Developmental stage determines the effects of MYC in the mammary epithelium

Development

Volumn 132, Issue 5, 2005, Pages 1147-1160

  Blakely, Collin M ^a   Sintasath, Louis ^a   D'Cruz, Celina M ^a   Hahn, Kristina T ^a   Dugan, Katherine D ^a   Belka, George K ^a   Chodosh, Lewis A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Caveolin1; Differentiation; Mammary; Mouse; Myc; Stat5; Tgf 3

Indexed keywords

CARCINOGEN; CAVEOLIN 1; JANUS KINASE 2; STAT5 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST CARCINOGENESIS; BREAST DEVELOPMENT; BREAST EPITHELIUM; CONTROLLED STUDY; DEVELOPMENTAL STAGE; DOWN REGULATION; ENZYME ACTIVATION; EPITHELIZATION; GENE ACTIVATION; GENE FUNCTION; GENE OVEREXPRESSION; HISTOPATHOLOGY; IN VIVO STUDY; LACTATION INHIBITION; MOUSE; MOUSE STRAIN; NONHUMAN; ONCOGENE MYC; PRIORITY JOURNAL; RISK ASSESSMENT; RISK FACTOR; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BLOTTING, NORTHERN; BLOTTING, WESTERN; CAVEOLIN 1; CAVEOLINS; CELL DIFFERENTIATION; CELL LINEAGE; DNA PRIMERS; DNA-BINDING PROTEINS; DOWN-REGULATION; EPITHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; LACTATION; MAMMARY GLANDS, ANIMAL; MICE; MICE, TRANSGENIC; MILK PROTEINS; PROTO-ONCOGENE PROTEINS C-MYC; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; STAT5 TRANSCRIPTION FACTOR; TIME FACTORS; TRANS-ACTIVATORS; UP-REGULATION;

ANIMALIA; JANUS; MUS MUSCULUS;

EID: 16844380414     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.01655     Document Type: Article

References (65)

