Pyk2 cytonuclear localization: Mechanisms and regulation by serine dephosphorylation

Cellular and Molecular Life Sciences

Volumn 70, Issue 1, 2013, Pages 137-152

  Faure, Camille ^a,b   Ramos, Mariana ^a,b   Girault, Jean Antoine ^a,b  

^a INSTITUT DU FER À MOULIN   (France)

^b SORBONNE UNIVERSITÉ   (France)

Author keywords

Calcineurin; Cytonuclear localization; Non receptor tyrosine kinase; Nucleus; Phosphorylation; Protein phosphatase

Indexed keywords

CALCINEURIN; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; FOCAL ADHESION KINASE 2; ISOPROTEIN; SERINE;

AMINO TERMINAL SEQUENCE; ARTICLE; AUTOPHOSPHORYLATION; BIOACCUMULATION; CELL MEMBRANE DEPOLARIZATION; CELL MIGRATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EVOLUTIONARY ADAPTATION; INTRACELLULAR SIGNALING; NERVE CELL; NUCLEAR EXPORT SIGNAL; NUCLEAR IMPORT; NUCLEAR LOCALIZATION SIGNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; REGULATORY MECHANISM;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID MOTIFS; ANIMALS; CALCINEURIN; CELL NUCLEUS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FOCAL ADHESION KINASE 2; GREEN FLUORESCENT PROTEINS; NUCLEAR EXPORT SIGNALS; NUCLEAR LOCALIZATION SIGNALS; PC12 CELLS; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN SPLICING; PROTEIN TRANSPORT; RATS; RECOMBINANT FUSION PROTEINS; SERINE;

EID: 84872334473     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-012-1075-5     Document Type: Article

References (55)

