Nuclear phospholipid signaling: Phosphatidylinositol-specific phospholipase C and phosphoinositide 3-kinase

Pflugers Archiv European Journal of Physiology

Volumn 455, Issue 1, 2007, Pages 19-30

  Visnjic, Dora ^a   Banfic, Hrvoje ^a  

^a UNIVERSITY OF ZAGREB   (Croatia)

Author keywords

Nuclei; Phosphoinositide 3 kinase; Phospholipase C; Phospholipid

Indexed keywords

ISOENZYME; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE PHOSPHODIESTERASE; PHOSPHOLIPASE C BETA1;

CELL CYCLE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL MEMBRANE; CELL NUCLEUS MEMBRANE; CELL SURVIVAL; MITOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVIEW;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; CELL CYCLE; CELL DIFFERENTIATION; CELL NUCLEUS; HUMANS; MITOSIS; PHOSPHOINOSITIDE PHOSPHOLIPASE C; PHOSPHOLIPIDS; SIGNAL TRANSDUCTION;

EID: 34548609312     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-007-0288-1     Document Type: Review

References (85)

1. Ahn JY, Rong R, Liu X, Ye K (2004) PIKE/nuclear PI 3-kinase signaling mediates the antiapoptotic actions of NGF in the nucleus. EMBO J 23:3995-4006
2. Ahn JY, Liu X, Cheng D, Peng J, Chan PK, Wade PA, Ye K (2005) Nucleophosmin/B23, a nuclear PI(3,4,5)P(3) receptor, mediates the antiapoptotic actions of NGF by inhibiting CAD. Mol Cell 13:435-445
3. Ahn JY, Liu X, Liu Z, Pereira L, Cheng D, Peng J, Wade PA, Hamburger AW, Ye K (2006) Nuclear Akt associates with PKC-phosphorylated Ebp1, preventing DNA fragmentation by inhibition of caspase-activated DNase. EMBO J 25:2083-2095
4. Bahk YY, Song H, Baek SH, Park BY, Kim H, Ryu SH, Suh PG (1998) Localization of two forms of phospholipase C-beta1, a and b, in C6Bu-1 cells. Biochim Biophys Acta 1389:76-80
5. Banfic H, Zizak M, Divecha N, Irvine RF (1993) Nuclear diacylglycerol is increased during cell proliferation in vivo. Biochem J 290:633-636
6. Bertagnolo V, Mazzoni M, Ricci D, Carini C, Neri LM, Previati M, Capitani S (1995) Identification of PI-PLC beta 1, gamma 1, and delta 1 in rat liver: subcellular distribution and relationship to inositol lipid nuclear signalling. Cell Signal 7:669-678
7. Bertagnolo V, Marchisio M, Capitani S, Neri LM (1997) Intranuclear translocation of phospholipase C beta2 during HL-60 myeloid differentiation. Biochem Biophys Res Commun 235:831-837
8. Bertagnolo V, Marchisio M, Volinia S, Caramelli E, Capitani S (1998) Nuclear association of tyrosine-phosphorylated Vav to phospholipase C-gamma1 and phosphoinositide 3-kinase during granulocytic differentiation of HL-60 cells. FEBS Lett 441:480-484
9. Bertagnolo V, Neri LM, Marchisio M, Mischiati C, Capitani S (1999) Phosphoinositide 3-kinase activity is essential for all-trans-retinoic acid-induced granulocytic differentiation of HL-60 cells. Cancer Res 59:542-546
10. Bertagnolo V, Brugnoli F, Marchisio M, Celeghini C, Carini C, Capitani S (2004) Association of PI 3-K with tyrosine phosphorylated Vav is essential for its activity in neutrophil-like maturation of myeloid cells. Cell Signal 16:423-433
11. Billi AM, Matteucci A, Faenza I, Manzoli L, Rubbini S, Gilmour RS, Rhee SG, Cocco L (1997) Control of expression of PLCbeta1 by LAC repressor system: relationship between nuclear PLCbeta1 overexpression and growth factor stimulation. Biochem Biophys Res Commun 241:122-126
