Leptin-induced epithelial-mesenchymal transition in breast cancer cells requires β-catenin activation via Akt/GSK3- and MTA1/Wnt1 protein-dependent pathways

Journal of Biological Chemistry

Volumn 287, Issue 11, 2012, Pages 8598-8612

  Yan, Dan ^a   Avtanski, Dimiter ^b   Saxena, Neeraj K ^c   Sharma, Dipali ^b  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AKT ACTIVATION; BREAST CANCER CELLS; BREAST TUMOR; E-CADHERIN EXPRESSION; EPITHELIAL-MESENCHYMAL TRANSITION; FUNCTIONAL INTERACTION; GLYCOGEN SYNTHASE KINASE-3; IN-VIVO; NUCLEAR ACCUMULATION; NUCLEAR TRANSLOCATIONS; SIGNALING COMPONENTS; SMALL MOLECULE INHIBITOR; UNDERLYING MECHANISM; VIMENTIN;

ACTIVATION ANALYSIS; CELLS; PATHOLOGY; PHOSPHORYLATION; SPHERES; TUMORS;

HORMONES;

BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; ICG 001; LEPTIN; METASTASIS ASSOCIATED PROTEIN 1; PROTEIN INHIBITOR; PROTEIN KINASE B; TUMOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN; VIMENTIN; WNT1 PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; CANCER CELL CULTURE; CANCER INVASION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR TRANSPORT; MOLECULAR INTERACTION; MOUSE; NEOPLASM; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TUMOR SPHERE;

BETA CATENIN; BICYCLO COMPOUNDS, HETEROCYCLIC; BREAST NEOPLASMS; CADHERINS; CELL LINE, TUMOR; CELL NUCLEUS; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOGEN SYNTHASE KINASE 3; HISTONE DEACETYLASES; HUMANS; LEPTIN; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PYRIMIDINONES; REPRESSOR PROTEINS; VIMENTIN; WNT SIGNALING PATHWAY; WNT1 PROTEIN;

EID: 84858019563     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.322800     Document Type: Article

References (65)

