Estrogen receptor (er)α-regulated lipocalin 2 expression in adipose tissue links obesity with breast cancer progression

Journal of Biological Chemistry

Volumn 290, Issue 9, 2015, Pages 5566-5581

  Drew, Brian G ^a,f   Hamidi, Habib ^a   Zhou, Zhenqi ^a   Villanueva, Claudio J ^b,g   Krum, Susan A ^b,h   Calkin, Anna C ^b,i   Parks, Brian W ^b   Ribas, Vicent ^a   Kalajian, Nareg Y ^a   Phun, Jennifer ^a   Daraei, Pedram ^a   Christofk, Heather R ^a   Hewitt, Sylvia C ^c   Korach, Kenneth S ^c   Tontonoz, Peter ^b   Lusis, Aldons J ^a   Slamon, Dennis J ^a,d   Hurvitz, Sara A ^a,d   Hevener, Andrea L ^a,e  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NATIONAL INSTITUTES OF HEALTH   (United States)

^d Translational Oncology Research International   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f MONASH UNIVERSITY   (Australia)

^g UNIVERSITY OF UTAH   (United States)

^h UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

ⁱ BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; DISEASES; MAMMALS; METABOLISM; MOLECULAR WEIGHT; NUTRITION; TUMORS;

3-HYDROXYBUTYRATE DEHYDROGENASE; CHROMATIN IMMUNOPRECIPITATION; CONDITIONED MEDIUM; ESTROGEN RECEPTOR; MICROENVIRONMENTS; SIGNALING PATHWAYS; TISSUE EXPRESSION; TISSUE SPECIFICS;

CELL SIGNALING;

2 HYDROXYBUTYRATE DEHYDROGENASE; ESTROGEN RECEPTOR ALPHA; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN; ACUTE PHASE PROTEIN; LCN2 PROTEIN, MOUSE; LIPOCALIN; ONCOPROTEIN; PROTEIN BINDING;

ADIPOSE TISSUE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BDH2 GENE; BREAST BIOPSY; BREAST CANCER; BREAST CARCINOGENESIS; CANCER GROWTH; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CELL SIZE; CELLS BY BODY ANATOMY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DISEASE ASSOCIATION; DISEASE SEVERITY; FEMALE; GENE DELETION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LCN2 GENE; MALE; MOUSE; NEUTROPHIL GELATINASE ASSOCIATED LIPOCALIN BLOOD LEVEL; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT; 3T3 CELL LINE; ADIPOCYTE; ANIMAL; BLOOD; BREAST TUMOR; C57BL MOUSE; CELL MOTION; CYTOLOGY; DISEASE COURSE; GENE EXPRESSION PROFILING; GENETICS; HEK293 CELL LINE; IMMUNOBLOTTING; KNOCKOUT MOUSE; METABOLISM; MOUSE MUTANT; PATHOLOGY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

MUS;

3T3-L1 CELLS; ACUTE-PHASE PROTEINS; ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL MOVEMENT; CELL PROLIFERATION; DISEASE PROGRESSION; ESTROGEN RECEPTOR ALPHA; FEMALE; GENE EXPRESSION PROFILING; HEK293 CELLS; HUMANS; IMMUNOBLOTTING; LIPOCALINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, OBESE; OBESITY; ONCOGENE PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84923872915     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.606459     Document Type: Article

References (60)

