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Phospholipase C

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Calcium Signaling

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1131))

Abstract

Phospholipase C (PLC) family members constitute a family of diverse enzymes. Thirteen different family members have been cloned. These family members have unique structures that mediate various functions. Although PLC family members all appear to signal through the bi-products of cleaving phospholipids, it is clear that each family member, and at times each isoform, contributes to unique cellular functions. This chapter provides a review of the current literature on PLC. In addition, references have been provided for more in-depth information regarding areas that are not discussed including tyrosine kinase activation of PLC. Understanding the roles of the individual PLC enzymes, and their distinct cellular functions, will lead to a better understanding of the physiological roles of these enzymes in the development of diseases and the maintenance of homeostasis.

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References

  1. Hokin MR, Hokin LE (1953) Enzyme secretion and the incorporation of P32 into phospholipides of pancreas slices. J Biol Chem 203(2):967–977

    CAS  PubMed  Google Scholar 

  2. Michell RH, Allan D (1975) Inositol cyclis phosphate as a product of phosphatidylinositol breakdown by phospholipase C (Bacillus cereus). FEBS Lett 53(3):302–304

    Article  CAS  PubMed  Google Scholar 

  3. Takenawa T, Nagai Y (1982) Effect of unsaturated fatty acids and Ca2+ on phosphatidylinositol synthesis and breakdown. J Biochem 91(3):793–799

    Article  CAS  PubMed  Google Scholar 

  4. Streb H et al (1983) Release of Ca2+ from a nonmitochondrial intracellular store in pancreatic acinar cells by inositol-1,4,5-trisphosphate. Nature 306(5938):67–69

    Article  CAS  PubMed  Google Scholar 

  5. Suh PG et al (1988) Inositol phospholipid-specific phospholipase C: complete cDNA and protein sequences and sequence homology to tyrosine kinase-related oncogene products. Proc Natl Acad Sci U S A 85(15):5419–5423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Suh PG et al (1988) Cloning and sequence of multiple forms of phospholipase C. Cell 54(2):161–169

    Article  CAS  PubMed  Google Scholar 

  7. Kelley GG et al (2001) Phospholipase C(epsilon): a novel Ras effector. EMBO J 20(4):743–754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hwang JI et al (2005) Molecular cloning and characterization of a novel phospholipase C, PLC-eta. Biochem J 389(Pt 1):181–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Nakahara M et al (2005) A novel phospholipase C, PLC(eta)2, is a neuron-specific isozyme. J Biol Chem 280(32):29128–29134

    Article  CAS  PubMed  Google Scholar 

  10. Saunders CM et al (2002) PLC zeta: a sperm-specific trigger of Ca2+ oscillations in eggs and embryo development. Development 129(15):3533–3544

    CAS  PubMed  Google Scholar 

  11. Albuquerque EX, Thesleff S (1967) Influence of phospholipase C on some electrical properties of the skeletal muscle membrane. J Physiol 190(1):123–137

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Macchia V, Pastan I (1967) Action of phospholipase C on the thyroid. Abolition of the response to thyroid-stimulating hormone. J Biol Chem 242(8):1864–1869

    CAS  PubMed  Google Scholar 

  13. Portela A et al (1966) Membrane response to phospholipase C and acetylcholine in cesium and potassium Ringer. Acta Physiol Lat Am 16(4):380–386

    CAS  PubMed  Google Scholar 

  14. Trifaro JM et al (2002) Pathways that control cortical F-actin dynamics during secretion. Neurochem Res 27(11):1371–1385

    Article  CAS  PubMed  Google Scholar 

  15. Fukami K et al (2010) Phospholipase C is a key enzyme regulating intracellular calcium and modulating the phosphoinositide balance. Prog Lipid Res 49(4):429–437

    Article  CAS  PubMed  Google Scholar 

  16. Kadamur G, Ross EM (2013) Mammalian phospholipase C. Annu Rev Physiol 75:127–154

    Article  CAS  PubMed  Google Scholar 

  17. Sun MK, Alkon DL (2010) Pharmacology of protein kinase C activators: cognition-enhancing and antidementic therapeutics. Pharmacol Ther 127(1):66–77

    Article  CAS  PubMed  Google Scholar 

  18. Rosse C et al (2010) PKC and the control of localized signal dynamics. Nat Rev Mol Cell Biol 11(2):103–112

    Article  CAS  PubMed  Google Scholar 

  19. Akutagawa A et al (2006) Disruption of phospholipase Cdelta4 gene modulates the liver regeneration in cooperation with nuclear protein kinase C. J Biochem 140(5):619–625

    Article  CAS  PubMed  Google Scholar 

  20. Hashimoto A et al (2000) Cutting edge: essential role of phospholipase C-gamma 2 in B cell development and function. J Immunol 165(4):1738–1742

    Article  CAS  PubMed  Google Scholar 

  21. Hong J et al (2010) Bile acid reflux contributes to development of esophageal adenocarcinoma via activation of phosphatidylinositol-specific phospholipase Cgamma2 and NADPH oxidase NOX5-S. Cancer Res 70(3):1247–1255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Li M et al (2009) Phospholipase Cepsilon promotes intestinal tumorigenesis of Apc(Min/+) mice through augmentation of inflammation and angiogenesis. Carcinogenesis 30(8):1424–1432

    Article  CAS  PubMed  Google Scholar 

  23. Sun C et al (2009) Inhibition of phosphatidylcholine-specific phospholipase C prevents bone marrow stromal cell senescence in vitro. J Cell Biochem 108(2):519–528

    Article  CAS  PubMed  Google Scholar 

  24. Varela D et al (2007) Activation of H2O2-induced VSOR Cl- currents in HTC cells require phospholipase Cgamma1 phosphorylation and Ca2+ mobilisation. Cell Physiol Biochem 20(6):773–780

    Article  CAS  PubMed  Google Scholar 

  25. Wahl MI et al (1989) Platelet-derived growth factor induces rapid and sustained tyrosine phosphorylation of phospholipase C-gamma in quiescent BALB/c 3T3 cells. Mol Cell Biol 9(7):2934–2943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Wang D et al (2000) Phospholipase Cgamma2 is essential in the functions of B cell and several Fc receptors. Immunity 13(1):25–35

    Article  PubMed  Google Scholar 

  27. Bunney TD, Katan M (2011) PLC regulation: emerging pictures for molecular mechanisms. Trends Biochem Sci 36(2):88–96

    Article  CAS  PubMed  Google Scholar 

  28. Suh PG et al (2008) Multiple roles of phosphoinositide-specific phospholipase C isozymes. BMB Rep 41(6):415–434

    Article  CAS  PubMed  Google Scholar 

  29. Rupwate SD, Rajasekharan R (2012) Plant phosphoinositide-specific phospholipase C: an insight. Plant Signal Behav 7(10):1281–1283