1. Cirillo, D., Rachiglio, A. M., la Montagna, R., Giordano, A., and Normanno, N. (2008) Leptin signaling in breast cancer. An overview. J. Cell. Biochem. 105, 956-964
2. Grossmann, M. E., Ray, A., Nkhata, K. J., Malakhov, D. A., Rogozina, O. P., Dogan, S., and Cleary, M. P. (2010) Obesity and breast cancer. Status of leptin and adiponectin in pathological processes. Cancer Metastasis Rev. 29, 641-653
3. Guo, S., and Gonzalez-Perez, R. R. (2011) Notch, IL-1, and leptin crosstalk outcome (NILCO) is critical for leptin-induced proliferation, migration, and VEGF/VEGFR-2 expression in breast cancer. PLoS One 6, e21467
4. Ray, A., and Cleary, M. P. (2010) Leptin as a potential therapeutic target for breast cancer prevention and treatment. Expert Opin. Ther. Targets 14, 443-451
5. Artac, M., and Altundag, K. (2011) Leptin and breast cancer: an overview. Med. Oncol., in press
6. Knight, B. B., Oprea-Ilies, G. M., Nagalingam, A., Yang, L., Cohen, C., Saxena, N. K., and Sharma, D. (2011) Survivin up-regulation, dependent on leptin-EGFR-Notch1 axis, is essential for leptin-induced migration of breast carcinoma cells. Endocr. Relat. Cancer 18, 413-428
7. Garofalo, C., and Surmacz, E. (2006) Leptin and cancer. J. Cell. Physiol. 207, 12-22
8. Ahima, R. S., and Osei, S. Y. (2004) Leptin signaling. Physiol. Behav. 81, 223-241 (Pubitemid 38670089)
9. Ishikawa, M., Kitayama, J., and Nagawa, H. (2004) Enhanced expression of leptin and leptin receptor (OB-R) in human breast cancer. Clin. Cancer Res. 10, 4325-4331 (Pubitemid 38878870)
10. Garofalo, C., Koda, M., Cascio, S., Sulkowska, M., Kanczuga-Koda, L., Golaszewska, J., Russo, A., Sulkowski, S., and Surmacz, E. (2006) Increased expression of leptin and the leptin receptor as a marker of breast cancer progression. Possible role of obesity-related stimuli. Clin. Cancer Res. 12, 1447-1453
11. Tessitore, L., Vizio, B., Jenkins, O., De Stefano, I., Ritossa, C., Argiles, J. M., Benedetto, C., and Mussa, A. (2000) Leptin expression in colorectal and breast cancer patients. Int. J. Mol. Med. 5, 421-426
12. Cleary, M. P., Phillips, F. C., Getzin, S. C., Jacobson, T. L., Jacobson, M. K., Christensen, T. A., Juneja, S. C., Grande, J. P., and Maihle, N. J. (2003) Genetically obese MMTV-TGF-α/Lep(ob)Lep(ob) female mice do not develop mammary tumors. Breast Cancer Res. Treat. 77, 205-215 (Pubitemid 36197635)
13. Cleary, M. P., Juneja, S. C., Phillips, F. C., Hu, X., Grande, J. P., and Maihle, N. J. (2004) Leptin receptor-deficient MMTV-TGF-α/Lepr(db) Lepr(db) female mice do not develop oncogene-induced mammary tumors. Exp. Biol. Med. 229, 182-193 (Pubitemid 38146562)
14. Chua, S. C., Jr., Liu, S. M., Li, Q., Sun, A., DeNino, W. F., Heymsfield, S. B., and Guo, X. E. (2004) Transgenic complementation of leptin receptor deficiency. II. Increased leptin receptor transgene dose effects on obesity/diabetes and fertility/lactation in lepr-db/db mice. Am. J. Physiol. Endocrinol. Metab. 286, E384-E392 (Pubitemid 38292688)
15. Park, J., Kusminski, C. M., Chua, S. C., and Scherer, P. E. (2010) Leptin receptor signaling supports cancer cell metabolism through suppression of mitochondrial respiration in vivo. Am. J. Pathol. 177, 3133-3144
16. Dogan, S., Hu, X., Zhang, Y., Maihle, N. J., Grande, J. P., and Cleary, M. P. (2007) Effects of high fat diet and/or body weight on mammary tumor leptin and apoptosis signaling pathways in MMTV-TGF-α mice. Breast Cancer Res. 9, R91
17. Nunez, N. P., Perkins, S. N., Smith, N. C., Berrigan, D., Berendes, D. M., Varticovski, L., Barrett, J. C., and Hursting, S. D. (2008) Obesity accelerates mouse mammary tumor growth in the absence of ovarian hormones. Nutr. Cancer 60, 534-541 (Pubitemid 351918549)