1. Andres, A. C., van der Valk, M. A., Schonenberger, C. A., Fluckiger, F., LeMeur, M., Gerlinger, P. and Groner, B. (1988). Ha-ras and c-myc oncogene expression interferes with morphological and functional differentiation of mammary epithelial cells in single and double transgenic mice. Genes Dev. 2, 1486-1495.
2. Arnold, I. and Watt, F. M. (2001). c-Myc activation in transgenic mouse epidermis results in mobilization of stem cells and differentiation of their progeny. Curr Biol. 11, 558-568.
3. Askew, D. S., Ashmun, R. A., Simmons, B. C. and Cleveland, J. L. (1991). Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6, 1915-1922.
4. Bain, C., Willett, W., Rosner, B., Speizer, F. E., Belanger, C. and Hennekens, C. H. (1981). Early age at first birth and decreased risk of breast cancer. Am. J. Epidemiol. 114, 705-709.
5. Battaglino, R., Kim, D., Fu, J., Vaage, B., Fu, X. Y. and Stashenko, P. (2002). c-myc is required for osteoclast differentiation. J Bone Miner. Res. 17, 763-773.
6. Berns, E. M., Klijn, J. G., Smid, M., van Staveren, I. L., Look, M. P., van Putten, W. L. and Foekens, J. A. (1996). TP53 and MYC gene alterations independently predict poor prognosis in breast cancer patients. Genes Chromosomes Cancer 16, 170-179.
7. Boice, J. D., Jr, Preston, D., Davis, F. G. and Monson, R. R. (1991). Frequent chest X-ray fluoroscopy and breast cancer incidence among tuberculosis patients in Massachusetts. Radiat. Res. 125, 214-222.
8. Bouchard, C., Staller, P. and Eilers, M. (1998). Control of cell proliferation by Myc. Trends Cell Biol. 8, 202-206.
9. Brandvold, K. A., Ewert, D. L., Kent, S. C., Neiman, P. and Ruddell, A. (2001). Blocked B cell differentiation and emigration support the early growth of Myc-induced lymphomas. Oncogene 20 3226-3234.
10. Brisken, C. (2002). Hormonal control of alveolar development and its implications for breast carcinogenesis. J. Mammary Gland Biol. Neoplasia 7, 39-48.
11. Chapman, R. S., Lourenco, P. C., Tonner, E., Flint, D. J., Selbert, S., Takeda, K., Akira, S., Clarke, A. R. and Watson, C. J. (1999). Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Star3. Genes Dev. 13, 2604-2616.
12. Chrzan, P., Skokowski, J., Karmolinski, A. and Pawelczyk, T. (2001). Amplification of c-myc gene and overexpression of c-Myc protein in breast cancer and adjacent non-neoplastic tissue. Clin. Biochem. 34, 557-562.
13. Coppola, J. A. and Cole, M. D. (1986). Constitutive c-myc oncogene expression blocks mouse erythroleukaemia cell differentiation but not commitment. Nature 320, 760-763.
14. D'Cruz, C. M., Gunther, E. J., Boxer, R. B., Hartman, J. L., Sintasath, L., Moody, S. E., Cox, J. D., Ha, S. I., Belka, G. K., Golant, A., Cardiff, R. D. and Chodosh, L. A. (2001). c-MYC induces mammary tumorigenesis by means of a preferred pathway involving spontaneous Kras2 mutations. Nat. Med. 7, 235-239.
15. Deming, S. L., Nass, S. J., Dickson, R. B. and Trock, B. J. (2000). C-myc amplification in breast cancer: a meta-analysis of its occurrence and prognostic relevance. Br. J. Cancer 83, 1688-1695.
16. Dores, G. M., Metayer, C., Curtis, R. E., Lynch, C. F., Clarke, E. A., Glimelius, B., Storm, H., Pukkala, E., van Leeuwen, F. E., Holowaty, E. J. et al. (2002). Second malignant neoplasms among long-term survivors of Hodgkin's disease: a population-based evaluation over 25 years. J. Clin. Oncol. 20, 3484-3494.
17. Evan, G. I., Wyllie, A. H., Gilbert, C. S., Littlewood, T. D., Land, H., Brooks, M., Waters, C. M., Penn, L. Z. and Hancock, D. C. (1992). Induction of apoptosis in fibroblasts by c-myc protein. Cell 69, 119-128.
18. Facchini, L. M., Chen, S., Marhin, W. W., Lear, J. N. and Penn, L. Z. (1997). The Myc negative autoregulation mechanism requires Myc-Max association and involves the c-myc P2 minimal promoter. Mol. Cell Biol. 17, 100-114.
19. Felsher, D. W. and Bishop, J. M. (1999). Reversible tumorigenesis by MYC in hematopoietic lineages. Mol. Cell 4, 199-207.
20. Freytag, S. O. (1988). Enforced expression of the c-myc oncogene inhibits cell differentiation by precluding entry into a distinct predifferentiation state in G0/G1. Mol. Cell. Biol. 8 1614-1624.
21. Gandarillas, A. and Watt, F. M. (1997). c-Myc promotes differentiation of human epidermal stem cells. Genes Dev. 11, 2869-2882.
22. Gardner, H. P., Belka, G. K., Wertheim, G. B., Hartman, J. L., Ha, S. I., Gimotty, P. A., Marquis, S. T. and Chodosh, L. A. (2000). Developmental role of the SNF1-related kinase Hunk in pregnancy-induced changes in the mammary gland. Development 127 4493-4509.
23. Gunther, E. J., Belka, G. K., Wertheim, G. B., Wang, J., Hartman, J. L., Boxer, R. B. and Chodosh, L. A. (2002). A novel doxycycline-inducible system for the transgenic analysis of mammary gland biology. FASEB J. 16, 283-292.