12. Bootman MD, Thomas D, Tovey SC, Berridge MJ, Lipp P (2000) Nuclear calcium signalling. Cell Mol Life Sci 57:371-378
13. Clarke JH, Letcher AJ, D'Santos CS, Halstead JR, Irvine RF, Divecha N (2001) Inositol lipids are regulated during cell cycle progression in the nuclei of murine erythroleukemia cells. Biochem J 357:905-910
14. Cocco L, Gilmour RS, Ognibene A, Letcher AJ, Manzoli FA, Irvine RF (1987) Synthesis of polyphosphoinositides in nuclei of Friend cells. Evidence for polyphosphoinositide metabolism inside the nucleus which changes with cell differentiation. Biochem J 248:765-770
15. 1 and nuclear lipid-dependent signaling. Biochim Biophys Acta 1761:509-521
16. Crljen V, Visnjic D, Banfic H (2004) Presence of different phospholipase C isoforms in the nucleus and their activation during compensatory liver growth. FEBS Lett 571:35-42
17. 2/M. J Cell Sci 115:983-989
18. Didichenko S, Thelen M (2001) Phosphatidylinositol 3-kinase c2alpha contains a nuclear localization sequence and associates with nuclear speckles. J Biol Chem 276:48135-48142
19. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651-657
20. Divecha N, Banfic H, Irvine RF (1991) The polyphosphoinositide cycle exists in the nuclei of Swiss 3T3 cells under the control of a receptor (for IGF-I) in the plasma membrane, and stimulation of the cycle increases nuclear diacylglycerol and apparently induces translocation of protein kinase C to the nucleus. EMBO J 10:3207-3214
21. Divecha N, Rhee SG, Letcher AJ, Irvine RF (1993) Phosphoinositide signalling enzymes in rat liver nuclei: phosphoinositidase C isoform beta1 is specifically, but not predominantly, located in the nucleus. Biochem J 289:617-620
22. Divecha N, Banfic H, Irvine RF (1993) Inositides and the nucleus and inositides in the nucleus. Cell 74:405-407
23. Divecha N, Roefs M, Los A, Halstead J, Bannister A, D'Santos C (2002) Type I PIPkinases interact with and are regulated by the retinoblastoma susceptibility gene product-pRb. Curr Biol 12:582-587
24. Engelman JA, Luo J, Cantley LC (2006) The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7:606-619
25. Faenza I, Matteucci A, Manzoli L, Billi AM, Aluigi M, Peruzzi D, Vitale M, Castorina S, Suh PG, Cocco L (2000) A role for nuclear phospholipase Cbeta 1 in cell cycle control. J Biol Chem 275:30520-30524
26. Faenza I, Bavelloni A, Fiume R, Lattanzi G, Maraldi NM, Gilmour RS, Martelli AM, Suh PG, Billi AM, Cocco L (2003) Up-regulation of nuclear PLCbeta1 in myogenic differentiation. J Cell Physiol 195:446-452
27. Fiume R, Faenza I, Matteucci A, Astolfi A, Vitale M, Martelli AM, Cocco L (2005) Nuclear phospholipase C beta1 (PLCbeta1) affects CD24 expression in murine erythroleukemia cells. J Biol Chem 280:24221-24226
28. Gonzales ML, Anderson RA (2006) Nuclear phosphoinositide kinases and inositol phospholipids. J Cell Biochem 97:252-260
29. Goss VL, Hocevar BA, Thompson LJ, Stratton CA, Burns DJ, Fields AP (1994) Identification of nuclear beta II protein kinase C as a mitotic lamin kinase. J Biol Chem 269:19074-19080
30. 32 into phosphoinositides of pancreas slices. J Biol Chem 203:967-977
31. Hu Y, Yao J, Liu Z, Liu X, Fu H, Ye K (2005) Akt phosphorylates acinus and inhibits its proteolytic cleavage, preventing chromatin condensation. EMBO J 24:3543-3554
