ATR/Chk1/Smurf1 pathway determines cell fate after DNA damage by controlling RhoB abundance

Nature Communications

Volumn 5, Issue , 2014, Pages

  Wang, Meilin ^a   Guo, Lei ^a   Wu, Qingang ^a   Zeng, Taoling ^a   Lin, Qi ^a   Qiao, Yikai ^a   Wang, Qun ^a   Liu, Mingdong ^a   Zhang, Xin ^a   Ren, Lan ^a   Zhang, Sheng ^a   Pei, Yihua ^a   Yin, Zhenyu ^a   Ding, Feng ^a   Wang, Hong Rui ^a  

^a XIAMEN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATING AGENT; ATR PROTEIN; CHECKPOINT KINASE 1; RHO FACTOR; RHOB PROTEIN; SMURF1 PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; ATM PROTEIN; ATR PROTEIN, HUMAN; MESYLIC ACID METHYL ESTER; PRIMER DNA; PROTEIN KINASE; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; SMURF1 PROTEIN, HUMAN; UBIQUITIN PROTEIN LIGASE;

ABUNDANCE; APOPTOSIS; DNA; ENZYME ACTIVITY; GERM CELL; SIGNALING; TUMOR; ULTRAVIOLET RADIATION;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER CELL; CARCINOGENESIS; CELL DEATH; CELL FATE; DNA DAMAGE; FEMALE; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; TRANSFORMED CELL; ULTRAVIOLET RADIATION; UPREGULATION; ANALYSIS OF VARIANCE; CELL FRACTIONATION; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; GENETICS; HEK293 CELL LINE; IMMUNOBLOTTING; METABOLISM; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UBIQUITINATION;

ANALYSIS OF VARIANCE; APOPTOSIS; ATAXIA TELANGIECTASIA MUTATED PROTEINS; CELL FRACTIONATION; DNA DAMAGE; DNA PRIMERS; FLUORESCENT ANTIBODY TECHNIQUE; GENE SILENCING; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; METHYL METHANESULFONATE; PROTEIN KINASES; REAL-TIME POLYMERASE CHAIN REACTION; RHOB GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

EID: 84923368480     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5901     Document Type: Article

References (61)

