Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Phospholipase D and Its Essential Role in Cancer

  • Cho, Ju Hwan (Arthur G. James Cancer Hospital Comprehensive Cancer Center, The Ohio State University) ;
  • Han, Joong-Soo (Biomedical Research Institute and Department of Biochemistry & Molecular Biology, College of Medicine, Hanyang University)
  • Received : 2017.09.28
  • Accepted : 2017.11.11
  • Published : 2017.11.30
Download PDF
⟨ Previous Next ⟩

Abstract

The role of phospholipase D (PLD) in cancer development and management has been a major area of interest for researchers. The purpose of this mini-review is to explore PLD and its distinct role during chemotherapy including anti-apoptotic function. PLD is an enzyme that belongs to the phospholipase super family and is found in a broad range of organisms such as viruses, yeast, bacteria, animals, and plants. The function and activity of PLD are widely dependent on and regulated by neurotransmitters, hormones, small monomeric GTPases, and lipids. A growing body of research has shown that PLD activity is significantly increased in cancer tissues and cells, indicating that it plays a critical role in signal transduction, cell proliferation, and anti-apoptotic processes. In addition, recent studies show that PLD is a downstream transcriptional target of proteins that contribute to inflammation and carcinogenesis such as Sp1, $NF{\kappa}B$, TCF4, ATF-2, NFATc2, and EWS-Fli. Thus, compounds that inhibit expression or activity of PLD in cells can be potentially useful in reducing inflammation and sensitizing resistant cancers during chemotherapy.

Keywords

References

  1. Alberghina, M. (2010). Phospholipase A(2): new lessons from endothelial cells. Microvasc. Res. 80, 280-285. https://doi.org/10.1016/j.mvr.2010.03.013
  2. Ammar, M.R., Kassas, N., Chasserot-Golaz, S., Bader, M.F., and Vitale, N. (2013). Lipids in Regulated Exocytosis: What are They Doing? Front. Endocrinol. 4, 125.
  3. Aoki, J. (2004). Mechanisms of lysophosphatidic acid production. Semin. Cell Dev. Biol. 15, 477-489. https://doi.org/10.1016/j.semcdb.2004.05.001
  4. Aoki, J., Inoue, A., Makide, K., Saiki, N., and Arai, H. (2007). Structure and function of extracellular phospholipase A1 belonging to the pancreatic lipase gene family. Biochimie 89, 197-204. https://doi.org/10.1016/j.biochi.2006.09.021
  5. Baba, T., Kashiwagi, Y., Arimitsu, N., Kogure, T., Edo, A., Maruyama, T., Nakao, K., Nakanishi, H., Kinoshita, M., Frohman, M.A., et al. (2014). Phosphatidic acid (PA)-preferring phospholipase A1 regulates mitochondrial dynamics. J. Biol. Chem. 289, 11497-11511. https://doi.org/10.1074/jbc.M113.531921
  6. Bae, E.J., Lee, H.J., Jang, Y.H., Michael, S., Masliah, E., Min, D.S., and Lee, S.J. (2014). Phospholipase D1 regulates autophagic flux and clearance of alpha-synuclein aggregates. Cell Death Differ. 21, 1132-1141. https://doi.org/10.1038/cdd.2014.30
  7. Bartel, D.P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233. https://doi.org/10.1016/j.cell.2009.01.002
  8. Billah, M.M., Eckel, S., Mullmann, T.J., Egan, R.W., and Siegel, M.I. (1989). Phosphatidylcholine hydrolysis by phospholipase D determines phosphatidate and diglyceride levels in chemotactic peptide-stimulated human neutrophils. Involvement of phosphatidate phosphohydrolase in signal transduction. J. Biol. Chem. 264, 17069-17077.
  9. Brown, H.A., Henage, L.G., Preininger, A.M., Xiang, Y., and Exton, J.H. (2007). Biochemical analysis of phospholipase D. Methods Enzymol. 434, 49-87.