18. Zheng, Q., Dunlap, S. M., Zhu, J., Downs-Kelly, E., Rich, J., Hursting, S. D., Berger, N. A., and Reizes, O. (2011) Leptin deficiency suppresses MMTV-Wnt-1 mammary tumor growth in obese mice and abrogates tumor initiating cell survival. Endocr. Relat. Cancer 18, 491-503
19. Saxena, N. K., Vertino, P. M., Anania, F. A., and Sharma, D. (2007) Leptininduced growth stimulation of breast cancer cells involves recruitment of histone acetyltransferases and mediator complex to CYCLIN D1 promoter via activation of Stat3. J. Biol. Chem. 282, 13316-13325 (Pubitemid 47100545)
20. Saxena, N. K., Sharma, D., Ding, X., Lin, S., Marra, F., Merlin, D., and Anania, F. A. (2007) Concomitant activation of the JAK/STAT, PI3K/AKT, and ERK signaling is involved in leptin-mediated promotion of invasion and migration of hepatocellular carcinoma cells. Cancer Res. 67, 2497-2507 (Pubitemid 46548934)
21. Saxena, N. K., Taliaferro-Smith, L., Knight, B. B., Merlin, D., Anania, F. A., O'Regan, R. M., and Sharma, D. (2008) Bidirectional cross-talk between leptin and insulin-like growth factor-I signaling promotes invasion and migration of breast cancer cells via transactivation of epidermal growth factor receptor. Cancer Res. 68, 9712-9722
22. Gonzalez, R. R., and Leavis, P. (2001) Leptin up-regulates αβ3-integrin expression and interleukin-1β, up-regulates leptin and leptin receptor expression in human endometrial epithelial cell cultures. Endocrine 16, 21-28 (Pubitemid 34017049)
23. Pinteaux, E., Inoue, W., Schmidt, L., Molina-Holgado, F., Rothwell, N. J., and Luheshi, G. N. (2007) Leptin induces interleukin-1β release from rat microglial cells through a caspase 1-independent mechanism. J. Neurochem. 102, 826-833 (Pubitemid 47057280)
24. Gonzalez, R. R., Devoto, L., Campana, A., and Bischof, P. (2001) Effects of leptin, interleukin-1β, interleukin-6, and transforming growth factor-α on markers of trophoblast invasive phenotype. Integrins and metalloproteinases. Endocrine 15, 157-164 (Pubitemid 32977325)
25. Gonzalez, R. R., Cherfils, S., Escobar, M., Yoo, J. H., Carino, C., Styer, A. K., Sullivan, B. T., Sakamoto, H., Olawaiye, A., Serikawa, T., Lynch, M. P., and Rueda, B. R. (2006) Leptin signaling promotes the growth of mammary tumors and increases the expression of vascular endothelial growth factor (VEGF) and its receptor type two (VEGF-R2). J. Biol. Chem. 281, 26320-26328 (Pubitemid 44401840)
26. Fusco, R., Galgani, M., Procaccini, C., Franco, R., Pirozzi, G., Fucci, L., Laccetti, P., and Matarese, G. (2010) Cellular and molecular cross-talk between leptin receptor and estrogen receptor-α in breast cancer. Molecular basis for a novel therapeutic setting. Endocr. Relat. Cancer 17, 373-382
27. Thiery, J. P. (2002) Epithelial-mesenchymal transitions in tumor progression. Nat. Rev. Cancer 2, 442-454
28. Yang, J., Mani, S. A., Donaher, J. L., Ramaswamy, S., Itzykson, R. A., Come, C., Savagner, P., Gitelman, I., Richardson, A., and Weinberg, R. A. (2004) Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117, 927-939 (Pubitemid 38798858)
29. Vernon, A. E., and LaBonne, C. (2004) Tumor metastasis. A new twist on epithelial-mesenchymal transitions. Curr. Biol. 14, R719-R721 (Pubitemid 39290047)
30. Hajra, K. M., Chen, D. Y., and Fearon, E. R. (2002) The SLUG zinc-finger protein represses E-cadherin in breast cancer. Cancer Res. 62, 1613-1618 (Pubitemid 34408479)
31. Cano, A., Pérez-Moreno, M. A., Rodrigo, I., Locascio, A., Blanco, M. J., del Barrio, M. G., Portillo, F., and Nieto, M. A. (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat. Cell Biol. 2, 76-83
32. Li, J., and Zhou, B. P. (2011) Activation of β-catenin and Akt pathways by Twist are critical for the maintenance of EMT-associated cancer stem cell-like characters. BMC Cancer 11, 49
33. Kanwar, S. S., Yu, Y., Nautiyal, J., Patel, B. B., and Majumdar, A. P. (2010) The Wnt/β-catenin pathway regulates growth and maintenance of colonospheres. Mol. Cancer 9, 212