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Harlan JE et al (1994) Pleckstrin homology domains bind to phosphatidylinositol-4,5-bisphosphate. Nature 371(6493):168–170

    Article  CAS  PubMed  Google Scholar 

  31. Ni T et al (2017) Structure and lipid-binding properties of the kindlin-3 pleckstrin homology domain. Biochem J 474(4):539–556

    Article  CAS  PubMed  Google Scholar 

  32. Kang JK et al (2017) Increased intracellular Ca2+ concentrations prevent membrane localization of PH domains through the formation of Ca2+-phosphoinositides. Proc Natl Acad Sci U S A 114(45):11926–11931

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Bilkova E et al (2017) Calcium directly regulates phosphatidylinositol 4,5-bisphosphate headgroup conformation and recognition. J Am Chem Soc 139(11):4019–4024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Jezyk MR et al (2006) Crystal structure of Rac1 bound to its effector phospholipase C-beta2. Nat Struct Mol Biol 13(12):1135–1140

    Article  CAS  PubMed  Google Scholar 

  35. Wen W, Yan J, Zhang M (2006) Structural characterization of the split pleckstrin homology domain in phospholipase C-gamma1 and its interaction with TRPC3. J Biol Chem 281(17):12060–12068

    Article  CAS  PubMed  Google Scholar 

  36. Touhara K et al (1994) Binding of G protein beta gamma-subunits to pleckstrin homology domains. J Biol Chem 269(14):10217–10220

    CAS  PubMed  Google Scholar 

  37. Wang T et al (1999) Differential association of the pleckstrin homology domains of phospholipases C-beta 1, C-beta 2, and C-delta 1 with lipid bilayers and the beta gamma subunits of heterotrimeric G proteins. Biochemistry 38(5):1517–1524

    Article  CAS  PubMed  Google Scholar 

  38. Strazza M et al (2017) PLCepsilon1 regulates SDF-1alpha-induced lymphocyte adhesion and migration to sites of inflammation. Proc Natl Acad Sci U S A 114(10):2693–2698

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Raaijmakers JH, Bos JL (2009) Specificity in Ras and Rap signaling. J Biol Chem 284(17):10995–10999

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Kawasaki H, Kretsinger RH (1994) Calcium-binding proteins. 1: EF-hands. Protein Profile 1(4):343–517

    CAS  PubMed  Google Scholar 

  41. Essen LO et al (1996) Crystal structure of a mammalian phosphoinositide-specific phospholipase C delta. Nature 380(6575):595–602

    Article  CAS  PubMed  Google Scholar 

  42. Rhee SG, Choi KD (1992) Regulation of inositol phospholipid-specific phospholipase C isozymes. J Biol Chem 267(18):12393–12396

    CAS  PubMed  Google Scholar 

  43. Essen LO et al (1997) A ternary metal binding site in the C2 domain of phosphoinositide-specific phospholipase C-delta1. Biochemistry 36(10):2753–2762

    Article  CAS  PubMed  Google Scholar 

  44. Otterhag L, Sommarin M, Pical C (2001) N-terminal EF-hand-like domain is required for phosphoinositide-specific phospholipase C activity in Arabidopsis thaliana. FEBS Lett 497(2-3):165–170

    Article  CAS  PubMed  Google Scholar 

  45. Nomikos M et al (2015) Essential role of the EF-hand domain in targeting sperm phospholipase Czeta to membrane phosphatidylinositol 4,5-bisphosphate (PIP2). J Biol Chem 290(49):29519–29530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Theodoridou M et al (2013) Chimeras of sperm PLCzeta reveal disparate protein domain functions in the generation of intracellular Ca2+ oscillations in mammalian eggs at fertilization. Mol Hum Reprod 19(12):852–864

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Ellis MV, S. U, Katan M (1995) Mutations within a highly conserved sequence present in the X region of phosphoinositide-specific phospholipase C-delta 1. Biochem J 307(Pt 1):69–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Nagano N, Orengo CA, Thornton JM (2002) One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J Mol Biol 321(5):741–765

    Article  CAS  PubMed  Google Scholar 

  49. Williams RL (1999) Mammalian phosphoinositide-specific phospholipase C. Biochim Biophys Acta 1441(2-3):255–267

    Article  CAS  PubMed  Google Scholar 

  50. Ryu SH et al (1987) Bovine brain cytosol contains three immunologically distinct forms of inositolphospholipid-specific phospholipase C. Proc Natl Acad Sci U S A 84(19):6649–6653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Margolis B et al (1990) Effect of phospholipase C-gamma overexpression on PDGF-induced second messengers and mitogenesis. Science 248(4955):607–610

    Article  CAS  PubMed  Google Scholar 

  52. Meisenhelder J et al (1989) Phospholipase C-gamma is a substrate for the PDGF and EGF receptor protein-tyrosine kinases in vivo and in vitro. Cell 57(7):1109–1122

    Article  CAS  PubMed  Google Scholar 

  53. Wahl MI, Daniel TO, Carpenter G (1988) Antiphosphotyrosine recovery of phospholipase C activity after EGF treatment of A-431 cells. Science 241(4868):968–970

    Article  CAS  PubMed  Google Scholar 

  54. Ronnstrand L et al (1992) Identification of two C-terminal autophosphorylation sites in the PDGF beta-receptor: involvement in the interaction with phospholipase C-gamma. EMBO J 11(11):3911–3919

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Kim HK et al (1991) PDGF stimulation of inositol phospholipid hydrolysis requires PLC-gamma 1 phosphorylation on tyrosine residues 783 and 1254. Cell 65(3):435–441

    Article  CAS  PubMed  Google Scholar 

  56. Gout I et al (1993) The GTPase dynamin binds to and is activated by a subset of SH3 domains. Cell 75(1):25–36

    Article  CAS  PubMed  Google Scholar 

  57. Bar-Sagi D et al (1993) SH3 domains direct cellular localization of signaling molecules. Cell 74(1):83–91

    Article  CAS  PubMed  Google Scholar 

  58. van Huizen R et al (1998) Two distantly positioned PDZ domains mediate multivalent INAD-phospholipase C interactions essential for G protein-coupled signaling. EMBO J 17(8):2285–2297

    Article  PubMed  PubMed Central  Google Scholar 

  59. Yamaguchi T et al (1993) Two functionally different domains of rabphilin-3A, Rab3A p25/smg p25A-binding and phospholipid- and Ca2+-binding domains. J Biol Chem 268(36):27164–27170

    CAS  PubMed  Google Scholar 

  60. Luo JH, Weinstein IB (1993) Calcium-dependent activation of protein kinase C. The role of the C2 domain in divalent cation selectivity. J Biol Chem 268(31):23580–23584

