Phosphatidic acid (PA)-Preferring phospholipase A1 regulates mitochondrial dynamics

Journal of Biological Chemistry

Volumn 289, Issue 16, 2014, Pages 11497-11511

  Baba, Takashi ^a   Kashiwagi, Yuriko ^a   Arimitsu, Nagisa ^a   Kogure, Takeshi ^a   Edo, Ayumi ^a   Maruyama, Tomohiro ^a   Nakao, Kazuki ^b   Nakanishi, Hiroki ^c   Kinoshita, Makoto ^d   Frohman, Michael A ^e   Yamamoto, Akitsugu ^f   Tani, Katsuko ^a  

^a TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^b RIKEN Center for Biosystems Dynamics Research   (Japan)

^c AKITA UNIVERSITY   (Japan)

^d NAGOYA UNIVERSITY   (Japan)

^e STONY BROOK UNIVERSITY   (United States)

^f NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; DYNAMICS;

ACTIVITY-DEPENDENT; GENE DISRUPTIONS; MEMBRANE DYNAMICS; MITOCHONDRIAL MEMBRANES; MITOCHONDRIAL MORPHOLOGY; PHOSPHATIDIC ACIDS; PHOSPHOLIPASES; POSSIBLE MECHANISMS;

MITOCHONDRIA;

CARDIOLIPIN; MITOCHONDRIAL PHOSPHOLIPASE D; PHOSPHATIDIC ACID; PHOSPHATIDIC ACID PREFERRING PHOSPHOLIPASE A1; PHOSPHOLIPASE A1; PHOSPHOLIPASE D; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; HELA CELL LINE; KNOCKOUT MOUSE; MALE; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEMEN ABNORMALITY; SPERMATOGENESIS; SPERMATOZOON MOTILITY; SPERMATOZOON TAIL; SUBFERTILITY; TESTIS;

MEMBRANE; MITOCHONDRIA; PHOSPHATIDIC ACID; PHOSPHOLIPASE A; SPERM;

ANIMALS; CARDIOLIPINS; HELA CELLS; HUMANS; MALE; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; PHOSPHATIDATE PHOSPHATASE; PHOSPHATIDIC ACIDS; PHOSPHOLIPASE D; SPERM TAIL; SPERMATOGENESIS;

EID: 84898995787     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.531921     Document Type: Article

References (46)