34. Yang, A. D., Camp, E. R., Fan, F., Shen, L., Gray, M. J., Liu, W., Somcio, R., Bauer, T. W., Wu, Y., Hicklin, D. J., and Ellis, L. M. (2006) Vascular endothelial growth factor receptor-1 activation mediates epithelial to mesenchymal transition in human pancreatic carcinoma cells. Cancer Res. 66, 46-51 (Pubitemid 43166007)
35. Sharma, D., Wang, J., Fu, P. P., Sharma, S., Nagalingam, A., Mells, J., Handy, J., Page, A. J., Cohen, C., Anania, F. A., and Saxena, N. K. (2010) Adiponectin antagonizes the oncogenic actions of leptin in hepatocellular carcinogenesis. Hepatology 52, 1713-1722
36. Taliaferro-Smith, L., Nagalingam, A., Zhong, D., Zhou, W., Saxena, N. K., and Sharma, D. (2009) LKB1 is required for adiponectin-mediated modulation of AMPK-S6K axis and inhibition of migration and invasion of breast cancer cells. Oncogene 28, 2621-2633
37. Sharma, D., and Fondell, J. D. (2002) Ordered recruitment of histone acetyltransferases and the TRAP-Mediator complex to thyroid hormone-responsive promoters in vivo. Proc. Natl. Acad. Sci. U.S.A. 99, 7934-7939 (Pubitemid 34650983)
38. Tomaskovic-Crook, E., Thompson, E. W., and Thiery, J. P. (2009) Epithelial to mesenchymal transition and breast cancer. Breast Cancer Res. 11, 213
39. Hugo, H., Ackland, M. L., Blick, T., Lawrence, M. G., Clements, J. A., Williams, E. D., and Thompson, E. W. (2007) Epithelial-mesenchymal and mesenchymal-epithelial transitions in carcinoma progression. J. Cell. Physiol. 213, 374-383 (Pubitemid 47509716)
40. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C., Shipitsin, M., Campbell, L. L., Polyak, K., Brisken, C., Yang, J., and Weinberg, R. A. (2008) The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715 (Pubitemid 351636299)
41. Morel, A. P., Lièvre, M., Thomas, C., Hinkal, G., Ansieau, S., and Puisieux, A. (2008) Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 3, e2888
42. Santisteban, M., Reiman, J. M., Asiedu, M. K., Behrens, M. D., Nassar, A., Kalli, K. R., Haluska, P., Ingle, J. N., Hartmann, L. C., Manjili, M. H., Radisky, D. C., Ferrone, S., and Knutson, K. L. (2009) Immune-induced epithelial to mesenchymal transition in vivo generates breast cancer stem cells. Cancer Res. 69, 2887-2895
43. Creighton, C. J., Li, X., Landis, M., Dixon, J. M., Neumeister, V. M., Sjolund, A., Rimm, D. L., Wong, H., Rodriguez, A., Herschkowitz, J. I., Fan, C., Zhang, X., He, X., Pavlick, A., Gutierrez, M. C., Renshaw, L., Larionov, A. A., Faratian, D., Hilsenbeck, S. G., Perou, C. M., Lewis, M. T., Rosen, J. M., and Chang, J. C. (2009) Residual breast cancers after conventional therapy display mesenchymal as well as tumor-initiating features. Proc. Natl. Acad. Sci. U.S.A. 106, 13820-13825
44. Brennan, K. R., and Brown, A. M. (2004) Wnt proteins in mammary development and cancer. J. Mammary Gland. Biol. Neoplasia 9, 119-131 (Pubitemid 39177498)
45. Turashvili, G., Bouchal, J., Burkadze, G., and Kolar, Z. (2006) Wnt signaling pathway in mammary gland development and carcinogenesis. Pathobiology 73, 213-223 (Pubitemid 46332829)
46. Lin, S. Y., Xia, W., Wang, J. C., Kwong, K. Y., Spohn, B., Wen, Y., Pestell, R. G., and Hung, M. C. (2000) β-Catenin, a novel prognostic marker for breast cancer. Its roles in cyclin D1 expression and cancer progression. Proc. Natl. Acad. Sci. U.S.A. 97, 4262-4266 (Pubitemid 30226121)
47. Nakopoulou, L., Mylona, E., Papadaki, I., Kavantzas, N., Giannopoulou, I., Markaki, S., and Keramopoulos, A. (2006) Study of phospho-β-catenin subcellular distribution in invasive breast carcinomas in relation to their phenotype and the clinical outcome. Mod. Pathol. 19, 556-563
48. Candidus, S., Bischoff, P., Becker, K. F., and Höfler, H. (1996) No evidence for mutations in the α- and β-catenin genes in human gastric and breast carcinomas. Cancer Res. 56, 49-52 (Pubitemid 26011460)
