Mechanism and preclinical prevention of increased breast cancer risk caused by pregnancy

eLife

Volumn 2013, Issue 2, 2013, Pages

  Haricharan, Svasti ^a   Dong, Jie ^a   Hein, Sarah ^a   Reddy, Jay P ^a   Du, Zhijun ^a   Toneff, Michael ^a   Holloway, Kimberly ^a   Hilsenbeck, Susan G ^a   Huang, Shixia ^a   Atkinson, Rachel ^b   Woodward, Wendy ^b   Jindal, Sonali ^c   Borges, Virginia F ^c   Gutierrez, Carolina ^a   Zhang, Hong ^b   Schedin, Pepper J ^c   Osborne, C Kent ^a   Tweardy, David J ^a   Li, Yi ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; C188 9; EPIDERMAL GROWTH FACTOR RECEPTOR 2; GLYCOGEN SYNTHASE KINASE 3BETA; JANUS KINASE 2; KI 67 ANTIGEN; N BENZYL 2 CYANO 3 (3, 4 DIHYDROXYPHENYL) ACRYLAMIDE; N BENZYL 2 CYANO 3 (3,4 DIHYDROXYPHENYL)ACRYLAMIDE; PROLACTIN RECEPTOR; PROTEIN BAK; PROTEIN BAX; PROTEIN P53; RUXOLITINIB; STAT1 PROTEIN; STAT3 PROTEIN; STAT5 PROTEIN; STAT5A PROTEIN; STAT6 PROTEIN; UNCLASSIFIED DRUG; WNT1 PROTEIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER GROWTH; CANCER RISK; CARCINOGENESIS; CELL SURVIVAL; CHICKEN; CONTROLLED STUDY; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; LACTATION; MOUSE; NICK END LABELING; NONHUMAN; ONCOGENE; PARITY; PRECANCER; PREGNANCY; RISK FACTOR; VIRAL GENE DELIVERY SYSTEM; WESTERN BLOTTING; ANIMAL; BREAST NEOPLASMS; CELL DIVISION; COMPLICATION; DISEASE MODEL; FEMALE; METABOLISM; MUTATION; PREGNANCY COMPLICATIONS, NEOPLASTIC;

ANIMALS; APOPTOSIS; BREAST NEOPLASMS; CARCINOGENESIS; CELL DIVISION; DISEASE MODELS, ANIMAL; FEMALE; MICE; MUTATION; ONCOGENES; PREGNANCY; PREGNANCY COMPLICATIONS, NEOPLASTIC; STAT5 TRANSCRIPTION FACTOR;

EID: 84891749436     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.00996     Document Type: Article

References (72)