1. Haucke, V., and Di Paolo, G. (2007) Lipids and lipid modifications in the regulation of membrane traffic. Curr. Opin. Cell Biol. 19, 426-435
2. Wang, X., Devaiah, S. P., Zhang, W., and Welti, R. (2006) Signaling functions of phosphatidic acid. Prog. Lipid Res. 45, 250-278
3. Ha, K. D., Clarke, B. A., and Brown, W. J. (2012) Regulation of the Golgi complex by phospholipid remodeling enzymes. Biochim. Biophys. Acta 1821, 1078-1088
4. Han, G. S., and Carman, G. M. (2010) Characterization of the human LPIN1-encoded phosphatidate phosphatase isoforms. J. Biol. Chem. 285, 14628-14638
5. Shindou, H., Hishikawa, D., Harayama, T., Eto, M., and Shimizu, T. (2013) Generation of membrane diversity by lysophospholipid acyltransferases. J. Biochem. 154, 21-28
6. Youle, R. J., and van der Bliek, A. M. (2012) Mitochondrial fission, fusion, and stress. Science 337, 1062-1065
7. Yang, C. Y., and Frohman, M. A. (2012) Mitochondria: Signaling with phosphatidic acid. Int. J. Biochem. Cell Biol. 44, 1346-1350
8. Choi, S. Y., Huang, P., Jenkins, G. M., Chan, D. C., Schiller, J., and Frohman, M. A. (2006) A common lipid links Mfn-mediated mitochondrial fusion and SNARE-regulated exocytosis. Nat. Cell Biol. 8, 1255-1262
9. Huang, H., Gao, Q., Peng, X., Choi, S. Y., Sarma, K., Ren, H., Morris, A. J., and Frohman, M. A. (2011) piRNA-Associated germline nuage formation and spermatogenesis require MitoPLD profusogenic mitochondrial-surface lipid signaling. Dev. Cell 20, 376-387
10. Muliyil, S., Krishnakumar, P., and Narasimha, M. (2011) Spatial, temporal and molecular hierarchies in the link between death, delamination and dorsal closure. Development 138, 3043-3054
11. Tani, K., Kogure, T., and Inoue, H. (2013) Intracellular phospholipase A1. Biomol. Concepts 3, 471-478
12. Higgs, H. N., Han, M. H., Johnson, G. E., and Glomset, J. A. (1998) Cloning of a phosphatidic acid-preferring phospholipase A1 from bovine testis. J. Biol. Chem. 273, 5468-5477
13. Nakajima, K., Sonoda, H., Mizoguchi, T., Aoki, J., Arai, H., Nagahama, M., Tagaya, M., and Tani, K. (2002) A novel phospholipase A1 with sequence homology to a mammalian Sec23p-interacting protein, p125. J. Biol. Chem. 277, 11329-11335
14. Tani, K., Mizoguchi, T., Iwamatsu, A., Hatsuzawa, K., and Tagaya, M. (1999) p125 is a novel mammalian Sec23p-interacting protein with structural similarity to phospholipid-modifying proteins. J. Biol. Chem. 274, 20505-20512
15. Higgs, H. N., and Glomset, J. A. (1994) Identification of a phosphatidic acid-preferring phospholipase Al from bovine brain and testis. Proc. Natl. Acad. Sci. U.S.A. 91, 9574-9578
16. Tesson, C., Nawara, M., Salih, M. A., Rossignol, R., Zaki, M. S., Al Balwi, M., Schule, R., Mignot, C., Obre, E., Bouhouche, A., Santorelli, F. M., Durand, C. M., Oteyza, A. C., El-Hachimi, K. H., Al Drees, A., Bouslam, N., Lamari, F., Elmalik, S. A., Kabiraj, M. M., Seidahmed, M. Z., Esteves, T., Gaussen, M., Monin, M. L., Gyapay, G., Lechner, D., Gonzalez, M., Depienne, C., Mochel, F., Lavie, J., Schols, L., Lacombe, D., Yahyaoui, M., Al Abdulkareem, I., Zuchner, S., Yamashita, A., Benomar A., Goizet, C., Durr A., Gleeson, J. G., Darios, F., Brice, A., and Stevanin, G. (2012) Alteration of fatty-Acid-metabolizing enzymes affects mitochondrial form and function in hereditary spastic paraplegia. Am. J. Hum. Genet. 91, 1051-1064
17. Blackstone, C. (2012) Cellular pathways of hereditary spastic paraplegia. Annu. Rev. Neurosci. 35, 25-47
18. Shimoi, W., Ezawa, I., Nakamoto, K., Uesaki, S., Gabreski, G., Aridor, M., Yamamoto, A., Nagahama, M., Tagaya, M., and Tani, K. (2005) p125 is localized in endoplasmic reticulum exit sites and involved in their organization. J. Biol. Chem. 280, 10141-10148
