcaccio M., Pinton P., Rizzuto R., Bernardi P., Paolucci F., Pelicci P.G. Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 2005, 122(2):221-233. http://www.ncbi.nlm.nih.gov/pubmed/16051147, 10.1016/j.cell.2005.05.011.
39. Kiselyov K., Jennigs J.J., Rbaibi Y., Chu C.T. Autophagy, mitochondria and cell death in lysosomal storage diseases. Autophagy 2007, 3(3):259-262. http://www.ncbi.nlm.nih.gov/pubmed/17329960, 10.4161/auto.3906.
40. Alroy J., Ucci A.A. Skin biopsy: a useful tool in the diagnosis of lysosomal storage diseases. Ultrastructural Pathology 2006, 30(6):489-503. http://www.ncbi.nlm.nih.gov/pubmed/17182441, 10.1080/01913120500520986.
41. Hammond V.J., Morgan A.H., Lauder S., Thomas C.P., Brown S., Freeman B.A., Lloyd C.M., Davies J., Bush A., Levonen A.L., Kansanen E., Villacorta L., Chen Y.E., Porter N., Garcia-Diaz Y.M., Schopfer F.J., O'Donnell V.B. Novel keto-phospholipids are generated by monocytes and macrophages, detected in cystic fibrosis, and activate peroxisome proliferator-activated receptor-γ. Journal of Biological Chemistry 2012, 287(50):41651-41666. http://www.ncbi.nlm.nih.gov/pubmed/23060450, 10.1074/jbc.M112.405407.
42. Huo Y., Zhao L., Hyman M.C., Shashkin P., Harry B.L., Burcin T., Forlow S.B., Stark M.A., Smith D.F., Clarke S., Srinivasan S., Hedrick C.C., Praticò D., Witztum J.L., Nadler J.L., Funk C.D., Ley K. Critical role of macrophage 12/15-lipoxygenase for atherosclerosis in apolipoprotein E-deficient mice. Circulation 2004, 110(14):2024-2031. http://www.ncbi.nlm.nih.gov/pubmed/15451785, 10.1161/01.CIR.0000143628.37680.F6.
43. Harats D., Shaish A., George J., Mulkins M., Kurihara H., Levkovitz H., Sigal E. Overexpression of 15-lipoxygenase in vascular endothelium accelerates early atherosclerosis in LDL receptor-deficient mice. Arteriosclerosis, Thrombosis, and Vascular Biology 2000, 20(9):2100-2105. http://www.ncbi.nlm.nih.gov/pubmed/10978255, 10.1161/01.ATV.20.9.2100.
44. Sanjuan M.A., Dillon C.P., Tait S.W., Moshiach S., Dorsey F., Connell S., Komatsu M., Tanaka K., Cleveland J.L., Withoff S., Green D.R. Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 2007, 450(7173):1253-1257. http://www.ncbi.nlm.nih.gov/pubmed/18097414, 10.1038/nature06421.