    CAS  PubMed  Google Scholar 

  61. Davletov BA, Sudhof TC (1993) A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding. J Biol Chem 268(35):26386–26390

    CAS  PubMed  Google Scholar 

  62. Kawasaki H, Nakayama S, Kretsinger RH (1998) Classification and evolution of EF-hand proteins. Biometals 11(4):277–295

    Article  CAS  PubMed  Google Scholar 

  63. Kim Y et al (2001) Chimeric HTH motifs based on EF-hands. J Biol Inorg Chem 6(2):173–181

    Article  PubMed  Google Scholar 

  64. Lomasney JW et al (1999) Activation of phospholipase C delta1 through C2 domain by a Ca2+-enzyme-phosphatidylserine ternary complex. J Biol Chem 274(31):21995–22001

    Article  CAS  PubMed  Google Scholar 

  65. Montaville P et al (2007) The C2A-C2B linker defines the high affinity Ca2+ binding mode of rabphilin-3A. J Biol Chem 282(7):5015–5025

    Article  CAS  PubMed  Google Scholar 

  66. Busch E et al (2000) Calcium affinity, cooperativity, and domain interactions of extracellular EF-hands present in BM-40. J Biol Chem 275(33):25508–25515

    Article  CAS  PubMed  Google Scholar 

  67. Gifford JL, Walsh MP, Vogel HJ (2007) Structures and metal-ion-binding properties of the Ca2+-binding helix-loop-helix EF-hand motifs. Biochem J 405(2):199–221

    Article  CAS  PubMed  Google Scholar 

  68. Linse S et al (1988) The role of protein surface charges in ion binding. Nature 335(6191):651–652

    Article  CAS  PubMed  Google Scholar 

  69. Fanning AS, Anderson JM (1996) Protein-protein interactions: PDZ domain networks. Curr Biol 6(11):1385–1388

    Article  CAS  PubMed  Google Scholar 

  70. Wang CK et al (2010) Extensions of PDZ domains as important structural and functional elements. Protein Cell 1(8):737–751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Kim JK et al (2011) Subtype-specific roles of phospholipase C-beta via differential interactions with PDZ domain proteins. Adv Enzym Regul 51(1):138–151

    Article  CAS  Google Scholar 

  72. Paris L et al (2017) Phosphatidylcholine-specific phospholipase C inhibition reduces HER2-overexpression, cell proliferation and in vivo tumor growth in a highly tumorigenic ovarian cancer model. Oncotarget 8(33):55022–55038

    Article  PubMed  PubMed Central  Google Scholar 

  73. Charnock-Jones DS, Day K, Smith SK (1996) Cloning, expression and genomic organization of human placental protein disulfide isomerase (previously identified as phospholipase C alpha). Int J Biochem Cell Biol 28(1):81–89

    Article  CAS  PubMed  Google Scholar 

  74. Bates RC et al (2014) Activation of Src and release of intracellular calcium by phosphatidic acid during Xenopus laevis fertilization. Dev Biol 386(1):165–180

    Article  CAS  PubMed  Google Scholar 

  75. Yelumalai S et al (2015) Total levels, localization patterns, and proportions of sperm exhibiting phospholipase C zeta are significantly correlated with fertilization rates after intracytoplasmic sperm injection. Fertil Steril 104(3):561–8.e4

    Article  CAS  PubMed  Google Scholar 

  76. Lagercrantz J et al (1995) Genomic organization and complete cDNA sequence of the human phosphoinositide-specific phospholipase C beta 3 gene (PLCB3). Genomics 26(3):467–472

    Article  CAS  PubMed  Google Scholar 

  77. Mao GF, Kunapuli SP, Koneti Rao A (2000) Evidence for two alternatively spliced forms of phospholipase C-beta2 in haematopoietic cells. Br J Haematol 110(2):402–408

    Article  CAS  PubMed  Google Scholar 

  78. Kim MJ et al (1998) A cytosolic, galphaq- and betagamma-insensitive splice variant of phospholipase C-beta4. J Biol Chem 273(6):3618–3624

    Article  CAS  PubMed  Google Scholar 

  79. Xiao W, Kawakami Y, Kawakami T (2013) Immune regulation by phospholipase C-beta isoforms. Immunol Res 56(1):9–19

    Article  CAS  PubMed  Google Scholar 

  80. Kawakami T, Xiao W (2013) Phospholipase C-beta in immune cells. Adv Biol Regul 53(3):249–257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Berstein G et al (1992) Phospholipase C-beta 1 is a GTPase-activating protein for Gq/11, its physiologic regulator. Cell 70(3):411–418

    Article  CAS  PubMed  Google Scholar 

  82. Runnels LW, Scarlata SF (1999) Determination of the affinities between heterotrimeric G protein subunits and their phospholipase C-beta effectors. Biochemistry 38(5):1488–1496

    Article  CAS  PubMed  Google Scholar 

  83. Hwang JI et al (2000) Regulation of phospholipase C-beta 3 activity by Na+/H+ exchanger regulatory factor 2. J Biol Chem 275(22):16632–16637

    Article  CAS  PubMed  Google Scholar 

  84. Camps M et al (1992) Isozyme-selective stimulation of phospholipase C-beta 2 by G protein beta gamma-subunits. Nature 360(6405):684–686

    Article  CAS  PubMed  Google Scholar 

  85. Lee SB et al (1993) Activation of phospholipase C-beta 2 mutants by G protein alpha q and beta gamma subunits. J Biol Chem 268(34):25952–25957

    CAS  PubMed  Google Scholar 

  86. Wang T et al (1999) Selective interaction of the C2 domains of phospholipase C-beta1 and -beta2 with activated Galphaq subunits: an alternative function for C2-signaling modules. Proc Natl Acad Sci U S A 96(14):7843–7846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Scarlata S et al (2016) Phospholipase Cbeta connects G protein signaling with RNA interference. Adv Biol Regul 61:51–57

    Article  CAS  PubMed  Google Scholar 

  88. Martelli AM et al (1992) Nuclear localization and signalling activity of phosphoinositidase C beta in Swiss 3T3 cells. Nature 358(6383):242–245

    Article  CAS  PubMed  Google Scholar 

  89. Kim CG, Park D, Rhee SG (1996) The role of carboxyl-terminal basic amino acids in Gqalpha-dependent activation, particulate association, and nuclear localization of phospholipase C-beta1. J Biol Chem 271(35):21187–21192

    Article  CAS  PubMed  Google Scholar 

  90. Payrastre B et al (1992) A differential location of phosphoinositide kinases, diacylglycerol kinase, and phospholipase C in the nuclear matrix. J Biol Chem 267(8):5078–5084

