Bidirectional signaling of mammary epithelium and stroma: Implications for breast cancer-preventive actions of dietary factors

Journal of Nutritional Biochemistry

Volumn 22, Issue 7, 2011, Pages 605-611

  Su, Ying ^a,c   Shankar, Kartik ^a,c   Rahal, Omar ^b,c   Simmen, Rosalia C M ^a,b,c  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c U S DEPARTMENT OF AGRICULTURE   (United States)

Author keywords

Adipocyte; Breast cancer; Diet; Epithelium; Mammary gland; Obesity

Indexed keywords

BREAST CANCER; BREAST EPITHELIUM; CANCER PREVENTION; CANCER RISK; CELL DIFFERENTIATION; DIET; DNA DAMAGE; GENE EXPRESSION; LIFESTYLE MODIFICATION; REVIEW; STROMA CELL; VITAMIN SUPPLEMENTATION;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; BREAST; BREAST NEOPLASMS; CELL DIFFERENTIATION; DIET; EPITHELIUM; FEMALE; HUMANS; MICE; RATS; RISK; SIGNAL TRANSDUCTION; STROMAL CELLS;

EID: 79958129216     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2010.09.008     Document Type: Review

References (107)

1. Jemal A., Siegel R., Ward E., Hao Y., Xu J., Thun M.J. Cancer statistics, 2009. CA Cancer J Clin 2009, 59:225-249.
2. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
3. Perou C.M., Sorlie T., Eisen M.B., van de R.M., Jeffrey S.S., Rees C.A., et al. Molecular portraits of human breast tumours. Nature 2000, 406:747-752.
4. Sorlie T., Wang Y., Xiao C., Johnsen H., Naume B., Samaha R.R., et al. Distinct molecular mechanisms underlying clinically relevant subtypes of breast cancer: gene expression analyses across three different platforms. BMC Genomics 2006, 7:127.
5. Arpino G., Laucirica R., Elledge R.M. Premalignant and in situ breast disease: biology and clinical implications. Ann Intern Med 2005, 143:446-457.
6. Wiechmann L., Kuerer H.M. The molecular journey from ductal carcinoma in situ to invasive breast cancer. Cancer 2008, 112:2130-2142.
7. Allred D.C., Wu Y., Mao S., Nagtegaal I.D., Lee S., Perou C.M., et al. Ductal carcinoma in situ and the emergence of diversity during breast cancer evolution. Clin Cancer Res 2008, 14:370-378.
8. Buerger H., Mommers E.C., Littmann R., Simon R., Diallo R., Poremba C., et al. Ductal invasive G2 and G3 carcinomas of the breast are the end stages of at least two different lines of genetic evolution. J Pathol 2001, 194:165-170.
9. Polyak K. Is breast tumor progression really linear?. Clin Cancer Res 2008, 14:339-341.
10. Li X., Lewis M.T., Huang J., Gutierrez C., Osborne C.K., Wu M.F., et al. Intrinsic resistance of tumorigenic breast cancer cells to chemotherapy. J Natl Cancer Inst 2008, 100:672-679.
11. Visvader J.E. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev 2009, 23:2563-2577.
12. Shackleton M., Vaillant F., Simpson K.J., Stingl J., Smyth G.K., Asselin-Labat M.L., et al. Generation of a functional mammary gland from a single stem cell. Nature 2006, 439:84-88.
13. Hennighausen L., Robinson G.W. Information networks in the mammary gland. Nat Rev 2005, 6:714-725.
14. Hovey R.C., Trott J.F., Vonderhaar B.K. Establishing a framework for the functional mammary gland: from endocrinology to morphology. J Mammary Gland Biol Neoplasia 2002, 7:17-38.
15. Arendt L.M., Rudnick J.A., Keller P.J., Kuperwasser C. Stroma in breast development and disease. Semin Cell Dev Biol 2009, 21:11-18.
16. Tlsty T.D., Hein P.W. Know thy neighbor: stromal cells can contribute oncogenic signals. Curr Opin Genet Dev 2001, 11:54-59.
