Changes in mammary caveolin-1 signaling pathways are associated with breast cancer risk in rats exposed to estradiol in utero or during prepuberty

Hormone Molecular Biology and Clinical Investigation

Volumn 2, Issue 2, 2010, Pages 227-234

  Shajahan, Ayesha N ^a   Goel, Shruti ^a   Assis, Sonia de ^a   Yu, Bin ^a   Clarke, Robert ^a   Hilakivi Clarke, Leena ^a,a  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

caveolin 1; estradiol; mammary gland

Indexed keywords

CAVEOLIN 1; CYCLIN D1; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE B;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; BREAST DEVELOPMENT; CANCER RISK; CANCER SUSCEPTIBILITY; CELL COUNT; CELL CULTURE; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; FEMALE; MYOEPITHELIUM CELL; NONHUMAN; PRENATAL EXPOSURE; PREPUBERTY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION;

EID: 78649588800     PISSN: 18681883     EISSN: 18681891     Source Type: Journal    
DOI: 10.1515/HMBCI.2010.031     Document Type: Article

References (51)

1. Hilakivi-Clarke L., Cabanes A., Olivo S., Kerr L., Bouker KB., Clarke R. Do estrogens always increase breast cancer risk? J Steroid Biochem Mol Biol 2002;80:163-74.
2. Ahlgren M., Melbye M., Wohlfahrt J., Sorensen TI. Growth patterns and the risk of breast cancer in women. N Engl J Med 2004;351:1619-26.
3. Hilakivi-Clarke L., Cho E., DeAssis S., Olivo S., Ealley E., Bouker KB., et al. Maternal and prepubertal diet., mammary development and breast cancer risk. J Nutr 2001;131:154S-7S.
4. Michels KB., Trichopoulos D., Robins JM., Rosner BA., Manson JE., Hunter DJ., et al. Birthweight as a risk factor for breast cancer. Lancet 1996;348:1542-6.
5. Trichopoulos D. Hypothesis: does breast cancer originate in utero? Lancet 1990;335:939-40.
6. Cabanes A., Wang M., Olivo S., DeAssis S., Gustafsson JA., Khan G., et al. Prepubertal estradiol and genistein exposures up-regu-late BRCA1 mRNA and reduce mammary tumorigenesis. Carcinogenesis 2004;25:741-8.
7. Hilakivi-Clarke L., Clarke R., Onojafe I., Raygada M., Cho E., Lippman M. A maternal diet high in n-6 polyunsaturated fats alters mammary gland development., puberty onset., and breast cancer risk among female rat offspring. Proc Natl Acad Sci USA 1997;94:9372-7.
8. Russo J., Russo IH. Biological and molecular bases of mammary carcinogenesis. Lab Invest 1987;57:112-37.
9. Russo J., Russo IH. Toward a unified concept of mammary car-cinogenesis. Prog Clin Biol Res 1997;396:1-16.
10. Klinge CM. Estrogen receptor interaction with co-activators and co-repressors. Steroids 2000;65:227-51.
11. Pearce ST., Jordan VC. The biological role of estrogen receptors alpha and beta in cancer. Crit Rev Oncol Hematol 2004;50: 3-22.
12. Hilakivi-Clarke L., Stoica A., Raygada M., Martin MB. Consumption of a high-fat diet alters estrogen receptor content., protein kinase C activity., and mammary gland morphology in virgin and pregnant mice and female offspring. Cancer Res 1998; 58:654-60.
13. Zhang X., Shen P., Coleman M., Zou W., Loggie BW., Smith LM., et al. Caveolin-1 down-regulation activates estrogen receptor alpha expression and leads to 17beta-estradiol-stimulated mammary tumorigenesis. Anticancer Res 2005;25:369-75.
14. Glenney JR Jr., Zokas L. Novel tyrosine kinase substrates from Rous sarcoma virus-transformed cells are present in the membrane skeleton. J Cell Biol 1989;108:2401-8.
15. Razani B., Lisanti MP. Caveolins and caveolae: molecular and functional relationships. Exp Cell Res 2001;271:36-44.
16. Anderson RG. The caveolae membrane system. Annu Rev Biochem 1998;67:199-225.
