Skip to main content
Log in

Phospholipase Superfamily: Structure, Functions, and Biotechnological Applications

  • Review
  • Published:
Biochemistry (Moscow) Aims and scope Submit manuscript

Abstract

Enzymes of the phospholipase superfamily are involved in lipid metabolism, as well as regulation of membrane composition, cell signaling, and inflammation. This review provides an insight into the structure, functional properties, and biotechnological application of phospholipase A2 and phospholipases in general.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

cPLA2:

cytosolic phospholipase A2

IP3:

inositol 1,4,5-trisphosphate

iPLA2:

calcium-independent phospholipase A2

PAF:

platelet-activating factor

PAF-AH:

platelet-activating factor acetylhydrolase

PIP2:

phosphatidylinositol 4,5-bisphosphate

PLA1(2):

phospholipase A1(2)

PLB(C,D):

phospholipase B(C,D)

sPLA2:

secretory phospholipase A2

sPLA2R:

secretory phospholipase A2 receptor

References

  1. Aloulou, A., Ali, Y. B., Bezzine, S., Gargouri, Y., and Gelb, M. H. (2012) Phospholipases: an overview, in Lipases and Phospholipases (Sandoval, G., ed.) Springer, pp. 63–85.

    Chapter  Google Scholar 

  2. Litvienko, N. M., and Kisel’, M. A. (1991) Endogenous Phospholipases A2. Structure and Functions [in Russian], Nauka i Tekhnika, Minsk, pp. 17–21.

    Google Scholar 

  3. Woolley, P., and Petersen, S. B. (1996) Lipases: their structure, biochemistry and application, Int. J. Biochem. Cell Biol., 28, 831–832.

    Article  Google Scholar 

  4. Brokerkhof, Kh., and Dzhensen, R. (1978) Lipolytic Enzymes [Russian translation] (Braunshtein, A. E., and Goryachenkova, E. V., eds.) Mir, Moscow.

  5. Cocco, L., Follo, M. Y., Manzoli, L., and Suh, P.-G. (2015) Phosphoinositide-specific phospholipase C in health and disease, J. Lipid Res., 56, 1853–1860.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Gresset, A., Sondek, J., and Harden, T. K. (2012) The phospholipase C isozymes and their regulation, in Phosphoinositides. I: Enzymes of Synthesis and Degradation (Balla, T., Wymann, M., and York, J. D., eds.) Springer, Springer, Netherlands, pp. 61–94.

    Chapter  Google Scholar 

  7. Gomez-Cambronero, J. (2014) Phospholipase D in cell signaling: from a myriad of cell functions to cancer growth and metastasis, J. Biol. Chem., 289, 22557–22566.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Cho, J. H., and Han, J.-S. (2017) Phospholipase D and its essential role in cancer, Mol. Cells, 40, 805.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Bruntz, R. C., Lindsley, C. W., and Brown, H. A. (2014) Phospholipase D signaling pathways and phosphatidic acid as therapeutic targets in cancer, Pharmacol. Rev., 66, 1033–1079.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Jaeger, K.-E., Ransac, S., Dijkstra, B. W., Colson, C., van Heuvel, M., and Misset, O. (1994) Bacterial lipases, FEMS Microbiol. Rev., 15, 29–63.

    Article  CAS  PubMed  Google Scholar 

  11. Nakazawa, Y. (2012) Streptomyces phospholipase D cloning and production, in Lipases and Phospholipases, Springer, pp. 179–200.

    Chapter  Google Scholar 

  12. Leslie, C. C. (2004) Regulation of the specific release of arachidonic acid by cytosolic phospholipase A2, Prostaglandins Leukot. Essent. Fatty Acids, 70, 373–376.

    Article  CAS  PubMed  Google Scholar 

  13. Murakami, M., Nakatani, Y., Atsumi, G., Inoue, K., and Kudo, I. (2017) Regulatory functions of phospholipase A2, Crit. Rev. Immunol., 37, 121–179.

    Article  Google Scholar 

  14. Van den Bergh, C. J., Bekkers, A. C., De Geus, P., Verheij, H. M., and de Haas, G. H. (1987) Secretion of biologically active porcine prophospholipase A2 by Saccharomyces cerevisiae. Use of the prepro sequence of the alpha-mating factor, Eur. J. Biochem., 170, 241–246.