17. Gupta G.P., Massague J. Cancer metastasis: building a framework. Cell 2006, 127:679-695.
18. Polyak K., Haviv I., Campbell I.G. Co-evolution of tumor cells and their microenvironment. Trends Genet 2009, 25:30-38.
19. Casey T., Bond J., Tighe S., Hunter T., Lintault L., Patel O., et al. Molecular signatures suggest a major role for stromal cells in development of invasive breast cancer. Breast Cancer Res Treat 2009, 114:47-62.
20. Shimoda M., Mellody K.T., Orimo A. Carcinoma-associated fibroblasts are a rate-limiting determinant for tumour progression. Semin Cell Dev Biol 2010, 21:19-25.
21. Maccio A., Madeddu C., Mantovani G. Adipose tissue as target organ in the treatment of hormone-dependent breast cancer: new therapeutic perspectives. Obes Rev 2009, 10:660-670.
22. Brennan S.F., Cantwell M.M., Cardwell C.R., Velentzis L.S., Woodside J.V. Dietary patterns and breast cancer risk: a systematic review and meta-analysis. Am J Clin Nutr 2010, 91:1294-1302.
23. Russo J., Mailo D., Hu Y.F., Balogh G., Sheriff F., Russo I.H. Breast differentiation and its implication in cancer. Clin Cancer Res 2010, 11:931s-936s.
24. Murrill W.B., Brown N.M., Zhang J.X., Manzolillo P.A., Barnes S., Lamartiniere C.A. Prepubertal genistein exposure suppresses mammary cancer and enhances gland differentiation in rats. Carcinogenesis 1996, 17:1451-1457.
25. Hilakivi-Clarke L., de Assis S. Fetal origins of breast cancer. Trends Endocrinol Metab 2006, 17:340-348.
26. Eason R.R., Velarde M.C., Chatman L., Till S.R., Geng Y., Ferguson M., et al. Dietary exposure to whey proteins alters rat mammary gland proliferation, apoptosis, and gene expression during postnatal development. J Nutr 2004, 134:3370-3377.
27. Su Y., Shankar K., Simmen R.C. Early soy exposure via maternal diet regulates rat mammary epithelial differentiation by paracrine signaling from stromal adipocytes. J Nutr 2009, 139:945-951.
28. Coughlin S.S., Ekwueme D.U. Breast cancer as a global health concern. Cancer Epidemiol 2009, 33:315-318.
29. Freedman L.S., Clifford C., Messina M. Analysis of dietary fat, calories, body weight, and the development of mammary tumors in rats and mice: a review. Cancer Res 1990, 50:5710-5719.
30. Welsch C.W. Relationship between dietary fat and experimental mammary tumorigenesis: a review and critique. Cancer Res 1992, 52:2040s-2048s.
31. Witt P.M., Christensen J.H., Schmidt E.B., Dethlefsen C., TjΦnneland A., Overvad K., Ewertz M Marine n-3 polyunsaturated fatty acids in adipose tissue and breast cancer risk: a case-cohort study from Denmark. Cancer Causes Control 2009, 20:1715-1721.
32. Hilakivi-Clarke L., Wang C., Kalil M., Riggins R., Pestell R.G. Nutritional modulation of the cell cycle and breast cancer. Endocr Relat Cancer 2004, 11:603-622.
33. Sasaki T., Kobayashi Y., Shimizu J., Wada M., Innami S., Kanke Y., Takita T. Effects of dietary n-3 to n-6 polyunstaurated fatty acid ratio on mammary carcinogenesis in rats. Nutr Cancer 1998, 30:137-143.
34. Mignone L.I., Giovannucci E., Newcomb P.A., Titus-Ernstoff L., Trentham-Dietz A., Hampton J.M., et al. Dietary carotenoids and the risk of invasive breast cancer. Int J Cancer 2009, 124:2929-2937.
35. Bertone-Johnson E.R. Prospective studies of dietary vitamin D and breast cancer: more questions raised than answered. Nutr Rev 2007, 65:459-466.
