Quantitative proteomics profiling of murine mammary gland cells unravels impact of annexin-1 on DNA damage response, cell adhesion, and migration

Molecular and Cellular Proteomics

Volumn 11, Issue 8, 2012, Pages 381-393

  Swa, Hannah L F ^a,b   Blackstock, Walter P ^a   Lim, Lina H K ^b   Gunaratne, Jayantha ^a  

^a INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; LIPOCORTIN 1; TRANSCRIPTION FACTOR YAP1;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; BREAST CANCER; BREAST CELL; CELL ADHESION; CELL CULTURE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; EPITHELIUM CELL; GENE OVEREXPRESSION; HEAT STRESS; MAMMARY GLAND; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; QUANTITATIVE STUDY; UPREGULATION; WOUND HEALING;

ANIMALS; ANNEXIN A1; BLOTTING, WESTERN; CELL ADHESION; CELL MOVEMENT; CELLS, CULTURED; COMET ASSAY; DNA DAMAGE; EPITHELIAL CELLS; FEMALE; HUMANS; HYDROGEN PEROXIDE; ISOTOPE LABELING; MAMMARY GLANDS, ANIMAL; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OXIDANTS; PEPTIDES; PROTEOME; PROTEOMICS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

MURINAE; MUS;

EID: 84864812287     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M111.011205     Document Type: Article

References (63)