1. Lev S et al (1995) Protein tyrosine kinase Pyk2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 376(6543):737-745
2. Salter MW, Kalia LV (2004) Src kinases: a hub for NMDA receptor regulation. Nat Rev Neurosci 5(4):317-328
3. Girault JA et al (1999) FAK and PYK2/CAK in the nervous system, a link between neuronal activity, plasticity and survival? Trends Neurosci 22:257-263
4. Hsin H et al (2010) Proline-rich tyrosine kinase 2 regulates hippocampal long-term depression. J Neurosci 30(36):11983-11993
5. Bartos JA et al (2010) Postsynaptic clustering and activation of Pyk2 by PSD-95. J Neurosci 30(2):449-463
6. Huang Y et al (2001) CAKbeta/Pyk2 kinase is a signaling link for induction of long-term potentiation in CA1 hippocampus. Neuron 29(2):485-496
7. Gil-Henn H et al (2007) Defective microtubule-dependent podosome organization in osteoclasts leads to increased bone density in Pyk2(-/-) mice. J Cell Biol 178(6):1053-1064
8. Okigaki M et al (2003) Pyk2 regulates multiple signaling events crucial for macrophage morphology and migration. Proc Natl Acad Sci USA 100(19):10740-10745
9. Hashido M et al (2006) Ca2+ lightning conveys cell-cell contact information inside the cells. EMBO Rep 7(11):1117-1123
10. Dikic I, Schlessinger J (1998) Identification of a new Pyk2 isoform implicated in chemokine and antigen receptor signaling. J Biol Chem 273(23):14301-14308
11. Li X et al (1998) A calcium-dependent tyrosine kinase splice variant in human monocytes. Activation by a two-stage process involving adherence and a subsequent intracellular signal. J Biol Chem 273:9361-9364
12. Xiong WC, Macklem M, Parsons JT (1998) Expression and characterization of splice variants of PYK2, a focal adhesion kinase-related protein. J Cell Sci 111(Pt 14):1981-1991
13. Kohno T et al (2008) Protein-tyrosine kinase CAKbeta/PYK2 is activated by binding Ca2+/calmodulin to FERM F2 alpha2 helix and thus forming its dimer. Biochem J 410(3):513-523
14. Park SY, Avraham HK, Avraham S (2004) RAFTK/Pyk2 activation is mediated by trans-acting autophosphorylation in a Src-independent manner. J Biol Chem 279(32):33315-33322
15. Avraham H et al (2000) RAFTK/Pyk2-mediated cellular signalling. Cell Signal 12(3):123-133
16. Schaller MD, Sasaki T (1997) Differential signaling by the focal adhesion kinase and cell adhesion kinase beta. J Biol Chem 272(40):25319-25325
17. Zheng C et al (1998) Differential regulation of Pyk2 and focal adhesion kinase (FAK). The C-terminal domain of FAK confers response to cell adhesion. J Biol Chem 273(4):2384-2389
18. Corvol JC et al (2005) Depolarization activates ERK and proline-rich tyrosine kinase 2 (PYK2) independently in different cellular compartments in hippocampal slices. J Biol Chem 280(1):660-668
19. Menegon A et al (1999) FAK+ and PYK2/CAKbeta, two related tyrosine kinases highly expressed in the central nervous system: similarities and differences in the expression pattern. Eur J Neurosci 11(11):3777-3788
20. Faure C et al (2007) Calcineurin is essential for depolarization-induced nuclear translocation and tyrosine phosphorylation of PYK2 in neurons. J Cell Sci 120(Pt 17):3034-3044
21. Aoto H et al (2002) Nuclear translocation of cell adhesion kinase beta/proline-rich tyrosine kinase 2. Cell Struct Funct 27(1):47-61
22. Arcucci A, Montagnani S, Gionti E (2006) Expression and intracellular localization of Pyk2 in normal and v-src transformed chicken epiphyseal chondrocytes. Biochimie 88(1):77-84
23. Lim ST et al (2008) Nuclear FAK promotes cell proliferation and survival through FERM-enhanced p53 degradation. Mol Cell 29(1):9-22
24. Schindler EM et al (2007) The role of proline-rich protein tyrosine kinase 2 in differentiation-dependent signaling in human epidermal keratinocytes. J Invest Dermatol 127(5):1094-1106
25. Sun L et al (2004) Role of the Pyk2-MAP kinase-cPLA2 signaling pathway in shear-dependent platelet aggregation. Ann Biomed Eng 32(9):1193-1201
26. Ding L, Guo D, Homandberg GA (2009) Fibronectin fragments mediate matrix metalloproteinase upregulation and cartilage damage through proline rich tyrosine kinase 2, c-src, NF-kappaB and protein kinase Cdelta. Osteoarthr Cartil 17(10):1385-1392
27. Farshori PQ et al (2003) Activation and nuclear translocation of PKCdelta, Pyk2 and ERK1/2 by gonadotropin releasing hormone in HEK293 cells. J Steroid Biochem Mol Biol 85(2-5):337-347
28. Gorlich D, Mattaj IW (1996) Nucleocytoplasmic transport. Science 271(5255):1513-1518
29. Stewart M (2007) Molecular mechanism of the nuclear protein import cycle. Nat Rev Mol Cell Biol 8(3):195-208
30. Yoneda Y (2000) Nucleocytoplasmic protein traffic and its significance to cell function. Genes Cells 5(10):777-787
31. Kutay U, Guttinger S (2005) Leucine-rich nuclear-export signals: born to be weak. Trends Cell Biol 15(3):121-124
32. Pemberton LF, Paschal BM (2005) Mechanisms of receptor-mediated nuclear import and nuclear export. Traffic 6(3):187-198
33. Siciliano JC et al (1996) Differential regulation of proline-rich tyrosine kinase 2/cell adhesion kinase beta (PYK2/CAKbeta) and pp 125(FAK) by glutamate and depolarization in rat hippocampus. J Biol Chem 271(46):28942-28946
34. Smith AG et al (1993) Enhancement by iron of hepatic neoplasia in rats caused by hexachlorobenzene. Carcinogenesis 14(7):1381-1387
35. Lim ST et al (2010) Pyk2 inhibition of p53 as an adaptive and intrinsic mechanism facilitating cell proliferation and survival. J Biol Chem 285(3):1743-1753
36. Hoelz A, Debler EW, Blobel G (2011) The structure of the nuclear pore complex. Annu Rev Biochem 80:613-643
37. Chuderland D, Konson A, Seger R (2008) Identification and characterization of a general nuclear translocation signal in signaling proteins. Mol Cell 31(6):850-861
38. Tang X et al (2010) Phosphorylation of the RNase III enzyme Drosha at Serine300 or Serine302 is required for its nuclear localization. Nucleic Acids Res 38(19):6610-6619
39. Fornerod M et al (1997) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90(6):1051-1060
40. Ossareh-Nazari B, Bachelerie F, Dargemont C (1997) Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science 278(5335):141-144
41. la Cour T et al (2004) Analysis and prediction of leucine-rich nuclear export signals. Protein Eng Des Sel 17(6):527-536
42. Poon IK, Jans DA (2005) Regulation of nuclear transport: central role in development and transformation? Traffic 6(3):173-186
43. Nardozzi JD, Lott K, Cingolani G (2010) Phosphorylation meets nuclear import: a review. Cell Commun Signal 8:32
44. Kennelly PJ, Krebs EG (1991) Consensus sequences as substrate specificity determinants for protein kinases and protein phosphatases. J Biol Chem 266(24):15555-15558
45. Hemmings HC Jr et al (1984) DARPP-32, a dopamine- and adenosine 3′:5′-monophosphate- regulated neuronal phosphoprotein. I. Amino acid sequence around the phosphorylated threonine. J Biol Chem 259:14486-14490
46. King MM et al (1984) Mammalian brain phosphoproteins as substrates for calcineurin. J Biol Chem 259:8080-8083
47. Wissing J et al (2007) Proteomics analysis of protein kinases by target class-selective prefractionation and tandem mass spectrometry. Mol Cell Proteomics 6(3):537-547
48. Oppermann FS et al (2009) Large-scale proteomics analysis of the human kinome. Mol Cell Proteomics 8(7):1751-1764
49. Gervasi N et al (2007) Dynamics of protein kinase A signaling at the membrane, in the cytosol, and in the nucleus of neurons in mouse brain slices. J Neurosci 27(11):2744-2750
50. Crabtree GR (1999) Generic signals and specific outcomes: signaling through Ca2+, calcineurin, and NF-AT. Cell 96(5):611-614
51. Cook PJ et al (2009) Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 458(7238):591-596
52. Singh RK, Gunjan A (2011) Histone tyrosine phosphorylation comes of age. Epigenetics 6(2):153-160
53. Takahashi A et al (2009) Nuclear localization of Src-family tyrosine kinases is required for growth factor-induced euchromatinization. Exp Cell Res 315(7):1117-1141
54. Jain AK, Jaiswal AK (2006) Phosphorylation of tyrosine 568 controls nuclear export of Nrf2. J Biol Chem 281(17):12132-12142
55. Jain AK, Jaiswal AK (2007) GSK-3beta acts upstream of Fyn kinase in regulation of nuclear export and degradation of NF-E2 related factor 2. J Biol Chem 282(22):16502-16510