    CAS  PubMed  Google Scholar 

  91. Ratti S et al (2017) Nuclear inositide signaling via phospholipase C. J Cell Biochem 118(8):1969–1978

    Article  CAS  PubMed  Google Scholar 

  92. Poli A et al (2016) Nuclear phosphatidylinositol signaling: focus on phosphatidylinositol phosphate kinases and phospholipases C. J Cell Physiol 231(8):1645–1655

    Article  CAS  PubMed  Google Scholar 

  93. Piazzi M et al (2015) PI-PLCbeta1b affects Akt activation, cyclin E expression, and caspase cleavage, promoting cell survival in pro-B-lymphoblastic cells exposed to oxidative stress. FASEB J 29(4):1383–1394

    Article  CAS  PubMed  Google Scholar 

  94. Navaratnarajah P, Gershenson A, Ross EM (2017) The binding of activated Galphaq to phospholipase C-beta exhibits anomalous affinity. J Biol Chem 292(40):16787–16801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Wang HL (1997) Basic amino acids at the C-terminus of the third intracellular loop are required for the activation of phospholipase C by cholecystokinin-B receptors. J Neurochem 68(4):1728–1735

    Article  CAS  PubMed  Google Scholar 

  96. Adamski FM, Timms KM, Shieh BH (1999) A unique isoform of phospholipase Cbeta4 highly expressed in the cerebellum and eye. Biochim Biophys Acta 1444(1):55–60

    Article  CAS  PubMed  Google Scholar 

  97. Min DS et al (1993) Purification of a novel phospholipase C isozyme from bovine cerebellum. J Biol Chem 268(16):12207–12212

    CAS  PubMed  Google Scholar 

  98. Alvarez RA et al (1995) cDNA sequence and gene locus of the human retinal phosphoinositide-specific phospholipase-C beta 4 (PLCB4). Genomics 29(1):53–61

    Article  CAS  PubMed  Google Scholar 

  99. Park D et al (1992) Cloning, sequencing, expression, and Gq-independent activation of phospholipase C-beta 2. J Biol Chem 267(23):16048–16055

    CAS  PubMed  Google Scholar 

  100. Harden TK, Hicks SN, Sondek J (2009) Phospholipase C isozymes as effectors of Ras superfamily GTPases. J Lipid Res 50(Suppl):S243–S248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Snyder JT et al (2003) The pleckstrin homology domain of phospholipase C-beta2 as an effector site for Rac. J Biol Chem 278(23):21099–21104

    Article  CAS  PubMed  Google Scholar 

  102. Jhon DY et al (1993) Cloning, sequencing, purification, and Gq-dependent activation of phospholipase C-beta 3. J Biol Chem 268(9):6654–6661

    CAS  PubMed  Google Scholar 

  103. Fukaya M et al (2008) Predominant expression of phospholipase Cbeta1 in telencephalic principal neurons and cerebellar interneurons, and its close association with related signaling molecules in somatodendritic neuronal elements. Eur J Neurosci 28(9):1744–1759

    Article  PubMed  Google Scholar 

  104. Watanabe M et al (1998) Patterns of expression for the mRNA corresponding to the four isoforms of phospholipase Cbeta in mouse brain. Eur J Neurosci 10(6):2016–2025

    Article  CAS  PubMed  Google Scholar 

  105. Yang YR et al (2016) Primary phospholipase C and brain disorders. Adv Biol Regul 61:80–85

    Article  CAS  PubMed  Google Scholar 

  106. Koh HY (2013) Phospholipase C-beta1 and schizophrenia-related behaviors. Adv Biol Regul 53(3):242–248

    Article  CAS  PubMed  Google Scholar 

  107. Schoonjans AS et al (2016) PLCB1 epileptic encephalopathies; Review and expansion of the phenotypic spectrum. Eur J Paediatr Neurol 20(3):474–479

    Article  PubMed  Google Scholar 

  108. Kim D et al (1997) Phospholipase C isozymes selectively couple to specific neurotransmitter receptors. Nature 389(6648):290–293

    Article  CAS  PubMed  Google Scholar 

  109. Cocco L et al (2016) Modulation of nuclear PI-PLCbeta1 during cell differentiation. Adv Biol Regul 60:1–5

    Article  CAS  PubMed  Google Scholar 

  110. Ramazzotti G et al (2017) PLC-beta1 and cell differentiation: An insight into myogenesis and osteogenesis. Adv Biol Regul 63:1–5

    Article  CAS  PubMed  Google Scholar 

  111. Brugnoli F et al (2017) Up-modulation of PLC-beta2 reduces the number and malignancy of triple-negative breast tumor cells with a CD133(+)/EpCAM(+) phenotype: a promising target for preventing progression of TNBC. BMC Cancer 17(1):617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Lu G et al (2016) Phospholipase C Beta 1: a candidate signature gene for proneural subtype high-grade glioma. Mol Neurobiol 53(9):6511–6525

    Article  CAS  PubMed  Google Scholar 

  113. Driscoll PC (2015) Exposed: the many and varied roles of phospholipase C gamma SH2 domains. J Mol Biol 427(17):2731–2733

    Article  CAS  PubMed  Google Scholar 

  114. Jang HJ et al (2013) Phospholipase C-gamma1 involved in brain disorders. Adv Biol Regul 53(1):51–62

    Article  CAS  PubMed  Google Scholar 

  115. Epple H et al (2008) Phospholipase Cgamma2 modulates integrin signaling in the osteoclast by affecting the localization and activation of Src kinase. Mol Cell Biol 28(11):3610–3622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Choi JH et al (2007) Phospholipase C-gamma1 potentiates integrin-dependent cell spreading and migration through Pyk2/paxillin activation. Cell Signal 19(8):1784–1796

    Article  CAS  PubMed  Google Scholar 

  117. Bunney TD et al (2012) Structural and functional integration of the PLCgamma interaction domains critical for regulatory mechanisms and signaling deregulation. Structure 20(12):2062–2075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Arkinstall S, Payton M, Maundrell K (1995) Activation of phospholipase C gamma in Schizosaccharomyces pombe by coexpression of receptor or nonreceptor tyrosine kinases. Mol Cell Biol 15(3):1431–1438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Phillippe M et al (2009) Role of nonreceptor protein tyrosine kinases during phospholipase C-gamma 1-related uterine contractions in the rat. Reprod Sci 16(3):265–273

    Article  CAS  PubMed  Google Scholar 

  120. Buitrago C, Gonzalez Pardo V, de Boland AR (2002) Nongenomic action of 1 alpha,25(OH)(2)-vitamin D3. Activation of muscle cell PLC gamma through the tyrosine kinase c-Src and PtdIns 3-kinase. Eur J Biochem 269(10):2506–2515