1. Crompton, M. R., Moss, S. E., and Crumpton, M. J. (1988) Diversity in the lipocortin/calpactin family. Cell 55, 1-3
2. Perretti, M., and D'Acquisto, F. (2009) Annexin A1 and glucocorticoids as effectors of the resolution of inflammation. Nat. Rev. Immunol. 9, 62-70
3. Wallner, B. P., Mattaliano, R. J., Hession, C., Cate, R. L., Tizard, R., Sinclair, L. K., Foeller, C., Chow, E. P., Browing, J. L., Ramachandran, K. L., and Pepinsky, B. R. (1986) Cloning and expression of human lipocortin, a phospholipase A2 inhibitor with potential anti-inflammatory activity. Nature 320, 77-81
4. De, B. K., Misono, K. S., Lukas, T. J., Mroczkowski, B., and Cohen, S. (1986) A calcium-dependent 35-kilodalton substrate for epidermal growth factor receptor/kinase isolated from normal tissue. J. Biol. Chem. 261, 13784-13792
5. Alldridge, L. C., Harris, H. J., Plevin, R., Hannon, R., and Bryant, C. E. (1999) The annexin protein lipocortin 1 regulates the MAPK/ERK pathway. J. Biol. Chem. 274, 37620-37628
6. Arur, S., Uche, U. E., Rezaul, K., Fong, M., Scranton, V., Cowan, A. E., Mohler, W., and Han, D. K. (2003) Annexin I is an endogenous ligand that mediates apoptotic cell engulfment. Dev. Cell 4, 587-598
7. Lim, L. H., and Pervaiz, S. (2007) Annexin 1: The new face of an old molecule. FASEB J. 21, 968-975
8. Hu, N., Flaig, M. J., Su, H., Shou, J. Z., Roth, M. J., Li, W. J., Wang, C., Goldstein, A. M., Li, G., Emmert-Buck, M. R., and Taylor, P. R. (2004) Comprehensive characterization of annexin I alterations in esophageal squamous cell carcinoma. Clin. Cancer Res. 10, 6013-6022
9. Xin, W., Rhodes, D. R., Ingold, C., Chinnaiyan, A. M., and Rubin, M. A. (2003) Dysregulation of the annexin family protein family is associated with prostate cancer progression. Am. J. Pathol. 162, 255-261
10. Garcia Pedrero, J. M., Fernandez, M. P., Morgan, R. O., Herrero Zapatero, A., Gonzalez, M. V., Suarez Nieto, C., and Rodrigo, J. P. (2004) Annexin A1 down-regulation in head and neck cancer is associated with epithelial differentiation status. Am. J. Pathol. 164, 73-79
11. de Coupade, C., Gillet, R., Bennoun, M., Briand, P., Russo-Marie, F., and Solito, E. (2000) Annexin 1 expression and phosphorylation are upregulated during liver regeneration and transformation in antithrombin III SV40 T large antigen transgenic mice. Hepatology 31, 371-380
12. Bai, X. F., Ni, X. G., Zhao, P., Liu, S. M., Wang, H. X., Guo, B., Zhou, L. P., Liu, F., Zhang, J. S., Wang, K., Xie, Y. Q., Shao, Y. F., and Zhao, X. H. (2004) Overexpression of annexin 1 in pancreatic cancer and its clinical significance. World J. Gastroenterol. 10, 1466-1470
13. Yi, M., and Schnitzer, J. E. (2009) Impaired tumor growth, metastasis, angiogenesis and wound healing in annexin A1-null mice. Proc. Natl. Acad. Sci. U.S.A. 106, 17886-17891
14. de Graauw, M., van Miltenburg, M. H., Schmidt, M. K., Pont, C., Lalai, R., Kartopawiro, J., Pardali, E., Le Dévédec, S. E., Smit, V. T., van der Wal, A., Van't Veer, L. J., Cleton-Jansen, A. M., ten Dijke, P., and van de Water, B. (2010) Annexin A1 regulates TGF-β signaling and promotes metastasis formation of basal-like breast cancer cells. Proc. Natl. Acad. Sci. U.S.A. 107, 6340-6345
15. Bist, P., Leow, S. C., Phua, Q. H., Shu, S., Zhuang, Q., Loh, W. T., Nguyen, T. H., Zhou, J. B., Hooi, S. C., and Lim, L. H. (2011) Annexin-1 interacts with NEMO and RIP1 to constitutively activate IKK complex and NF-κB: Implication in breast cancer metastasis. Oncogene 30, 3174-3185
16. Rhee, D. K., Park, S. H., and Jang, Y. K. (2008) Molecular signatures associated with transformation and progression to breast cancer in the isogenic MCF10 model. Genomics 92, 419-428
17. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1, 376-386
18. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860
19. Cox, J., and Mann, M. (2008) MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26, 1367-1372
20. Cox, J., Matic, I., Hilger, M., Nagaraj, N., Selbach, M., Olsen, J. V., and Mann, M. (2009) A practical guide to the MaxQuant computational platform for SILAC-based quantitative proteomics. Nat. Protoc. 4, 698-705
21. Beere, H. M., Wolf, B. B., Cain, K., Mosser, D. D., Mahboubi, A., Kuwana, T., Tailor, P., Morimoto, R. I., Cohen, G. M., and Green, D. R. (2000) Heat-shock protein 70 inhibits apoptosis by preventing recruitment of procaspase-9 to the Apaf-1 apoptosome. Nat. Cell Biol. 2, 469-475