1. Cimprich, K. A. & Cortez, D. ATR: an essential regulator of genome integrity. Nat. Rev. Mol. Cell Biol. 9, 616-627 (2008).
2. Smith, J., Tho, L. M., Xu, N. & Gillespie, D. A. The ATM-Chk2 and ATR-Chk1 pathways in DNA damage signaling and cancer. Adv. Cancer Res. 108, 73-112 (2010).
3. Xu, Y. et al. Targeted disruption of ATM leads to growth retardation, chromosomal fragmentation during meiosis, immune defects, and thymic lymphoma. Genes Dev. 10, 2411-2422 (1996).
4. Brown, E. J. & Baltimore, D. ATR disruption leads to chromosomal fragmentation and early embryonic lethality. Genes Dev. 14, 397-402 (2000).
5. Liu, Q. et al. Chk1 is an essential kinase that is regulated by Atr and required for the G(2)/M DNA damage checkpoint. Genes Dev. 14, 1448-1459 (2000).
6. Takai, H. et al. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J. 21, 5195-5205 (2002).
7. Gonzalez, S., Prives, C. & Cordon-Cardo, C. p73alpha regulation by Chk1 in response to DNA damage. Mol. Cell Biol. 23, 8161-8171 (2003).
8. Suzuki, H. et al. Lats2 phosphorylates p21/CDKN1A after UV irradiation and regulates apoptosis. J. Cell Sci. 126, 4358-4368 (2013).
9. Zhu, H., Kavsak, P., Abdollah, S., Wrana, J. L. & Thomsen, G. H. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400, 687-693 (1999).
10. Jin, Y. H. et al. Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation. J. Biol. Chem. 279, 29409-29417 (2004).
11. Narimatsu, M. et al. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 137, 295-307 (2009).
12. Ozdamar, B. et al. Regulation of the polarity protein Par6 by TGFbeta receptors controls epithelial cell plasticity. Science 307, 1603-1609 (2005).
13. Wang, H. R. et al. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302, 1775-1779 (2003).
14. Yamashita, M. et al. Ubiquitin ligase Smurf1 controls osteoblast activity and bone homeostasis by targeting MEKK2 for degradation. Cell 121, 101-113 (2005).
15. Zhao, M., Qiao, M., Oyajobi, B. O., Mundy, G. R. & Chen, D. E3 ubiquitin ligase Smurf1 mediates core-binding factor alpha1/Runx2 degradation and plays a specific role in osteoblast differentiation. J. Biol. Chem. 278, 27939-27944 (2003).
16. Wang, X., Jin, C., Tang, Y., Tang, L. Y. & Zhang, Y. E. Ubiquitination of tumor necrosis factor receptor-Associated factor 4 (TRAF4) by Smad ubiquitination regulatory factor 1 (Smurf1) regulates motility of breast epithelial and cancer cells. J. Biol. Chem. 288, 21784-21792 (2013).
17. Cao, Y. & Zhang, L. A Smurf1 tale: function and regulation of an ubiquitin ligase in multiple cellular networks. Cell Mol. Life Sci. 70, 2305-2317 (2013).
18. Birnbaum, D. J. et al. Genome profiling of pancreatic adenocarcinoma. Genes Chromosomes Cancer 50, 456-465 (2011).
19. Nie, J. et al. CKIP-1 acts as a colonic tumor suppressor by repressing oncogenic Smurf1 synthesis and promoting Smurf1 autodegradation. Oncogene 33, 3677-3687 (2014).
20. Suzuki, A. et al. Identification of SMURF1 as a possible target for 7q21.3-22.1 amplification detected in a pancreatic cancer cell line by in-house array-based comparative genomic hybridization. Cancer Sci. 99, 986-994 (2008).
21. Xie, P. et al. The covalent modifier Nedd8 is critical for the activation of Smurf1 ubiquitin ligase in tumorigenesis. Nat. Commun. 5, 3733 (2014).
22. Kwon, A., Lee, H. L., Woo, K. M., Ryoo, H. M. & Baek, J. H. SMURF1 plays a role in EGF-induced breast cancer cell migration and invasion. Mol. Cells 36, 548-555 (2013).
23. Kwei, K. A. et al. SMURF1 amplification promotes invasiveness in pancreatic cancer. PLoS ONE 6, e23924 (2011).
24. Fukunaga, E. et al. Smurf2 induces ubiquitin-dependent degradation of Smurf1 to prevent migration of breast cancer cells. J. Biol. Chem. 283, 35660-35667 (2008).
25. Sahai, E., Garcia-Medina, R., Pouyssegur, J. & Vial, E. Smurf1 regulates tumor cell plasticity and motility through degradation of RhoA leading to localized inhibition of contractility. J. Cell Biol. 176, 35-42 (2007).
26. Kaibuchi, K., Kuroda, S. & Amano, M. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68, 459-486 (1999).
27. Etienne-Manneville, S. & Hall, A. Rho GTPases in cell biology. Nature 420, 629-635 (2002).
28. Bustelo, X. R., Sauzeau, V. & Berenjeno, I. M. GTP-binding proteins of the Rho/ Rac family: regulation, effectors and functions in vivo. Bioessays 29, 356-370 (2007).
29. Jaffe, A. B. & Hall, A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269 (2005).
30. Wheeler, A. P. & Ridley, A. J. Why three Rho proteins?. RhoA, RhoB, RhoC, and cell motility. Exp. Cell Res. 301, 43-49 (2004).
31. Karlsson, R., Pedersen, E. D., Wang, Z. & Brakebusch, C. Rho GTPase function in tumorigenesis. Biochim. Biophys. Acta 1796, 91-98 (2009).
32. Adnane, J., Muro-Cacho, C., Mathews, L., Sebti, S. M. & Munoz-Antonia, T. Suppression of rho B expression in invasive carcinoma from head and neck cancer patients. Clin. Cancer Res. 8, 2225-2232 (2002).