32. Hunt AN (2006) Dynamic lipidomics of the nucleus. J Cell Biochem 97:244-251
33. Irvine RF (2003) Nuclear lipid signalling. Nat Rev Mol Cell Biol 4:349-360
34. Irvine RF (2006) Nuclear inositide signalling-expansion, structures and clarification. Biochim Biophys Acta 1761:505-508
35. Jones DR, Divecha N (2004) Linking lipids to chromatin. Curr Opin Genet Dev 14:196-202
36. Larman MG, Saunders CM, Carrol J, Lai FA, Swann K (2004) Cell cycle-dependent Ca2+ oscillations in mouse embryos are regulated by nuclear targeting of PLCzeta. J Cell Sci 117:2513-2521
37. Lin H, Choi JH, Hasek J, DeLillo N, Lou W, Vancura A (2000) Phospholipase C is involved in kinetochore function in Saccharomyces cerevisiae. Mol Cell Biol 20:3597-3607
38. Los A, Vinke FP, de Widt J, Topham MK, van Blitterswijk WJ, Divecha N (2006) The retinoblastoma family proteins bind to and activate diacylglycerol kinase ζ. J Biol Chem 281:858-866
39. Lu PJ, Hsu AL, Wang DS, Yan HY, Yin HL, Chen CS (1998) Phosphoinositide 3-kinase in rat liver nuclei. Biochemistry 37:5738-5745
40. 1 phase in nocodazole-synchronized HL-60 cells. Biochim Biophys Acta 1733:148-156
41. Lukinovic-Skudar V, Visnjic D, Crljen-Manestar V, Matkovic K, Banfic H (2006) Role of nuclear phospholipase C in regulation of cell cycle. Period Biol 108:571-580
42. 1 phase of the cell cycle. Biochim Biophys Acta 1771:514-521
43. Macbeth MR, Schubert HL, Vandemark AP, Lingam AT, Hill CP, Bass BL (2005) Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing. Science 309:1534-1539
44. Manzoli L, Billi AM, Rubbini S, Bavelloni A, Faenza I, Gilmour RS, Rhee SG, Cocco L (1997) Essential role for nuclear phospholipase C beta1 in insulin-like growth factor I-induced mitogenesis. Cancer Res 57:2137-2139
45. Marchisio M, Bertagnolo V, Colamussi ML, Capitani S, Neri LM (1998) Phosphatidylinositol 3-kinase in HL-60 nuclei is bound to the nuclear matrix and increases during granulocytic differentiation. Biochem Biophys Res Commun 253:346-351
46. Martelli AM, Gilmour RS, Bertagnolo V, Neri LM, Manzoli L, Cocco L (1992) Nuclear localization and signalling activity of phosphoinositidase C beta in Swiss 3T3 cells. Nature 358:242-245
47. Martelli AM, Cocco L, Bareggi R, Tabellini G, Rizzoli R, Ghibellini MD, Narducci P (1999) Insulin-like growth factor-1-dependent stimulation of nuclear phospholipase C-β1 activity in Swiss 3T3 cells requires an intact cytoskeleton and is paralleled by increased phosphorylation of the phospholipase. J Cell Biochem 72:339-348
48. Martelli AM, Billi AM, Manzoli L, Faenza I, Aluigi M, Falconi M, De Pol A, Gilmour RS, Cocco L (2000) Insulin selectively stimulates nuclear phosphoinositide-specific phospholipase C (PI-PLC) beta1 activity through a mitogen-activated protein (MAP) kinase-dependent serine phosphorylation. FEBS Lett 486:230-236
49. Martelli AM, Manzoli L, Cocco L (2004) Nuclear inositides: facts and perspectives. Pharmacol Ther 101:47-64
50. Martelli AM, Evangelisti C, Nyakern M, Manzoli FA (2006) Nuclear protein kinase C. Biochim Biophys Acta 1761:542-551
51. Martelli AM, Faenza I, Billi AM, Manzoli L, Evangelisti C, Fala F, Cocco L (2006) Intranuclear 3′-phosphoinositide metabolism and Akt signaling: new mechanisms for tumorigenesis and protection against apoptosis? Cell Signal 18:1101-1107