36. Lof M., Weiderpass E. Impact of diet on breast cancer risk. Curr Opin Obstet Gynecol 2009, 21:80-85.
37. Aggarwal B.B., Harikumar K.B. Potential therapeutic effects of curcumin, the anti-inflammatory agent, against neurodegenerative, cardiovascular, pulmonary, metabolic, autoimmune and neoplastic diseases. Int J Biochem Cell Biol 2009, 41:40-59.
38. Das S., Das D.K. Anti-inflammatory responses of resveratrol. Inflamm Allergy Drug Targets 2007, 6:168-173.
39. Thoennissen N.H., O'Kelly J., Lu D., Iwanski G.B., La D.T., Abbassi S., et al. Capsaicin causes cell-cycle arrest and apoptosis in ER-positive and-negative breast cancer cells by modulating the EGFR/HER-2 pathway. Oncogene 2010, 29:285-296.
40. So F.V., Guthrie N., Chambers A.F., Moussa M., Carroll K.K. Inhibition of human breast cancer cell proliferation and delay of mammary tumorigenesis by flavonoids and citrus juices. Nutr Cancer 1996, 26:167-181.
41. Tomar R.S., Shiao R. Early life and adult exposure to isoflavones and breast cancer risk. J Environ Sci Health Environ Carcinog Ecotoxicol Rev 2008, 26:113-173.
42. Harmon A.W., Patel Y.M. Naringenin inhibits glucose uptake in MCF-7 breast cancer cells: a mechanism for impaired cellular proliferation. Breast Cancer Res Treat 2004, 85:103-110.
43. Clement Y. Can green tea do that? A literature review of the clinical evidence. Prev Med 2009, 49:83-87.
44. de Assis S., Hilakivi-Clarke L. Timing of dietary estrogenic exposures and breast cancer risk. Ann NY Acad Sci 2006, 1089:14-35.
45. Aggarwal B.B., Shishodia S. Molecular targets of dietary agents for prevention and therapy of cancer. Biochem Pharmacol 2006, 71:1397-1421.
46. Chen C., Kong A.N. Dietary cancer-chemopreventive compounds: from signaling and gene expression to pharmacological effects. Trends Pharmacol Sci 2005, 26:318-326.
47. Hilakivi-Clarke L. Nutritional modulation of terminal end buds: its relevance to breast cancer prevention. Curr Cancer Drug Targets 2007, 7:465-474.
48. Gago-Dominguez M., Jiang X., Castelao J.E. Lipid peroxidation, oxidative stress genes and dietary factors in breast cancer protection: a hypothesis. Breast Cancer Res 2007, 9:201.
49. Vogelstein B., Kinzler K.W. Cancer genes and the pathways they control. Nat Med 2004, 10:789-799.
50. Su Y., Simmen F.A., Xiao R., Simmen R.C.M. Expression profiling of rat mammary epithelial cells reveals candidate signaling pathways in dietary protection from mammary tumors. Physiol Genomics 2007, 30:8-16.
51. Lamartiniere C.A., Cotroneo M.S., Fritz W.A., Wang J., Mentor-Marcel R., Elgavish A. Genistein chemoprevention: timing and mechanisms of action in murine mammary and prostate. J Nutr 2002, 132:552S-558S.
52. Simmen R.C., Eason R.R., Till S.R., Chatman L., Velarde M.C., Geng Y., et al. Inhibition of NMU-induced mammary tumorigenesis by dietary soy. Cancer Lett 2005, 224:45-52.
53. Dave B., Eason R.R., Till S.R., Geng Y., Velarde M.C., Badger T.M., Simmen R.C. The soy isoflavone genistein promotes apoptosis in mammary epithelial cells by inducing the tumor suppressor PTEN. Carcinogenesis 2005, 26:1793-1803.
54. Su Y., Simmen R.C. Soy isoflavone genistein upregulates epithelial adhesion molecule E-cadherin expression and attenuates beta-catenin signaling in mammary epithelial cells. Carcinogenesis 2009, 30:331-339.
55. Korkaya H., Paulson A., Charafe-Jauffret E., Ginestier C., Brown M., Dutcher J., et al. Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol 2009, e1000121:7.
