Lamin A Ser404 Is a nuclear target of akt phosphorylation in C2C12 cells

Journal of Proteome Research

Volumn 7, Issue 11, 2008, Pages 4727-4735

  Cenni, Vittoria ^a,b   Bertacchini, Jessika ^a   Beretti, Francesca ^a   Lattanzi, Giovanna ^b   Bavelloni, Alberto ^c   Riccio, Massimo ^a   Ruzzene, Maria ^d   Marin, Orlano ^d   Arrigoni, Giorgio ^d   Parnaik, Veena ^f   Wehnert, Manfred ^g   Maraldi, Nadir M ^b,c   De Pol, Anto ^a   Cocco, Lucio ^e   Marmiroli, Sandra ^a,b  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b CNR   (Italy)

^c RIZZOLI ORTHOPAEDIC INSTITUTE   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

^e CENTRE FOR CELLULAR AND MOLECULAR BIOLOGY   (India)

^f Institute of Human Genetics   (Germany)

^g Cellular Signalling Laboratory   (Italy)

Author keywords

2D electrophoresis; Akt pkb; Lamin A C; Nucleus; Phosphorylation; Proteomics

Indexed keywords

INSULIN; LAMIN A; LAMIN C; PHOSPHOPEPTIDE; PROTEIN KINASE B; SERINE; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMERY DREIFUSS MUSCULAR DYSTROPHY; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MOUSE; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; ANIMAL; CELL LINE; CELL NUCLEUS; CYTOLOGY; GENETIC TRANSFECTION; GENETICS; KIDNEY; METABOLISM; METHODOLOGY; MYOBLAST; PHOSPHORYLATION; PROTEOMICS;

ANIMALS; CELL LINE; CELL NUCLEUS; HUMANS; KIDNEY; LAMIN TYPE A; MICE; MYOBLASTS; PHOSPHORYLATION; PROTEOMICS; PROTO-ONCOGENE PROTEINS C-AKT; RECOMBINANT PROTEINS; SERINE; TRANSFECTION;

EID: 58149389535     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr800262g     Document Type: Article

References (59)