  10. Bruntz, R.C., Lindsley, C.W., and Brown, H.A. (2014a). Phospholipase D signaling pathways and phosphatidic acid as therapeutic targets in cancer. Pharmacol. Rev. 66, 1033-1079. https://doi.org/10.1124/pr.114.009217
  11. Bruntz, R.C., Taylor, H.E., Lindsley, C.W., and Brown, H.A. (2014b). Phospholipase D2 mediates survival signaling through direct regulation of Akt in glioblastoma cells. J. Biol. Chem. 289, 600-616. https://doi.org/10.1074/jbc.M113.532978
  12. Burkhardt, U., Stegner, D., Hattingen, E., Beyer, S., Nieswandt, B., and Klein, J. (2014). Impaired brain development and reduced cognitive function in phospholipase D-deficient mice. Neurosci. Lett. 572, 48-52. https://doi.org/10.1016/j.neulet.2014.04.052
  13. Chabner, B.A., and Roberts, T.G., Jr. (2005). Timeline: Chemotherapy and the war on cancer. Nat. Rev. Cancer 5, 65-72. https://doi.org/10.1038/nrc1529
  14. Chen, Y., Jungsuwadee, P., Vore, M., Butterfield, D.A., and St Clair, D.K. (2007). Collateral damage in cancer chemotherapy: oxidative stress in nontargeted tissues. Mol. Inter. 7, 147-156. https://doi.org/10.1124/mi.7.3.6
  15. Chen, Q., Hongu, T., Sato, T., Zhang, Y., Ali, W., Cavallo, J.A., van der Velden, A., Tian, H., Di Paolo, G., Nieswandt, B., et al. (2012). Key roles for the lipid signaling enzyme phospholipase d1 in the tumor microenvironment during tumor angiogenesis and metastasis. Sci. Signal. 5, ra79.
  16. Chen, Z., Li, D., Cheng, Q., Ma, Z., Jiang, B., Peng, R., Chen, R., Cao, Y., and Wan, X. (2014). MicroRNA-203 inhibits the proliferation and invasion of U251 glioblastoma cells by directly targeting PLD2. Mol. Med. Rep. 9, 503-508. https://doi.org/10.3892/mmr.2013.1814
  17. Cho, C.H., Lee, C.S., Chang, M., Jang, I.H., Kim, S.J., Hwang, I., Ryu, S.H., Lee, C.O., and Koh, G.Y. (2004). Localization of VEGFR-2 and PLD2 in endothelial caveolae is involved in VEGF-induced phosphorylation of MEK and ERK. American journal of physiology. Heart Circ. Physiol. 286, H1881-1888. https://doi.org/10.1152/ajpheart.00786.2003
  18. Cho, J.H., Hong, S.K., Kim, E.Y., Park, S.Y., Park, C.H., Kim, J.M., Kwon, O.J., Kwon, S.J., Lee, K.S., and Han, J.S. (2008). Overexpression of phospholipase D suppresses taxotere-induced cell death in stomach cancer cells. Biochim. Biophys. Acta 1783, 912-923. https://doi.org/10.1016/j.bbamcr.2007.11.019
  19. Cho, J.H., Oh, D.Y., Kim, H.J., Park, S.Y., Choi, H.J., Kwon, S.J., Lee, K.S., and Han, J.S. (2011). The TSP motif in AP180 inhibits phospholipase D1 activity resulting in increased efficacy of anticancer drug via its direct binding to carboxyl terminal of phospholipase D1. Cancer Lett. 302, 144-154. https://doi.org/10.1016/j.canlet.2011.01.005
  20. Choi, W.S., Chahdi, A., Kim, Y.M., Fraundorfer, P.F., and Beaven, M.A. (2002). Regulation of phospholipase D and secretion in mast cells by protein kinase A and other protein kinases. Ann. N Y Acad. Sci. 968, 198-212. https://doi.org/10.1111/j.1749-6632.2002.tb04336.x
  21. Choi, W.S., Hiragun, T., Lee, J.H., Kim, Y.M., Kim, H.P., Chahdi, A., Her, E., Han, J.W., and Beaven, M.A. (2004). Activation of RBL-2H3 mast cells is dependent on tyrosine phosphorylation of phospholipase D2 by Fyn and Fgr. Mol. Cell. Biol. 24, 6980-6992. https://doi.org/10.1128/MCB.24.16.6980-6992.2004
  22. Choi, H.J., Lee, J.H., Park, S.Y., Cho, J.H., and Han, J.S. (2009). STAT3 is involved in phosphatidic acid-induced Bcl-2 expression in HeLa cells. Exp. Mol. Med. 41, 94-101. https://doi.org/10.3858/emm.2009.41.2.012