17. Witkiewicz AK., Dasgupta A., Nguyen KH., Liu C., Kovatich AJ., Schwartz GF., et al. Stromal caveolin-1 levels predict early DCIS progression to invasive breast cancer. Cancer Biol Ther 2009; 8:1071-9.
18. Razandi M., Pedram A., Merchenthaler I., Greene GL., Levin ER. Plasma membrane estrogen receptors exist and functions as dimers. Mol Endocrinol 2004;18:2854-65.
19. Couet J., Sargiacomo M., Lisanti MP. Interaction of a receptor tyrosine kinase., EGF-R., with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J Biol Chem 1997;272:30429-38.
20. Li S., Couet J., Lisanti MP. Src tyrosine kinases., Galpha subunits., and H-Ras share a common membrane-anchored scaffolding protein., caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J Biol Chem 1996; 271:29182-90.
21. Belanger MM., Roussel E., Couet J. Caveolin-1 is down-regulated in human lung carcinoma and acts as a candidate tumor suppressor gene. Chest 2004;125(Suppl 5):106S.
22. Zou W., McDaneld L., Smith LM. Caveolin-1 haploinsufficiency leads to partial transformation of human breast epithelial cells. Anticancer Res 2003;23:4581-6.
23. Sunaga N., Miyajima K., Suzuki M., Sato M., White MA., Ramirez RD., et al. Different roles for caveolin-1 in the development of non-small cell lung cancer versus small cell lung cancer. Cancer Res 2004;64:4277-85.
24. Williams TM., Lisanti MR The Caveolin genes: from cell biology to medicine. Ann Med 2004;36:584-95.
25. Yang G., Timme TL., Frolov A., Wheeler TM., Thompson TC. Combined c-Myc and caveolin-1 expression in human prostate carcinoma predicts prostate carcinoma progression. Cancer 2005;103:1186-94.
26. Marino M., Acconcia F., Bresciani F., Weisz A., Trentalance A. Distinct nongenomic signal transduction pathways controlled by 17beta-estradiol regulate DNA synthesis and cyclin D(1) gene transcription in HepG2 cells. Mol Biol Cell 2002;13:3720-9.
27. Hulit J., Bash T., Fu M., Galbiati F., Albanese C., Sage DR., et al. The cyclin D1 gene is transcriptionally repressed by caveolin-1. J Biol Chem 2000;275:21203-9.
28. Bouras T., Lisanti MR., Restell RG. Caveolin-1 in breast cancer. Cancer Biol Ther 2004;3:931-41.
29. Acconcia F., Ascenzi R., Bocedi A., Spisni E., Tomasi V., Trenta-lance A., et al. Ralmitoylation-dependent estrogen receptor alpha membrane localization: regulation by 17beta-estradiol. Mol Biol Cell 2005;16:231-7.
30. Engelman JA., Lee RJ., Karnezis A., Bearss DJ., Webster M., Sie-gel R., et al. Reciprocal regulation of neu tyrosine kinase activity and caveolin-1 protein expression in vitro and in vivo. Implications for human breast cancer. J Biol Chem 1998;273: 20448-55.
31. Lee H., Woodman SE., Engelman JA., Volonte D., Galbiati F., Kaufman HL., et al. Ralmitoylation of caveolin-1 at a single site (Cys-156) controls its coupling to the c-Src tyrosine kinase: targeting of dually acylated molecules (GRI-linked., transmem-brane., or cytoplasmic) to caveolae effectively uncouples c-Src and caveolin-1 (TYR-14). J Biol Chem 2001;276:35150-8.
32. Minshall RD., Tiruppathi C., Vogel SM., Niles WD., Gilchrist A., Hamm HE., et al. Endothelial cell-surface gp60 activates vesicle formation and trafficking via G(i)-coupled Src kinase signaling pathway. J Cell Biol 2000;150:1057-70.
33. Zivadinovic D., Watson CS. Membrane estrogen receptor-alpha levels predict estrogen-induced ERK1/2 activation in MCF-7 cells. Breast Cancer Res 2005;7:R130-44.
34. Fiucci G., Ravid D., Reich R., Liscovitch M. Caveolin-1 inhibits anchorage-independent growth., anoikis and invasiveness in MCF-7 human breast cancer cells. Oncogene 2002;21:2365-75.