1. Bellacosa, A.; Testa, J. R.; Staal, S. P.; Tsichlis, P. N. A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science 1991, 254, 274-277.
2. Staal, G. E.; Kalff, A.; Heesbeen, E. C; van Veelen, C. W.; Rijksen, G. Subunit composition, regulatory properties, and phosphorylation of phosphofructokinase from human gliomas. Cancer Res. 1987, 47, 5047-5051.
3. Jones, P. R; Jakubowicz, T.; Pitossi, F. J.; Maurer, F.; Hemmings, B. A.) Molecular cloning and identification of a serine/threonine protein kinase of the second-messenger subfamily. Proc. Natl. Acad. Sci. U.SA. 1991, 88, 4171-4175.
4. Franke, T.; Kaplan, R. D.; Cantley, L. C; Toker, A. Direct regulation of the Akt proto-oncogene product by phosphatidylinositol-3,4-bisphosphate. Science 1997, 275, 665-668.
5. Stokoe, D.; Stephens, L. R.; Copeland, T.; Gaffney, P. R. J.; Painter, G. F.; Holmes, A. B.; McCormick, F.; Hawkins, P. T. Dual role of phosphatidylinositol-3,4,5-trisphosphate in the activation of protein kinase B. Science 1997, 277, 567-570.
6. Yang, Z. Z.; Tschopp, O.; Baudry, A.; Dümmler, B.; Hynx, D.; Hemmings, B. A. Physiological functions of protein kinase B/Akt. Biochem. Soc. Trans. 2004, 32, 350-354.
7. Andjelkovic, M.; Alessi, D. R.; Meier, R.; Fernandez, A.; Lamb, N. J.; Freeh, M.; Cron, P.; Cohen, P.; Lucocq, J. M.; Hemmings, B. A. Role of translocation in the activation and function of protein kinase B. J. Biol. Chem. 1997, 272, 31515-31524.
8. Alessi, D. R.; James, S. R.; Downes, C. P.; Holmes, A. B.; Gaffney, P. R.; Reese, C. B.; Cohen, P. Characterization of a 3-phosphoi-nositide-dependent protein kinase which phosphorylates and activates protein kinase Balpha. Curr. Biol. 1997, 7 (4), 261-269.
9. Toker, A.; Newton, A. C. Akt/protein kinase B is regulated by autophosphorylation at the hypothetical PDK-2 site. J. Biol. Chem. 2000, 275, 8271-8274.
10. Persad, S.; Attwell, S.; Gray, V.; Mawji, N.; Deng, J. T.; Leung, D.; Yan, J.; Sanghera, J.; Walsh, M. P.; Dedhar, S. Regulation of protein kinase B/Akt-serine 473 phosphorylation by integrin-linked kinase: critical roles for kinase activity and amino acids arginine 211 and serine 343. J. Biol Chem. 2001, 276, 27462-27469.
11. Feng, J.; Park, J.; Cron, P.; Hess, D.; Hemmings, B. A. Identification of a PKB/Akt hydrophobic motif Ser-473 kinase as DNA-dependent protein kinase. J. Biol. Chem. 2004, 279, 41189-41196.
12. Scheid, M. P.; Marignani, P. A.; Woodgett, J. R. Multiple phos-phoinositide 3-kinase-dependent steps in activation of protein kinase B. Mol. Cell. Biol. 2002, 22, 6247-6260.
13. Sarbassov, D. D.; Guertin, D. A.; Siraj, M. A.; Sabatini, D. M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 2005, 307, 1098-1101.
14. Gao, T.; Furnari, F.; Newton, A. C. PHLPP: a phosphatase that directly dephosphorylates Akt, promotes4 apoptosis, and suppresses tumor growth. Mol. Cell 2005, 18, 13-24.
15. Brognard, J.; Sierecki, E.; Gao, T.; Newton, A. C. PHLPP and a second isoform, PHLPP2, differentially attenuate the amplitude of Akt signaling by regulating distinct Akt isoforms. Mol. Cell 2007, 25, 917-931.
16. Manning, B. D.; Cantley, L. C. AKT/PKB signaling: navigating downstream. Cell 2007, 129, 1261-1274.
17. Martelli, A. M.; Nyakern, M.; Tabellini, G.; Borrul, R.; Tazzari, P. L.; Evangelisti, C; Cocco, L. Phosphoinositide 3-kinase/Akt signaling pathway and its therapeutical implications for human acute myeloid leukemia. Leukemia 2006, 20, 911-928.
18. Kunkel, M. T.; Tsien, R. Y.; Zhang, J.; Newton, A. C. Spatio-temporal dynamics of protein kinase B/Akt signaling revealed by a genetically encoded fluorescent reporter. J. Biol. Chem. 2005, 280, 5581-5587.
19. Zhu, L.; Hu, C; Li, J.; Xue, P.; He, X.; Ge, C; Qin, W.; Yao, G.; Gu, J. Real-time imaging nuclear translocation of Aktl in HCC cells. Biochem. Biophys. Res. Commun. 2007, 356, 1038-1043.
20. Cenni, V.; Sirri, A.; Riccio, M.; Lattanzi, G.; Santi, S.; de Pol, A.; Maraldi, N. M.; Marmiroli, S. Targeting of the Akt/PKB kinase to the actin skeleton. Cell. Mol. Life Sci. 2003, 60, 2710-2720.