24. Haggerty, T. J., Zeller, K. I., Osthus, R. C., Wonsey, D. R. and Dang, C. V. (2003). A strategy for identifying transcription factor binding sites reveals two classes of genomic c-Myc target sites. Proc. Natl. Acad. Sci. USA 100, 5313-5318.
25. Heath, V. J., Gillespie, D. A. and Crouch, D. H. (2000). Inhibition of the terminal stages of adipocyte differentiation by cMyc. Exp. Cell Res. 254, 91-98.
26. Helmrich, S. P., Shapiro, S., Rosenberg, L., Kaufman, D. W., Slone, D., Bain, C., Miettinen, O. S., Stolley, P. D., Rosenshein, N. B., Knapp, R. C. et al. (1983). Risk factors for breast cancer. Am. J. Epidemiol. 117, 35-45.
27. Hennighausen, L. G. and Sippel, A. E. (1982). Characterization and cloning of the mRNAs specific for the lactating mouse mammary gland. Eur. J. Biochem. 125, 131-141.
28. Hennighausen, L., Robinson, G. W., Wagner, K. U. and Liu, X. (1997). Developing a mammary gland is a stat affair. J. Mammary Gland Biol. Neoplasia 2, 365-372.
29. Hildreth, N. G., Shore, R. E. and Dvoretsky, P. M. (1989). The risk of breast cancer after irradiation of the thymus in infancy. N. Engl. J. Med. 321, 1281-1284.
30. Humphreys, R. C. and Hennighausen, L. (1999). Signal transducer and activator of transcription 5a influences mammary epithelial cell survival and tumorigenesis. Cell Growth Differ. 10, 685-694.
31. Humphreys, R. C., Bierie, B., Zhao, L., Raz, R., Levy, D. and Hennighausen, L. (2002). Deletion of Stat3 blocks mammary gland involution and extends functional competence of the secretory epithelium in the absence of lactogenic stimuli. Endocrinology 143, 3641-3650.
32. Hynes, N. E., Cella, N. and Wartmann, M. (1997). Prolactin mediated intracellular signaling in mammary epithelial cells. J. Mammary Gland Biology and Neoplasia 2, 19-27.
33. Iavnilovitch, E., Groner, B. and Barash, I. (2002). Overexpression and forced activation of stat5 in mammary gland of transgenic mice promotes cellular proliferation, enhances differentiation, and delays postlactational apoptosis. Mol. Cancer Res. 1, 32-47.
34. Kelly, P. A., Bachelot, A., Kedzia, C., Hennighausen, L., Ormandy, C. J., Kopchick, J. J. and Binart, N. (2002). The role of prolactin and growth hormone in mammary gland development. Mol. Cell. Endocrinol. 197, 127-131.
35. Kile, B. T. and Alexander, W. S. (2001). The suppressors of cytokine signalling (SOCS). Cell Mol. Life Sci. 58, 1627-1635.
36. Land, C. E., Tokunaga, M., Koyama, K., Soda, M., Preston, D. L., Nishimori, I. and Tokuoka, S. (2003). Incidence of female breast cancer among atomic bomb survivors, Hiroshima and Nagasaki, 1950-1990. Radiat. Res. 160, 707-717.
37. Layde, P. M., Webster, L. A., Baughman, A. L., Wingo, P. A., Rubin, G. L. and Ory, H. W. (1989). The independent associations of parity, age at first full term pregnancy, and duration of breastfeeding with the risk of breast cancer. Cancer and Steroid Hormone Study Group. J. Clin. Epidemiol. 42, 963-973.
38. Lindeman, G. J., Wittlin, S., Lada, H., Naylor, M. J., Santamaria, M., Zhang, J. G., Starr, R., Hilton, D. J., Alexander, W. S., Ormandy, C. J. and Visvader, J. (2001). SOCS1 deficiency results in accelerated mammary gland Development and rescues lactation in prolactin receptor-deficient mice. Genes & Dev. 15, 1631-1636.
39. Liu, X., Robinson, G. W. and Hennighausen, L. (1996). Activation of Stat5a and Stat5b by tyrosine phosphorylation is tightly linked to mammary gland differentiation. Mol. Endocrinol. 10, 1496-1506.
40. MacMahon, B., Cole, P., Lin, T. M., Lowe, C. R., Mirra, A. P., Ravnihar, B., Salber, E. J., Valaoras, V. G. and Yuasa, S. (1970). Age at first birth and breast cancer risk. Bull. World Health Organ. 43, 209-221.
41. MacMahon, B., Purde, M., Cramer, D. and Hint, E. (1982). Association of breast cancer risk with age at first and subsequent births: a study in the population of the Estonian Republic. J. Natl. Cancer Inst. 69, 1035-1038.
42. Marquis, S. T., Rajan, J. V., Wynshaw-Boris, A., Xu, J., Yin, G. Y., Abel, K. J., Weber, B. L. and Chodosh, L. A. (1995). The developmental pattern of Brcal expression implies a role in differentiation of the breast and other tissues. Nat. Genet. 11 17-26.
43. Master, S. R., Hartman, J. L., D'Cruz, C. M., Moody, S. E., Keiper, E. A., Ha, S. I., Cox, J. D., Belka, G. K. and Chodosh, L. A. (2002). Functional microarray analysis of mammary organogenesis reveals a developmental role in adaptive thermogenesis. Mol. Endocrinol. 16, 1185-1203.
44. Master, S. R., Stoddard, A. J., Bailey, L. C., Pan, T-C., Dugan, K. D. and Chodosh, L. A. (2005). Genomic analysis of early murine mammary gland development. Genome Biol. (in press).