  23. Colley, W.C., Sung, T.C., Roll, R., Jenco, J., Hammond, S.M., Altshuller, Y., Bar-Sagi, D., Morris, A.J., and Frohman, M.A. (1997). Phospholipase D2, a distinct phospholipase D isoform with novel regulatory properties that provokes cytoskeletal reorganization. Curr. Biol. 7, 191-201. https://doi.org/10.1016/S0960-9822(97)70090-3
  24. Corrotte, M., Chasserot-Golaz, S., Huang, P., Du, G., Ktistakis, N.T., Frohman, M.A., Vitale, N., Bader, M.F., and Grant, N.J. (2006). Dynamics and function of phospholipase D and phosphatidic acid during phagocytosis. Traffic 7, 365-377. https://doi.org/10.1111/j.1600-0854.2006.00389.x
  25. Cruchaga, C., Karch, C.M., Jin, S.C., Benitez, B.A., Cai, Y., Guerreiro, R., Harari, O., Norton, J., Budde, J., Bertelsen, S., et al. (2014). Rare coding variants in the phospholipase D3 gene confer risk for Alzheimer's disease. Nature 505, 550-554. https://doi.org/10.1038/nature12825
  26. Csaki, L.S., Dwyer, J.R., Fong, L.G., Tontonoz, P., Young, S.G., and Reue, K. (2013). Lipins, lipinopathies, and the modulation of cellular lipid storage and signaling. Prog. Lipid Res. 52, 305-316. https://doi.org/10.1016/j.plipres.2013.04.001
  27. Cunningham, D., Atkin, W., Lenz, H.J., Lynch, H.T., Minsky, B., Nordlinger, B., and Starling, N. (2010). Colorectal cancer. Lancet 375, 1030-1047. https://doi.org/10.1016/S0140-6736(10)60353-4
  28. Dent, M.R., Singal, T., Dhalla, N.S., and Tappia, P.S. (2004). Expression of phospholipase D isozymes in scar and viable tissue in congestive heart failure due to myocardial infarction. J. Cell. Mol. Med. 8, 526-536. https://doi.org/10.1111/j.1582-4934.2004.tb00477.x
  29. DeVita, V.T., Jr. (2002). A perspective on the war on cancer. Cancer J. 8, 352-356. https://doi.org/10.1097/00130404-200209000-00002
  30. DeVita, V.T., Jr., and Chu, E. (2008). A history of cancer chemotherapy. Cancer Res. 68, 8643-8653. https://doi.org/10.1158/0008-5472.CAN-07-6611
  31. Dhingra, S., Rodriguez, M.E., Shen, Q., Duan, X., Stanton, M.L., Chen, L., Zhang, R., and Brown, R.E. (2010). Constitutive activation with overexpression of the mTORC2-phospholipase D1 pathway in uterine leiomyosarcoma and STUMP: morphoproteomic analysis with therapeutic implications. Int. J. Clin. Exp. Pathol. 4, 134-146.
  32. Elvers, M., Stegner, D., Hagedorn, I., Kleinschnitz, C., Braun, A., Kuijpers, M.E., Boesl, M., Chen, Q., Heemskerk, J.W., Stoll, G., et al. (2010). Impaired alpha(IIb)beta(3) integrin activation and sheardependent thrombus formation in mice lacking phospholipase D1. Sci. Signal. 3, ra1.
  33. Fabbrocini, G., Cameli, N., Romano, M.C., Mariano, M., Panariello, L., Bianca, D., and Monfrecola, G. (2012). Chemotherapy and skin reactions. J. Exp. Clin. Cancer Res. 31, 50. https://doi.org/10.1186/1756-9966-31-50
  34. Farooqui, A.A., and Horrocks, L.A. (2005). Signaling and interplay mediated by phospholipases A2, C, and D in LA-N-1 cell nuclei. Reprod. Nutr. Dev. 45, 613-631. https://doi.org/10.1051/rnd:2005049
  35. Fite, K., Elkhadragy, L., and Gomez-Cambronero, J. (2016). A repertoire of microRNAs regulates cancer cell starvation by targeting phospholipase D in a feedback loop that operates maximally in cancer cells. Mol. Cell. Biol. 36, 1078-1089. https://doi.org/10.1128/MCB.00711-15
  36. Foster, D.A., Salloum, D., Menon, D., and Frias, M.A. (2014). Phospholipase D and the maintenance of phosphatidic acid levels for regulation of mammalian target of rapamycin (mTOR). J. Biol. Chem. 289, 22583-22588. https://doi.org/10.1074/jbc.R114.566091
