The p57 CDKi integrates stress signals into cell-cycle progression to promote cell survival upon stress

EMBO Journal

Volumn 31, Issue 13, 2012, Pages 2952-2964

  Joaquin, Manel ^a   Gubern, Albert ^a   González Nuñez, Daniel ^a   Josue Ruiz E ^b   Ferreiro, Isabel ^a   De Nadal, Eulalia ^a   Nebreda, Angel R ^b,c   Posas, Francesc ^a  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b Centro Nacional de Investigaciones Oncológicas   (Spain)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

Author keywords

cell cycle; cell stress; cell survival; p38 SAPK; p57 CDKi

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 1C; IONOMYCIN; MITOGEN ACTIVATED PROTEIN KINASE P38;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CYCLE PROGRESSION; CELL SURVIVAL; CELL VIABILITY; CELLULAR STRESS SIGNAL; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; ENZYME ACTIVITY; FEMALE; GENE INACTIVATION; HELA CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; IN VITRO STUDY; INHIBITION KINETICS; OSMOTIC STRESS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN STABILITY; PROTEIN TARGETING; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WILD TYPE;

ANIMALS; CALCIUM IONOPHORES; CELL SURVIVAL; CYCLIN-DEPENDENT KINASE INHIBITOR P57; HEK293 CELLS; HUMANS; IONOMYCIN; MICE; OSMOTIC PRESSURE; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

EID: 84863822868     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.122     Document Type: Article

References (54)

