Rac1/p21-activated kinase pathway controls retinoblastoma protein phosphorylation and E2F transcription factor activation in B lymphocytes

FEBS Journal

Volumn 283, Issue 4, 2016, Pages 647-661

  Zaldua, Natalia ^a,b   Llavero, Francisco ^c,d   Artaso, Alain ^c   Gálvez, Patricia ^e   Lacerda, Hadriano M ^f   Parada, Luis A ^g   Zugaza, José L ^c,d,h  

^a CIC BIOGUNE   (Spain)

^b Idem Biotechnology SL   (Spain)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^d ACHUCARRO BASQUE CENTER FOR NEUROSCIENCE   (Spain)

^e Technological Park of Health Sciences   (Spain)

^f Three R Labs   (Spain)

^g UNIVERSIDAD NACIONAL DE SALTA   (Argentina)

^h BASQUE FOUNDATION FOR SCIENCE   (Spain)

Author keywords

E2F; p21 activated kinase; Rac1; retinoblastoma protein; Vav

Indexed keywords

B LYMPHOCYTE RECEPTOR; CELL PROTEIN; P21 ACTIVATED KINASE 1; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPASE; PHOSPHOLIPASE CC2; PROTEIN CDC42; PROTEIN KINASE C; PROTEIN P21; RAC1 PROTEIN; RAS PROTEIN; RETINOBLASTOMA PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSCRIPTION FACTOR E2F; UNCLASSIFIED DRUG; VAV3 PROTEIN; P21 ACTIVATED KINASE;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; CELL PROLIFERATION; COMPLEX FORMATION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; IMMORTALIZED CELL LINE; INTRACELLULAR SIGNALING; LYMPHOCYTE PROLIFERATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; TRANSCRIPTION INITIATION; UPREGULATION; ANIMAL; CELL LINE; CHICKEN; CYTOLOGY; METABOLISM; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; B-LYMPHOCYTES; CELL LINE; CELL PROLIFERATION; CHICKENS; E2F TRANSCRIPTION FACTORS; P21-ACTIVATED KINASES; PHOSPHORYLATION; RAC1 GTP-BINDING PROTEIN; RETINOBLASTOMA PROTEIN; SIGNAL TRANSDUCTION;

EID: 84958871158     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13617     Document Type: Article

References (52)