1. Romeo, G. R., Lee, J., and Shoelson, S. E. (2012) Metabolic syndrome, insulin resistance, and roles of inflammation: mechanisms and therapeutic targets. Arterioscler. Thromb. Vasc. Biol. 32, 1771-1776
2. Ouchi, N., Parker, J. L., Lugus, J. J., and Walsh, K. (2011) Adipokines in inflammation and metabolic disease. Nat. Rev. Immunol. 11, 85-97
3. Calle, E. E., and Kaaks, R. (2004) Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat. Rev. Cancer 4, 579-591
4. Renehan, A. G., Tyson, M., Egger, M., Heller, R. F., and Zwahlen, M. (2008) Body-mass index and incidence of cancer: a systematic review and metaanalysis of prospective observational studies. Lancet 371, 569-578
5. Turati, F., Talamini, R., Pelucchi, C., Polesel, J., Franceschi, S., Crispo, A., Izzo, F., La Vecchia, C., Boffetta, P., and Montella, M. (2013) Metabolic syndrome and hepatocellular carcinoma risk. Br. J. Cancer 108, 222-228
6. Harima, S., Hashimoto, S., Shibata, H., Matsunaga, T., Tanabe, R., Terai, S., and Sakaida, I. (2013) Correlations between obesity/metabolic syn-drome-related factors and risk of developing colorectal tumors. Hepatogastroenterology 60, 733-737
7. Wang, Y. Y., Lehuédé, C., Laurent, V., Dirat, B., Dauvillier, S., Bochet, L., Le Gonidec, S., Escourrou, G., Valet, P., and Muller, C. (2012) Adipose tissue and breast epithelial cells: a dangerous dynamic duo in breast cancer. Cancer Lett. 324, 142-151
8. Dirat, B., Bochet, L., Dabek, M., Daviaud, D., Dauvillier, S., Majed, B., Wang, Y. Y., Meulle, A., Salles, B., Le Gonidec, S., Garrido, I., Escourrou, G., Valet, P., and Muller, C. (2011) Cancer-associated adipocytes exhibit an activated phenotype and contribute to breast cancer invasion. Cancer Res. 71, 2455-2465
9. Vona-Davis, L., and Rose, D. P. (2007) Adipokines as endocrine, paracrine, and autocrine factors in breast cancer risk and progression. Endocr. Relat. Cancer 14, 189-206
10. Park, J., and Scherer, P. E. (2012) Adipocyte-derived endotrophin promotes malignant tumor progression. J. Clin. Invest. 122, 4243-4256
11. Reimann, M., Vafeiadou, K., Hall, W. L., Dierkes, J., Nilsson, M., Dahlman-Wright, K., Ferrari, M., Huebner, U., Hallund, J., Bugel, S., Branca, F., Williams, C. M., and Koebnick, C. (2006) Evidence for associations between common polymorphisms of estrogen receptor β gene with homocysteine and nitric oxide. Climacteric 9, 215-223
12. Smith, E. P., Boyd, J., Frank, G. R., Takahashi, H., Cohen, R. M., Specker, B., Williams, T. C., Lubahn, D. B., and Korach, K. S. (1994) Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N. Engl. J. Med. 331, 1056-1061
13. Okura, T., Koda, M., Ando, F., Niino, N., Ohta, S., and Shimokata, H. (2003) Association of polymorphisms in the estrogen receptor α gene with body fat distribution. Int. J. Obes. Relat. Metab. Disord. 27, 1020-1027
14. Dahlman, I., Vaxillaire, M., Nilsson, M., Lecoeur, C., Gu, H. F., Cavalcanti-Proença, C., Efendic, S., Ostenson, C. G., Brismar, K., Charpentier, G., Gustafsson, J. A., Froguel, P., Dahlman-Wright, K., and Steffensen, K. R. (2008) Estrogen receptor alpha gene variants associate with type 2 diabetes and fasting plasma glucose. Pharmacogenet. Genomics 18, 967-975
15. Nilsson, M., Dahlman, I., Ryden, M., Nordstrom, E. A., Gustafsson, J. A., Arner, P., and Dahlman-Wright, K. (2007) Oestrogen receptor α gene expression levels are reduced in obese compared to normal weight females. Int. J. Obes. 31, 900-907