22. Takahashi, A., Matsumoto, H., Nagayama, K., Kitano, M., Hirose, S., Tanaka, H., Mori, E., Yamakawa, N., Yasumoto, J., Yuki, K., Ohnishi, K., and Ohnishi, T. (2004) Evidence for the involvement of double-strand breaks in heat-induced cell killing. Cancer Res. 64, 8839-8845
23. Greenbaum, D., Colangelo, C., Williams, K., and Gerstein, M. (2003) Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol. 4, 117
24. Strano, S., Monti, O., Pediconi, N., Baccarini, A., Fontemaggi, G., Lapi, E., Mantovani, F., Damalas, A., Citro, G., Sacchi, A., Del Sal, G., Levrero, M., and Blandino, G. (2005) The transcriptional coactivator Yes-associated protein drives p73 gene-target specificity in response to DNA Damage. Mol. Cell 18, 447-459
25. Levy, D., Adamovich, Y., Reuven, N., and Shaul, Y. (2007) The Yes-associated protein 1 stabilizes p73 by preventing Itch-mediated ubiquitination of p73. Cell Death Differ. 14, 743-751
26. Kastan, M. B., Canman, C. E., and Leonard, C. J. (1995) p53, cell cycle control and apoptosis: Implications for cancer. Cancer Metastasis Rev. 14, 3-15
27. Wei, C. L., Wu, Q., Vega, V. B., Chiu, K. P., Ng, P., Zhang, T., Shahab, A., Yong, H. C., Fu, Y., Weng, Z., Liu, J., Zhao, X. D., Chew, J. L., Lee, Y. L., Kuznetsov, V. A., Sung, W. K., Miller, L. D., Lim, B., Liu, E. T., Yu, Q., Ng, H. H., and Ruan, Y. (2006) A global map of p53 transcription-factor binding sites in the human genome. Cell 124, 207-219
28. Kastan, M. B., Onyekwere, O., Sidransky, D., Vogelstein, B., and Craig, R. W. (1991) Participation of p53 protein in the cellular response to DNA damage. Cancer Res. 51, 6304-6311
29. García-Cao, I., García-Cao, M., Martín-Caballero, J., Criado, L. M., Klatt, P., Flores, J. M., Weill, J. C., Blasco, M. A., and Serrano, M. (2002) "Super p53" mice exhibit enhanced DNA damage response, are tumor resistant and age normally. EMBO J. 21, 6225-6235
30. Sharpless, N. E., and DePinho, R. A. (1999) The INK4A/ARF locus and its two gene products. Curr. Opin. Genet. Dev. 9, 22-30
31. Sherr, C. J. (1998) Tumor surveillance via the ARF-p53 pathway. Genes Dev. 12, 2984-2991
32. Frosina, G., Fortini, P., Rossi, O., Carrozzino, F., Raspaglio, G., Cox, L. S., Lane, D. P., Abbondandolo, A., and Dogliotti, E. (1996) Two pathways for base excision repair in mammalian cells. J. Biol. Chem. 271, 9573-9578
33. Nair, S., Hande, M. P., and Lim, L. H. (2010) Annexin-1 protects MCF7 breast cancer cells against heat-induced growth arrest and DNA damage. Cancer Lett. 294, 111-117
34. Fadeel, B., Ottosson, A., and Pervaiz, S. (2008) Big wheel keeps on turning: Apoptosome regulation and its role in chemoresistance. Cell Death Differ. 15, 443-452
35. Zha, J., Weiler, S., Oh, K. J., Wei, M. C., and Korsmeyer, S. J. (2000) Posttranslational N-myristoylation of BID as a molecular switch for targeting mitochondria and apoptosis. Science 290, 1761-1765
36. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998) Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490
37. Li, H., Zhu, H., Xu, C. J., and Yuan, J. (1998) Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501
38. Petrella, A., Festa, M., Ercolino, S. F., Zerilli, M., Stassi, G., Solito, E., and Parente, L. (2005) Induction of annexin-1 during TRAIL-induced apoptosis in thyroid carcinoma cells. Cell Death Differ. 12, 1358-1360
39. Solito, E., Kamal, A., Russo-Marie, F., Buckingham, J. C., Marullo, S., and Perretti, M. (2003) A novel calcium-dependent proapoptotic effect of annexin 1 on human neutrophils. FASEB J. 17, 1544-1546
40. Wiseman, H., and Halliwell, B. (1996) Damage to DNA by reactive oxygen and nitrogen species: Role in inflammatory disease and progression to cancer. Biochem. J. 313, 17-29
41. Shaw, T. J., and Martin, P. (2009) Wound repair at a glance. J. Cell Sci. 122, 3209-3213
42. Perretti, M., and Gavins, F. N. (2003) Annexin 1: An endogenous antiinflammatory protein. News Physiol. Sci. 18, 60-64
43. Parente, L., and Solito, E. (2004) Annexin 1: More than an anti-phospholipase protein. Inflamm. Res. 53, 125-132
44. Lim, L. H., Solito, E., Russo-Marie, F., Flower, R. J., and Perretti, M. (1998) Promoting detachment of neutrophils adherent to murine postcapillary venules to control inflammation: Effect of lipocortin 1. Proc. Natl. Acad. Sci. U.S.A. 95, 14535-14539