35. Williams TM., Lee H., Cheung MW., Cohen AW., Razani B., Iyengar R., et al. Combined loss of INK4a and caveolin-1 synergis-tically enhances cell proliferation and oncogene-induced tumorigenesis: role of INK4a/CAV-1 in mammary epithelial cell hyperplasia. J Biol Chem 2004;279:24745-56.
36. Xie Z., Zeng X., Waldman T., Glazer RI. Transformation of mammary epithelial cells by 3-phosphoinositide-dependent protein kinase-1 activates beta-catenin and c-Myc., and down-regulates caveolin-1. Cancer Res 2003;63:5370-5.
37. Aaltomaa S., Lipponen R., Syrjanen K. Rrognostic value of cell proliferation in breast cancer as determined by proliferating cell nuclear antigen (RCNA) immunostaining. Anticancer Res 1992; 12:1281-6.
38. Lee H., Rark DS., Razani B., Russell RG., Restell RG., Lisanti MR. Caveolin-1 mutations (R132L and null) and the pathogenesis of breast cancer: caveolin-1 (R132L) behaves in a dominant-negative manner and caveolin-1 (-/-) null mice show mammary epithelial cell hyperplasia. Am J Rathol 2002;161:1357-69.
39. Russo J., Gusterson BA., Rogers AE., Russo IH., Wellings SR., van Zwieten MJ. Comparative study of human and rat mammary tumorigenesis. Lab Invest 1990;62:244-78.
40. Hilakivi-Clarke L. Nutritional modulation of terminal end buds: its relevance to breast cancer prevention. Curr Cancer Drug Targets 2007;7:465-74.
41. Scherer RE., Lisanti MR., Baldini G., Sargiacomo M., Mastick CC., Lodish HF. Induction of caveolin during adipogenesis and association of GLUT4 with caveolin-rich vesicles. J Cell Biol 1994; 127:1233-43.
42. Schlegel A., Wang C., Katzenellenbogen BS., Restell RG., Lisanti MR. Caveolin-1 potentiates estrogen receptor alpha (ERalpha) signaling. Caveolin-1 drives ligand-independent nuclear trans-location and activation of ERalpha. J Biol Chem 1999;274: 33551-6.
43. Hui R., Cornish AL., McClelland RA., Robertson JF., Blamey RW., Musgrove EA., et al. Cyclin D1 and estrogen receptor messenger RNA levels are positively correlated in primary breast cancer. Clin Cancer Res 1996;2:923-8.
44. Lukas J., Bartkova J., Bartek J. Convergence of mitogenic signalling cascades from diverse classes of receptors at the cyclin D-cyclin-dependent kinase-pRb-controlled G1 checkpoint. Mol Cell Biol 1996;16:6917-25.
45. Slamon DJ., Clark GM., Wong SG., Levin WJ., Ullrich A., Mc-Guire WL. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science 1987;235:177-82.
46. Engelman JA., Chu C., Lin A., Jo H., Ikezu T., Okamoto T., et al. Caveolin-mediated regulation of signaling along the p42/44 MAR kinase cascade in vivo. A role for the caveolin-scaffolding domain. FEBS Lett 1998;428:205-11.
47. Heffelfinger SC., Lower EE., Miller MA., Fenoglio-Rreiser CM. Rlasma membrane phosphotyrosine., Her2-NEU., and epidermal growth factor receptor in human breast cancer. A comparative study. Am J Clin Oncol 1996;19:552-7.
48. Hazan R., Margolis B., Dombalagian M., Ullrich A., Zilberstein A., Schlessinger J. Identification of autophosphorylation sites of HER2/neu. Cell Growth Differ 1990;1:3-7.
49. Shajahan AN., Tiruppathi C., Smrcka AV., Malik AB., Minshall RD. Gbetagamma activation of Src induces caveolae-mediated endocytosis in endothelial cells. J Biol Chem 2004;279:48055-62.
50. Stover DR., Becker M., Liebetanz J., Lydon NB. Src phospho-rylation of the epidermal growth factor receptor at novel sites mediates receptor interaction with Src and R85 alpha. J Biol Chem 1995;270:15591-7.
51. Hilakivi-Clarke L., Cho E., Cabanes A., DeAssis S., Olivo S., Helferich W., et al. Dietary modulation of pregnancy estrogen levels and breast cancer risk among female rat offspring. Clin Cancer Res 2002;8:3601-10.