1. Andrechek ER, Hardy WR, Laing MA, Muller WJ. 2004. Germ-line expression of an oncogenic erbB2 allele confers resistance to erbB2-induced mammary tumorigenesis. Proceedings of the National Academy of Sciences of the United States of America 101:4984-4989. doi: 10.1073/pnas.0306802101.
2. Bargmann CI, Weinberg RA. 1988. Oncogenic activation of the neu-encoded receptor protein by point mutation and deletion. The EMBO Journal 7:2043-2052.
3. Bartow SA, Pathak DR, Black WC, Key CR, Teaf SR. 1987. Prevalence of benign, atypical, and malignant breast lesions in populations at different risk for breast cancer. A forensic autopsy study. Cancer 60:2751-2760. doi: 10.1002/1097-0142(19871201)60:11<2751::AID-CNCR2820601127>3.0.CO;2-M.
4. Baselga J, Swain SM. 2009. Novel anticancer targets: revisiting ERBB2 and discovering ERBB3. Nature Reviews Cancer 9:463-475. doi: 10.1038/nrc2656.
5. Bode AM, Dong Z. 2009. Cancer prevention research-then and now. Nature Reviews Cancer 9:508-516. doi: 10.1038/nrc2646.
6. Borges VF, Schedin PJ. 2012. Pregnancy-associated breast cancer: an entity needing refinement of the definition. Cancer 118:3226-3228. doi: 10.1002/cncr.26643.
7. Brockman JL, Schroeder MD, Schuler LA. 2002. PRL activates the cyclin D1 promoter via the Jak2/Stat pathway. Molecular Endocrinology 16:774-784. doi: 10.1210/me.16.4.774.
8. Bu W, Xin L, Toneff M, Li L, Li Y. 2009. Lentivirus vectors for stably introducing genes into mammary epithelial cells in vivo. Journal of Mammary Gland Biology and Neoplasia 14:401-404. doi: 10.1007/s10911-009-9154-4.
9. Burdelya L, Catlett-Falcone R, Levitzki A, Cheng F, Mora LB, Sotomayor E, Coppola D, Sun J, Sebti S, Dalton WS, Jove R, Yu H. 2002. Combination therapy with AG-490 and interleukin 12 achieves greater antitumor effects than either agent alone. Molecular Cancer Therapeutics 1:893-899.
10. Chapman RS, Lourenco PC, Tonner E, Flint DJ, Selbert S, Takeda K, Akira S, Clarke AR, Watson CJ. 1999. Suppression of epithelial apoptosis and delayed mammary gland involution in mice with a conditional knockout of Stat3. Genes and Development 13:2604-2616. doi: 10.1101/gad.13.19.2604.
11. Cotarla I, Ren S, Zhang Y, Gehan E, Singh B, Furth PA. 2004. Stat5a is tyrosine phosphorylated and nuclear localized in a high proportion of human breast cancers. International Journal of Cancer 108:665-671. doi: 10.1002/ijc.11619.
12. Crowley C, Curtis HJ. 1963. The development of somatic mutations in mice with age. Proceedings of the National Academy of Sciences of the United States of America 49:626-628. doi: 10.1073/pnas.49.5.626.
13. Degnim AC, Visscher DW, Berman HK, Frost MH, Sellers TA, Vierkant RA, Maloney SD, Pankratz VS, de Groen PC, Lingle WL, Ghosh K, Penheiter L, Tlsty T, Melton LJ III, Reynolds CA, Hartmann LC. 2007. Stratification of breast cancer risk in women with atypia: a Mayo cohort study. Journal of Clinical Oncology 25:2671-2677. doi: 10.1200/JCO.2006.09.0217.
14. Dong J, Tong T, Reynado AM, Rosen JM, Huang S, Li Y. 2010. Genetic manipulation of individual somatic mammary cells in vivo reveals a master role of STAT5a in inducing alveolar fate commitment and lactogenesis even in the absence of ovarian hormones. Developmental Biology 346:196-203. doi: 10.1016/j.ydbio.2010.07.027.
15. Du Z, Podsypanina K, Huang S, McGrath A, Toneff MJ, Bogoslovskaia E, Zhang X, Moraes RC, Fluck M, Allred DC, Lewis MT, Varmus HE, Li Y. 2006. Introduction of oncogenes into mammary glands in vivo with an avian retroviral vector initiates and promotes carcinogenesis in mouse models. Proceedings of the National Academy of Sciences of the United States of America 103:17396-17401. doi: 10.1073/pnas.0608607103.
16. Dunn KJ, Williams BO, Li Y, Pavan WJ. 2000. Neural crest-directed gene transfer demonstrates Wnt1 role in melanocyte expansion and differentiation during mouse development. Proceedings of the National Academy of Sciences of the United States of America 97:10050-10055. doi: 10.1073/pnas.97.18.10050.
17. Furth PA, Nakles RE, Millman S, Diaz-Cruz ES, Cabrera MC. 2011. Signal transducer and activator of transcription 5 as a key signaling pathway in normal mammary gland developmental biology and breast cancer. Breast Cancer Research: BCR 13:220. doi: 10.1186/bcr2921.
18. Gazit A, Osherov N, Posner I, Yaish P, Poradosu E, Gilon C, Levitzki A. 1991. Tyrphostins. 2. Heterocyclic and alpha-substituted benzylidenemalononitrile tyrphostins as potent inhibitors of EGF receptor and ErbB2/neu tyrosine kinases. Journal of Medicinal Chemistry 34:1896-1907. doi: 10.1021/jm00110a022.
19. Green DR, Kroemer G. 2009. Cytoplasmic functions of the tumour suppressor p53. Nature 458:1127-1130. doi: 10.1038/nature07986.
20. Guzman RC, Yang J, Rajkumar L, Thordarson G, Chen X, Nandi S. 1999. Hormonal prevention of breast cancer: mimicking the protective effect of pregnancy. Proceedings of the National Academy of Sciences of the United States of America 96:2520-2525. doi: 10.1073/pnas.96.5.2520.
21. Halazonetis TD, Gorgoulis VG, Bartek J. 2008. An oncogene-induced DNA damage model for cancer development. Science 319:1352-1355. doi: 10.1126/science.1140735.