56. Guo S., Lu J., Subramanian A., Sonenshein G.E. Microarray-assisted pathway analysis identifies mitogen-activated protein kinase signaling as a mediator of resistance to the green tea polyphenol epigallocatechin 3-gallate in her-2/neu-overexpressing breast cancer cells. Cancer Res 2006, 66:5322-5329.
57. Dip R., Lenz S., Antignac J.P., Le Bizec B., Gmuender H., Naegeli H. Global gene expression profiles induced by phytoestrogens in human breast cancer cells. Endocr Relat Cancer 2008, 15:161-173.
58. Olivo-Marston S.E., Zhu Y., Lee R.Y., Cabanes A., Khan G., Zwart A., et al. Gene signaling pathways mediating the opposite effects of prepubertal low-fat and high-fat n-3 polyunsaturated fatty acid diets on mammary cancer risk. Cancer Prev Res 2008, 1:532-545.
59. Orimo A., Weinberg R.A. Stromal fibroblasts in cancer: a novel tumor-promoting cell type. Cell Cycle 2006, 5:1597-1601.
60. Trimboli A.J., Cantemir-Stone C.Z., Li F., Wallace J.A., Merchant A., Creasap N., et al. Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 2009, 461:1084-1091.
61. Su G., Blaine S.A., Qiao D., Friedl A. Shedding of syndecan-1 by stromal fibroblasts stimulates human breast cancer cell proliferation via FGF2 activation. J Biol Chem 2007, 282:14906-14915.
62. Farmer P., Bonnefoi H., Anderle P., Cameron D., Wirapati P., Becette V., et al. A stroma-related gene signature predicts resistance to neoadjuvant chemotherapy in breast cancer. Nat Med 2009, 15:68-74.
63. Stuelten C.H., Busch J.I., Tang B., Flanders K.C., Oshima A., Sutton E., et al. Transient tumor-fibroblast interactions increase tumor cell malignancy by a TGF-beta mediated mechanism in a mouse xenograft model of breast cancer. PLoS One 2010, e9832:5.
64. Kratchmarova I., Kalume D.E., Blagoev B., Scherer P.E., Podtelejnikov A.V., Molina H., et al. A proteomic approach for identification of secreted proteins during the differentiation of 3T3-L1 preadipocytes to adipocytes. Mol Cell Proteomics 2002, 1:213-222.
65. Celis J.E., Moreira J.M., Cabezon T., Gromov P., Friis E., Rank F., Gromova I. Identification of extracellular and intracellular signaling components of the mammary adipose tissue and its interstitial fluid in high risk breast cancer patients: towards dissecting the molecular circuitry of epithelial-adipocyte stromal cell interactions. Mol Cell Proteomics 2005, 4:492-522.
66. Harvie M., Hooper L., Howell A.H. Central obesity and breast cancer risk: a systematic review. Obes Rev 2003, 4:157-173.
67. Kamikawa A., Ichii O., Yamaji D., Imao T., Suzuki C., Okamatsu-Ogura Y., et al. Diet-induced obesity disrupts ductal development in the mammary glands of nonpregnant mice. Dev Dynamics 2009, 238:1092-1099.
68. Considine R.V., Sinha M.K., Heiman M.L., Kriauciunas A., Stephens T.W., Nyce M.R., et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 1996, 334:292-295.
69. Matsuzawa Y. Adiponectin: a key player in obesity related disorders. Curr Pharm Des 2010, 16:1896-1901.
70. Lam J.B., Chow K.H., Xu A., Lam K.S., Liu J., Wong N.S., et al. Adiponectin haploinsufficiency promotes mammary tumor development in MMTV-PyVT mice by modulation of phosphatase and tensin homolog activities. PLoS One 2009, e4968:4.
71. Cho S.Y., Park P.J., Shin H.J., Kim Y.K., Shin D.W., Shin E.S., et al. (-)-Catechin suppresses expression of Kruppel-like factor 7 and increases expression and secretion of adiponectin protein in 3T3-L1 cells. Am J Physiol Endocrinol Metab 2007, 292:E1166-E1172.