19. Ihara, M., Kinoshita, A., Yamada, S., Tanaka, H., Tanigaki, A., Kitano, A., Goto, M., Okubo, K., Nishiyama, H., Ogawa, O., Takahashi, C., Itohara, S., Nishimune, Y., Noda, M., and Kinoshita, M. (2005) Cortical organization by the septin cytoskeleton is essential for structural and mechanical integrity of mammalian spermatozoa. Dev. Cell 8, 343-352
20. Iinuma, T., Shiga, A., Nakamoto, K., O'Brien, M. B., Aridor, M., Arimitsu, N., Tagaya, M., and Tani, K. (2007) Mammalian Sec16/p250 plays a role in membrane traffic from the endoplasmic reticulum. J. Biol. Chem. 282, 17632-17639
21. Arimitsu, N., Kogure, T., Baba, T., Nakao, K., Hamamoto, H., Sekimizu, K., Yamamoto, A., Nakanishi, H., Taguchi, R., Tagaya, M., and Tani, K. (2011) p125/Sec23-interacting protein (Sec23ip) is required for spermiogenesis. FEBS Lett. 585, 2171-2176
22. Baba, T., Yamamoto, A., Tagaya, M., and Tani, K. (2013) A lysophospholipid acyltransferase antagonist, CI-976, creates novel membrane tubules marked by intracellular phospholipase A1 KIAA0725p. Mol. Cell. Biochem. 376, 151-161
23. Inoue, H., Baba, T., Sato, S., Ohtsuki, R., Takemori, A., Watanabe, T., Tagaya, M., and Tani, K. (2012) Roles of SAM and DDHD domains in mammalian intracellular phospholipase A1 KIAA0725p. Biochim. Biophys. Acta 1823, 930-939
24. Suzuki, J., Sukezane, T., Akagi, T., Georgescu, M. M., Ohtani, M., Inoue, H., Jat, P. S., Goff, S. P., Hanafusa, H., and Shishido, T. (2004) Loss of c-Abl facilitates anchorage-independent growth of p53-And RB-deficient primary mouse embryonic fibroblasts. Oncogene 23, 8527-8534
25. Ishihara, N., Jofuku, A., Eura, Y., and Mihara, K. (2003) Regulation of mitochondrial morphology by membrane potential, and DRP1-dependen division and FZO1-dependent fusion reaction in mammalian cells. Biochem. Biophys. Res. Commun. 301, 891-898
26. Smirnova, E., Griparic, L., Shurland, D. L., and van der Bliek, A. M. (2001) Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol. Biol. Cell 12, 2245-2256
27. Zhao, J., Liu, T., Jin, S., Wang, X., Qu, M., Uhlén, P., Tomilin, N., Shupliakov, O., Lendahl, U., and Nistér, M. (2011) Human MIEF1 recruits Drp1 to mitochondrial outer membranes and promotes mitochondrial fusion rather than fission. EMBO J. 30, 2762-2778
28. Rizzo, M. A., Shome, K., Watkins, S. C., and Romero, G. (2000) The recruitment of Raf-1 to membranes is mediated by direct interaction with phosphatidic acid and is independent of association with Ras. J. Biol. Chem. 275, 23911-23918
29. Bligh, E. G., and Dyer, W. J. (1959)Arapid method for total lipid extraction and purification. Can. J. Biochem. Physiol. 37, 911-917
30. Fawcett, D. W. (1970) A comparative view of sperm ultrastructure. Biol. Reprod. 2, Suppl. 2, 90-127
31. Russell, L. D. (1990) Histological and Histopathological Evaluation of the Testis, pp. 119-161, Cache River Press, Clearwater, FL
32. Imai, H., Hakkaku, N., Iwamoto, R., Suzuki, J., Suzuki, T., Tajima, Y., Konishi, K., Minami, S., Ichinose, S., Ishizaka, K., Shioda, S., Arata, S., Nishimura, M., Naito, S., and Nakagawa, Y. (2009) Depletion of selenoprotein GPx4 in spermatocytes causes male infertility in mice. J. Biol. Chem. 284, 32522-32532
33. Schneider, M., Förster, H., Boersma, A., Seiler, A., Wehnes, H., Sinowatz, F., Neumüller, C., Deutsch, M. J., Walch, A., Hrabé de Angelis, M., Wurst, W., Ursini, F., Roveri, A., Maleszewski, M., Maiorino, M., and Conrad M. (2009) Mitochondrial glutathione peroxidase 4 disruption causes male infertility. FASEB J. 23, 3233-3242
34. Huh, W. K., Falvo, J. V., Gerke, L. C., Carroll, A. S., Howson, R. W., Weissman, J. S., and O'Shea, E. K. (2003) Global analysis of protein localization in budding yeast. Nature 425, 686-691