  37. Frohman, M.A. (2015). The phospholipase D superfamily as therapeutic targets. Trends Pharmacol. Sci. 36, 137-144. https://doi.org/10.1016/j.tips.2015.01.001
  38. Ghim, J., Moon, J.S., Lee, C.S., Lee, J., Song, P., Lee, A., Jang, J.H., Kim, D., Yoon, J.H., Koh, Y.J., et al. (2014). Endothelial deletion of phospholipase D2 reduces hypoxic response and pathological angiogenesis. Arterioscler. Thromb. Vasc. Biol. 34, 1697-1703. https://doi.org/10.1161/ATVBAHA.114.303416
  39. Gobel, K., Schuhmann, M.K., Pankratz, S., Stegner, D., Herrmann, A.M., Braun, A., Breuer, J., Bittner, S., Ruck, T., Wiendl, H., et al. (2014). Phospholipase D1 mediates lymphocyte adhesion and migration in experimental autoimmune encephalomyelitis. Eur. J. Immunol. 44, 2295-2305. https://doi.org/10.1002/eji.201344107
  40. Gomez-Cambronero, J. (2010). New concepts in phospholipase D signaling in inflammation and cancer. TheScientificWorldJournal 10, 1356-1369. https://doi.org/10.1100/tsw.2010.116
  41. Gozgit, J.M., Pentecost, B.T., Marconi, S.A., Ricketts-Loriaux, R.S., Otis, C.N., and Arcaro, K.F. (2007). PLD1 is overexpressed in an ER-negative MCF-7 cell line variant and a subset of phospho-Akt-negative breast carcinomas. Br. J. Cancer 97, 809-817. https://doi.org/10.1038/sj.bjc.6603926
  42. Hammond, S.M., Altshuller, Y.M., Sung, T.C., Rudge, S.A., Rose, K., Engebrecht, J., Morris, A.J., and Frohman, M.A. (1995). Human ADP-ribosylation factor-activated phosphatidylcholine-specific phospholipase D defines a new and highly conserved gene family. J. Biol. Chem. 270, 29640-29643. https://doi.org/10.1074/jbc.270.50.29640
  43. Han, S., Huh, J., Kim, W., Jeong, S., Min do, S., and Jung, Y. (2014). Phospholipase D activates HIF-1-VEGF pathway via phosphatidic acid. Exp. Mol. Med. 46, e126. https://doi.org/10.1038/emm.2014.86
  44. Henkels, K.M., Boivin, G.P., Dudley, E.S., Berberich, S.J., and Gomez-Cambronero, J. (2013). Phospholipase D (PLD) drives cell invasion, tumor growth and metastasis in a human breast cancer xenograph model. Oncogene 32, 5551-5562. https://doi.org/10.1038/onc.2013.207
  45. Jang, Y.H., Ahn, B.H., Namkoong, S., Kim, Y.M., Jin, J.K., Kim, Y.S., and Min do, S. (2008). Differential regulation of apoptosis by caspase-mediated cleavage of phospholipase D isozymes. Cell. Signal. 20, 2198-2207. https://doi.org/10.1016/j.cellsig.2008.07.010
  46. Jang, J.H., Lee, C.S., Hwang, D., and Ryu, S.H. (2012). Understanding of the roles of phospholipase D and phosphatidic acid through their binding partners. Prog. Lipid Res. 51, 71-81. https://doi.org/10.1016/j.plipres.2011.12.003
  47. 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. https://doi.org/10.1016/j.neulet.2006.08.062
  48. Joseph, T., Bryant, A., Frankel, P., Wooden, R., Kerkhoff, E., Rapp, U.R., and Foster, D.A. (2002). Phospholipase D overcomes cell cycle arrest induced by high-intensity Raf signaling. Oncogene 21, 3651-3658. https://doi.org/10.1038/sj.onc.1205380
  49. Kang, D.W., Choi, K.Y., and Min do, S. (2014). Functional regulation of phospholipase D expression in cancer and inflammation. J. Biol. Chem. 289, 22575-22582. https://doi.org/10.1074/jbc.R114.569822
  50. Kushi, L.H., Doyle, C., McCullough, M., Rock, C.L., Demark-Wahnefried, W., Bandera, E.V., Gapstur, S., Patel, A.V., Andrews, K., and Gansler, T. (2012). American Cancer Society Guidelines on nutrition and physical activity for cancer prevention: reducing the risk of cancer with healthy food choices and physical activity. CA Cancer J. Clin. 62, 30-67. https://doi.org/10.3322/caac.20140