45. Mancuso, F., Flower, R. J., and Perretti, M. (1995) Leukocyte transmigration, but not rolling or adhesion, is selectively inhibited by dexamethasone in the hamster post-capillary venule. Involvement of endogenous lipocortin 1. J. Immunol. 155, 377-386
46. Strausbaugh, H. J., and Rosen, S. D. (2001) A potential role for annexin 1 as a physiologic mediator of glucocorticoid-induced L-selectin shedding from myeloid cells. J. Immunol. 166, 6294-6300
47. de Coupade, C., Solito, E., and Levine, J. D. (2003) Dexamethasone enhances interaction of endogenous annexin 1 with L-selectin and triggers shedding of L-selectin in the monocytic cell line U-937. Br. J. Pharmacol. 140, 133-145
48. Babbin, B. A., Lee, W. Y., Parkos, C. A., Winfree, L. M., Akyildiz, A., Perretti, M., and Nusrat, A. (2006) Annexin I regulates SKCO-15 cell invasion by signaling through formyl peptide receptors. J. Biol. Chem. 281, 19588-19599
49. Lauffenburger, D. A., and Horwitz, A. F. (1996) Cell migration: A physically integrated molecular process. Cell 84, 359-369
50. Nieves, B., Jones, C. W., Ward, R., Ohta, Y., Reverte, C. G., and LaFlamme, S. E. (2010) The NPIY motif in the integrin β1 tail dictates the requirement for talin-1 in outside-in signaling. J. Cell Sci. 123, 1216-1226
51. Zhang, X., Jiang, G., Cai, Y., Monkley, S. J., Critchley, D. R., and Sheetz, M. P. (2008) Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat. Cell Biol. 10, 1062-1068
52. Yamaji, S., Suzuki, A., Kanamori, H., Mishima, W., Yoshimi, R., Takasaki, H., Takabayashi, M., Fujimaki, K., Fujisawa, S., Ohno, S., and Ishigatsubo, Y. (2004) Affixin interacts with α-actinin and mediates integrin signaling for reorganization of F-actin induced by initial cell-substrate interaction. J. Cell Biol. 165, 539-551
53. Matsuda, C., Kameyama, K., Suzuki, A., Mishima, W., Yamaji, S., Okamoto, H., Nishino, I., and Hayashi, Y. K. (2008) Affixin activates Rac1 via βPIX in C2C12 myoblast. FEBS Lett. 582, 1189-1196
54. Sepulveda, J. L., and Wu, C. (2006) The parvins. Cell Mol Life Sci 63, 25-35
55. Mongroo, P. S., Johnstone, C. N., Naruszewicz, I., Leung-Hagesteijn, C., Sung, R. K., Carnio, L., Rustgi, A. K., and Hannigan, G. E. (2004) β-Parvin inhibits integrin-linked kinase signaling and is downregulated in breast cancer. Oncogene 23, 8959-8970
56. Zaman, M. H., Trapani, L. M., Sieminski, A. L., Mackellar, D., Gong, H., Kamm, R. D., Wells, A., Lauffenburger, D. A., and Matsudaira, P. (2006) Migration of tumor cells in 3D matrices is governed by matrix stiffness along with cell-matrix adhesion and proteolysis. Proc. Natl. Acad. Sci. U.S.A. 103, 10889-10894
57. Andl, C. D., Mizushima, T., Oyama, K., Bowser, M., Nakagawa, H., and Rustgi, A. K. (2004) EGFR-induced cell migration is mediated predominantly by the JAK-STAT pathway in primary esophageal keratinocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 287, G1227-G1237
58. Verbeek, B. S., Adriaansen-Slot, S. S., Vroom, T. M., Beckers, T., and Rijksen, G. (1998) Overexpression of EGFR and c-erbB2 causes enhanced cell migration in human breast cancer cells and NIH3T3 fibroblasts. FEBS Lett. 425, 145-150
59. Xie, H., Pallero, M. A., Gupta, K., Chang, P., Ware, M. F., Witke, W., Kwiatkowski, D. J., Lauffenburger, D. A., Murphy-Ullrich, J. E., and Wells, A. (1998) EGF receptor regulation of cell motility: EGF induces disassembly of focal adhesions independently of the motility-associated PLCγ signaling pathway. J. Cell Sci. 111, 615-624
60. Nagase, H., and Woessner, J. F., Jr. (1999) Matrix metalloproteinases. J. Biol. Chem. 274, 21491-21494
61. Nagakawa, O., Murakami, K., Yamaura, T., Fujiuchi, Y., Murata, J., Fuse, H., and Saiki, I. (2000) Expression of membrane-type 1 matrix metalloproteinase (MT1-MMP) on prostate cancer cell lines. Cancer Lett. 155, 173-179
62. Nomura, H., Sato, H., Seiki, M., Mai, M., and Okada, Y. (1995) Expression of membrane-type matrix metalloproteinase in human gastric carcinomas. Cancer Res. 55, 3263-3266
63. Singh, S., Singh, U. P., Grizzle, W. E., and Lillard, J. W., Jr. (2004) CXCL12- CXCR4 interactions modulate prostate cancer cell migration, metalloproteinase expression and invasion. Lab. Invest. 84, 1666-1676