1. Adrover M, Zi Z, Duch A, Schaber J, González-Novo A, Jimenez J, Nadal-Ribelles M, Clotet J, Klipp E, Posas F (2011) Time-dependent quantitative multicomponent control of the G1-S network by the stress-activated protein kinase Hog1 upon osmostress. Sci Signal 4: ra63
2. Ambrosino C, Mace G, Galban S, Fritsch C, Vintersten K, Black E, Gorospe M, Nebreda AR (2003) Negative feedback regulation of MKK6 mRNA stability by p38alpha mitogen-activated protein kinase. Mol Cell Biol 23: 370-381 (Pubitemid 36008527)
3. Ambrosino C, Nebreda AR (2001) Cell cycle regulation by p38 MAP kinases. Biol Cell 93: 47-51 (Pubitemid 33040859)
4. Besson A, Dowdy S, Roberts J (2008) CDK inhibitors: cell cycle regulators and beyond. Dev Cell 14: 159-169 (Pubitemid 351189186)
5. Borriello A, Caldarelli I, Bencivenga D, Criscuolo M, Cucciolla V, Tramontano A, Oliva A, Perrotta S, Della Ragione F (2011) p57(Kip2) and cancer: time for a critical appraisal. Mol Cancer Res 9: 1269-1284
6. Brown N, Noble M, Endicott J, Garman E, Wakatsuki S, Mitchell E, Rasmussen B, Hunt T, Johnson L (1995) The crystal structure of cyclin A. Structure 3: 1235-1247 (Pubitemid 3001419)
7. Brown N, Noble M, Endicott J, Johnson L (1999) The structural basis for specificity of substrate and recruitment peptides for cyclin-dependent kinases. Nat Cell Biol 1: 438-443 (Pubitemid 129502811)
8. Bulavin D, Higashimoto Y, Popoff I, Gaarde W, Basrur V, Potapova O, Appella E, Fornace AJ (2001) Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature 411: 102-107 (Pubitemid 32428198)
9. Bulavin DV, Fornace AJ (2004) p38 MAP kinase's emerging role as a tumor suppressor. Adv Cancer Res 92: 95-118 (Pubitemid 39458114)
10. Bulavin DV, Saito S, Hollander MC, Sakaguchi K, Anderson CW, Appella E, Fornace AJ (1999) Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J 18: 6845-6854
11. Chandrasekaran S, Tan TX, Hall JR, Cook JG (2011) Stress-stimulated mitogen-activated protein kinases control the stability and activity of the Cdt1 DNA replication licensing factor. Mol Cell Biol 31: 4405-4416
12. Chang TS, Kim MJ, Ryoo K, Park J, Eom SJ, Shim J, Nakayama KI, Nakayama K, Tomita M, Takahashi K, Lee MJ, Choi EJ (2003) p57KIP2 modulates stress-activated signaling by inhibiting c-Jun NH2-terminal kinase/stress- activated protein kinase. J Biol Chem 278: 48092-48098 (Pubitemid 37523260)
13. Chua PJ, Yip GW, Bay BH (2009) Cell cycle arrest induced by hydrogen peroxide is associated with modulation of oxidative stress related genes in breast cancer cells. Exp Biol Med (Maywood) 234: 1086-1094
14. Clotet J, Escoté X, Adrover M, Yaakov G, Garí E, Aldea M, de Nadal E, Posas F (2006) Phosphorylation of Hsl1 by Hog1 leads to a G2 arrest essential for cell survival at high osmolarity. EMBO J 25: 2338-2346 (Pubitemid 44012217)
15. Cuadrado M, Gutierrez-Martinez P, Swat A, Nebreda A, Fernandez- Capetillo O (2009) p27Kip1 stabilization is essential for the maintenance of cell cycle arrest in response to DNA damage. Cancer Res 69: 8726-8732
16. de Nadal E, Alepuz PM, Posas F (2002) Dealing with osmostress through MAP kinase activation. EMBO Rep 3: 735-740 (Pubitemid 34966011)
17. de Nadal E, Ammerer G, Posas F (2011) Controlling gene expression in response to stress. Nat Rev Genet 12: 833-845
18. Dmitrieva N, Bulavin D, Fornace AJ, Burg M (2002) Rapid activation of G2/M checkpoint after hypertonic stress in renal inner medullary epithelial (IME) cells is protective and requires p38 kinase. Proc Natl Acad Sci USA 99: 184-189 (Pubitemid 34060338)
19. Elzi DJ, Bjornsen AJ, MacKenzie T, Wyman TH, Silliman CC (2001) Ionomycin causes activation of p38 and p42/44 mitogenactivated protein kinases in human neutrophils. Am J Physiol Cell Physiol 281: C350-C360
20. Escoté X, Zapater M, Clotet J, Posas F (2004) Hog1 mediates cellcycle arrest in G1 phase by the dual targeting of Sic1. Nat Cell Biol 6: 997-1002 (Pubitemid 39359853)
21. Ferby I, Blazquez M, Palmer A, Eritja R, Nebreda A (1999) A novel p34(cdc2)-binding and activating protein that is necessary and sufficient to trigger G(2)/M progression in Xenopus oocytes. Genes Dev 13: 2177-2189 (Pubitemid 29407356)
22. Galcheva-Gargova Z, Dérijard B, Wu IH, Davis RJ (1994) An osmosensing signal transduction pathway in mammalian cells. Science 265: 806-808 (Pubitemid 24266144)
23. Han J, Lee JD, Bibbs L, Ulevitch RJ (1994) A MAP kinase targeted by endotoxin and hyperosmolarity in mammalian cells. Science 265: 808-811 (Pubitemid 24266145)
24. Hashimoto Y, Kohri K, Kaneko Y, Morisaki H, Kato T, Ikeda K, Nakanishi M (1998) Critical role for the 310 helix region of p57(Kip2) in cyclin-dependent kinase 2 inhibition and growth suppression. J Biol Chem 273: 16544-16550 (Pubitemid 28311440)
25. Huot J, Houle F, Marceau F, Landry J (1997) Oxidative stress-induced actin reorganization mediated by the p38 mitogen-activated protein kinase/heat shock protein 27 pathway in vascular endothelial cells. Circ Res 80: 383-392 (Pubitemid 27093353)
26. Ishida N, Hara T, Kamura T, Yoshida M, Nakayama K, Nakayama K (2002) Phosphorylation of p27Kip1 on serine 10 is required for its binding to CRM1 and nuclear export. J Biol Chem 277: 14355-14358 (Pubitemid 34952496)
27. Kamura T, Hara T, Kotoshiba S, Yada M, Ishida N, Imaki H, Hatakeyama S, Nakayama K, Nakayama K (2003) Degradation of p57Kip2 mediated by SCFSkp2-dependent ubiquitylation. Proc Natl Acad Sci USA 100: 10231-10236 (Pubitemid 37071861)