21. Laine, J.; Kunstle, G.; Obata, T.; Sha, M.; Noguchi, M. Differential regulation of Akt kinase isoforms by the members of the TCL1 oncogene family. Mol. Cell 2000, 6, 395-407.
22. Brunei, A.; Bonni, A.; Zigmond, M. J.; Lin, M. Z.; Juo, P.; Hu, L. S.; Anderson, M. J.; Arden, K. G; Blenis, J.; Greenberg, M. E. Akt promotes cell survival by phosphorylating and inhibiting a Fork-head transcription factor. Cell 1999, 96, 857-868.
23. Hribal, M. L.; Nakae, J.; Kitamura, T.; Shutter, J. R.; Accili, D. Regulation of insulin-like growth factor-dependent myoblast differentiation by Foxo forkhead transcription factors. J. Cell. Biol. 2003, 162, 535-541.
24. Zhang, H.; Zha, X.; Tan, Y.; Hornbeck, P. V.; Mastrangelo, A. J.; Alessi, D. R.; Polakiewicz, R. D.; Comb, M. J. Phosphoprotein analysis using antibodies broadly reactive against phosphorylated motifs. J. Biol. Chem. 2002, 277, 39379-39387.
25. Manning, B. D.; Tee, A. R.; Logsdon, M. N.; Blenis, J.; Cantley, L. C. Identification of the tuberous sclerosis complex-2 tumor suppressor gene product tuberin as a target of the phosphoinositide 3-kinase/akt pathway. Mol. Cell 2002, 10, 151-162.
26. Konishi, H.; Namikawa, K.; Shikata, K.; Kobatake, Y; Tachibana, T.; Kiyama, H. Identification of peripherin as a Akt substrate in neurons. J. Biol. Chem. 2007, 282, 23491-23499.
27. Hutchison, C. J.; Worman, H. J. A-type lamins: guardians of the soma. Nat. Cell Biol. 2004, 6, 1062-1067.
28. Shumaker, D. K.; Kuczmarski, E. R.; Goldman, R. D. The nucleosk-eleton: lamins and Actin are major players in essential nuclear. Curr. Opin. Cell. Biol. 2003, 15, 358-366.
29. Bridger, J. M.; Foeger, N.; Kill, I. R.; Herrmann, H. The nuclear lamina. Both a structural framework and a platform for genome organization. FEBS J. 2007, 274, 1354-1361.
30. Kumaran, R. I.; Muralikrishna, B.; Parnaik, V. K. Lamin A/C speckles mediate spatial organization of splicing factor compartments and RNA polymerase II transcription. J. Cell Biol. 2002, 159, 783-793.
31. Vojtek, A. B.; Taylor, J.; DeRuiter, S. L.; Yu, J. Y.; Figueroa, C; Kwok, R. P.; Turner, D. L. Akt regulates basic helix-loop-helix transcription factor-coactivator complex formation and activity during neuronal differentiation. Mol. Cell. Biol. 2003, 23, 4417-4427.
32. Cenni, V.; Sirri, A.; De Pol, A.; Maraldi, N. M.; Marmiroli, S. Interleukin-1-receptor-associated kinase 2 (IRAK2)-mediated in-terleukin-1- dependent nuclear factor kappaB transactivation in Saos2 cells requires the Akt/protein kinase B kinase. Biochem. J. 2003, 376, 303-311.
33. Cenni, V.; Sabatelli, P.; Mattioli, E.; Marmiroli, S.; Capanni, C; Ognibene, A.; Squarzoni, S.; Maraldi, N. M.; Bonne, G.; Columbaro, M.; Merlini, L.; Lattanzi, G. J. Lamin A N-terminal phosphorylation is associated with myoblast activation: impairment in Emery-Dreifuss muscular dystrophy. J. Med. Genet. 2005, 42, 214-220.
34. Barati, M. T.; Rane, M. J.; Klein, I. B.; McLeish, K. R. A proteomic screen identified stress-induced chaperone proteins as targets of Akt phosphorylation in mesangial cells. J. Proteome Res. 2006, 5, 1636-1646.
35. Vandermoere, F.; El Yazidi-Belkoura, I.; Demont, Y.; Slomianny, C; Antol, J.; Lemoine, J.; Hondermarck, H. Proteomics exploration reveals that Actin is a signaling target of the kinase Akt. Mol. Cell. Proteomics 2007, 6, 114-124.
36. Wilson, E. M.; Rotwein, P. Selective control of skeletal muscle differentiation by AktI. J. Biol. Chem. 2007, 282, 5106-5110.
37. Muchir, A.; Worman, H. J. Emery-Dreifuss muscular dystrophy. Curr. Neurol. Neurosci. Rep. 2007, 7, 78-83.
38. Gruenbaum, Y.; Margalit, A.; Goldman, R. D.; Shumaker, D. K.; Wilson, K. L. The nuclear lamina comes of age. Nat. Rev. Mol. Cell. Biol. 2005, 6, 21-31.
39. Bonne, G.; Di Barletta, M. R.; Varnous, S.; Becane, H. M.; Han-nouda, E. H.; Merlini, L.; Muntoni, F.; Greenberg, C. R.; Gary, F.; Urtizberea, J. A. Mutations in the gene encoding lamin A/C cause autosomal dominant Emery-Dreifuss muscular dystrophy. Nat. Genet. 1999, 21, 285-288.