    Article  PubMed  Google Scholar 

  15. Kramer, R. M., Hession, C., Johansen, B., Hayes, G., McGray, P., Chow, E. P., Tizard, R., and Pepinsky, R. B. (1989) Structure and properties of a human non-pancreatic phospholipase A2, J. Biol. Chem., 264, 5768–5775.

    CAS  PubMed  Google Scholar 

  16. Burke, J. E., Karbarz, M. J., Deems, R. A., Li, S., Woods, V. L., and Dennis, E. A. (2008) Interaction of group IA phospholipase A2 with metal ions and phospholipid vesicles probed with deuterium exchange mass spectrometry, Biochemistry, 47, 6451–6459.

    Article  CAS  PubMed  Google Scholar 

  17. Han, S. K., Kim, K. P., Koduri, R., Bittova, L., Munoz, N. M., Leff, A. R., Wilton, D. C., Gelb, M. H., and Cho, W. (1999) Roles of Trp31 in high membrane binding and proinflammatory activity of human group V phospholipase A2, J. Biol. Chem., 274, 11881–11888.

    Article  CAS  PubMed  Google Scholar 

  18. Bezzine, S., Bollinger, J. G., Singer, A. G., Veatch, S. L., Keller, S. L., and Gelb, M. H. (2002) On the binding preference of human groups IIA and X phospholipases A2 for membranes with anionic phospholipids, J. Biol. Chem., 277, 48523–48534.

    Article  CAS  PubMed  Google Scholar 

  19. Pan, Y. H., and Bahnson, B. J. (2010) Structure of a premicellar complex of alkyl sulfates with the interfacial binding surfaces of four subunits of phospholipase A2, Biochim. Biophys. Acta, 1804, 1443–1448.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Bollinger, J. G., Diraviyam, K., Ghomashchi, F., Murray, D., and Gelb, M. H. (2004) Interfacial binding of bee venom secreted phospholipase A2 to membranes occurs predominantly by a non-electrostatic mechanism, Biochemistry, 43, 13293–13304.

    Article  CAS  PubMed  Google Scholar 

  21. Murakami, M., Sato, H., Miki, Y., Yamamoto, K., and Taketomi, Y. (2015) A new era of secreted phospholipase A2 (sPLA2), J. Lipid Res., 56, 1248–1261.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Sato, H., Taketomi, Y., and Murakami, M. (2016) Metabolic regulation by secreted phospholipase A2, Inflamm. Regen., 36, 7.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Nambi, V., and Ballantyne, C. M. (2006) Lipoprotein-associated phospholipase A2: pathogenic mechanisms and clinical utility for predicting cardiovascular events, Curr. Atheroscler. Rep., 8, 374–381.

    Article  CAS  PubMed  Google Scholar 

  24. Ishizaki, J., Hanasaki, K., Higashino, K., Kishino, J., Kikuchi, N., Ohara, O., and Arita, H. (1994) Molecular cloning of pancreatic group I phospholipase A2 receptor, J. Biol. Chem., 269, 5897–5904.

    CAS  PubMed  Google Scholar 

  25. Lambeau, G., Ancian, P., Barhanin, J., and Lazdunski, M. (1994) Cloning and expression of a membrane receptor for secretory phospholipases A2, J. Biol. Chem., 269, 1575–1578.

    CAS  PubMed  Google Scholar 

  26. Hanasaki, K., and Arita, H. (2002) Phospholipase A2 receptor: a regulator of biological functions of secretory phospholipase A2, Prostaglandins Other Lipid Mediat., 68, 71–82.

    Article  PubMed  Google Scholar 

  27. Fry, B. G. (2005) From genome to “venome”: molecular origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences and related body proteins, Genome Res., 15, 403–420.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kini, R. M. (2005) Structure-function relationships and mechanism of anticoagulant phospholipase A2 enzymes from snake venoms, Toxicon, 45, 1147–1161.

    Article  CAS  PubMed  Google Scholar 

  29. Ackermann, E. J., Kempner, E. S., and Dennis, E. A. (1994) Ca2+-independent cytosolic phospholipase A2 from macrophage-like P388D1 cells. Isolation and characterization, J. Biol. Chem., 269, 9227–9233.