28. Kim G, Mercer S, Ewton D, Yan Z, Jin K, Friedman E (2002) The stress-activated protein kinases p38 alpha and JNK1 stabilize p21(Cip1) by phosphorylation. J Biol Chem 277: 29792-29802
29. Kossatz U, Vervoorts J, Nickeleit I, Sundberg H, Arthur J, Manns M, Malek N (2006) C-terminal phosphorylation controls the stability and function of p27kip1. EMBO J 25: 5159-5170 (Pubitemid 44658533)
30. Kotake Y, Nakayama K, Ishida N, Nakayama K (2005) Role of serine 10 phosphorylation in p27 stabilization revealed by analysis of p27 knock-in mice harboring a serine 10 mutation. J Biol Chem 280: 1095-1102
31. Lafarga V, Cuadrado A, Lopez de Silanes I, Bengoechea R, Fernandez-Capetillo O, Nebreda A (2009) p38 Mitogen-activated protein kinase- and HuR-dependent stabilization of p21(Cip1) mRNA mediates the G(1)/S checkpoint. Mol Cell Biol 29: 4341-4351
32. Lee MH, Reynisdóttir I, Massagué J (1995) Cloning of p57KIP2, a cyclin-dependent kinase inhibitor with unique domain structure and tissue distribution. Genes Dev 9: 639-649
33. Liang J, Zubovitz J, Petrocelli T, Kotchetkov R, Connor M, Han K, Lee J, Ciarallo S, Catzavelos C, Beniston R, Franssen E, Slingerland J (2002) PKB/Akt phosphorylates p27, impairs nuclear import of p27 and opposes p27-mediated G1 arrest. Nat Med 8: 1153-1160 (Pubitemid 35175971)
34. Malumbres M, Barbacid M (2005) Mammalian cyclin-dependent kinases. Trends Biochem Sci 30: 630-641 (Pubitemid 41540083)
35. Manke I, Nguyen A, Lim D, Stewart M, Elia A, Yaffe M (2005) MAPKAP kinase-2 is a cell cycle checkpoint kinase that regulates the G2/M transition and S phase progression in response to UV irradiation. Mol Cell 17: 37-48 (Pubitemid 40075363)
36. Matsumoto A, Takeishi S, Kanie T, Susaki E, Onoyama I, Tateishi Y, Nakayama K, Nakayama KI (2011) p57 is required for quiescence and maintenance of adult hematopoietic stem cells. Cell Stem Cell 9: 262-271
37. Matsuoka S, Edwards MC, Bai C, Parker S, Zhang P, Baldini A, Harper JW, Elledge SJ (1995) p57KIP2, a structurally distinct member of the p21CIP1 Cdk inhibitor family, is a candidate tumor suppressor gene. Genes Dev 9: 650-662
38. Orlow I, Iavarone A, Crider-Miller SJ, Bonilla F, Latres E, Lee MH, Gerald WL, Massagué J, Weissman BE, Cordón-Cardó C (1996) Cyclin-dependent kinase inhibitor p57KIP2 in soft tissue sarcomas and Wilms'tumors. Cancer Res 56: 1219-1221
39. Pateras IS, Apostolopoulou K, Niforou K, Kotsinas A, Gorgoulis VG (2009) p57KIP2: "Kip"ing the cell under control. Mol Cancer Res 7: 1902-1919
40. Pedraza-Alva G, Koulnis M, Charland C, Thornton T, Clements J, Schlissel M, Rincón M (2006) Activation of p38 MAP kinase by DNA double-strand breaks in V(D)J recombination induces a G2/M cell cycle checkpoint. EMBO J 25: 763-773 (Pubitemid 43292438)
41. Reinhardt H, Aslanian A, Lees J, Yaffe M (2007) p53-deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell 11: 175-189 (Pubitemid 46209849)
42. Scotto C, Delphin C, Deloulme JC, Baudier J (1999) Concerted regulation of wild-type p53 nuclear accumulation and activation by S100B and calcium-dependent protein kinase C. Mol Cell Biol 19: 7168-7180 (Pubitemid 29441897)
43. Shin I, Yakes F, Rojo F, Shin N, Bakin A, Baselga J, Arteaga C (2002) PKB/Akt mediates cell-cycle progression by phosphorylation of p27(Kip1) at threonine 157 and modulation of its cellular localization. Nat Med 8: 1145-1152 (Pubitemid 35175970)
44. Sinha RP, Häder DP (2002) UV-induced DNA damage and repair: a review. Photochem Photobiol Sci 1: 225-236 (Pubitemid 37069733)
45. Swat A, Dolado I, Rojas JM, Nebreda AR (2009) Cell densitydependent inhibition of epidermal growth factor receptor signaling by p38alpha mitogen-activated protein kinase via Sprouty2 downregulation. Mol Cell Biol 29: 3332-3343
46. Tesio M, Trumpp A (2011) Breaking the cell cycle of HSCs by p57 and friends. Cell Stem Cell 9: 187-192
47. Todaro G, Green H (1963) Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J Cell Biol 17: 299-313
48. Todd DE, Densham RM, Molton SA, Balmanno K, Newson C, Weston CR, Garner AP, Scott L, Cook SJ (2004) ERK1/2 and p38 cooperate to induce a p21CIP1-dependent G1 cell cycle arrest. Oncogene 23: 3284-3295 (Pubitemid 38669818)
49. Tsvetkov L, Yeh K, Lee S, Sun H, Zhang H (1999) p27(Kip1) ubiquitination and degradation is regulated by the SCF(Skp2) complex through phosphorylated Thr187 in p27. Curr Biol 9: 661-664
50. Vidal A, Koff A (2000) Cell-cycle inhibitors: three families united by a common cause. Gene 247: 1-15 (Pubitemid 30201556)
51. Yaakov G, Duch A, García-Rubio M, Clotet J, Jimenez J, Aguilera A, Posas F (2009) The stress-activated protein kinase Hog1 mediates S phase delay in response to osmostress. Mol Biol Cell 20: 3572-3582
52. Yan Y, Frisén J, Lee MH, Massagué J, Barbacid M (1997) Ablation of the CDK inhibitor p57Kip2 results in increased apoptosis and delayed differentiation during mouse development. Genes Dev 11: 973-983 (Pubitemid 27199877)
53. Zhang P, Liégeois NJ, Wong C, Finegold M, Hou H, Thompson JC, Silverman A, Harper JW, DePinho RA, Elledge SJ (1997) Altered cell differentiation and proliferation in mice lacking p57KIP2 indicates a role in Beckwith-Wiedemann syndrome. Nature 387: 151-158 (Pubitemid 27209424)
54. Zou P, Yoshihara H, Hosokawa K, Tai I, Shinmyozu K, Tsukahara F, Maru Y, Nakayama K, Nakayama KI, Suda T (2011) p57(Kip2) and p27(Kip1) cooperate to maintain hematopoietic stem cell quiescence through interactions with Hsc70. Cell Stem Cell 9: 247-261