  51. Lavieri, R., Scott, S.A., Lewis, J.A., Selvy, P.E., Armstrong, M.D., Alex Brown, H., and Lindsley, C.W. (2009). Design and synthesis of isoform-selective phospholipase D (PLD) inhibitors. Part II. Identification of the 1,3,8-triazaspiro[4,5]decan-4-one privileged structure that engenders PLD2 selectivity. Bioorganic Med. Chem. Lett. 19, 2240-2243. https://doi.org/10.1016/j.bmcl.2009.02.125
  52. Lavieri, R.R., Scott, S.A., Selvy, P.E., Kim, K., Jadhav, S., Morrison, R.D., Daniels, J.S., Brown, H.A., and Lindsley, C.W. (2010). Design, synthesis, and biological evaluation of halogenated N-(2-(4-oxo-1-phenyl-1,3,8-triazaspiro[4.5]decan-8-yl)ethyl)benzamides: discovery of an isoform-selective small molecule phospholipase D2 inhibitor. J. Med. Chem. 53, 6706-6719. https://doi.org/10.1021/jm100814g
  53. Le Stunff, H., Peterson, C., Liu, H., Milstien, S., and Spiegel, S. (2002). Sphingosine-1-phosphate and lipid phosphohydrolases. Biochimica et biophysica acta 1582, 8-17. https://doi.org/10.1016/S1388-1981(02)00132-4
  54. Lee, C.S., Bae, Y.S., Lee, S.D., Suh, P.G., and Ryu, S.H. (2001). ATP-induced mitogenesis is modulated by phospholipase D2 through extracellular signal regulated protein kinase dephosphorylation in rat pheochromocytoma PC12 cells. Neurosci. Lett. 313, 117-120. https://doi.org/10.1016/S0304-3940(01)02233-9
  55. Lee, S.Y., Oh, J.Y., Lee, M.J., Jang, M.J., Park, H.Y., Kim, J.W., Min, D.S., Park, Y.M., Chang, Y.C., Bae, Y.S., et al. (2004). Anti-apoptotic mechanism and reduced expression of phospholipase D in spontaneous and Fas-stimulated apoptosis of human neutrophils. Eur. J. Immunol. 34, 2760-2770. https://doi.org/10.1002/eji.200425117
  56. Lee, C.S., Kim, K.L., Jang, J.H., Choi, Y.S., Suh, P.G., and Ryu, S.H. (2009). The roles of phospholipase D in EGFR signaling. Biochimi. Biophys. Acta 1791, 862-868. https://doi.org/10.1016/j.bbalip.2009.04.007
  57. Lerchner, A., Mansfeld, J., Schaffner, I., Schops, R., Beer, H.K., and Ulbrich-Hofmann, R. (2005). Two highly homologous phospholipase D isoenzymes from Papaver somniferum L. with different transphosphatidylation potential. Biochim. Biophys. Acta 1737, 94-101. https://doi.org/10.1016/j.bbalip.2005.09.010
  58. Lewis, J.A., Scott, S.A., Lavieri, R., Buck, J.R., Selvy, P.E., Stoops, S.L., Armstrong, M.D., Brown, H.A., and Lindsley, C.W. (2009). Design and synthesis of isoform-selective phospholipase D (PLD) inhibitors. Part I: Impact of alternative halogenated privileged structures for PLD1 specificity. Bioorganic Med. Chem. Lett. 19, 1916-1920. https://doi.org/10.1016/j.bmcl.2009.02.057
  59. Lim, S.Y., Lee, S.C., Shin, I., and Han, J.S. (2002). Differential effects of Fas cross-linking on phospholipase D activation and related lipid metabolism in Fas-resistant A20 cells. Exp. Mol. Med. 34, 201-210. https://doi.org/10.1038/emm.2002.29
  60. Liscovitch, M., Ben-Av, P., Danin, M., Faiman, G., Eldar, H., and Livneh, E. (1993). Phospholipase D-mediated hydrolysis of phosphatidylcholine: role in cell signalling. J. Lipid Mediat. 8, 177-182.
  61. Liu, M., Du, K., Fu, Z., Zhang, S., and Wu, X. (2015). Hypoxia-inducible factor 1-alpha up-regulates the expression of phospholipase D2 in colon cancer cells under hypoxic conditions. Med. Oncol. 32, 394. https://doi.org/10.1007/s12032-014-0394-9
  62. Lopez, I., Arnold, R.S., and Lambeth, J.D. (1998). Cloning and initial characterization of a human phospholipase D2 (hPLD2). ADP-ribosylation factor regulates hPLD2. J. Biol. Chem. 273, 12846-12852. https://doi.org/10.1074/jbc.273.21.12846
