AMPKα1 deficiency promotes cellular proliferation and DNA damage via p21 reduction in mouse embryonic fibroblasts

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1853, Issue 1, 2015, Pages 65-73

  Xu, Hairong ^a,b   Zhou, Yanhong ^a,c   Coughlan, Kathleen A ^a   Ding, Ye ^a   Wang, Shaobin ^a   Wu, Yue ^a   Song, Ping ^a   Zou, Ming Hui ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b YANGZHOU UNIVERSITY   (China)

^c HUBEI UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

53BP1; AMPK ; Apoptosis; Cell proliferation; DNA damage; P21

Indexed keywords

ADENOSINE MONOPHOSPHATE ACTIVATED PROTEIN KINASE ALPHA 1; ADENOSINE MONOPHOSPHATE ACTIVATED PROTEIN KINASE ALPHA 2; BINDING PROTEIN; DOUBLE STRANDED DNA; PROTEIN KINASE; PROTEIN P21; PROTEIN P53 BINDING PROTEIN 1; UNCLASSIFIED DRUG; AMPK ALPHA1 SUBUNIT, MOUSE; AMPK ALPHA2 SUBUNIT, MOUSE; CDKN1A PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DNA BINDING PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; NONHISTONE PROTEIN; TRP53BP1 PROTEIN, MOUSE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIVISION; CELL PROLIFERATION; CHROMATIN; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; ENZYME DEFICIENCY; FIBROBLAST; FLOW CYTOMETRY; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; PROTEIN LOCALIZATION; WESTERN BLOTTING; ANIMAL; C57BL MOUSE; CELL CULTURE; PHYSIOLOGY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELL PROLIFERATION; CELLS, CULTURED; CHROMOSOMAL PROTEINS, NON-HISTONE; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DNA DAMAGE; DNA-BINDING PROTEINS; FIBROBLASTS; MICE; MICE, INBRED C57BL;

EID: 84908345791     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.10.002     Document Type: Article

References (66)