40. Lee, K. K.; Gruenbaum, Y.; Spann, P.; Liu, J.; Wilson, K. L. C. elegans nuclear envelope proteins emerin, MAN1, lamin, and nucleoporins reveal unique timing of nuclear envelope breakdown during mitosis. Mol. Biol. Cell 2000, 11, 3089-3099.
41. Buendia, B.; Courvalin, J. C; Collas, P. Dynamics of the nuclear envelope at mitosis and during apoptosis. Cell. Mol. Life Sci. 2001, 58, 1781-1789.
42. Friedman, D,L.; Ken, R. Insulin stimulates incorporation of 32Pi into nuclear lamins A and C in quiescent BHK-21 cells. J. Biol. Chem. 1988, 263, 1103-1106.
43. Martelli, A. M.; Bortul, R.; Tabellini, G.; Faenza, I.; Cappellini, A.; Bareggi, R.; Manzoli, L.; Cocco, L. Molecular characterization of protein kinase C-alpha binding to lamin A. J. Cell Biochem. 2002, 86, 320-330.
44. Muranyi, W.; Haas, J.; Wagner, M.; Krohne, G.; Koszinowski, U. H. Cytomegalovirus recruitment of cellular kinases to dissolve the nuclear lamina. Science 2002, 297, 854-857.
45. Lawlor, M. A.; Rotwein, P. Insulin-like growth factor-mediated muscle cell survival: central roles for Akt and cyclin-dependent kinase inhibitor p21. Mol. Cell. Biol. 2000, 20, 8983-8995.
46. Wilson, E. M.; Tureckova, J.; Rotwein, P. Permissive roles of phosphatidyl inositol 3-kinase and Akt in skeletal myocyte maturation. Mol. Biol. Cell 2004, 15, 497-505.
47. Xu, Q.; Wu, Z. The insulin-like growth factor-phosphatidylinositol 3-kinase-Akt signaling pathway regulates myogenin expression in normal myogenic cells but not in rhabdomyosarcoma-derived RD cells. J. Biol. Chem. 2000, 275, 36750-36757.
48. Jiang, B. H.; Aoki, M.; Zheng, J. Z.; Li, J.; Vogt, P. K. Myogenic signaling of phosphatidylinositol 3-kinase requires the serine-threonine kinase Akt/protein kinase B. Proc. Natl. Acad. Sci. U.SA. 1999, 96, 2077-2081.
49. Rommel, C; Bodine, S. C; Clarke, B. A.; Rossman, R.; Nunez, L.; Stitt, T. N.; Yancopoulos, G. D.; Glass, D. J. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI(3)K/Akt/mTOR and PI(3)K/Akt/GSK3 pathways. Nat. Cell Biol. 2001, 3, 1009-1013.
50. Takahashi, A.; Kureishi, Y.; Yang, J.; Luo, Z.; Guo, K.; Mukho-padhyay, D.; Ivashchenko, Y.; Branellec, D.; Walsh, K. Myogenic Akt signaling regulates blood vessel recruitment during myofiber growth. Mol. Cell. Biol. 2002, 22, 4803-4814.
51. Tamir, Y.; Bengal, E. Phosphoinositide 3-kinase induces the transcriptional activity of MEF2 proteins during muscle differentiation. J. Biol. Chem. 2000, 275, 34424-34432.
52. Maraldi, N. M.; Lattanzi, G. Involvement of prelamin A in lami-nopathies. Crit. Rev. Eukaryotic Gene Expression 2007, 317, 17-34.
53. Maraldi, N. M.; Squarzoni, S.; Sabatelli, P.; Capanni, C; Mattioli, E.; Ognibene, A.; Lattanzi, G. Laminopathies: involvement of structural nuclear proteins in the pathogenesis of an increasing number of human diseases. J. Cell Physiol. 2005, 203, 319-327.
54. Yaffe, M. B. How do 14-3-3 proteins work? Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 2002, 513, 53-57.
55. Aitken, A. 14-3-3 proteins: a historic overview. Semin. Cancer Biol. 2006, 16, 162-172.
56. Bridges, D.; Moorhead, G. B. 14-3-3 Proteins: a number of functions for a numbered protein. Sci. STKE 2005, 296, re10.
57. Meek, S. E.; Lane, W. S.; Piwnica-Worms, H. M. Comprehensive proteomic analysis of interphase and mitotic 14-3-3-binding proteins. J. Biol. Chem. 2004, 279, 32046-32054.
58. Leukel, M.; Jost, E. Two conserved serines in the nuclear localization signal flanking region are involved in the nuclear targeting of human lamin A. Eur. J. Cell. Biol. 1995, 68, 133-142.
59. Capanni, C; Mattioli, E.; Columbaro, M.; Lucarelli, E.; Parnaik, V. K.; Novelli, G.; Wehnert, M.; Cenni, V.; Maraldi, N. M.; Squarzoni, S.; Lattanzi, G. Altered pre-lamin A processing is a common mechanism leading to lipodystrophy. Hum. Mol. Genet. 2005, 14, 1489-1502.