  63. MacDonald, V. (2009). Chemotherapy: managing side effects and safe handling. Can. Vet. J. 50, 665-668.
  64. Mantovani, A. (2010). Molecular pathways linking inflammation and cancer. Curr. Mol. Med. 10, 369-373. https://doi.org/10.2174/156652410791316968
  65. Min, D.S., Kwon, T.K., Park, W.S., Chang, J.S., Park, S.K., Ahn, B.H., Ryoo, Z.Y., Lee, Y.H., Lee, Y.S., Rhie, D.J., et al. (2001). Neoplastic transformation and tumorigenesis associated with overexpression of phospholipase D isozymes in cultured murine fibroblasts. Carcinogenesis 22, 1641-1647. https://doi.org/10.1093/carcin/22.10.1641
  66. Monovich, L., Mugrage, B., Quadros, E., Toscano, K., Tommasi, R., LaVoie, S., Liu, E., Du, Z., LaSala, D., Boyar, W., et al. (2007). Optimization of halopemide for phospholipase D2 inhibition. Bioorganic. Med. Chem. Lett. 17, 2310-2311. https://doi.org/10.1016/j.bmcl.2007.01.059
  67. Murakami, M., Taketomi, Y., Miki, Y., Sato, H., Hirabayashi, T., and Yamamoto, K. (2011). Recent progress in phospholipase A(2) research: from cells to animals to humans. Prog. Lipid Res. 50, 152-192. https://doi.org/10.1016/j.plipres.2010.12.001
  68. Nakashima, S., Matsuda, Y., Akao, Y., Yoshimura, S., Sakai, H., Hayakawa, K., Andoh, M., and Nozawa, Y. (1997). Molecular cloning and chromosome mapping of rat phospholipase D genes, Pld1a, Pld1b and Pld2. Cytogenetics Cell Genet. 79, 109-113. https://doi.org/10.1159/000134694
  69. Nanjundan, M., and Possmayer, F. (2003). Pulmonary phosphatidic acid phosphatase and lipid phosphate phosphohydrolase. American journal of physiology. Lung Cell. Mol. Physiol. 284, L1-23. https://doi.org/10.1152/ajplung.00029.2002
  70. Nelson, R.K., and Frohman, M.A. (2015). Physiological and pathophysiological roles for phospholipase D. J. Lipid Res. 56, 2229-2237. https://doi.org/10.1194/jlr.R059220
  71. Nishikimi, A., Fukuhara, H., Su, W., Hongu, T., Takasuga, S., Mihara, H., Cao, Q., Sanematsu, F., Kanai, M., Hasegawa, H., et al. (2009). Sequential regulation of DOCK2 dynamics by two phospholipids during neutrophil chemotaxis. Science 324, 384-387. https://doi.org/10.1126/science.1170179
  72. Osisami, M., Ali, W., and Frohman, M.A. (2012). A role for phospholipase D3 in myotube formation. PloS one 7, e33341. https://doi.org/10.1371/journal.pone.0033341
  73. Oude Weernink, P.A., Lopez de Jesus, M., and Schmidt, M. (2007). Phospholipase D signaling: orchestration by PIP2 and small GTPases. Naunyn-Schmiedeberg's Arch. Pharmacol. 374, 399-411. https://doi.org/10.1007/s00210-007-0131-4
  74. Pannequin, J., Delaunay, N., Darido, C., Maurice, T., Crespy, P., Frohman, M.A., Balda, M.S., Matter, K., Joubert, D., Bourgaux, J.F., et al. (2007). Phosphatidylethanol accumulation promotes intestinal hyperplasia by inducing ZONAB-mediated cell density increase in response to chronic ethanol exposure. Mol. Cancer Res. 5, 1147-1157. https://doi.org/10.1158/1541-7786.MCR-07-0198
  75. Park, M.H., Ahn, B.H., Hong, Y.K., and Min do, S. (2009). Overexpression of phospholipase D enhances matrix metalloproteinase-2 expression and glioma cell invasion via protein kinase C and protein kinase A/NF-kappaB/Sp1-mediated signaling pathways. Carcinogenesis 30, 356-365. https://doi.org/10.1093/carcin/bgn287
  76. Park, J.B., Lee, C.S., Jang, J.H., Ghim, J., Kim, Y.J., You, S., Hwang, D., Suh, P.G., and Ryu, S.H. (2012). Phospholipase signalling networks in cancer. Nat. Rev. Cancer 12, 782-792. https://doi.org/10.1038/nrc3379
  77. Pedraza-Farina, L.G. (2006). Mechanisms of oncogenic cooperation in cancer initiation and metastasis. Yale J. Biol. Med, 79, 95-103.
  78. Preininger, A.M., Henage, L.G., Oldham, W.M., Yoon, E.J., Hamm, H.E., and Brown, H.A. (2006). Direct modulation of phospholipase D activity by Gbetagamma. Mol. Pharmacol. 70, 311-318.
  79. Pyne, S., and Pyne, N.J. (2000). Sphingosine 1-phosphate signalling in mammalian cells. Biochem. J. 349, 385-402. https://doi.org/10.1042/bj3490385
  80. Saito, M., Iwadate, M., Higashimoto, M., Ono, K., Takebayashi, Y., and Takenoshita, S. (2007). Expression of phospholipase D2 in human colorectal carcinoma. Oncol. Rep. 18, 1329-1334.