    Article  CAS  PubMed  Google Scholar 

  121. Kusuyama J et al (2018) Spleen tyrosine kinase influences the early stages of multilineage differentiation of bone marrow stromal cell lines by regulating phospholipase C gamma activities. J Cell Physiol 233(3):2549–2559

    Article  CAS  PubMed  Google Scholar 

  122. Rivas M, Santisteban P (2003) TSH-activated signaling pathways in thyroid tumorigenesis. Mol Cell Endocrinol 213(1):31–45

    Article  CAS  PubMed  Google Scholar 

  123. Kroczek C et al (2010) Swiprosin-1/EFhd2 controls B cell receptor signaling through the assembly of the B cell receptor, Syk, and phospholipase C gamma2 in membrane rafts. J Immunol 184(7):3665–3676

    Article  CAS  PubMed  Google Scholar 

  124. Sato K et al (2003) Reconstitution of Src-dependent phospholipase Cgamma phosphorylation and transient calcium release by using membrane rafts and cell-free extracts from Xenopus eggs. J Biol Chem 278(40):38413–38420

    Article  CAS  PubMed  Google Scholar 

  125. Kim MJ et al (2000) Direct interaction of SOS1 Ras exchange protein with the SH3 domain of phospholipase C-gamma1. Biochemistry 39(29):8674–8682

    Article  CAS  PubMed  Google Scholar 

  126. Braiman A et al (2006) Recruitment and activation of PLCgamma1 in T cells: a new insight into old domains. EMBO J 25(4):774–784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Barbosa CM et al (2014) PLCgamma2 and PKC are important to myeloid lineage commitment triggered by M-SCF and G-CSF. J Cell Biochem 115(1):42–51

    Article  CAS  PubMed  Google Scholar 

  128. Wen R et al (2002) Phospholipase C gamma 2 is essential for specific functions of Fc epsilon R and Fc gamma R. J Immunol 169(12):6743–6752

    Article  CAS  PubMed  Google Scholar 

  129. Todt JC, Hu B, Curtis JL (2004) The receptor tyrosine kinase MerTK activates phospholipase C gamma2 during recognition of apoptotic thymocytes by murine macrophages. J Leukoc Biol 75(4):705–713

    Article  CAS  PubMed  Google Scholar 

  130. Ting AT et al (1992) Fc gamma receptor activation induces the tyrosine phosphorylation of both phospholipase C (PLC)-gamma 1 and PLC-gamma 2 in natural killer cells. J Exp Med 176(6):1751–1755

    Article  CAS  PubMed  Google Scholar 

  131. Hiller G, Sundler R (2002) Regulation of phospholipase C-gamma 2 via phosphatidylinositol 3-kinase in macrophages. Cell Signal 14(2):169–173

    Article  CAS  PubMed  Google Scholar 

  132. Kagan JC, Medzhitov R (2006) Phosphoinositide-mediated adaptor recruitment controls Toll-like receptor signaling. Cell 125(5):943–955

    Article  CAS  PubMed  Google Scholar 

  133. Finco TS et al (1998) LAT is required for TCR-mediated activation of PLCgamma1 and the Ras pathway. Immunity 9(5):617–626

    Article  CAS  PubMed  Google Scholar 

  134. Stoica B et al (1998) The amino-terminal Src homology 2 domain of phospholipase C gamma 1 is essential for TCR-induced tyrosine phosphorylation of phospholipase C gamma 1. J Immunol 160(3):1059–1066

    CAS  PubMed  Google Scholar 

  135. Zhang W et al (2000) Association of Grb2, Gads, and phospholipase C-gamma 1 with phosphorylated LAT tyrosine residues. Effect of LAT tyrosine mutations on T cell angigen receptor-mediated signaling. J Biol Chem 275(30):23355–23361

    Article  CAS  PubMed  Google Scholar 

  136. Dower NA et al (2000) RasGRP is essential for mouse thymocyte differentiation and TCR signaling. Nat Immunol 1(4):317–321

    Article  CAS  PubMed  Google Scholar 

  137. Ebinu JO et al (2000) RasGRP links T-cell receptor signaling to Ras. Blood 95(10):3199–3203

    Article  CAS  PubMed  Google Scholar 

  138. Shannon LA et al (2010) CCR7/CCL21 migration on fibronectin is mediated by phospholipase Cgamma1 and ERK1/2 in primary T lymphocytes. J Biol Chem 285(50):38781–38787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  139. Ji QS et al (1997) Essential role of the tyrosine kinase substrate phospholipase C-gamma1 in mammalian growth and development. Proc Natl Acad Sci U S A 94(7):2999–3003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Wonerow P et al (2003) A critical role for phospholipase Cgamma2 in alphaIIbbeta3-mediated platelet spreading. J Biol Chem 278(39):37520–37529

    Article  CAS  PubMed  Google Scholar 

  141. Inoue O et al (2003) Integrin alpha2beta1 mediates outside-in regulation of platelet spreading on collagen through activation of Src kinases and PLCgamma2. J Cell Biol 160(5):769–780

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  142. Garcia-Diaz Barriga G et al (2017) 7,8-dihydroxyflavone ameliorates cognitive and motor deficits in a Huntington’s disease mouse model through specific activation of the PLCgamma1 pathway. Hum Mol Genet 26(16):3144–3160

    PubMed  Google Scholar 

  143. Sims R et al (2017) Rare coding variants in PLCG2, ABI3, and TREM2 implicate microglial-mediated innate immunity in Alzheimer’s disease. Nat Genet 49(9):1373–1384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Jiang D et al (2017) Phospholipase Cgamma1 mediates intima formation through Akt-Notch1 signaling independent of the phospholipase activity. J Am Heart Assoc 6(7)

    Google Scholar 

  145. Zhu L et al (2016) PLC-gamma1 is involved in the inflammatory response induced by influenza A virus H1N1 infection. Virology 496:131–137

    Article  CAS  PubMed  Google Scholar 

  146. Jang HJ et al (2018) PLCgamma1: potential arbitrator of cancer progression. Adv Biol Regul 67:179–189

    Article  CAS  PubMed  Google Scholar 

  147. Cai S et al (2017) Expression of phospholipase C isozymes in human breast cancer and their clinical significance. Oncol Rep 37(3):1707–1715

    Article  CAS  PubMed  Google Scholar 

  148. Woyach JA et al (2014) Resistance mechanisms for the Bruton’s tyrosine kinase inhibitor ibrutinib. N Engl J Med 370(24):2286–2294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Koss H et al (2014) Dysfunction of phospholipase Cgamma in immune disorders and cancer. Trends Biochem Sci 39(12):603–611

    Article  CAS  PubMed  Google Scholar 

  150. Meldrum E et al (1991) A second gene product of the inositol-phospholipid-specific phospholipase C delta subclass. Eur J Biochem 196(1):159–165