    CAS  PubMed  Google Scholar 

  30. Burke, J. E., and Dennis, E. A. (2009) Phospholipase A2 structure/function, mechanism, and signaling, J. Lipid Res., 50, S237–S242.

    Article  CAS  Google Scholar 

  31. Elimam, H., Papillon, J., Takano, T., and Cybulsky, A. V. (2013) Complement-mediated activation of calcium-independent phospholipase A2γ role of protein kinases and phosphorylation, J. Biol. Chem., 288, 3871–3885.

    Article  CAS  PubMed  Google Scholar 

  32. Ramanadham, S., Ali, T., Ashley, J. W., Bone, R. N., Hancock, W. D., and Lei, X. (2015) Calcium-independent phospholipases A2 (iPLA2s) and their roles in biological processes and diseases, J. Lipid Res., 56, 1643–1668.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Frei, E., and Zahler, P. (1979) Phospholipase A2 from sheep erythrocyte membrane Ca2+ dependence and localization, Biochim. Biophys. Acta BBA–Biomembranes, 550, 450–463.

    Article  CAS  PubMed  Google Scholar 

  34. Lopez-Vales, R., Navarro, X., Shimizu, T., Baskakis, C., Kokotos, G., Constantinou-Kokotou, V., Stephens, D., Dennis, E. A., and David, S. (2008) Intracellular phospholipase A2 group IVA and group VIA play important roles in Wallerian degeneration and axon regeneration after peripheral nerve injury, Brain, 131, 2620–2631.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Kramer, R. M., and Sharp, J. D. (1997) Structure, function and regulation of Ca2+-sensitive cytosolic phospholipase A2 (cPLA2), FEBS Lett., 410, 49–53.

    Article  CAS  PubMed  Google Scholar 

  36. Leslie, C. C. (2015) Cytosolic phospholipase A2: physiological function and role in disease, J. Lipid Res., 56, 1386–1402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Dessen, A., Tang, J., Schmidt, H., Stahl, M., Clark, J. D., Seehra, J., and Somers, W. S. (1999) Crystal structure of human cytosolic phospholipase A2 reveals a novel topology and catalytic mechanism, Cell, 97, 349–360.

    Article  CAS  PubMed  Google Scholar 

  38. Lichtenbergova, L., Yoon, E. T., and Cho, W. (1998) Membrane penetration of cytosolic phospholipase A2 is necessary for its interfacial catalysis and arachidonate specificity, Biochemistry, 37, 14128–14136.

    Article  CAS  PubMed  Google Scholar 

  39. Murakami, M. (2017) Lipoquality control by phospholipase A2 enzymes, Proc. Jpn. Acad. Ser. B, 93, 677–702.

    Article  CAS  Google Scholar 

  40. Sun, G. Y., Chuang, D. Y., Zong, Y., Jiang, J., Lee, J. C., Gu, Z., and Simonyi, A. (2014) Role of cytosolic phospholipase A2 in oxidative and inflammatory signaling pathways in different cell types in the central nervous system, Mol. Neurobiol., 50, 6–14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Bonventre, J. V., Huang, Z., Taheri, M. R., O’Leary, E., Li, E., Moskowitz, M. A., and Sapirstein, A. (1997) Reduced fertility and postischemic brain injury in mice deficient in cytosolic phospholipase A2, Nature, 390, 622–625.

    Article  CAS  PubMed  Google Scholar 

  42. Korneeva, O. S., and Annenkov, V. A. (2014) Producing lipase enzyme preparation by using recombinant DNA, TFPI AIC Healthy Food, 3, 59–62.

    Google Scholar 

  43. Roberts, I. N., Jeenes, D. J., MacKenzie, D. A., Wilkinson, A. P., Sumner, I. G., and Archer, D. B. (1992) Heterologous gene expression in Aspergillus niger: a glucoamylase-porcine pancreatic prophospholipase A2 fusion protein is secreted and processed to yield mature enzyme, Gene, 122, 155–161.

    Article  CAS  PubMed  Google Scholar 

  44. Stadel, J. M., Jones, C., Livi, G. P., Hoyle, K., Kurdyla, J., Roshak, A., McLaughlin, M. M., Pfarr, D. A., Comer, S., and Strickler, J. (1992) Recombinant human secretory phospholipase A2: purification and characterization of the enzyme for active site studies, J. Mol. Recognit. JMR, 5, 145–153.