1. Jones R.M., Petermann E. Replication fork dynamics and the DNA damage response. Biochem. J. 2012, 443:13-26.
2. Heyer W.D., Ehmsen K.T., Liu J. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 2010, 44:113-139.
3. Jackson S.P., Durocher D. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 2013, 49:795-807.
4. Betermier M., Bertrand P., Lopez B.S. Is non-homologous end-joining really an inherently error-prone process?. PLoS Genet. 2014, 10:e1004086.
5. Strande N., Roberts S.A., Oh S., Hendrickson E.A., Ramsden D.A. Specificity of the dRP/AP lyase of Ku promotes nonhomologous end joining (NHEJ) fidelity at damaged ends. J. Biol. Chem. 2012, 287:13686-13693.
6. Renkawitz J., Lademann C.A., Kalocsay M., Jentsch S. Monitoring homology search during DNA double-strand break repair in vivo. Mol. Cell 2013, 50:261-272.
7. Polo S.E., Jackson S.P. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 2011, 25:409-433.
8. Ward I.M., Minn K., van Deursen J., Chen J. p53 Binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 2003, 23:2556-2563.
9. Panier S., Boulton S.J. Double-strand break repair: 53BP1 comes into focus. Nat. Rev. Mol. Cell Biol. 2014, 15:7-18.
10. Fradet-Turcotte A., Canny M.D., Escribano-Diaz C., Orthwein A., Leung C.C., Huang H., Landry M.C., Kitevski-LeBlanc J., Noordermeer S.M., Sicheri F., Durocher D. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 2013, 499:50-54.
11. Tang J., Cho N.W., Cui G., Manion E.M., Shanbhag N.M., Botuyan M.V., Mer G., Greenberg R.A. Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat. Struct. Mol. Biol. 2013, 20:317-325.
12. Pei H., Zhang L., Luo K., Qin Y., Chesi M., Fei F., Bergsagel P.L., Wang L., You Z., Lou Z. MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 2011, 470:124-128.
13. Callen E., Di Virgilio M., Kruhlak M.J., Nieto-Soler M., Wong N., Chen H.T., Faryabi R.B., Polato F., Santos M., Starnes L.M., Wesemann D.R., Lee J.E., Tubbs A., Sleckman B.P., Daniel J.A., Ge K., Alt F.W., Fernandez-Capetillo O., Nussenzweig M.C., Nussenzweig A. 53BP1 mediates productive and mutagenic DNA repair through distinct phosphoprotein interactions. Cell 2013, 153:1266-1280.
14. Satyanarayana A., Hilton M.B., Kaldis P. p21 Inhibits Cdk1 in the absence of Cdk2 to maintain the G1/S phase DNA damage checkpoint. Mol. Biol. Cell 2008, 19:65-77.
15. Lindqvist A., van Zon W., Karlsson Rosenthal C., Wolthuis R.M. Cyclin B1-Cdk1 activation continues after centrosome separation to control mitotic progression. PLoS Biol. 2007, 5:e123.
16. Deibler R.W., Kirschner M.W. Quantitative reconstitution of mitotic CDK1 activation in somatic cell extracts. Mol. Cell 2010, 37:753-767.
17. Deng C., Zhang P., Harper J.W., Elledge S.J., Leder P. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 1995, 82:675-684.
18. Perucca P., Cazzalini O., Mortusewicz O., Necchi D., Savio M., Nardo T., Stivala L.A., Leonhardt H., Cardoso M.C., Prosperi E. Spatiotemporal dynamics of p21CDKN1A protein recruitment to DNA-damage sites and interaction with proliferating cell nuclear antigen. J. Cell Sci. 2006, 119:1517-1527.
19. Viale A., De Franco F., Orleth A., Cambiaghi V., Giuliani V., Bossi D., Ronchini C., Ronzoni S., Muradore I., Monestiroli S., Gobbi A., Alcalay M., Minucci S., Pelicci P.G. Cell-cycle restriction limits DNA damage and maintains self-renewal of leukaemia stem cells. Nature 2009, 457:51-56.
20. Banko M.R., Allen J.J., Schaffer B.E., Wilker E.W., Tsou P., White J.L., Villen J., Wang B., Kim S.R., Sakamoto K., Gygi S.P., Cantley L.C., Yaffe M.B., Shokat K.M., Brunet A. Chemical genetic screen for AMPKalpha2 substrates uncovers a network of proteins involved in mitosis. Mol. Cell 2011, 44:878-892.
21. Vazquez-Martin A., Lopez-Bonet E., Oliveras-Ferraros C., Perez-Martinez M.C., Bernado L., Menendez J.A. Mitotic kinase dynamics of the active form of AMPK (phospho-AMPKalphaThr172) in human cancer cells. Cell Cycle 2009, 8:788-791.
22. Thaiparambil J.T., Eggers C.M., Marcus A.I. AMPK regulates mitotic spindle orientation through phosphorylation of myosin regulatory light chain. Mol. Cell. Biol. 2012, 32:3203-3217.
23. Song P., Zou M.H. Regulation of NAD(P)H oxidases by AMPK in cardiovascular systems. Free Radic. Biol. Med. 2012, 52:1607-1619.
24. Zhou J., Huang W., Tao R., Ibaragi S., Lan F., Ido Y., Wu X., Alekseyev Y.O., Lenburg M.E., Hu G.F., Luo Z. Inactivation of AMPK alters gene expression and promotes growth of prostate cancer cells. Oncogene 2009, 28:1993-2002.