49. Micalizzi, D. S., Farabaugh, S. M., and Ford, H. L. (2010) Epithelial-mesenchymal transition in cancer. Parallels between normal development and tumor progression. J. Mammary Gland. Biol. Neoplasia 15, 117-134
50. Moon, R. T., Bowerman, B., Boutros, M., and Perrimon, N. (2002) The promise and perils of Wnt signaling through β-catenin. Science 296, 1644-1646 (Pubitemid 34579151)
51. Jope, R. S., and Johnson, G. V. (2004) The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 29, 95-102 (Pubitemid 38186580)
52. Kimelman, D., and Xu, W. (2006) β-Catenin destruction complex. Insights and questions from a structural perspective. Oncogene 25, 7482-7491 (Pubitemid 44885747)
53. Cadigan, K. M., and Liu, Y. I. (2006) Wnt signaling. Complexity at the surface. J. Cell Sci. 119, 395-402
54. Kumar, R., Balasenthil, S., Pakala, S. B., Rayala, S. K., Sahin, A. A., and Ohshiro, K. (2010) Metastasis-associated protein 1 short form stimulates Wnt1 pathway in mammary epithelial and cancer cells. Cancer Res. 70, 6598-6608
55. Kumar, R., Balasenthil, S., Manavathi, B., Rayala, S. K., and Pakala, S. B. (2010) Metastasis-associated protein 1 and its short form variant stimulates Wnt1 transcription through promoting its derepression from Six3 corepressor. Cancer Res. 70, 6649-6658
56. Singh, R. R., and Kumar, R. (2007) MTA family of transcriptional metaregulators in mammary gland morphogenesis and breast cancer. J. Mammary Gland. Biol. Neoplasia 12, 115-125 (Pubitemid 47215429)
57. Emami, K. H., Nguyen, C., Ma, H., Kim, D. H., Jeong, K. W., Eguchi, M., Moon, R. T., Teo, J. L., Oh, S. W., Kim, H. Y., Moon, S. H., Ha, J. R., and Kahn, M. (2004) A small molecule inhibitor of β-catenin/CREB-binding protein transcription [corrected]. Proc. Natl. Acad. Sci. U.S.A. 101, 12682-12687 (Pubitemid 39122083)
58. Henderson, W. R., Jr., Chi, E. Y., Ye, X., Nguyen, C., Tien, Y. T., Zhou, B., Borok, Z., Knight, D. A., and Kahn, M. (2010) Inhibition of Wnt/β-catenin/CREB binding protein (CBP) signaling reverses pulmonary fibrosis. Proc. Natl. Acad. Sci. U.S.A. 107, 14309-14314
59. Creighton, C. J., Chang, J. C., and Rosen, J. M. (2010) Epithelial-mesenchymal transition (EMT) in tumor-initiating cells and its clinical implications in breast cancer. J. Mammary Gland. Biol. Neoplasia 15, 253-260
60. McMurtry, V., Simeone, A. M., Nieves-Alicea, R., and Tari, A. M. (2009) Leptin utilizes Jun N-terminal kinases to stimulate the invasion of MCF-7 breast cancer cells. Clin. Exp. Metastasis 26, 197-204
61. Hao, S., He, W., Li, Y., Ding, H., Hou, Y., Nie, J., Hou, F. F., Kahn, M., and Liu, Y. (2011) Targeted inhibition of β-catenin/CBP signaling ameliorates renal interstitial fibrosis. J. Am. Soc. Nephrol. 22, 1642-1653
62. McManus, E. J., Sakamoto, K., Armit, L. J., Ronaldson, L., Shpiro, N., Marquez, R., and Alessi, D. R. (2005) Role that phosphorylation of GSK3 plays in insulin and Wnt signaling defined by knock-in analysis. EMBO J. 24, 1571-1583 (Pubitemid 40646447)
63. Lagutin, O. V., Zhu, C. C., Kobayashi, D., Topczewski, J., Shimamura, K., Puelles, L., Russell, H. R., McKinnon, P. J., Solnica-Krezel, L., and Oliver, G. (2003) Six3 repression of Wnt signaling in the anterior neuroectoderm is essential for vertebrate forebrain development. Genes Dev. 17, 368-379 (Pubitemid 36182196)
64. Zhu, C. C., Dyer, M. A., Uchikawa, M., Kondoh, H., Lagutin, O. V., and Oliver, G. (2002) Six3-mediated autorepression and eye development requires its interaction with members of the Groucho-related family of corepressors. Development 129, 2835-2849 (Pubitemid 34874264)
65. Gertler, A. (2006) Development of leptin antagonists and their potential use in experimental biology and medicine. Trends Endocrinol. Metab. 17, 372-378