  81. Samaras, V., Rafailidis, P.I., Mourtzoukou, E.G., Peppas, G., and Falagas, M.E. (2010). Chronic bacterial and parasitic infections and cancer: a review. J. Infect. Dev. Ctries. 4, 267-281.
  82. Schonberger, T., Jurgens, T., Muller, J., Armbruster, N., Niermann, C., Gorressen, S., Sommer, J., Tian, H., di Paolo, G., Scheller, J., et al. (2014). Pivotal role of phospholipase D1 in tumor necrosis factoralpha-mediated inflammation and scar formation after myocardial ischemia and reperfusion in mice. Am. J. Pathol. 184, 2450-2464. https://doi.org/10.1016/j.ajpath.2014.06.005
  83. Scott, S.A., Selvy, P.E., Buck, J.R., Cho, H.P., Criswell, T.L., Thomas, A.L., Armstrong, M.D., Arteaga, C.L., Lindsley, C.W., and Brown, H.A. (2009). Design of isoform-selective phospholipase D inhibitors that modulate cancer cell invasiveness. Nat. Chem. Biol. 5, 108-117. https://doi.org/10.1038/nchembio.140
  84. Scott, S.A., O'Reilly, M.C., Daniels, J.S., Morrison, R., Ptak, R., Dawson, E.S., Tower, N., Engers, J.L., Engers, D.W., Oguin, T., et al. (2010). Development of a Selective, Allosteric PLD1/2 Inhibitor in a Novel Scaffold. In Probe Reports from the NIH Molecular Libraries Program (Bethesda (MD)).
  85. Selvy, P.E., Lavieri, R.R., Lindsley, C.W., and Brown, H.A. (2011). Phospholipase D: enzymology, functionality, and chemical modulation. Chem. Rev. 111, 6064-6119. https://doi.org/10.1021/cr200296t
  86. Stegner, D., Thielmann, I., Kraft, P., Frohman, M.A., Stoll, G., and Nieswandt, B. (2013). Pharmacological inhibition of phospholipase D protects mice from occlusive thrombus formation and ischemic stroke--brief report. Arterioscler. Thromb. Vasc. Biol. 33, 2212-2217. https://doi.org/10.1161/ATVBAHA.113.302030
  87. Stringer, A.M., Gibson, R.J., Bowen, J.M., Logan, R.M., Yeoh, A.S., and Keefe, D.M. (2007). Chemotherapy-induced mucositis: the role of gastrointestinal microflora and mucins in the luminal environment. J. Support. Oncol. 5, 259-267.
  88. Su, W., Chen, Q., and Frohman, M.A. (2009). Targeting phospholipase D with small-molecule inhibitors as a potential therapeutic approach for cancer metastasis. Future Oncol. 5, 1477-1486. https://doi.org/10.2217/fon.09.110
  89. Suh, P.G., Park, J.I., Manzoli, L., Cocco, L., Peak, J.C., Katan, M., Fukami, K., Kataoka, T., Yun, S., and Ryu, S.H. (2008). Multiple roles of phosphoinositide-specific phospholipase C isozymes. BMB Rep. 41, 415-434. https://doi.org/10.5483/BMBRep.2008.41.6.415
  90. Sultani, M., Stringer, A.M., Bowen, J.M., and Gibson, R.J. (2012). Anti-inflammatory cytokines: important immunoregulatory factors contributing to chemotherapy-induced gastrointestinal mucositis. Chemother. Res. Pract. 2012, 490804.
  91. Takuwa, Y., Okamoto, H., Takuwa, N., Gonda, K., Sugimoto, N., and Sakurada, S. (2001). Subtype-specific, differential activities of the EDG family receptors for sphingosine-1-phosphate, a novel lysophospholipid mediator. Mol. Cell. Endocrinol. 177, 3-11. https://doi.org/10.1016/S0303-7207(01)00441-5
  92. Toschi, A., Edelstein, J., Rockwell, P., Ohh, M., and Foster, D.A. (2008). HIF alpha expression in VHL-deficient renal cancer cells is dependent on phospholipase D. Oncogene 27, 2746-2753. https://doi.org/10.1038/sj.onc.1210927
  93. Walker, S.J., and Brown, H.A. (2004). Measurement of G protein-coupled receptor-stimulated phospholipase D activity in intact cells. Methods Mol. Biol. 237, 89-97.