    Article  CAS  PubMed  Google Scholar 

  45. Vind, J., and Patkar, S. A. (2005) Preparing modified polypeptide comprises providing a sequence encoding a parent polypeptide comprising at least two Cys residues forming a disulfide bond, Novozymes A/S, Denmark, WO2005/024012.

    Google Scholar 

  46. Janssen, M. J., Burghout, P. J., Verheij, H. M., Slotboom, A. J., and Egmond, M. R. (1999) Introduction of a C-terminal aromatic sequence from snake venom phospholipases A2 into the porcine pancreatic isozyme dramatically changes the interfacial kinetics, Eur. J. Biochem., 263, 782–788.

    Article  CAS  PubMed  Google Scholar 

  47. Nevalainen, K. M. H., Te’o, V. S. J., and Bergquist, P. L. (2005) Heterologous protein expression in filamentous fungi, Trends Biotechnol., 23, 468–474.

    Article  CAS  PubMed  Google Scholar 

  48. Sugiyama, M., Ohtani, K., Izuhara, M., Koike, T., Suzuki, K., Imamura, S., and Misaki, H. (2002) A novel prokaryotic phospholipase A2. Characterization, gene cloning, and solution structure, J. Biol. Chem., 277, 20051–20058.

    Article  CAS  PubMed  Google Scholar 

  49. Liu, A., Yu, X.-W., Sha, C., and Xu, Y. (2015) Streptomyces violaceoruber phospholipase A2: expression in Pichia pastoris, properties, and application in oil degumming, Appl. Biochem. Biotechnol., 175, 3195–3206.

    Article  CAS  PubMed  Google Scholar 

  50. Yu, X.-W., Sun, W.-H., Wang, Y.-Z., and Xu, Y. (2017) Identification of novel factors enhancing recombinant protein production in multi-copy Komagataella phaffii based on transcriptomic analysis of overexpression effects, Sci. Rep., 7, 16249.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Boilard, E., Lai, Y., Larabee, K., Balestrieri, B., Ghomashchi, F., Fujioka, D., Gobezie, R., Coblyn, J. S., Weinblatt, M. E., Massarotti, E. M., Thornhill, T. S., Divangahi, M., Remold, H., Lambeau, G., Gelb, M. H., Arm, J. P., and Lee, D. M. (2010) A novel anti-inflammatory role for secretory phospholipase A2 in immune complex-mediated arthritis, EMBO Mol. Med., 2, 172–187.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Rosenson, R. S., and Hurt-Camejo, E. (2012) Phospholipase A2 enzymes and the risk of atherosclerosis, Eur. Heart J., 33, 2899–2909.

    Article  CAS  PubMed  Google Scholar 

  53. Quach, N. D., Arnold, R. D., and Cummings, B. S. (2014) Secretory phospholipase A2 enzymes as pharmacological targets for treatment of disease, Biochem. Pharmacol., 90, 338–348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Bragina, N. A., Chupin, V. V., Bulgakov, V. G., and Shal’nev, A. N. (1999) Phospholipases A2 lipid inhibitors, Bioorg. Khim., 25, 83–96.

    CAS  PubMed  Google Scholar 

  55. Thompson, W., Oslund, R. C., Bollinger, J., Ewing, H., and Gelb, M. H. (2012) High-throughput assay of secreted phospholipases A2 inhibitors, in Lipases and Phospholipases, Springer, pp. 149–158.

    Chapter  Google Scholar 

  56. Fraser, H., Hislop, C., Christie, R. M., Rick, H. L., Reidy, C. A., Chouinard, M. L., Eacho, P. I., Gould, K. E., and Trias, J. (2009) Varespladib (A-002), a secretory phospholipase A2 inhibitor, reduces atherosclerosis and aneurysm formation in ApoE–/–mice, J. Cardiovasc. Pharmacol., 53, 60–65.