72. Kao Y.H., Hiipakka R.A., Liao S. Modulation of obesity by a green tea catechin. Am J Clin Nutr 2000, 72:1232-1234.
73. Kavanagh K.T., Hafer L.J., Kim D.W., Mann K.K., Sherr D.H., Rogers A.E., et al. Green tea extracts decrease carcinogen-induced mammary tumor burden in rats and rate of breast cancer cell proliferation in culture. J Cell Biochem 2001, 82:387-398.
74. Su Y., Eason R.R., Geng Y., Till S.R., Badger T.M., Simmen R.C. In utero exposure to maternal diets containing soy protein isolate but not genistein alone, protects young adult offspring from NMU-induced mammary tumorigenesis. Carcinogenesis 2007, 28:1046-1051.
75. Wu A.H., Yu M.C., Tseng C.C., Pike M.C. Epidemiology of soy exposures and breast cancer risk. Br J Cancer 2008, 98:9-14.
76. Tong Q., Hotamisligil G.S. Molecular mechanisms of adipocyte differentiation. Rev Endocr Metab Disord 2001, 2:349-355.
77. Rangwala S.M., Lazar M.A. Transcriptional control of adipogenesis. Annu Rev Nutr 2000, 20:535-559.
78. Tontonoz P., Hu E., Graves R.A., Budavari A.I., Spiegelman B.M. mPPAR gamma 2: tissue-specific regulator of an adipocyte enhancer. Genes Dev 1994, 8:1224-1234.
79. Cao Z., Umek R.M., McKnight S.L. Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev 1991, 5:1538-1552.
80. Wu Z., Rosen E.D., Brun R., Hauser S., Adelmant G., Troy A.E., et al. Cross-regulation of C/EBP alpha and PPAR gamma controls the transcriptional pathway of adipogenesis and insulin sensitivity. Mol Cell 1999, 3:151-158.
81. Tontonoz P., Kim J.B., Graves R.A., Spiegelman B.M. ADD1: a novel helix-loop-helix transcription factor associated with adipocyte determination and differentiation. Mol Cell Biol 1993, 13:4753-4759.
82. Tang W., Zeve D., Suh J.M., Bosnakovski D., Kyba M., Hammer R.E., Tallquist M.D., Graff J.M. Science 2008, 322:583-586.
83. Rodeheffer M.S., Birsoy K., Friedman J.M. Identification of white adipocyte progenitor cells in vivo. Cell 2008, 135:240-249.
84. Grossmann M.E., Nkhata K.J., Mizuno N.K., Ray A., Cleary M.P. Effects of adiponectin on breast cancer cell growth and signaling. Br J Cancer 2008, 98:370-379.
85. Liu J., Lam J.B., Chow K.H., Xu A., Lam K.S., Moon R.T., et al. Adiponectin stimulates Wnt inhibitory factor-1 expression through epigenetic regulations involving the transcription factor specificity protein 1. Carcinogenesis 2008, 29:2195-2202.
86. Treeck O., Lattrich C., Juhasz-Boess I., Bucholz S., Pfeiffer G., Ortmann O. Adiponectin differentially affects gene expression in human mammary epithelial and breast cancer cells. Br J Cancer 2008, 99:1256-1350.
87. Jarde T., Caldefie-Chezet F., Goncalves-Mendes N., Mishellany F., Buechler C., Penault-Llorca F., et al. Involvement of adiponectin and leptin in breast cancer: clinical and in vitro studies. Endocr Relat Cancer 2009, 16:1197-1210.
88. Vona-Davis L., Howard-McNatt M., Rose D.P. Adiposity, type 2 diabetes and the metabolic syndrome in breast cancer. ObesRev 2007, 8:395-408.
89. Wu M.H., Chou Y.C., Chou W.Y., Hsu G.C., Chu C.H., Yu C.P., et al. Circulating levels of leptin, adiposity and breast cancer risk. Br J Cancer 2009, 100:578-582.
90. Szkudelski T., Nogowski L., Pruszynska-Osmatek E., Kaczmarek P., Szkudelska K. Genistein restritcs leptin secretion from rat adipocytes. J Steroid Biochem Mol Biol. 2005, 96:301-307.