52. Matkovic K, Brugnoli F, Bertagnolo V, Banfic H, Visnjic D (2006) The role of the nuclear Akt activation and Akt inhibitors in all-trans-retinoic acid-differentiated HL-60 cells. Leukemia 20:941-951
53. Neri LM, Ricci D, Carini C, Marchisio M, Capitani S, Bertagnolo V (1997) Changes of nuclear PI-PLC gamma1 during rat liver regeneration. Cell Signal 9:353-362
54. Neri LM, Marchisio M, Colamussi ML, Bertagnolo V (1999) Monocytic differentiation of HL-60 cells is characterized by the nuclear translocation of phosphatidylinositol 3-kinase and of definite phosphatidylinositol-specific phospholipase C isoforms. Biochem Biophys Res Commun 259:314-320
55. Neri LM, Martelli AM, Borgatti P, Colamussi ML, Marchisio M, Capitani S (1999) Increase in nuclear phosphatidylinositol 3-kinase activity and phosphatidylinositol (3,4,5) trisphosphate synthesis precede PKC-zeta translocation to the nucleus of NGF-treated PC12 cells. FASEB J 13:2299-2310
56. Neri LM, Bortul R, Borgatti P, Tabellini G, Baldini G, Capitani S, Martelli AM (2002) Proliferating or differentiating stimuli act on different lipid-dependent signaling pathways in nuclei of human leukemia cells. Mol Biol Cell 13:947-964
57. Odom AR, Stahlberg A, Wente SR, York JD (2000) A role for nuclear inositol 1,4,5-triphosphate kinase in transcriptional control. Science 287:2026-2029
58. Okada M, Fujii M, Yamaga M, Sugimoto H, Sadano H, Osumi T, Kamata H, Hirata H, Yagisawa H (2002) Carboxyl-terminal basic amino acids in the X domain are essential for the nuclear import of phospholipase C delta 1. Genes Cells 7:985-996
59. Okada M, Ishimoto T, Naito Y, Hirata H, Yagisawa H (2005) Phospholipase C delta (1) associates with importin beta1 and translocates into the nucleus in a Ca2+-dependent manner. FEBS Lett 579:4949-4954
60. Osborne SL, Thomas CL, Gschmeissner S, Schiavo G (2001) Nuclear PtdIns(4,5)P2 assembles in a mitotically regulated particle involved in pre-mRNA splicing. J Cell Sci 114:2501-2511
61. Rhee SG (2001) Regulation of phosphoinositide-specific phospholipase C. Annu Rev Biochem 70:281-312
62. Rose HG, Frenster JH (1965) Composition and metabolism of lipids within repressed and active chromatin of interphase lymphocytes. Biochim Biophys Acta 106:577-591
63. Sindic A, Aleksandrova A, Fields AP, Volinia S, Banfic H (2001) Presence and activation of nuclear phosphoinositide 3-kinase C2beta during compensatory liver growth. J Biol Chem 276:17754-17761
64. Sindic A, Crljen V, Matkovic K, Lukinovic-Skudar V, Visnjic D, Banfic H (2006) Activation of phosphoinositide 3-kinase C2 beta in the nuclear matrix during compensatory liver growth. Adv Enzyme Regul 46:280-287
65. Smith CD, Wells WW (1983) Phosphorylation of rat liver nuclear envelopes. II. Characterization of in vitro lipid phosphorylation. J Biol Chem 258:59368-59373
66. Smith MR, Liu YL, Matthews NT, Rhee SG, Sung WK, Kung HF (1994) Phospholipase C-gamma 1 can induce DNA synthesis by a mechanism independent of its lipase activity. Proc Natl Acad Sci USA 91:6554-6558
67. Stallings JD, Tall EG, Pentyala S, Rebecchi MJ (2005) Nuclear translocation of phospholipase C-delta1 is linked to the cell cycle and nuclear phosphatidylinositol 4,5-bisphosphate. J Biol Chem 280:22060-22069
68. Sun B, Murray NR, Fields AP (1997) A role for nuclear phosphatidylinositol-specific phospholipase C in the G2/M phase transition. J Biol Chem 272:26313-26317