    Article  CAS  PubMed  Google Scholar 

  57. O’Donoghue, M. L., Braunwald, E., White, H. D., Steen, D. P., Lukas, M. A., Tarka, E., Steg, P. G., Hochman, J. S., Bode, C., Maggioni, A. P., Im, K., Shannon, J. B., Davies, R. Y., Murphy, S. A., Crugnale, S. E., Wiviott, S. D., Bonaca, M. P., Watson, D. F., Weaver, W. D., Serruys, P. W., Cannon, C. P., SOLID-TIMI 52 Investigators, and Steen, D. L. (2014) Effect of darapladib on major coronary events after an acute coronary syndrome: the SOLID-TIMI 52 randomized clinical trial, JAMA, 312, 1006–1015.

    Article  PubMed  CAS  Google Scholar 

  58. Wilensky, R. L., and Macphee, C. H. (2009) Lipoprotein-associated phospholipase A2 and atherosclerosis, Curr. Opin. Lipidol., 20, 415–420.

    Article  CAS  PubMed  Google Scholar 

  59. Lp-PLA2 Studies Collaboration, Thompson, A., Gao, P., Orfei, L., Watson, S., Di Angelantonio, E., Kaptoge, S., Ballantyne, C., Cannon, C. P., Criqui, M., Cushman, M., Hofman, A., Packard, C., Thompson, S. G., Collins, R., and Danesh, J. (2010) Lipoprotein-associated phospholipase A2 and risk of coronary disease, stroke, and mortality: collaborative analysis of 32 prospective studies, Lancet, 375, 1536–1544.

    Article  CAS  PubMed  Google Scholar 

  60. Li, J., Wang, H., Tian, J., Chen, B., and Du, F. (2018) Change in lipoprotein-associated phospholipase A2 and its association with cardiovascular outcomes in patients with acute coronary syndrome, Medicine (Baltimore), 97, e11517.

    Article  CAS  Google Scholar 

  61. Markovic, M., Ben-Shabat, S., Keinan, S., Aponick, A., Zimmermann, E. M., and Dahan, A. (2019) Molecular modeling-guided design of phospholipid-based prodrugs, Int. J. Mol. Sci., 20, E2210.

    Article  PubMed  CAS  Google Scholar 

  62. Fernandes, P. (2010) Enzymes in food processing: a condensed overview on strategies for better biocatalysts, Enzyme Res., 2010, 862537.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  63. Raveendran, S., Parameswaran, B., Ummalyma, S. B., Abraham, A., Mathew, A. K., Madhavan, A., Rebello, S., and Pandey, A. (2018) Applications of microbial enzymes in food industry, Food Technol. Biotechnol., 56, 16–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. De Maria, L., Vind, J., Oxenboll, K. M., Svendsen, A., and Patkar, S. (2007) Phospholipases and their industrial applications, Appl. Microbiol. Biotechnol., 74, 290–300.

    Article  CAS  PubMed  Google Scholar 

  65. Alekseenko, A. V., and Predybaylo, A. V. (2008) Transesterification of oils and fats, Moloch. Prom., 11, 24.

    Google Scholar 

  66. Borrelli, G., and Trono, D. (2015) Recombinant lipases and phospholipases and their use as biocatalysts for industrial applications, Int. J. Mol. Sci., 16, 20774–20840.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Dijkstra, A. J. (2010) Enzymatic degumming, Eur. J. Lipid Sci., 112, 1178–1189.

    Article  CAS  Google Scholar 

  68. Yang, B., Wang, Y.-H., and Yang, J.-G. (2006) Optimization of enzymatic degumming process for rapeseed oil, J. Am. Oil Chem. Soc., 83, 653–658.

    Article  CAS  Google Scholar 

  69. Yu, D., Ma, Y., Jiang, L., Walid, E., He, S., He, Y., Xiaoyu, Z., Zhang, J., and Hu, L. (2014) Stability of soybean oil degumming using immobilized phospholipase A2, J. Oleo Sci., 63, 25–30.

    Article  CAS  PubMed  Google Scholar 

  70. Casado, V., Martin, D., Torres, C., and Reglero, G. (2012) Phospholipases in food industry: a review, in Lipases and Phospholipases, Springer, pp. 495–523.

    Chapter  Google Scholar 

  71. Madoery, R., Gattone, C. G., and Fidelio, G. (1995) Bioconversion of phospholipids by immobilized phospholipase A2, J. Biotechnol., 40, 145–153.