91. Jeon B.S., Park J.W., Kim B.K., Kim H.K., Jung T.S., Hahm J.R., et al. Fermented mushroom milk-supplemented dietary fibre prevents the onset of obesity and hypertriglyceridaemia in Otsuka Long-Evans Tokushima fatty rats. Diabetes Obes Metab 2005, 7:709-715.
92. Neyrinck A.M., Bindels L.B., De Backer F., Pachikian B.D., Cani P.D., Delzenne N.M. Dietary supplementation with chitosan derived from mushrooms changes adipocytokine profile in diet-induced obese mice, a phenomenon linked to its lipid-lowering action. Int Immunopharmacol 2009, 9:767-773.
93. Adlercreutz H. Lignans and human health. Crit Rev Clin Lab Sci 2007, 44:483-525.
94. Al-Lahham S.H., Roelofsen H., Priebe M., Weening D., Dijkstra M., Hoek A., et al. Regulation of adipokine production in human adipose tissue by propionic acid. Eur J Clin Invest 2010, 40:401-407.
95. Sun C.A., Wu M.H., Chu C.H., Chou Y.C., Hsu G.C., Yang T., et al. Adipocytokine resistin and breast cancer risk. Breast Cancer Res Treat 2010, 123:869-876.
96. Galie M., Sorrentino C., Montani M., Micossi L., Di Carlo E., D'Antuono T., et al. Mammary carcinoma provides highly tumourigenic and invasive reactive stromal cells. Carcinogenesis 2005, 26:1868-1878.
97. Zvonic S., Lefevre M., Kilroy G., Floyd Z.E., DeLany J.P., Kheterpal I., et al. Secretome of primary cultures of human adipose-derived stem cells: modulation of serpins by adipogenesis. Mol Cell Proteomics 2007, 6:18-28.
98. Wang Z.V., Deng Y., Wang Q.A., Sun K., Scherer P.E Identification and characterization of a promoter cassette conferring adipocyte-specific gene expression. Endocrinology 2010, 151:2933-2939.
99. Rees E.D., Shuck A.E., Ackermann H. Lipid composition of rat mammary carcinomas, mammary glands, and related tissues: endocrine influences. J Lipid Res 1966, 7:396-402.
100. Medina D., Kittrell F. Stroma is not a major target in DMBA-mediated tumorigenesis of mouse mammary preneoplasia. J Cell Sci 2005, 118:123-127.
101. Nakatani H., Aoki N., Okajima T., Nadano D., Flint D., Masuda T. Establishment of a mammary stromal fibroblastic cell line for in vitro studies in mice of mammary adipocyte differentiation. Biol Reprod 2010, 82:44-53.
102. Boulanger C.A., Mack D.L., Booth B.W., Smith G.H. Interaction with the mammary microenvironment redirects spermatogenic cell fate in vivo. Proc Natl Acad Sci U S A 2007, 104:3871-3876.
103. Booth B.W., Mack D.L., Androutsellis-Theotokis A., McKay R.D., Boulanger C.A., Smith G.H. The mammary microenvironment alters the differentiation repertoire of neural stem cells. Proc Natl Acad Sci U S A 2008, 105:14891-14896.
104. Damonte P., Hodgson J.G., Chen J.Q., Young L.J., Cardiff R.D., Borowsky A.D. Mammary carcinoma behavior is programmed in the precancer stem cell. Breast Cancer Res 2008, 10:R50.
105. Kakarala M., Brenner D.E., Korkaya H., Cheng C., Tazi K., Ginestier C., et al. Targeting breast stem cells with the cancer preventive compounds curcumin and piperine. Breast Cancer Res Treat 2009.
106. Krichner S., Kleu T., Chow C., Casey S., Blumberg B. Prenatal exposure to the environmental obesogen tributylin predisposes multipotent stem cells to become adipocytes. Mol Endocrinol 2010, 24:526-539.
107. Liao D., Luo Y., Markowitz D., Xiang R., Reisfeld R.A. Cancer associated fibroblasts promote tumor growth and metastasis by modulating the tumor immune microenvironment in 4T1 murine breast cancer model. PLoS One 2009, e7965:4.