33. Mazieres, J. et al. Loss of RhoB expression in human lung cancer progression. Clin. Cancer Res. 10, 2742-2750 (2004).
34. Zhou, J. et al. A distinct role of RhoB in gastric cancer suppression. Int. J. Cancer 128, 1057-1068 (2011).
35. Liu, Y. et al. Expression loss and revivification of RhoB gene in ovary carcinoma carcinogenesis and development. PLoS ONE 8, e78417 (2013).
36. Chen, Z. et al. Both farnesylated and geranylgeranylated RhoB inhibit malignant transformation and suppress human tumor growth in nude mice. J. Biol. Chem. 275, 17974-17978 (2000).
37. Couderc, B. et al. In vivo restoration of RhoB expression leads to ovarian tumor regression. Cancer Gene Ther. 15, 456-464 (2008).
38. Kim, B. K. et al. NSC126188, a piperazine alkyl derivative, induces apoptosis via upregulation of RhoB in HeLa cells. Invest. New Drugs 29, 853-860 (2011).
39. Liu, A. X., Rane, N., Liu, J. P. & Prendergast, G. C. RhoB is dispensable for mouse development, but it modifies susceptibility to tumor formation as well as cell adhesion and growth factor signaling in transformed cells. Mol. Cell Biol. 21, 6906-6912 (2001).
40. Liu, A. X., Cerniglia, G. J., Bernhard, E. J. & Prendergast, G. C. RhoB is required to mediate apoptosis in neoplastically transformed cells after DNA damage. Proc. Natl Acad. Sci. USA 98, 6192-6197 (2001).
41. Won, K. J. et al. NSC126188 induces apoptosis of prostate cancer PC-3 cells through inhibition of Akt membrane translocation, FoxO3a activation, and RhoB transcription. Apoptosis 19, 179-190 (2014).
42. Du, W. & Prendergast, G. C. Geranylgeranylated RhoB mediates suppression of human tumor cell growth by farnesyl transferase inhibitors. Cancer Res. 59, 5492-5496 (1999).
43. Kim, B. K. et al. Upregulation of RhoB via c-Jun N-Terminal kinase signaling induces apoptosis of the human gastric carcinoma NUGC-3 cells treated with NSC12618. Carcinogenesis 32, 254-261 (2011).
44. Liu, M. et al. miR-21 targets the tumor suppressor RhoB and regulates proliferation, invasion and apoptosis in colorectal cancer cells. FEBS Lett. 585, 2998-3005 (2011).
45. Kim, D. M. et al. RhoB induces apoptosis via direct interaction with TNFAIP1 in HeLa cells. Int. J. Cancer 125, 2520-2527 (2009).
46. Prendergast, G. C. Actin' up: RhoB in cancer and apoptosis. Nat. Rev. Cancer 1, 162-168 (2001).
47. Tian, M. et al. Binding of RhoA by the C2 domain of E3 ligase Smurf1 is essential for Smurf1-regulated RhoA ubiquitination and cell protrusive activity. FEBS Lett. 585, 2199-2204 (2011).
48. Fei, C. et al. Smurf1-mediated Lys29-linked nonproteolytic polyubiquitination of axin negatively regulates Wnt/beta-catenin signaling. Mol. Cell Biol. 33, 4095-4105 (2013).
49. Lin, H. et al. PKA/Smurf1 signaling-mediated stabilization of Nur77 is required for anticancer drug cisplatin-induced apoptosis. Oncogene 33, 1629-1639 (2014).
50. Ahn, J. et al. The activation of p38 MAPK primarily contributes to UV-induced RhoB expression by recruiting the c-Jun and p300 to the distal CCAAT box of the RhoB promoter. Biochem. Biophys. Res. Commun. 409, 211-216 (2011).
51. Fritz, G., Kaina, B. & Aktories, K. The ras-related small GTP-binding protein RhoB is immediate-early inducible by DNA damaging treatments. J. Biol. Chem. 270, 25172-25177 (1995).
52. Lu, K. et al. Pivotal role of the C2 domain of the Smurf1 ubiquitin ligase in substrate selection. J. Biol. Chem. 286, 16861-16870 (2011).
53. Patil, M., Pabla, N. & Dong, Z. Checkpoint kinase 1 in DNA damage response and cell cycle regulation. Cell Mol. Life Sci. 70, 4009-4021 (2013).
54. Perez-Sala, D., Boya, P., Ramos, I., Herrera, M. & Stamatakis, K. The C-Terminal sequence of RhoB directs protein degradation through an endolysosomal pathway. PLoS ONE 4, e8117 (2009).
55. Zalcman, G. et al. Regulation of Ras-related RhoB protein expression during the cell cycle. Oncogene 10, 1935-1945 (1995).
56. Jahner, D. & Hunter, T. The ras-related gene rhoB is an immediate-early gene inducible by v-Fps, epidermal growth factor, and platelet-derived growth factor in rat fibroblasts. Mol. Cell Biol. 11, 3682-3690 (1991).
57. Engel, M. E., Datta, P. K. & Moses, H. L. RhoB is stabilized by transforming growth factor beta and antagonizes transcriptional activation. J. Biol. Chem. 273, 9921-9926 (1998).
58. Nie, J. et al. Smad ubiquitylation regulatory factor 1/2 (Smurf1/2) promotes p53 degradation by stabilizing the E3 ligase MDM2. J. Biol. Chem. 285, 22818-22830 (2010).
59. Cotter, T. G. Apoptosis and cancer: the genesis of a research field. Nat. Rev. Cancer 9, 501-507 (2009).
60. Loukopoulos, P. et al. Genome-wide array-based comparative genomic hybridization analysis of pancreatic adenocarcinoma: identification of genetic indicators that predict patient outcome. Cancer Sci. 98, 392-400 (2007).
61. Wang, H. R. et al. Degradation of RhoA by Smurf1 ubiquitin ligase. Methods Enzymol. 406, 437-447 (2006).