    Article  CAS  Google Scholar 

  72. Lilbaek, H. M., Broe, M. L., Hoier, E., Fatum, T. M., Ipsen, R., and Sorensen, N. K. (2006) Improving the yield of Mozzarella cheese by phospholipase treatment of milk, J. Dairy Sci., 89, 4114–4125.

    Article  CAS  PubMed  Google Scholar 

  73. Berestova, A. V., Zinyukhin, G. B., and Mezhueva, L. V. (2014) Technological specifics for functional food fat-and-oil emulsions, Vestnik Orenburg. Gos. Univ., 1, 150–155.

    Google Scholar 

  74. Karray, A., Gargouri, Y., Verger, R., and Bezzine, S. (2012) Phospholipase A2 purification and characterization: a case study, in Lipases and Phospholipases, Springer, pp. 283–297.

    Chapter  Google Scholar 

  75. Kaambre, T., Tougu, V., Kaambre, P., Vija, H., and Sikk, P. (1999) Hydrolysis of emulsified mixtures of triacylglycerols by pancreatic lipase, Biochim. Biophys. Acta, 1431, 97–106.

    Article  CAS  PubMed  Google Scholar 

  76. Starovoytova, K. V., and Tereshchuk, L. V. (2018) Development of mayonnaise recipes in the light of pivotal trends for improving assortment, Tekhn. Tekhnol. Pishch. Proizvodstv, 48, 92–98.

    Google Scholar 

  77. Hasan, F., Shah, A. A., and Hameed, A. (2006) Industrial applications of microbial lipases, Enzyme Microb. Technol., 39, 235–251.

    Article  CAS  Google Scholar 

  78. 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.

    Article  CAS  PubMed  Google Scholar 

  79. Richmond, G. S., and Smith, T. K. (2011) Phospholipases A1, Int. J. Mol. Sci., 12, 588–612.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Ishiguro, S., Kawai-Oda, A., Ueda, J., Nishida, I., and Okada, K. (2001) The DEFECTIVE IN ANTHER DEHI-SCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis, Plant Cell, 13, 2191–2209.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Murayama, K., Kano, K., Matsumoto, Y., and Sugimori, D. (2013) Crystal structure of phospholipase A1 from Streptomyces albidoflavus NA297, J. Struct. Biol., 182, 192–196.

    Article  CAS  PubMed  Google Scholar 

  82. Schaloske, R. H., and Dennis, E. A. (2006) The phospholipase A2 superfamily and its group numbering system, Biochim. Biophys. Acta, 1761, 1246–1259.

    Article  CAS  PubMed  Google Scholar 

  83. Verlotta, A., Liberatore, M. T., Cattivelli, L., and Trono, D. (2013) Secretory phospholipases A2 in durum wheat (Triticum durum Desf.): gene expression, enzymatic activity, and relation to drought stress adaptation, Int. J. Mol. Sci., 14, 5146–5169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Matos, A. R., and Pham-Thi, A.-T. (2009) Lipid deacylating enzymes in plants: old activities, new genes, Plant Physiol. Biochem., 47, 491–503.

    Article  CAS  PubMed  Google Scholar 

  85. Scherer, G. F. E., Ryu, S. B., Wang, X., Matos, A. R., and Heitz, T. (2010) Patatin-related phospholipase A: nomenclature, subfamilies and functions in plants, Trends Plant Sci., 15, 693–700.

    Article  CAS  PubMed  Google Scholar 

  86. Kohler, G. A., Brenot, A., Haas-Stapleton, E., Agabian, N., Deva, R., and Nigam, S. (2006) Phospholipase A2 and phospholipase B activities in fungi, Biochim. Biophys. Acta, 1761, 1391–1399.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  87. Zadori, Z., Szelei, J., Lacoste, M. C., Li, Y., Gariepy, S., Raymond, P., Allaire, M., Nabi, I. R., and Tijssen, P. (2001) A viral phospholipase A2 is required for parvovirus infectivity, Dev. Cell, 1, 291–302.

    Article  CAS  PubMed  Google Scholar 

  88. Xu, S., Zhao, L., Larsson, A., and Venge, P. (2009) The identification of a phospholipase B precursor in human neutrophils, FEBS J., 276, 175–186.