16. Bryzgalova, G., Gao, H., Ahren, B., Zierath, J. R., Galuska, D., Steiler, T. L., Dahlman-Wright, K., Nilsson, S., Gustafsson, J. A., Efendic, S., and Khan, A. (2006) Evidence that oestrogen receptor-α plays an important role in the regulation of glucose homeostasis in mice: insulin sensitivity in the liver. Diabetologia 49, 588-597
17. Ribas, V., Nguyen, M. T., Henstridge, D. C., Nguyen, A. K., Beaven, S. W., Watt, M. J., and Hevener, A. L. (2010) Impaired oxidative metabolism and inflammation are associated with insulin resistance in ERα-deficient mice. Am. J. Physiol. Endocrinol. Metab. 298, E304-319
18. Hewitt, S. C., Kissling, G. E., Fieselman, K. E., Jayes, F. L., Gerrish, K. E., and Korach, K. S. (2010) Biological and biochemical consequences of global deletion of exon 3 from the ERα gene. FASEB J. 24, 4660-4667
19. He, W., Barak, Y., Hevener, A., Olson, P., Liao, D., Le, J., Nelson, M., Ong, E., Olefsky, J. M., and Evans, R. M. (2003) Adipose-specific peroxisome proliferator-activated receptor γ knockout causes insulin resistance in fat and liver but not in muscle. Proc. Natl. Acad. Sci. U.S.A. 100, 15712-15717
20. Hewitt, S. C., Li, L., Grimm, S. A., Winuthayanon, W., Hamilton, K. J., Pockette, B., Rubel, C. A., Pedersen, L. C., Fargo, D., Lanz, R. B., DeMayo, F. J., Schütz, G., and Korach, K. S. (2014) NovelDNAmotif binding activity observed in vivo with an estrogen receptor α mutant mouse. Mol. Endocrinol. 28, 899-911
21. Ahlbory-Dieker, D. L., Stride, B. D., Leder, G., Schkoldow, J., Trölenberg, S., Seidel, H., Otto, C., Sommer, A., Parker, M. G., Schütz, G., and Wintermantel, T. M. (2009) DNA binding by estrogen receptor-α is essential for the transcriptional response to estrogen in the liver and the uterus. Mol. Endocrinol. 23, 1544-1555
22. Parks, B. W., Nam, E., Org, E., Kostem, E., Norheim, F., Hui, S. T., Pan, C., Civelek, M., Rau, C. D., Bennett, B. J., Mehrabian, M., Ursell, L. K., He, A., Castellani, L. W., Zinker, B., Kirby, M., Drake, T. A., Drevon, C. A., Knight, R., Gargalovic, P., Kirchgessner, T., Eskin, E., and Lusis, A. J. (2013) Genetic control of obesity and gut microbiota composition in response to high-fat, high-sucrose diet in mice. Cell Metab. 17, 141-152
23. Hurvitz, S. A., Allen, H. J., Moroose, R. L., Chan, D., Hagenstad, C., Applebaum, S. H., Patel, G., Hu, E. H., Ryba, N., Lin, L. S., Wang, H., Glaspy, J., Slamon, D. J., and Kabbinavar, F. (2010) A phase II trial of docetaxel with bevacizumab as first-line therapy for HER2-negative metastatic breast cancer (TORI B01). Clin. Breast Cancer 10, 307-312
24. Néchad, M. (1983) Development of brown fat cells in monolayer culture: II. ultrastructural characterization of precursors, differentiating adipocytes and their mitochondria. Exp. Cell Res. 149, 119-127
25. Rodriguez-Cuenca, S., Monjo, M., Frontera, M., Gianotti, M., Proenza, A. M., and Roca, P. (2007) Sex steroid receptor expression profile in brown adipose tissue: effects of hormonal status. Cell Physiol. Biochem. 20, 877-886
26. Neve, R. M., Chin, K., Fridlyand, J., Yeh, J., Baehner, F. L., Fevr, T., Clark, L., Bayani, N., Coppe, J. P., Tong, F., Speed, T., Spellman, P. T., DeVries, S., Lapuk, A., Wang, N. J., Kuo, W. L., Stilwell, J. L., Pinkel, D., Albertson, D. G., Waldman, F. M., McCormick, F., Dickson, R. B., Johnson, M. D., Lippman, M., Ethier, S., Gazdar, A., and Gray, J. W. (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10, 515-527
27. Devireddy, L. R., Gazin, C., Zhu, X., and Green, M. R. (2005) A cell-surface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell 123, 1293-1305