    Article  CAS  PubMed  Google Scholar 

  151. Allen V et al (1997) Regulation of inositol lipid-specific phospholipase cdelta by changes in Ca2+ ion concentrations. Biochem J 327(Pt 2):545–552

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Kim YH et al (1999) Phospholipase C-delta1 is activated by capacitative calcium entry that follows phospholipase C-beta activation upon bradykinin stimulation. J Biol Chem 274(37):26127–26134

    Article  CAS  PubMed  Google Scholar 

  153. Yamaga M et al (1999) Phospholipase C-delta1 contains a functional nuclear export signal sequence. J Biol Chem 274(40):28537–28541

    Article  CAS  PubMed  Google Scholar 

  154. Kunrath-Lima M et al (2018) Phospholipase C delta 4 (PLCdelta4) is a nuclear protein involved in cell proliferation and senescence in mesenchymal stromal stem cells. Cell Signal 49:59–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. Stallings JD et al (2005) Nuclear translocation of phospholipase C-delta1 is linked to the cell cycle and nuclear phosphatidylinositol 4,5-bisphosphate. J Biol Chem 280(23):22060–22069

    Article  CAS  PubMed  Google Scholar 

  156. Yoko-o T et al (1993) The putative phosphoinositide-specific phospholipase C gene, PLC1, of the yeast Saccharomyces cerevisiae is important for cell growth. Proc Natl Acad Sci U S A 90(5):1804–1808

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Murthy KS et al (2004) Activation of PLC-delta1 by Gi/o-coupled receptor agonists. Am J Phys Cell Phys 287(6):C1679–C1687

    Article  CAS  Google Scholar 

  158. Kanemaru K et al (2017) Phospholipase Cdelta1 regulates p38 MAPK activity and skin barrier integrity. Cell Death Differ 24(6):1079–1090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Sakurai K et al (2011) Phospholipase Cdelta3 is a novel binding partner of myosin VI and functions as anchoring of myosin VI on plasma membrane. Adv Enzym Regul 51(1):171–181

    Article  CAS  Google Scholar 

  160. Kouchi Z et al (2011) Phospholipase Cdelta3 regulates RhoA/Rho kinase signaling and neurite outgrowth. J Biol Chem 286(10):8459–8471

    Article  CAS  PubMed  Google Scholar 

  161. Nakamura Y et al (2005) Phospholipase C-delta1 and -delta3 are essential in the trophoblast for placental development. Mol Cell Biol 25(24):10979–10988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. Shimohama S et al (1991) Aberrant accumulation of phospholipase C-delta in Alzheimer brains. Am J Pathol 139(4):737–742

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Yagisawa H, Tanase H, Nojima H (1991) Phospholipase C-delta gene of the spontaneously hypertensive rat harbors point mutations causing amino acid substitutions in a catalytic domain. J Hypertens 9(11):997–1004

    Article  CAS  PubMed  Google Scholar 

  164. Vachel L et al (2015) The low PLC-delta1 expression in cystic fibrosis bronchial epithelial cells induces upregulation of TRPV6 channel activity. Cell Calcium 57(1):38–48

    Article  CAS  PubMed  Google Scholar 

  165. Nakamura Y et al (2008) Phospholipase C-delta1 is an essential molecule downstream of Foxn1, the gene responsible for the nude mutation, in normal hair development. FASEB J 22(3):841–849

    Article  CAS  PubMed  Google Scholar 

  166. Ichinohe M et al (2007) Lack of phospholipase C-delta1 induces skin inflammation. Biochem Biophys Res Commun 356(4):912–918

    Article  CAS  PubMed  Google Scholar 

  167. Fukami K et al (2003) Phospholipase Cdelta4 is required for Ca2+ mobilization essential for acrosome reaction in sperm. J Cell Biol 161(1):79–88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Fukami K et al (2001) Requirement of phospholipase Cdelta4 for the zona pellucida-induced acrosome reaction. Science 292(5518):920–923

    Article  CAS  PubMed  Google Scholar 

  169. Shao Q et al (2017) Phospholipase Cdelta1 suppresses cell migration and invasion of breast cancer cells by modulating KIF3A-mediated ERK1/2/beta- catenin/MMP7 signalling. Oncotarget 8(17):29056–29066

    Article  PubMed  PubMed Central  Google Scholar 

  170. Satow R et al (2014) Phospholipase Cdelta1 induces E-cadherin expression and suppresses malignancy in colorectal cancer cells. Proc Natl Acad Sci U S A 111(37):13505–13510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Shimozawa M et al (2017) Phospholipase C delta1 negatively regulates autophagy in colorectal cancer cells. Biochem Biophys Res Commun 488(4):578–583

    Article  CAS  PubMed  Google Scholar 

  172. Shibatohge M et al (1998) Identification of PLC210, a Caenorhabditis elegans phospholipase C, as a putative effector of Ras. J Biol Chem 273(11):6218–6222

    Article  CAS  PubMed  Google Scholar 

  173. Sorli SC et al (2005) Signaling properties and expression in normal and tumor tissues of two phospholipase C epsilon splice variants. Oncogene 24(1):90–100

    Article  CAS  PubMed  Google Scholar 

  174. Lopez I et al (2001) A novel bifunctional phospholipase c that is regulated by Galpha 12 and stimulates the Ras/mitogen-activated protein kinase pathway. J Biol Chem 276(4):2758–2765

    Article  CAS  PubMed  Google Scholar 

  175. Song C et al (2001) Regulation of a novel human phospholipase C, PLCepsilon, through membrane targeting by Ras. J Biol Chem 276(4):2752–2757

    Article  CAS  PubMed  Google Scholar 

  176. Wing MR et al (2003) Direct activation of phospholipase C-epsilon by Rho. J Biol Chem 278(42):41253–41258

    Article  CAS  PubMed  Google Scholar 

  177. Wing MR, Bourdon DM, Harden TK (2003) PLC-epsilon: a shared effector protein in Ras-, Rho-, and G alpha beta gamma-mediated signaling. Mol Interv 3(5):273–280

    Article  CAS  PubMed  Google Scholar 

  178. Malik S et al (2015) G protein betagamma subunits regulate cardiomyocyte hypertrophy through a perinuclear Golgi phosphatidylinositol 4-phosphate hydrolysis pathway. Mol Biol Cell 26(6):1188–1198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  179. Madukwe JC et al (2018) G protein betagamma subunits directly interact with and activate phospholipase C. J Biol Chem 293(17):6387–6397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Schmidt M et al (2001) A new phospholipase-C calcium signaling pathway mediated by cyclic AMP and a Rap GTPase. Nat Cell Biol 3(11):1020–1024