35. Connerth, M., Tatsuta, T., Haag, M., Klecker, T., Westermann, B., and Langer, T. (2012) Intramitochondrial transport of phosphatidic acid in yeast by a lipid transfer protein. Science 338, 815-818
36. Cowell, C. F., Döppler, H., Yan, I. K., Hausser, A., Umezawa, Y., and Storz, P. (2009) Mitochondrial diacylglycerol initiates protein-kinase D1-mediated ROS signaling. J. Cell Sci. 122, 919-928
37. Jin, J. K., Kim, N. H., Lee, Y. J., Kim, Y. S., Choi, E. K., Kozlowski, P. B., Park, M. H., Kim, H. S., and Min do, S. (2006) Phospholipase D1 is up-regulated in the mitochondrial fraction from the brains of Alzheimer's disease patients. Neurosci. Lett. 407, 263-267
38. Watanabe, T., Chuma, S., Yamamoto, Y., Kuramochi-Miyagawa, S., Totoki, Y., Toyoda, A., Hoki, Y., Fujiyama, A., Shibata, T., Sado, T., Noce, T., Nakano, T., Nakatsuji, N., Lin, H., and Sasaki, H. (2011) MITOPLD is a mitochondrial protein essential for nuage formation and piRNA biogenesis in the mouse germline. Dev. Cell 20, 364-375
39. Pillai, R. S., and Chuma, S. (2012) piRNAs and their involvement in male germline development in mice. Dev. Growth Differ. 54, 78-92
40. Hales, K. G., and Fuller, M. T. (1997) Developmentally regulated mitochondrial fusion mediated by a conserved, novel, predicted GTPase. Cell 90, 121-129
41. Honda, S., and Hirose, S. (2003) Stage-specific enhanced expression of mitochondrial fusion and fission factors during spermatogenesis in rat testis. Biochem. Biophys. Res. Commun. 311, 424-432
42. Schuurs-Hoeijmakers, J. H., Geraghty, M. T., Kamsteeg, E. J., Ben-Salem, S., de Bot, S. T., Nijhof, B., van de Vondervoort, I. I., van der Graaf, M., Nobau, A. C., Otte-Höller, I., Vermeer, S., Smith, A. C., Humphreys, P., Schwartzentruber, J., FORGE Canada Consortium., Ali, B. R., Al-Yahyaee, S. A., Tariq, S., Pramathan, T., Bayoumi, R., Kremer, H. P., van de Warrenburg, B. P., van den Akker, W. M., Gilissen, C., Veltman, J. A., Janssen, I. M., Vulto-van Silfhout, A. T., van der Velde-Visser, S., Lefeber, D. J., Diekstra, A., Erasmus, C. E., Willemsen, M. A., Vissers, L. E., Lammens, M., van Bokhoven, H., Brunner, H. G., Wevers, R. A., Schenck, A., Al-Gazali, L., de Vries, B. B., and de Brouwer, A. P. (2012) Mutations in DDHD2, encoding an intracellular phospholipase A1, cause a recessive form of complex hereditary spastic paraplegia. Am. J. Hum. Genet. 91, 1073-1081
43. Gonzalez, M., Nampoothiri, S., Kornblum, C., Oteyza, A. C., Walter, J., Konidari, I., Hulme, W., Speziani, F., Schöls, L., Züchner, S., and Schüle, R. (2013) Mutations in phospholipase DDHD2 cause autosomal recessive hereditary spastic paraplegia (SPG54). Eur. J. Hum. Genet. 21, 1214-1218
44. Douglas, D. S., Moran, J. L., Bermingham, J. R. Jr., Chen, X. J., Brindley, D. N., Soliven, B., Beier, D. R., and Popko, B. (2009) Concurrent Lpin1 and Nrcam mouse mutations result in severe peripheral neuropathy with transitory hindlimb paralysis. J. Neurosci. 29, 12089-12100
45. Nadra, K., de Preux Charles, A. S., Médard, J. J., Hendriks, W. T., Han, G. S., Grès, S., Carman, G. M., Saulnier-Blache, J. S., Verheijen, M. H., and Chrast, R. (2008) Phosphatidic acid mediates demyelination in Lpin1 mutant mice. Genes Dev. 22, 1647-1661
46. Mul, J. D., Nadra, K., Jagalur, N. B., Nijman, I. J., Toonen, P. W., Médard, J. J., Grès, S., de Bruin, A., Han, G. S., Brouwers, J. F., Carman, G. M., Saulnier-Blache, J. S., Meijer, D., Chrast, R., and Cuppen, E. (2011) A hypomorphic mutation in Lpin1 induces progressively improving neuropathy and lipodystrophy in the rat. J. Biol. Chem. 286, 26781-26793