25. Luo Z., Zang M., Guo W. AMPK as a metabolic tumor suppressor: control of metabolism and cell growth. Future Oncol. 2010, 6:457-470.
26. Wu C.L., Qiang L., Han W., Ming M., Viollet B., He Y.Y. Role of AMPK in UVB-induced DNA damage repair and growth control. Oncogene 2013, 32:2682-2689.
27. Ui A., Ogiwara H., Nakajima S., Kanno S., Watanabe R., Harata M., Okayama H., Harris C.C., Yokota J., Yasui A., Kohno T. Possible involvement of LKB1-AMPK signaling in non-homologous end joining. Oncogene 2014, 33:1640-1648.
28. Viollet B., Andreelli F., Jorgensen S.B., Perrin C., Geloen A., Flamez D., Mu J., Lenzner C., Baud O., Bennoun M., Gomas E., Nicolas G., Wojtaszewski J.F., Kahn A., Carling D., Schuit F.C., Birnbaum M.J., Richter E.A., Burcelin R., Vaulont S. The AMP-activated protein kinase alpha2 catalytic subunit controls whole-body insulin sensitivity. J. Clin. Invest. 2003, 111:91-98.
29. Song P., Wang S., He C., Liang B., Viollet B., Zou M.H. AMPKalpha2 deletion exacerbates neointima formation by upregulating Skp2 in vascular smooth muscle cells. Circ. Res. 2011, 109:1230-1239.
30. Wang S., Song P., Zou M.H. Inhibition of AMP-activated protein kinase alpha (AMPKalpha) by doxorubicin accentuates genotoxic stress and cell death in mouse embryonic fibroblasts and cardiomyocytes: role of p53 and SIRT1. J. Biol. Chem. 2012, 287:8001-8012.
31. Todaro G.J., Green H. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 1963, 17:299-313.
32. Xu M.J., Song P., Shirwany N., Liang B., Xing J.J., Viollet B., Wang X., Zhu Y., Zou M.H. Impaired expression of uncoupling protein 2 causes defective postischemic angiogenesis in mice deficient in AMP-activated protein kinase alpha subunits. Arterioscler. Thromb. Vasc. Biol. 2011, 31:1757-1765.
33. Ward I.M., Difilippantonio S., Minn K., Mueller M.D., Molina J.R., Yu X., Frisk C.S., Ried T., Nussenzweig A., Chen J. 53BP1 cooperates with p53 and functions as a haploinsufficient tumor suppressor in mice. Mol. Cell. Biol. 2005, 25:10079-10086.
34. Song P., Wei J., Wang H.C. Distinct roles of the ERK pathway in modulating apoptosis of Ras-transformed and non-transformed cells induced by anticancer agent FR901228. FEBS Lett. 2005, 579:90-94.
35. Terry N.H., White R.A. Flow cytometry after bromodeoxyuridine labeling to measure S and G2+M phase durations plus doubling times in vitro and in vivo. Nat. Protoc. 2006, 1:859-869.
36. Song P., Wu Y., Xu J., Xie Z., Dong Y., Zhang M., Zou M.H. Reactive nitrogen species induced by hyperglycemia suppresses Akt signaling and triggers apoptosis by upregulating phosphatase PTEN (phosphatase and tensin homologue deleted on chromosome 10) in an LKB1-dependent manner. Circulation 2007, 116:1585-1595.
37. Song P., Zhang M., Wang S., Xu J., Choi H.C., Zou M.H. Thromboxane A2 receptor activates a Rho-associated kinase/LKB1/PTEN pathway to attenuate endothelium insulin signaling. J. Biol. Chem. 2009, 284:17120-17128.
38. Phoenix K.N., Devarakonda C.V., Fox M.M., Stevens L.E., Claffey K.P. AMPKalpha2 suppresses murine embryonic fibroblast transformation and tumorigenesis. Genes Cancer 2012, 3:51-62.
39. Jiang W., Zhu Z., Thompson H.J. Dietary energy restriction modulates the activity of AMP-activated protein kinase, Akt, and mammalian target of rapamycin in mammary carcinomas, mammary gland, and liver. Cancer Res. 2008, 68:5492-5499.
40. Wei Y., Yu L., Bowen J., Gorovsky M.A., Allis C.D. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 1999, 97:99-109.
41. Mao L., Li N., Guo Y., Xu X., Gao L., Xu Y., Zhou L., Liu W. AMPK phosphorylates GBF1 for mitotic Golgi disassembly. J. Cell Sci. 2013, 126:1498-1505.
42. Jones R.G., Plas D.R., Kubek S., Buzzai M., Mu J., Xu Y., Birnbaum M.J., Thompson C.B. AMP-activated protein kinase induces a p53-dependent metabolic checkpoint. Mol. Cell 2005, 18:283-293.
43. Coulonval K., Kooken H., Roger P.P. Coupling of T161 and T14 phosphorylations protects cyclin B-CDK1 from premature activation. Mol. Biol. Cell 2011, 22:3971-3985.
44. Zhang S., Liu X., Bawa-Khalfe T., Lu L.S., Lyu Y.L., Liu L.F., Yeh E.T. Identification of the molecular basis of doxorubicin-induced cardiotoxicity. Nat. Med. 2012, 18:1639-1642.
45. Rogakou E.P., Pilch D.R., Orr A.H., Ivanova V.S., Bonner W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273:5858-5868.
46. Sluss H.K., Armata H., Gallant J., Jones S.N. Phosphorylation of serine 18 regulates distinct p53 functions in mice. Mol. Cell. Biol. 2004, 24:976-984.