    Article  CAS  PubMed  Google Scholar 

  181. Evellin S et al (2002) Stimulation of phospholipase C-epsilon by the M3 muscarinic acetylcholine receptor mediated by cyclic AMP and the GTPase Rap2B. J Biol Chem 277(19):16805–16813

    Article  CAS  PubMed  Google Scholar 

  182. Jin TG et al (2001) Role of the CDC25 homology domain of phospholipase Cepsilon in amplification of Rap1-dependent signaling. J Biol Chem 276(32):30301–30307

    Article  CAS  PubMed  Google Scholar 

  183. Xiang SY et al (2013) PLCepsilon, PKD1, and SSH1L transduce RhoA signaling to protect mitochondria from oxidative stress in the heart. Sci Signal 6(306):ra108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Wang H et al (2005) Phospholipase C epsilon modulates beta-adrenergic receptor-dependent cardiac contraction and inhibits cardiac hypertrophy. Circ Res 97(12):1305–1313

    Article  CAS  PubMed  Google Scholar 

  185. Tadano M et al (2005) Congenital semilunar valvulogenesis defect in mice deficient in phospholipase C epsilon. Mol Cell Biol 25(6):2191–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  186. Chan JJ, Katan M (2013) PLCvarepsilon and the RASSF family in tumour suppression and other functions. Adv Biol Regul 53(3):258–279

    Article  CAS  PubMed  Google Scholar 

  187. Tyutyunnykova A, Telegeev G, Dubrovska A (2017) The controversial role of phospholipase C epsilon (PLCepsilon) in cancer development and progression. J Cancer 8(5):716–729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  188. Zhang RY et al (2016) PLCepsilon signaling in cancer. J Cancer Res Clin Oncol 142(4):715–722

    Article  CAS  PubMed  Google Scholar 

  189. Popovics P et al (2014) A canonical EF-loop directs Ca2+ -sensitivity in phospholipase C-eta2. J Cell Biochem 115(3):557–565

    Article  CAS  PubMed  Google Scholar 

  190. Smrcka AV, Brown JH, Holz GG (2012) Role of phospholipase Cepsilon in physiological phosphoinositide signaling networks. Cell Signal 24(6):1333–1343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  191. Yang YR et al (2013) The physiological roles of primary phospholipase C. Adv Biol Regul 53(3):232–241

    Article  CAS  PubMed  Google Scholar 

  192. Stewart AJ et al (2005) Identification of a novel class of mammalian phosphoinositol-specific phospholipase C enzymes. Int J Mol Med 15(1):117–121

    CAS  PubMed  Google Scholar 

  193. Zhou Y et al (2005) Molecular cloning and characterization of PLC-eta2. Biochem J 391(Pt 3):667–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  194. Kouchi Z et al (2005) The role of EF-hand domains and C2 domain in regulation of enzymatic activity of phospholipase Czeta. J Biol Chem 280(22):21015–21021

    Article  CAS  PubMed  Google Scholar 

  195. Lo Vasco VR (2011) Role of Phosphoinositide-Specific Phospholipase C eta2 in Isolated and Syndromic Mental Retardation. Eur Neurol 65(5):264–269

    Article  CAS  PubMed  Google Scholar 

  196. Popovics P et al (2013) Phospholipase C-eta2 is required for retinoic acid-stimulated neurite growth. J Neurochem 124(5):632–644

    Article  CAS  PubMed  Google Scholar 

  197. Popovics P, Stewart AJ (2012) Phospholipase C-eta activity may contribute to Alzheimer’s disease-associated calciumopathy. J Alzheimers Dis 30(4):737–744

    Article  CAS  PubMed  Google Scholar 

  198. Cox LJ et al (2002) Sperm phospholipase Czeta from humans and cynomolgus monkeys triggers Ca2+ oscillations, activation and development of mouse oocytes. Reproduction 124(5):611–623

    Article  CAS  PubMed  Google Scholar 

  199. Fujimoto S et al (2004) Mammalian phospholipase Czeta induces oocyte activation from the sperm perinuclear matrix. Dev Biol 274(2):370–383

    Article  CAS  PubMed  Google Scholar 

  200. Jones KT et al (2000) Different Ca2+-releasing abilities of sperm extracts compared with tissue extracts and phospholipase C isoforms in sea urchin egg homogenate and mouse eggs. Biochem J 346(Pt 3):743–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  201. Kashir J et al (2017) Antigen unmasking enhances visualization efficacy of the oocyte activation factor, phospholipase C zeta, in mammalian sperm. Mol Hum Reprod 23(1):54–67

    Article  CAS  PubMed  Google Scholar 

  202. Kashir J, Nomikos M, Lai FA (2018) Phospholipase C zeta and calcium oscillations at fertilisation: the evidence, applications, and further questions. Adv Biol Regul 67:148–162

    Article  CAS  PubMed  Google Scholar 

  203. Aarabi M et al (2014) Sperm-derived WW domain-binding protein, PAWP, elicits calcium oscillations and oocyte activation in humans and mice. FASEB J 28(10):4434–4440

    Article  CAS  PubMed  Google Scholar 

  204. Aarabi M et al (2010) Sperm-borne protein, PAWP, initiates zygotic development in Xenopus laevis by eliciting intracellular calcium release. Mol Reprod Dev 77(3):249–256

    CAS  PubMed  Google Scholar 

  205. Wu AT et al (2007) PAWP, a sperm-specific WW domain-binding protein, promotes meiotic resumption and pronuclear development during fertilization. J Biol Chem 282(16):12164–12175

    Article  CAS  PubMed  Google Scholar 

  206. Escoffier J et al (2016) Homozygous mutation of PLCZ1 leads to defective human oocyte activation and infertility that is not rescued by the WW-binding protein PAWP. Hum Mol Genet 25(5):878–891

    Article  CAS  PubMed  Google Scholar 

  207. Kashir J et al (2015) PLCzeta or PAWP: revisiting the putative mammalian sperm factor that triggers egg activation and embryogenesis. Mol Hum Reprod 21(5):383–388

    Article  CAS  PubMed  Google Scholar 

  208. Nomikos M et al (2015) Functional disparity between human PAWP and PLCzeta in the generation of Ca2+ oscillations for oocyte activation. Mol Hum Reprod 21(9):702–710

    Article  CAS  PubMed  Google Scholar 

  209. Nomikos M et al (2014) Sperm-specific post-acrosomal WW-domain binding protein (PAWP) does not cause Ca2+ release in mouse oocytes. Mol Hum Reprod 20(10):938–947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  210. Satouh Y, Nozawa K, Ikawa M (2015) Sperm postacrosomal WW domain-binding protein is not required for mouse egg activation. Biol Reprod 93(4):94

    Article  CAS  PubMed  Google Scholar 

  211. Grasa P et al (2008) The pattern of localization of the putative oocyte activation factor, phospholipase Czeta, in uncapacitated, capacitated, and ionophore-treated human spermatozoa. Hum Reprod 23(11):2513–2522