45. Miller, A. B., Howe, G. R., Sherman, G. J., Lindsay, J. P., Yaffe, M. J., Dinner, P. J., Risch, H. A. and Preston, D. L. (1989). Mortality from breast cancer after irradiation during fluoroscopic examinations in patients being treated for tuberculosis. New Engl. J. Med. 321, 1285-1289.
46. Miner, J. H. and Wold, B. J. (1991). c-myc inhibition of MyoD and myogenin-initiated myogenic differentiation. Mol. Cell. Biol. 11, 2842-2851.
47. Miyoshi, K., Shillingford, J. M., Smith, G. H., Grimm, S. L., Wagner, K. U., Oka, T., Rosen, J. M., Robinson, G. W. and Hennighausen, L. (2001). Signal transducer and activator of transcription (Stat) 5 controls the proliferation and differentiation of mammary alveolar epithelium. J. Cell Biol. 155, 531-542.
48. Murphy, W., Sarid, J., Taub, R., Vasicek, T., Battey, J., Lenoir, G. and Leder, P. (1986). A translocated human c-myc oncogene is altered in a conserved coding sequence. Proc. Natl. Acad. Sci. USA 83, 2939-2943.
49. Myal, Y., Robinson, D. B., Iwasiow, B., Tsuyuki, D., Wong, P. and Shiu, R. P. (1991). The prolactin-inducible protein (PIP/GCDFP-15) gene: cloning, structure and regulation. Mol. Cell. Endocrinol. 80, 165-175.
50. Neville, M. C., McFadden, T. B. and Forsyth, I. (2002). Hormonal regulation of mammary differentiation and milk secretion. J. Mammary Gland Biol. Neoplasia 7, 49-66.
51. Nguyen, A. V. and Pollard, J. W. (2000). Transforming growth factor beta3 induces cell death during the first stage of mammary gland involution. Development 127, 3107-3118.
52. Park, D. S., Razani, B., Lasorella, A., Schreiber-Agus, N., Pestell, R. G., Iavarone, A. and Lisanti, M. P. (2001). Evidence that Myc isoforms transcriptionally repress caveolin-1 gene expression via an INR-dependent mechanism. Biochemistry 40, 3354-3362.
53. Park, D. S., Lee, H., Frank, P. G., Razani, B., Nguyen, A. V., Parlow, A. F., Russell, R. G., Hulit, J., Pestell, R. G. and Lisanti, M. P. (2002). Caveolin-1-deficient mice show accelerated mammary gland development during pregnancy, premature lactation, and hyperactivation of the Jak-2/STAT5a signaling cascade. Mol. Biol. Cell 13, 3416-3430.
54. Pelengaris, S., Littlewood, T. D., Khan, M., Elia, G. and Evan, G. (1999). Reversible activation of c-Myc in skin: induction of a complex neoplastic phenotype by a single oncogenic lesion. Mol. Cell 3, 565-577.
55. Pelengaris, S., Khan, M. and Evan, G. I. (2002). Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell 109 , 321-334.
56. Quarrie, L. H., Addey, C. V. and Wilde, C. J. (1996). Programmed cell death during mammary tissue involution induced by weaning, litter removal, and milk stasis. J. Cell Physiol. 168 559-569.
57. Ren, S., Cai, H. R., Li, M. and Furth, P. A. (2002). Loss of Stat5a delays mammary cancer progression in a mouse model. Oncogene 21, 4335-4339.
58. Russo, J., Rivera, R. and Russo, I. H. (1992). Influence of age and parity on the Development of the human breast. Breast Cancer Res. Treat. 23, 211-218.
59. Schoenenberger, C. A., Andres, A. C., Groner, B., van der Valk, M., LeMeur, M. and Gerlinger, P. (1988). Targeted c-myc gene expression in mammary glands of transgenic mice induces mammary tumours with constitutive milk protein gene transcription. EMBO J. 7, 169-175.
60. Shore, R. E., Hempelmann, L. H., Kowaluk, E., Mansur, P. S., Pasternack, B. S., Albert, R. E. and Haughie, G. E. (1977). Breast neoplasms in women treated with x-rays for acute postpartum mastitis. J. Natl. Cancer Inst. 59, 813-822.
61. Stampfer, M. R., Yaswen, P., Alhadeff, M. and Hosoda, J. (1993). TGF beta induction of extracellular matrix associated proteins in normal and transformed human mammary epithelial cells in culture is independent of growth effects. J. Cell Physiol. 155, 210-221.
62. Stewart, T. A., Pattengale, P. K. and Leder, P. (1984). Spontaneous mammary adenocarcinomas in transgenic mice that carry and express MTV/myc fusion genes. Cell 38, 627-637.
63. Teglund, S., McKay, C., Schuetz, E., van Deursen, J. M., Stravopodis, D., Wang, D., Brown, M., Bodner, S., Grosveld, G. and Ihle, J. N. (1998). Stat5a and Stat5b proteins have essential and nonessential, or redundant, roles in cytokine responses. Cell 93 841-850.
64. Timme, T. L., Goltsov, A., Tahir, S., Li, L., Wang, J., Ren, C., Johnston, R. N. and Thompson, T. C. (2000). Caveolin-1 is regulated by c-myc and suppresses c-myc-induced apoptosis. Oncogene 19, 3256-3265.
65. Watson, P. H., Safneck, J. R., Le, K., Dubik, D. and Shin, R. P. (1993). Relationship of c-myc amplification to progression of breast cancer from in situ to invasive tumor and lymph node metastasis. J. Natl. Cancer Inst. 85, 902-907.