    Article  CAS  PubMed  Google Scholar 

  89. Kim, D. K., Lee, H. J., and Lee, Y. (1994) Detection of two phospholipase A2 (PLA2) activities in leaves of higher plant Vicia faba and comparison with mammalian PLA2′s, FEBS Lett., 343, 213–218.

    Article  CAS  PubMed  Google Scholar 

  90. Helmy, M., Lombard, S., and Pieroni, G. (1999) Ricin RCA60: evidence of its phospholipase activity, Biochem. Biophys. Res. Commun., 258, 252–255.

    Article  CAS  PubMed  Google Scholar 

  91. Djordjevic, J. T. (2010) Role of phospholipases in fungal fitness, pathogenicity, and drug development–lessons from Cryptococcus neoformans, Front. Microbiol., 1, 125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Morgan, C. P., Insall, R., Haynes, L., and Cockcroft, S. (2004) Identification of phospholipase B from Dictyostelium discoideum reveals a new lipase family present in mammals, flies and nematodes, but not yeast, Biochem. J., 382, 441–449.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Jiang, F., Huang, S., Imadad, K., and Li, C. (2012) Cloning and expression of a gene with phospholipase B activity from Pseudomonas fluorescens in Escherichia coli, Bioresour. Technol., 104, 518–522.

    Article  CAS  PubMed  Google Scholar 

  94. Masayama, A., Kato, S., Terashima, T., Molgaard, A., Hemmi, H., Yoshimura, T., and Moriyama, R. (2010) Bacillus subtilis spore coat protein LipC is a phospholipase B, Biosci. Biotechnol. Biochem., 74, 24–30.

    Article  CAS  PubMed  Google Scholar 

  95. Matsumoto, Y., Mineta, S., Murayama, K., and Sugimori, D. (2013) A novel phospholipase B from Streptomyces sp. NA684–purification, characterization, gene cloning, extracellular production and prediction of the catalytic residues, FEBS J., 280, 3780–3796.

    Article  CAS  PubMed  Google Scholar 

  96. Gresset, A., Sondek, J., and Harden, T. K. (2012) The phospholipase C isozymes and their regulation, in Phosphoinositides. I: Enzymes of Synthesis and Degradation (Balla, T., Wymann, M., and York, J. D., eds.) Springer, Netherlands, pp. 61–94.

    Chapter  Google Scholar 

  97. Szumilo, M., and Rahden-Staron, I. (2008) Biological role of phosphatidylcholine-specific phospholipase C in mammalian cells, Postepy Hig. Med. Doswiadczalnej Online, 62, 593–598.

    Google Scholar 

  98. Pokotylo, I., Kolesnikov, Y., Kravets, V., Zachowski, A., and Ruelland, E. (2014) Plant phosphoinositide-dependent phospholipases C: variations around a canonical theme, Biochimie, 96, 144–157.

    Article  CAS  PubMed  Google Scholar 

  99. Pokotylo, I., Pejchar, P., Potocky, M., Kocourkova, D., Krckova, Z., Ruelland, E., Kravets, V., and Martinec, J. (2013) The plant non-specific phospholipase C gene family. Novel competitors in lipid signaling, Prog. Lipid Res., 52, 62–79.

    Article  CAS  PubMed  Google Scholar 

  100. 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Khatoon, H., Mansfeld, J., Schierhorn, A., and Ulbrich-Hofmann, R. (2015) Purification, sequencing and characterization of phospholipase D from Indian mustard seeds, Phytochemistry, 117, 65–75.

    Article  CAS  PubMed  Google Scholar 

  102. Waksman, M., Tang, X., Eli, Y., Gerst, J. E., and Liscovitch, M. (1997) Identification of a novel Ca2+-dependent, phosphatidylethanolamine-hydrolyzing phospholipase D in yeast bearing a disruption in PLD1, J. Biol. Chem., 272, 36–39.

    Article  CAS  PubMed  Google Scholar 

  103. Dennis, E. A., Cao, J., Hsu, Y.-H., Magrioti, V., and Kokotos, G. (2011) Phospholipase A2 enzymes: physical structure, biological function, disease implication, chemical inhibition, and therapeutic intervention, Chem. Rev., 111, 6130–6185.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Canaan, S., Zadori, Z., Ghomashchi, F., Bollinger, J., Sadilek, M., Moreau, M. E., Tijssen, P., and Gelb, M. H. (2004) Interfacial enzymology of parvovirus phospholipases A2, J. Biol. Chem., 279, 14502–14508.