  94. Wang, X., Devaiah, S.P., Zhang, W., and Welti, R. (2006). Signaling functions of phosphatidic acid. Prog. Lipid Res. 45, 250-278. https://doi.org/10.1016/j.plipres.2006.01.005
  95. Weaver, B.A. (2014). How taxol/paclitaxel kills cancer cells. Mol. Biol. Cell 25, 2677-2681. https://doi.org/10.1091/mbc.E14-04-0916
  96. Weir, H.K., Anderson, R.N., Coleman King, S.M., Soman, A., Thompson, T.D., Hong, Y., Moller, B., and Leadbetter, S. (2016). Heart disease and cancer deaths - trends and projections in the United States, 1969-2020. Prev. Chronic Dis. 13, E157.
  97. Wettergren, Y., Carlsson, G., Odin, E., and Gustavsson, B. (2012). Pretherapeutic uracil and dihydrouracil levels of colorectal cancer patients are associated with sex and toxic side effects during adjuvant 5-fluorouracil-based chemotherapy. Cancer 118, 2935-2943. https://doi.org/10.1002/cncr.26595
  98. Yamada, Y., Hamajima, N., Kato, T., Iwata, H., Yamamura, Y., Shinoda, M., Suyama, M., Mitsudomi, T., Tajima, K., Kusakabe, S., et al. (2003). Association of a polymorphism of the phospholipase D2 gene with the prevalence of colorectal cancer. J. Mol. Med. 81, 126-131. https://doi.org/10.1007/s00109-002-0411-x
  99. Yang, S.F., Freer, S., and Benson, A.A. (1967). Transphosphatidylation by phospholipase D. J. Biol. Chem. 242, 477-484.
  100. Zhang, Y., and Frohman, M.A. (2014). Cellular and physiological roles for phospholipase D1 in cancer. J. Biol. Chem. 289, 22567-22574. https://doi.org/10.1074/jbc.R114.576876
  101. Zhao, Y., and Natarajan, V. (2009). Lysophosphatidic acid signaling in airway epithelium: role in airway inflammation and remodeling. Cell. Signal. 21, 367-377. https://doi.org/10.1016/j.cellsig.2008.10.010
  102. Zhao, C., Du, G., Skowronek, K., Frohman, M.A., and Bar-Sagi, D. (2007). Phospholipase D2-generated phosphatidic acid couples EGFR stimulation to Ras activation by Sos. Nat. Cell Biol. 9, 706-712.

Cited by

  1. New Mammalian Target of Rapamycin (mTOR) Modulators Derived from Natural Product Databases and Marine Extracts by Using Molecular Docking Techniques vol.16, pp.10, 2018, https://doi.org/10.3390/md16100385
  2. Colocalization Features for Classification of Tumors Using Desorption Electrospray Ionization Mass Spectrometry Imaging vol.91, pp.10, 2017, https://doi.org/10.1021/acs.analchem.8b05598
  3. Preparation and Evaluation of Liposomes Co-Loaded with Doxorubicin, Phospholipase D Inhibitor 5-Fluoro-2-Indolyl Deschlorohalopemide (FIPI) and D-Alpha Tocopheryl Acid Succinate (α-TOS) for Anti vol.14, pp.1, 2019, https://doi.org/10.1186/s11671-019-2964-4
  4. Reprogramming of fatty acid metabolism in cancer vol.122, pp.1, 2017, https://doi.org/10.1038/s41416-019-0650-z
  5. Phospholipase Superfamily: Structure, Functions, and Biotechnological Applications vol.85, pp.suppl1, 2017, https://doi.org/10.1134/s0006297920140096
  6. Phosphoinositide-Dependent Signaling in Cancer: A Focus on Phospholipase C Isozymes vol.21, pp.7, 2017, https://doi.org/10.3390/ijms21072581
  7. Coenzyme Q10 attenuates rat hepatocarcinogenesis via the reduction of CD59 expression and phospholipase D activity vol.38, pp.4, 2017, https://doi.org/10.1002/cbf.3487
  8. Genome-Wide Analysis and Expression Profiling of the Phospholipase D Gene Family in Solanum tuberosum vol.10, pp.8, 2017, https://doi.org/10.3390/biology10080741
  9. Network Pharmacology-Based Study to Uncover Potential Pharmacological Mechanisms of Korean Thistle (Cirsium japonicum var. maackii (Maxim.) Matsum.) Flower against Cancer vol.26, pp.19, 2017, https://doi.org/10.3390/molecules26195904
  10. Genome-wide circular RNA (circRNA) and mRNA profiling identify a circMET-miR-410-3p regulatory motif for cell growth in colorectal cancer vol.114, pp.1, 2022, https://doi.org/10.1016/j.ygeno.2021.11.038
  11. Targeting PLD2 in adipocytes augments adaptive thermogenesis by improving mitochondrial quality and quantity in mice vol.219, pp.2, 2017, https://doi.org/10.1084/jem.20211523