28. Zhang, S., Ma, Y., Jiang, J., Dai, Z., Gao, X., Yin, X., Xi, W., and Min, W. (2014) Inhibition of urokinase-type plasminogen activator expression by dihydroartemisinin in breast cancer cells. Oncol. Lett. 7, 1375-1380
29. Murray, D., Horgan, G., Macmathuna, P., and Doran, P. (2008) NET1-mediated RhoA activation facilitates lysophosphatidic acid-induced cell migration and invasion in gastric cancer. Br. J. Cancer 99, 1322-1329
30. Villanueva, C. J., Waki, H., Godio, C., Nielsen, R., Chou, W. L., Vargas, L., Wroblewski, K., Schmedt, C., Chao, L. C., Boyadjian, R., Mandrup, S., Hevener, A., Saez, E., and Tontonoz, P. (2011) TLE3 is a dual-function transcriptional coregulator of adipogenesis. Cell Metab. 13, 413-427
31. Ribas, V., Drew, B. G., Le, J. A., Soleymani, T., Daraei, P., Sitz, D., Mohammad, L., Henstridge, D. C., Febbraio, M. A., Hewitt, S. C., Korach, K. S., Bensinger, S. J., and Hevener, A. L. (2011) Myeloid-specific estrogen receptor α deficiency impairs metabolic homeostasis and accelerates atherosclerotic lesion development. Proc. Natl. Acad. Sci. U.S.A. 108, 16457-16462
32. Hewitt, S. C., Li, Y., Li, L., and Korach, K. S. (2010) Estrogen-mediated regulation of Igf1 transcription and uterine growth involves direct binding of estrogen receptor α to estrogen-responsive elements. J. Biol. Chem. 285, 2676-2685
33. Yan, Q. W., Yang, Q., Mody, N., Graham, T. E., Hsu, C. H., Xu, Z., Houstis, N. E., Kahn, B. B., and Rosen, E. D. (2007) The adipokine lipocalin 2 is regulated by obesity and promotes insulin resistance. Diabetes 56, 2533-2540
34. Yang, J., Bielenberg, D. R., Rodig, S. J., Doiron, R., Clifton, M. C., Kung, A. L., Strong, R. K., Zurakowski, D., and Moses, M. A. (2009) Lipocalin 2 promotes breast cancer progression. Proc. Natl. Acad. Sci. U.S.A. 106, 3913-3918
35. Panidis, D., Tziomalos, K., Koiou, E., Kandaraki, E. A., Tsourdi, E., Delkos, D., Kalaitzakis, E., and Katsikis, I. (2010) The effects of obesity and polycystic ovary syndrome on serum lipocalin-2 levels: a cross-sectional study. Reprod. Biol. Endocrinol. 8, 151
36. Lee, Y. H., Lee, S. H., Jung, E. S., Kim, J. S., Shim, C. Y., Ko, Y. G., Choi, D., Jang, Y., Chung, N., and Ha, J. W. (2010) Visceral adiposity and the severity of coronary artery disease in middle-aged subjects with normal waist circumference and its relation with lipocalin-2 and MCP-1. Atherosclerosis 213, 592-597
37. Seth, P., Porter, D., Lahti-Domenici, J., Geng, Y., Richardson, A., and Polyak, K. (2002) Cellular and molecular targets of estrogen in normal human breast tissue. Cancer Res. 62, 4540-4544
38. Boruk, M., Savory, J. G., and Haché, R. J. (1998) AF-2-dependent potentiation of CCAAT enhancer binding protein β-mediated transcriptional activation by glucocorticoid receptor. Mol. Endocrinol. 12, 1749-1763
39. Stein, B., and Yang, M. X. (1995) Repression of the interleukin-6 promoter by estrogen receptor is mediated by NF-κB and C/EBPβ. Mol. Cell. Biol. 15, 4971-4979
40. Tan, J., Buache, E., Chenard, M. P., Dali-Youcef, N., and Rio, M. C. (2011) Adipocyte is a non-trivial, dynamic partner of breast cancer cells. Int. J. Dev. Biol. 55, 851-859
41. Chakraborty, S., Kaur, S., Guha, S., and Batra, S. K. (2012) The multifaceted roles of neutrophil gelatinase associated lipocalin (NGAL) in inflammation and cancer. Biochim. Biophys. Acta 1826, 129-169
42. Bauer, M., Eickhoff, J. C., Gould, M. N., Mundhenke, C., Maass, N., and Friedl, A. (2008) Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Res. Treat 108, 389-397