69. Swann K, Saunders CM, Rogers NT, Lai FA (2006) PLCzeta: a sperm protein that triggers Ca2+ oscillations and egg activation in mammals. Semin Cell Dev Biol 17:264-273
70. Tanaka K, Horiguchi K, Yoshida T, Takeda M, Fujisawa H, Takeuchi K, Umeda M, Kato S, Ihara S, Nagata S, Fukui Y (1999) Evidence that a phosphatidylinositol 3,4,5-triphosphate-binding protein can function in nucleus. J Biol Chem 274:3919-3922
71. 2/M phase transition of cell cycle. J Biol Chem 271:15045-15053
72. Toker A (2002) Phosphoinositides and signal transduction. Cell Mol Life Sci 59:761-779
73. Visnjic D, Crljen V, Curic J, Batinic D, Volinia S, Banfic H (2002) The activation of nuclear phosphoinositide 3-kinase C2beta in all-trans-retinoic acid-differentiated HL-60 cells. FEBS Lett 529:268-274
74. Visnjic D, Curic J, Crljen V, Batinic D, Volinia S, Banfic H (2003) Nuclear phosphoinositide 3-kinase C2beta activation during G2/M phase of the cell cycle in HL-60 cells. Biochim Biophys Acta 1631:61-71
75. Vitale M, Matteucci A, Manzoli L, Rodella L, Mariani AR, Zauli G, Falconi M, Billi AM, Martelli AM, Gilmour RS, Cocco L (2001) Interleukin 2 activates nuclear phospholipase C beta by mitogen-activated protein kinase-dependent phosphorylation in human natural killer cells. FASEB J 15:1789-1791
76. Watt SA, Kular G, Fleming IN, Downes CP, Lucocq JM (2002) Subcellular localization of phosphatidylinositol 4,5-bisphosphate using the pleckstrin homology domain of phospholipase C delta1. Biochem J 363:657-666
77. Xu A, Suh PG, Marmy-Conus N, Pearson RB, Seok OY, Cocco L, Gilmour RS (2001) Phosphorylation of nuclear phospholipase C beta1 by extracellular signal-regulated kinase mediates the mitogenic action of insulin-like growth factor I. Mol Cell Biol 21:2981-2990
78. Xu A, Wang Y, Xu LY, Gilmour RS (2001) Protein kinase C alpha-mediated negative feedback regulation is responsible for the termination of insulin-like growth factor I-induced activation of nuclear phospholipase C beta1 in Swiss 3T3 cells. J Biol Chem 276:14980-14986
79. Yagisawa H, Okada M, Naito Y, Sasaki K, Yamaga M, Fujii M (2006) Coordinated intracellular translocation of phosphoinositide-specific phospholipase C-δ with the cell cycle. Biochim Biophys Acta 1761:522-534
80. Yamaga M, Fujii M, Kamata H, Hirata H, Yagisawa H (1999) Phospholipase C-delta1 contains a functional nuclear export signal sequence. J Biol Chem 274:28537-28541
81. Ye K, Hurt KJ, Wu FY, Fang M, Luo HR, Hong JJ, Blackshaw S, Ferris CD, Snyder SH (2000) Pike. A Nuclear GTPase that enhances PI3Kinase activity and is regulated by protein 4.1N. Cell 103:919-930
82. Ye K, Aghdasi B, Luo HR, Moriarity JL, Wu FY, Hong JJ, Hurt KJ, Bae SS, Suh PG, Snyder SH (2002) Phospholipase C gamma 1 is a physiological guanine nucleotide exchange factor for the nuclear GTPase PIKE. Nature 415:541-544
83. York JD, Odom AR, Murphy R, Ives EB, Wente SR (1999) A phospholipase C- dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science 285:96-100
84. York JD (2006) Regulation of nuclear processes by inositol polyphosphates. Biochim Biophys Acta 1761:552-559
85. York SJ, Armbruster BN, Greenwell P, Petes TD, York JD (2005) Inositol diphosphate signaling regulates telomere length. J Biol Chem 280:4264-4269