1. Hobeika E, Nielsen PJ, &, Medgyesi D, (2015) Signaling mechanisms regulating B-lymphocyte activation and tolerance. J Mol Med (Berl) 93, 143-158.
2. Caloca MJ, Zugaza JL, Matallanas D, Crespo P, &, Bustelo XR, (2003) Vav mediates Ras stimulation by direct activation of the GDP/GTP exchange factor Ras GRP1. EMBO J 22, 3326-3336.
3. Zugaza JL, Caloca MJ, &, Bustelo XR, (2004) Inverted signaling hierarchy between RAS and RAC in T-lymphocytes. Oncogene 23, 5823-5833.
4. Arrizabalaga O, Lacerda HM, Zubiaga AM, &, Zugaza JL, (2012) Rac1 protein regulates glycogen phosphorylase activation and controls interleukin (IL)-2-dependent T cell proliferation. J Biol Chem 287, 11878-11890.
5. Llavero F, Urzelai B, Osinalde N, Galvez P, Lacerda HM, Parada LA, &, Zugaza JL, (2015) Guanine nucleotide exchange factor αPIX leads to activation of the Rac 1 GTPase/glycogen phosphorylase pathway in interleukin (IL)-2-stimulated T cells. J Biol Chem 290, 9171-9182.
6. Pruitt K, &, Der CJ, (2001) Ras and Rho regulation of the cell cycle and oncogenesis. Cancer Lett 171, 1-10.
7. Caloca MJ, Zugaza JL, &, Bustelo XR, (2008) Mechanistic analysis of the amplification and diversification events induced by Vav proteins in B-lymphocytes. J Biol Chem 283, 36454-36464.
8. Boykevisch S, Zhao C, Sondermann H, Philippidou P, Halegoua S, Kuriyan J, &, Bar-Sagi D, (2006) Regulation of ras signaling dynamics by Sos-mediated positive feedback. Curr Biol 16, 2173-2179.
9. Scheele JS, Marks RE, &, Boss GR, (2007) Signaling by small GTPases in the immune system. Immunol Rev 218, 92-101.
10. Kurosaki T, Takata M, Yamanashi Y, Inazu T, Taniguchi T, Yamamoto T, &, Yamamura H, (1994) Syk activation by the Src-family tyrosine kinase in the B cell receptor signaling. J Exp Med 179, 1725-1729.
11. Packard TA, &, Cambier JC, (2013) B lymphocyte antigen receptor signaling: initiation, amplification, and regulation. F1000Prime Rep 5, 40.
12. Stepanek O, Draber P, Drobek A, Horejsi V, &, Brdicka T, (2013) Nonredundant roles of Src-family kinases and Syk in the initiation of B-cell antigen receptor signaling. J Immunol 190, 1807-1818.
13. Fruman DA, Satterthwaite AB, &, Witte ON, (2000) Xid-like phenotypes: a B cell signalosome takes shape. Immunity 13, 1-3.
14. DeFranco AL, (2001) Vav and the B cell signalosome. Nat Immunol 2, 482-484.
15. Hogan PG, Lewis RS, &, Rao A, (2010) Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu Rev Immunol 28, 491-533.
16. Kurosaki T, (2000) Functional dissection of BCR signaling pathways. Curr Opin Immunol 12, 276-281.
17. Beaulieu N, Zahedi B, Goulding RE, Tazmini G, Anthony KV, Omeis SL, de Jong DR, &, Kay RJ, (2007) Regulation of RasGRP1 by B cell antigen receptor requires cooperativity between three domains controlling translocation to the plasma membrane. Mol Biol Cell 18, 3156-3168.
18. Clark EA, Golub TR, Lander ES, &, Hynes RO, (2000) Genomic analysis of metastasis reveals an essential role for RhoC. Nature 406, 532-535.
19. Coughlin SR, (2005) Protease-activated receptors in hemostasis, thrombosis and vascular biology. J Thromb Haemost 3, 1800-1814.
20. Coleman ML, Marshall CJ, &, Olson MF, (2004) RAS and RHO GTPases in G1-phase cell-cycle regulation. Nat Rev Mol Cell Biol 5, 355-366.
21. Gjoerup O, Lukas J, Bartek J, &, Willumsen BM, (1998) Rac and Cdc42 are potent stimulators of E2F-dependent transcription capable of promoting retinoblastoma susceptibility gene product hyperphosphorylation. J Biol Chem 273, 18812-18818.
22. Benitah SA, Valeron PF, van Aelst L, Marshall CJ, &, Lacal JC, (2004) Rho GTPases in human cancer: an unresolved link to upstream and downstream transcriptional regulation. Biochim Biophys Acta 1705, 121-132.
23. Alinikula J, Lassila O, &, Nera KP, (2006) DT40 mutants: a model to study transcriptional regulation of B cell development and function. Subcell Biochem 40, 189-205.
24. Van Aelst L, &, D'Souza-Schorey C, (1997) Rho GTPases and signaling networks. Genes Dev 11, 2295-2322.
25. Joneson T, McDonough M, Bar-Sagi D, &, Van Aelst L, (1996) RAC regulation of actin polymerization and proliferation by a pathway distinct from Jun kinase. Science 274, 1374-1376.
26. Joneson T, &, Bar-Sagi D, (1998) Rac1 effector site controlling mitogenesis through superoxide production. J Biol Chem 273, 17991-17994.
27. Inabe K, &, Kurosaki T, (2002) Tyrosine phosphorylation of B-cell adaptor for phosphoinositide 3-kinase is required for Akt activation in response to CD19 engagement. Blood 99, 584-589.