43. Macciò, A., Madeddu, C., and Mantovani, G. (2009) Adipose tissue as target organ in the treatment of hormone-dependent breast cancer: new therapeutic perspectives. Obes. Rev. 10, 660-670
44. Park, J., Euhus, D. M., and Scherer, P. E. (2011) Paracrine and endocrine effects of adipose tissue on cancer development and progression. Endocr. Rev. 32, 550-570
45. Park, J., and Scherer, P. E. (2011) Leptin and cancer: from cancer stem cells to metastasis. Endocr. Relat. Cancer 18, C25-29
46. Carr, M. C. (2003) The emergence of the metabolic syndrome with menopause. J. Clin. Endocrinol. Metab. 88, 2404-2411
47. Devireddy, L. R., Hart, D. O., Goetz, D. H., and Green, M. R. (2010) A mammalian siderophore synthesized by an enzyme with a bacterial homolog involved in enterobactin production. Cell 141, 1006-1017
48. Yang, J., and Moses, M. A. (2009) Lipocalin 2: a multifaceted modulator of human cancer. Cell Cycle 8, 2347-2352
49. Shi, H., Gu, Y., Yang, J., Xu, L., Mi, W., and Yu, W. (2008) Lipocalin 2 promotes lung metastasis of murine breast cancer cells. J. Exp. Clin. Cancer Res. 27, 83
50. Stoesz, S. P., and Gould, M. N. (1995) Overexpression of neu-related lipocalin (NRL) in neu-initiated but not ras or chemically initiated rat mammary carcinomas. Oncogene 11, 2233-2241
51. Leng, X., Wu, Y., and Arlinghaus, R. B. (2011) Relationships of lipocalin 2 with breast tumorigenesis and metastasis. J. Cell. Physiol. 226, 309-314
52. Berger, T., Cheung, C. C., Elia, A. J., and Mak, T. W. (2010) Disruption of the Lcn2 gene in mice suppresses primary mammary tumor formation but does not decrease lung metastasis. Proc. Natl. Acad. Sci. U.S.A. 107, 2995-3000
53. Leng, X., Ding, T., Lin, H., Wang, Y., Hu, L., Hu, J., Feig, B., Zhang, W., Pusztai, L., Symmans, W. F., Wu, Y., and Arlinghaus, R. B. (2009) Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Res. 69, 8579-8584
54. Fernández, C. A., Yan, L., Louis, G., Yang, J., Kutok, J. L., and Moses, M. A. (2005) The matrix metalloproteinase-9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients. Clin. Cancer Res. 11, 5390-5395
55. Carter, J. C., and Church, F. C. (2012) Mature breast adipocytes promote breast cancer cell motility. Exp. Mol. Pathol. 92, 312-317
56. Iyengar, P., Combs, T. P., Shah, S. J., Gouon-Evans, V., Pollard, J. W., Albanese, C., Flanagan, L., Tenniswood, M. P., Guha, C., Lisanti, M. P., Pestell, R. G., and Scherer, P. E. (2003) Adipocyte-secreted factors synergistically promote mammary tumorigenesis through induction of antiapoptotic transcriptional programs and proto-oncogene stabilization. Oncogene 22, 6408-6423
57. Yan, L., Borregaard, N., Kjeldsen, L., and Moses, M. A. (2001) The high molecular weight urinary matrix metalloproteinase (MMP) activity is a complex of gelatinase B/MMP-9 and neutrophil gelatinase-associated lipocalin (NGAL): modulation of MMP-9 activity by NGAL. J. Biol. Chem. 276, 37258-37265
58. Jiralerspong, S., Kim, E. S., Dong, W., Feng, L., Hortobagyi, G. N., and Giordano, S. H. (2013) Obesity, diabetes, and survival outcomes in a large cohort of early-stage breast cancer patients. Ann. Oncol. 24, 2506-2514
59. Sparano, J. A., Wang, M., Zhao, F., Stearns, V., Martino, S., Ligibel, J. A., Perez, E. A., Saphner, T., Wolff, A. C., Sledge, G. W., Jr., Wood, W. C., Fetting, J., and Davidson, N. E. (2012) Obesity at diagnosis is associated with inferior outcomes in hormone receptor-positive operable breast cancer. Cancer 118, 5937-5946
60. Calle, E. E., Rodriguez, C., Walker-Thurmond, K., and Thun, M. J. (2003) Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N. Engl. J. Med. 348, 1625-1638