    Article  CAS  PubMed  Google Scholar 

  212. Kashir J et al (2014) Sperm-induced Ca2+ release during egg activation in mammals. Biochem Biophys Res Commun 450(3):1204–1211

    Article  CAS  PubMed  Google Scholar 

  213. Young C et al (2009) Phospholipase C zeta undergoes dynamic changes in its pattern of localization in sperm during capacitation and the acrosome reaction. Fertil Steril 91(5 Suppl):2230–2242

    Article  CAS  PubMed  Google Scholar 

  214. Heytens E et al (2009) Reduced amounts and abnormal forms of phospholipase C zeta (PLCzeta) in spermatozoa from infertile men. Hum Reprod 24(10):2417–2428

    Article  CAS  PubMed  Google Scholar 

  215. Kashir J et al (2013) Variance in total levels of phospholipase C zeta (PLC-zeta) in human sperm may limit the applicability of quantitative immunofluorescent analysis as a diagnostic indicator of oocyte activation capability. Fertil Steril 99(1):107–117

    Article  CAS  PubMed  Google Scholar 

  216. Yoon SY et al (2008) Human sperm devoid of PLC, zeta 1 fail to induce Ca2+ release and are unable to initiate the first step of embryo development. J Clin Invest 118(11):3671–3681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  217. Swann K et al (2006) PLCzeta(zeta): a sperm protein that triggers Ca2+ oscillations and egg activation in mammals. Semin Cell Dev Biol 17(2):264–273

    Article  CAS  PubMed  Google Scholar 

  218. Nomikos M et al (2005) Role of phospholipase C-zeta domains in Ca2+-dependent phosphatidylinositol 4,5-bisphosphate hydrolysis and cytoplasmic Ca2+ oscillations. J Biol Chem 280(35):31011–31018

    Article  CAS  PubMed  Google Scholar 

  219. Halet G et al (2003) Ca2+ oscillations at fertilization in mammals. Biochem Soc Trans 31(Pt 5):907–911

    Article  CAS  PubMed  Google Scholar 

  220. Marangos P, FitzHarris G, Carroll J (2003) Ca2+ oscillations at fertilization in mammals are regulated by the formation of pronuclei. Development 130(7):1461–1472

    Article  CAS  PubMed  Google Scholar 

  221. Amdani SN et al (2016) Phospholipase C zeta (PLCzeta) and male infertility: Clinical update and topical developments. Adv Biol Regul 61:58–67

    Article  CAS  PubMed  Google Scholar 

  222. Wang C et al (2005) Binding of PLCdelta1PH-GFP to PtdIns(4,5)P2 prevents inhibition of phospholipase C-mediated hydrolysis of PtdIns(4,5)P2 by neomycin. Acta Pharmacol Sin 26(12):1485–1491

    Article  CAS  PubMed  Google Scholar 

  223. Klein RR et al (2011) Direct activation of human phospholipase C by its well known inhibitor u73122. J Biol Chem 286(14):12407–12416

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  224. Dwyer L et al (2010) Phospholipase C-independent effects of 3M3FBS in murine colon. Eur J Pharmacol 628(1-3):187–194

    Article  CAS  PubMed  Google Scholar 

  225. Frei E, Hofmann F, Wegener JW (2009) Phospholipase C mediated Ca2+ signals in murine urinary bladder smooth muscle. Eur J Pharmacol 610(1-3):106–109

    Article  CAS  PubMed  Google Scholar 

  226. Xu S et al (2009) Phospholipase Cgamma2 is critical for Dectin-1-mediated Ca2+ flux and cytokine production in dendritic cells. J Biol Chem 284(11):7038–7046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  227. Shi TJ et al (2008) Phospholipase C{beta}3 in mouse and human dorsal root ganglia and spinal cord is a possible target for treatment of neuropathic pain. Proc Natl Acad Sci U S A 105(50):20004–20008

    Article  PubMed  PubMed Central  Google Scholar 

  228. Ibrahim S et al (2007) The transfer of VLDL-associated phospholipids to activated platelets depends upon cytosolic phospholipase A2 activity. J Lipid Res 48(7):1533–1538

    Article  CAS  PubMed  Google Scholar 

  229. Sickmann T et al (2008) Unexpected suppression of neuronal G protein-activated, inwardly rectifying K+ current by common phospholipase C inhibitor. Neurosci Lett 436(2):102–106

    Article  CAS  PubMed  Google Scholar 

  230. Kim DD, Ramirez MM, Duran WN (2000) Platelet-activating factor modulates microvascular dynamics through phospholipase C in the hamster cheek pouch. Microvasc Res 59(1):7–13

    Article  CAS  PubMed  Google Scholar 

  231. Muto Y, Nagao T, Urushidani T (1997) The putative phospholipase C inhibitor U73122 and its negative control, U73343, elicit unexpected effects on the rabbit parietal cell. J Pharmacol Exp Ther 282(3):1379–1388

    CAS  PubMed  Google Scholar 

  232. Amtmann E (1996) The antiviral, antitumoural xanthate D609 is a competitive inhibitor of phosphatidylcholine-specific phospholipase C. Drugs Exp Clin Res 22(6):287–294

    CAS  PubMed  Google Scholar 

  233. Powis G et al (1992) Selective inhibition of phosphatidylinositol phospholipase C by cytotoxic ether lipid analogues. Cancer Res 52(10):2835–2840

    CAS  PubMed  Google Scholar 

  234. Suzuki H et al (2002) Effects of RHC-80267, an inhibitor of diacylglycerol lipase, on excitation of circular smooth muscle of the guinea-pig gastric antrum. J Smooth Muscle Res 38(6):153–164

    Article  CAS  PubMed  Google Scholar 

  235. Bae YS et al (2003) Identification of a compound that directly stimulates phospholipase C activity. Mol Pharmacol 63(5):1043–1050

    Article  CAS  PubMed  Google Scholar 

  236. Bassett AR et al (2013) Highly efficient targeted mutagenesis of Drosophila with the CRISPR/Cas9 system. Cell Rep 4(1):220–228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  237. Friedland AE et al (2013) Heritable genome editing in C. elegans via a CRISPR-Cas9 system. Nat Methods 10(8):741–743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  238. Raimondi C et al (2016) A Small Molecule Inhibitor of PDK1/PLCgamma1 Interaction Blocks Breast and Melanoma Cancer Cell Invasion. Sci Rep 6:26142

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Bill, C.A., Vines, C.M. (2020). Phospholipase C. In: Islam, M. (eds) Calcium Signaling. Advances in Experimental Medicine and Biology, vol 1131. Springer, Cham. https://doi.org/10.1007/978-3-030-12457-1_9

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