47. Smits V.A., Reaper P.M., Jackson S.P. Rapid PIKK-dependent release of Chk1 from chromatin promotes the DNA-damage checkpoint response. Curr. Biol. 2006, 16:150-159.
48. Collins A.R. The comet assay for DNA damage and repair: principles, applications, and limitations. Mol. Biotechnol. 2004, 26:249-261.
49. Wang X., Zeng L., Wang J., Chau J.F., Lai K.P., Jia D., Poonepalli A., Hande M.P., Liu H., He G., He L., Li B. A positive role for c-Abl in Atm and Atr activation in DNA damage response. Cell Death Differ. 2011, 18:5-15.
50. Vaudry D., Gonzalez B.J., Basille M., Pamantung T.F., Fontaine M., Fournier A., Vaudry H. The neuroprotective effect of pituitary adenylate cyclase-activating polypeptide on cerebellar granule cells is mediated through inhibition of the CED3-related cysteine protease caspase-3/CPP32. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:13390-13395.
51. Ozoren N., Kim K., Burns T.F., Dicker D.T., Moscioni A.D., El-Deiry W.S. The caspase 9 inhibitor Z-LEHD-FMK protects human liver cells while permitting death of cancer cells exposed to tumor necrosis factor-related apoptosis-inducing ligand. Cancer Res. 2000, 60:6259-6265.
52. Schulte-Uentrop L., El-Awady R.A., Schliecker L., Willers H., Dahm-Daphi J. Distinct roles of XRCC4 and Ku80 in non-homologous end-joining of endonuclease- and ionizing radiation-induced DNA double-strand breaks. Nucleic Acids Res. 2008, 36:2561-2569.
53. Tawa N.E., Odessey R., Goldberg A.L. Inhibitors of the proteasome reduce the accelerated proteolysis in atrophying rat skeletal muscles. J. Clin. Invest. 1997, 100:197-203.
54. Gu Y., Rosenblatt J., Morgan D.O. Cell cycle regulation of CDK2 activity by phosphorylation of Thr160 and Tyr15. EMBO J. 1992, 11:3995-4005.
55. Sugasawa K., Ng J.M., Masutani C., Iwai S., van der Spek P.J., Eker A.P., Hanaoka F., Bootsma D., Hoeijmakers J.H. Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol. Cell 1998, 2:223-232.
56. Hong H., Takahashi K., Ichisaka T., Aoi T., Kanagawa O., Nakagawa M., Okita K., Yamanaka S. Suppression of induced pluripotent stem cell generation by the p53-p21 pathway. Nature 2009, 460:1132-1135.
57. He G., Siddik Z.H., Huang Z., Wang R., Koomen J., Kobayashi R., Khokhar A.R., Kuang J. Induction of p21 by p53 following DNA damage inhibits both Cdk4 and Cdk2 activities. Oncogene 2005, 24:2929-2943.
58. Kim H.S., Hwang J.T., Yun H., Chi S.G., Lee S.J., Kang I., Yoon K.S., Choe W.J., Kim S.S., Ha J. Inhibition of AMP-activated protein kinase sensitizes cancer cells to cisplatin-induced apoptosis via hyper-induction of p53. J. Biol. Chem. 2008, 283:3731-3742.
59. Nicol S.M., Bray S.E., Derek Black H., Lorimore S.A., Wright E.G., Lane D.P., Meek D.W., Coates P.J., Fuller-Pace F.V. The RNA helicase p68 (DDX5) is selectively required for the induction of p53-dependent p21 expression and cell-cycle arrest after DNA damage. Oncogene 2013, 32:3461-3469.
60. Igata M., Motoshima H., Tsuruzoe K., Kojima K., Matsumura T., Kondo T., Taguchi T., Nakamaru K., Yano M., Kukidome D., Matsumoto K., Toyonaga T., Asano T., Nishikawa T., Araki E. Adenosine monophosphate-activated protein kinase suppresses vascular smooth muscle cell proliferation through the inhibition of cell cycle progression. Circ. Res. 2005, 97:837-844.
61. Humbert N., Navaratnam N., Augert A., Da Costa M., Martien S., Wang J., Martinez D., Abbadie C., Carling D., de Launoit Y., Gil J., Bernard D. Regulation of ploidy and senescence by the AMPK-related kinase NUAK1. EMBO J. 2010, 29:376-386.
62. Barboza J.A., Liu G., Ju Z., El-Naggar A.K., Lozano G. p21 delays tumor onset by preservation of chromosomal stability. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:19842-19847.
63. Hiraku Y., Yamashita N., Nishiguchi M., Kawanishi S. Catechol estrogens induce oxidative DNA damage and estradiol enhances cell proliferation. Int. J. Cancer 2001, 92:333-337.
64. Di Micco R., Fumagalli M., Cicalese A., Piccinin S., Gasparini P., Luise C., Schurra C., Garre M., Nuciforo P.G., Bensimon A., Maestro R., Pelicci P.G., d'Adda di Fagagna F. Oncogene-induced senescence is a DNA damage response triggered by DNA hyper-replication. Nature 2006, 444:638-642.
65. Ogrunc M., Di Micco R., Liontos M., Bombardelli L., Mione M., Fumagalli M., Gorgoulis V.G., d'Adda di Fagagna F. Oncogene-induced reactive oxygen species fuel hyperproliferation and DNA damage response activation. Cell Death Differ. 2014, 21:998-1012.
66. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.