28. Zugaza JL, Sinnett-Smith J, Van Lint J, &, Rozengurt E, (1996) Protein kinase D (PKD) activation in intact cells through a protein kinase C-dependent signal transduction pathway. EMBO J 15, 6220-6230.
29. Manterola L, Hernando-Rodríguez M, Ruiz A, Apraiz A, Arrizabalaga O, Vellõn L, Alberdi E, Cavaliere F, Lacerda HM, Jimenez S, et al,. (2013) 1-42 β-amyloid peptide requires PDK1/nPKC/Rac 1 pathway to induce neuronal death. Transl Psychiatry 3, e219.
30. Toullec D, Pianetti P, Coste H, Bellevergue P, Grand-Perret T, Ajakane M, Baudet V, Boissin P, Boursier E, Loriolle F, et al,. (1991) The bisindolylmaleimide GF 109203X is a potent and selective inhibitor of protein kinase C. J Biol Chem 266, 15771-15781.
31. Johnson JA, Gray MO, Chen CH, &, Mochly-Rosen D, (1996) A protein kinase C translocation inhibitor as an isozyme-selective antagonist of cardiac function. J Biol Chem 271, 24962-24966.
32. Parri M, &, Chiarugi P, (2010) Rac and Rho GTPases in cancer cell motility control. Cell Commun Signal 8, 23.
33. Bustelo XR, Sauzeau V, &, Berenjeno IM, (2007) GTP-binding proteins of the Rho/Rac family: regulation, effectors and functions in vivo. BioEssays 29, 356-370.
34. Cherfils J, &, Zeghouf M, (2013) Regulation of small GTPases by GEFs, GAPs, and GDIs. Physiol Rev 93, 269-309.
35. Mittnacht S, Paterson H, Olson MF, &, Marshall CJ, (1997) Ras signalling is required for inactivation of the tumour suppressor pRb cell-cycle control protein. Curr Biol 7, 219-221.
36. Malumbres M, &, Pellicer A, (1998) RAS pathways to cell cycle control and cell transformation. Front Biosci 3, d887-d912.
37. Peeper DS, Upton TM, Ladha MH, Neuman E, Zalvide J, Bernards R, DeCaprio JA, &, Ewen ME, (1997) Ras signalling linked to the cell-cycle machinery by the retinoblastoma protein. Nature 386, 177-181.
38. Caloca MJ, Zugaza JL, &, Bustelo XR, (2003) Exchange factors of the RasGRP family mediate Ras activation in the Golgi. J Biol Chem 278, 33465-33473.
39. Bustelo XR, (2014) Vav family exchange factors: an integrated regulatory and functional view. Small GTPases 5, 9.
40. Costello PS, Walters AE, Mee PJ, Turner M, Reynolds LF, Prisco A, Sarner N, Zamoyska R, &, Tybulewicz VL,. (1999) The Rho-family GTP exchange factor Vav is a critical transducer of T cell receptor signals to the calcium, ERK, and NF-kappaB pathways. Proc Natl Acad Sci USA 96, 3035-3040.
41. Guo F, Cancelas JA, Hildeman D, Williams DA, &, Zheng Y, (2008) Rac GTPase isoforms Rac1 and Rac2 play a redundant and crucial role in T-cell development. Blood 112, 1767-1775.
42. Nevins JR, (2001) The Rb/E2F pathway and cancer. Hum Mol Genet 10, 699-703.
43. Westwick JK, Lambert QT, Clark GJ, Symons M, Van Aelst L, Pestell RG, &, Der CJ, (1997) Rac regulation of transformation, gene expression, and actin organization by multiple, PAK-independent pathways. Mol Cell Biol 17, 1324-1335.
44. Lamarche N, Tapon N, Stowers L, Burbelo PD, Aspenstrom P, Bridges T, Chant J, &, Hall A, (1996) Rac and Cdc42 induce actin polymerization and G1 cell cycle progression independently of p65PAK and the JNK/SAPK MAP kinase cascade. Cell 87, 519-529.
45. Zhao ZS, Manser E, Chen XQ, Chong C, Leung T, &, Lim L, (1998) A conserved negative regulatory region in alphaPAK: inhibition of PAK kinases reveals their morphological roles downstream of Cdc42 and Rac1. Mol Cell Biol 18, 2153-2163.
46. Li F, Adam L, Vadlamudi RK, Zhou H, Sen S, Chernoff J, Mandal M, &, Kumar R, (2002) p21-activated kinase 1 interacts with and phosphorylates histone H3 in breast cancer cells. EMBO Rep 3, 767-773.
47. Nheu T, He H, Hirokawa Y, Walker F, Wood J, &, Maruta H, (2004) PAK is essential for RAS-induced upregulation of cyclin D1 during the G1 to S transition. Cell Cycle 3, 71-74.
48. Thullberg M, Gad A, Beeser A, Chernoff J, &, Stromblad S, (2007) The kinase-inhibitory domain of p21-activated kinase 1 (PAK1) inhibits cell cycle progression independent of PAK1 kinase activity. Oncogene 26, 1820-1828.
49. Park ER, Eblen ST, &, Catling AD, (2007) MEK1 activation by PAK: a novel mechanism. Cell Signal 19, 1488-1496.
50. Black JD, (2000) Protein kinase C-mediated regulation of the cell cycle. Front Biosci 5, D 406-D 423.
51. Gavrielides MV, Frijhoff AF, Conti CJ, &, Kazanietz MG, (2004) Protein kinase C and prostate carcinogenesis: targeting the cell cycle and apoptotic mechanisms. Curr Drug Targets 5, 431-443.
52. Basu A, &, Sivaprasad U, (2007) Protein kinase Cepsilon makes the life and death decision. Cell Signal 19, 1633-1642.