    Article  CAS  PubMed  Google Scholar 

  105. Soragni, E., Bolchi, A., Balestrini, R., Gambaretto, C., Percudani, R., Bonfante, P., and Ottonello, S. (2001) A nutrient-regulated, dual localization phospholipase A2 in the symbiotic fungus Tuber borchii, EMBO J., 20, 5079–5090.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  106. Valentin, E., Ghomashchi, F., Gelb, M. H., Lazdunski, M., and Lambeau, G. (2000) Novel human secreted phospholipase A2 with homology to the group III bee venom enzyme, J. Biol. Chem., 275, 7492–7496.

    Article  CAS  PubMed  Google Scholar 

  107. Oslund, R. C., Cermak, N., Verlinde, C. L. M. J., and Gelb, M. H. (2008) Simplified YM-26734 inhibitors of secreted phospholipase A2 group IIA, Bioorg. Med. Chem. Lett., 18, 5415–5419.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Oslund, R. C., Cermak, N., and Gelb, M. H. (2008) Highly specific and broadly potent inhibitors of mammalian secreted phospholipases A2, J. Med. Chem., 51, 4708–4714.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Levick, S., Loch, D., Rolfe, B., Reid, R. C., Fairlie, D. P., Taylor, S. M., and Brown, L. (2006) Antifibrotic activity of an inhibitor of group IIA secretory phospholipase A2 in young spontaneously hypertensive rats, J. Immunol. (Baltimore), 176, 7000–7007.

    CAS  Google Scholar 

  110. Touaibia, M., Djimde, A., Cao, F., Boilard, E., Bezzine, S., Lambeau, G., Redeuilh, C., Lamouri, A., Massicot, F., Chau, F., Dong, C. Z., and Heymans, F. (2007) Inhibition of secreted phospholipase A2. 4-Glycerol derivatives of 4,5dihydro-3-(4-tetradecyloxybenzyl)-1,2,4-4H-oxadiazol-5-one with broad activities, J. Med. Chem., 50, 1618–1626.

    Article  CAS  PubMed  Google Scholar 

  111. Iyer, A., Lim, J., Poudyal, H., Reid, R. C., Suen, J. Y., Webster, J., Prins, J. B., Whitehead, J. P., Fairlie, D. P., and Brown, L. (2012) An inhibitor of phospholipase A2 group IIA modulates adipocyte signaling and protects against diet-induced metabolic syndrome in rats, Diabetes, 61, 2320–2329.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Moon, T. C., Quan, Z., Kim, J., Kim, H. P., Kudo, I., Murakami, M., Park, H., and Chang, H. W. (2007) Inhibitory effect of synthetic C–C biflavones on various phospholipase A2’s activity, Bioorg. Med. Chem., 15, 7138–7143.

    Article  CAS  PubMed  Google Scholar 

  113. Quach, N. D., Arnold, R. D., and Cummings, B. S. (2014) Secretory phospholipase A2 enzymes as pharmacological targets for treatment of disease, Biochem. Pharmacol., 90, 338–348.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

Funding This study was supported by the Ministry of Science and Higher Education of the Russian Federation (agreement no. 14.607.21.0207; RFMEFI60718X0207; 31.05.2018) within the framework of the Federal Target Program “Research and Development in the Priority Areas of the Science and Technology Complex of Russia for 2014-2020”.

Author information

Authors and Affiliations

Authors

Ethics declarations

Ethical approval This article does not contain description of studies with human participants or animals performed by any of the authors.

Additional information

Conflict of interest The authors declare no conflict of interest in financial or any other area.

Russian Text © The Author(s), 2020, published in Uspekhi Biologicheskoi Khimii, 2020, Vol. 60, pp. 369–410.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Filkin, S.Y., Lipkin, A.V. & Fedorov, A.N. Phospholipase Superfamily: Structure, Functions, and Biotechnological Applications. Biochemistry Moscow 85 (Suppl 1), 177–195 (2020). https://doi.org/10.1134/S0006297920140096

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0006297920140096

Keywords

Navigation