22. Hand TW, Cui W, Jung YW, Sefik E, Joshi NS, Chandele A, Liu Y, Kaech SM. 2010. Differential effects of STAT5 and PI3K/AKT signaling on effector and memory CD8 T-cell survival. Proceedings of the National Academy of Sciences of the United States of America 107:16601-16606. doi: 10.1073/pnas.1003457107.
23. Haricharan S, Hein S, Toneff MJ, Dong J, Aina OH, Rao PH, Cardiff RD, Li Y. 2013. Contribution of an alveolar cell of origin to the aggressive phenotype of pregnancy-associated breast cancer. Oncogene. doi: 10.1038/onc.2013.521.
24. Haricharan S, Li Y. 2014. STAT signaling in mammary gland differentiation, cell survival and tumorigenesis. Molecular and Cellular Endocrinology 382:560-569. (Available online 28 March 2013) doi: 10.1016/j.mce.2013.03.014.
25. Hennighausen L, Robinson GW. 1998. Think globally, act locally: the making of a mouse mammary gland. Genes and Development 12:449-455. doi: 10.1101/gad.12.4.449.
26. Hennighausen L, Robinson GW. 2001. Signaling pathways in mammary gland development. Developmental Cell 1:467-475. doi: 10.1016/S1534-5807(01)00064-8.
27. Hennighausen L, Robinson GW. 2005. Information networks in the mammary gland. Nature Reviews Molecular Cell Biology 6:715-725. doi: 10.1038/nrm1714.
28. Hennighausen L, Robinson GW. 2008. Interpretation of cytokine signaling through the transcription factors STAT5A and STAT5B. Genes and Development 22:711-721. doi: 10.1101/gad.1643908.
29. Henry MD, Triplett AA, Oh KB, Smith GH, Wagner KU. 2004. Parity-induced mammary epithelial cells facilitate tumorigenesis in MMTV-neu transgenic mice. Oncogene 23:6980-6985. doi: 10.1038/sj.onc.1207827.
30. Humphreys RC, Hennighausen L. 1999. Signal transducer and activator of transcription 5a influences mammary epithelial cell survival and tumorigenesis. Cell Growth and Differentiation: the Molecular Biology Journal of the American Association for Cancer Research 10:685-694.
31. Hutchinson L. 2011. Prevention: MAPping out breast cancer chemoprevention. Nature Reviews Clinical Oncology 8:445. doi: 10.1038/nrclinonc.2011.102.
32. Iavnilovitch E, Groner B, Barash I. 2002. Overexpression and forced activation of stat5 in mammary gland of transgenic mice promotes cellular proliferation, enhances differentiation, and delays postlactational apoptosis. Molecular Cancer Research 1:32-47.
33. Jeselsohn R, Brown NE, Arendt L, Klebba I, Hu MG, Kuperwasser C, Hinds PW. 2010. Cyclin D1 kinase activity is required for the self-renewal of mammary stem and progenitor cells that are targets of MMTV-ErbB2 tumorigenesis. Cancer Cell 17:65-76. doi: 10.1016/j.ccr.2009.11.024.
34. Kazansky AV, Raught B, Lindsey SM, Wang YF, Rosen JM. 1995. Regulation of mammary gland factor/Stat5a during mammary gland development. Molecular Endocrinology 9:1598-1609. doi: 10.1210/me.9.11.1598.
35. Khaled WT, Read EK, Nicholson SE, Baxter FO, Brennan AJ, Came PJ, Sprigg N, McKenzie AN, Watson CJ. 2007. The IL-4/IL-13/Stat6 signalling pathway promotes luminal mammary epithelial cell development. Development 134:2739-2750. doi: 10.1242/dev.003194.
36. Klaus A, Birchmeier W. 2008. Wnt signalling and its impact on development and cancer. Nature Reviews Cancer 8:387-398. doi: 10.1038/nrc2389.
37. Kreuzaler PA, Staniszewska AD, Li W, Omidvar N, Kedjouar B, Turkson J, Poli V, Flavell RA, Clarkson RW, Watson CJ. 2011. Stat3 controls lysosomal-mediated cell death in vivo. Nature Cell Biology 13:303-309. doi: 10.1038/ncb2171.
38. Levitzki A, Gazit A. 1995. Tyrosine kinase inhibition: an approach to drug development. Science 267:1782-1788. doi: 10.1126/science.7892601.
39. Li M, Liu X, Robinson G, Bar-Peled U, Wagner KU, Young WS, Hennighausen L, Furth PA. 1997. Mammary-derived signals activate programmed cell death during the first stage of mammary gland involution. Proceedings of the National Academy of Sciences of the United States of America 94:3425-3430. doi: 10.1073/pnas.94.7.3425.
40. Li Y, Ferris A, Lewis BC, Orsulic S, Williams BO, Holland EC, Hughes SH. 2011. The RCAS/TVA somatic gene transfer method in modeling human cancer. In: Green JE, Ried T, editors. Genetically-engineered mice for cancer research: design, analysis, pathways, validation and pre-clinical testing. Springer. p. 83-111.
41. Li Y, Podsypanina K, Liu X, Crane A, Tan LK, Parsons R, Varmus HE. 2001. Deficiency of Pten accelerates mammary oncogenesis in MMTV-Wnt-1 transgenic mice. BMC Molecular Biology 2:2. doi: 10.1186/1471-2199-2-2.
42. Li Y, Welm B, Podsypanina K, Huang S, Chamorro M, Zhang X, Rowlands T, Egeblad M, Cowin P, Werb Z, Tan LK, Rosen JM, Varmus HE. 2003. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proceedings of the National Academy of Sciences of the United States of America 100:15853-15858. doi: 10.1073/pnas.2136825100.
43. Liu X, Robinson GW, Gouilleux F, Groner B, Hennighausen L. 1995. Cloning and expression of Stat5 and an additional homologue (Stat5b) involved in prolactin signal transduction in mouse mammary tissue. Proceedings of the National Academy of Sciences of the United States of America 92:8831-8835. doi: 10.1073/pnas.92.19.8831.
44. Liu X, Robinson GW, Wagner KU, Garrett L, Wynshaw-Boris A, Hennighausen L. 1997. Stat5a is mandatory for adult mammary gland development and lactogenesis. Genes and Development 11:179-186. doi: 10.1101/gad.11.2.179.
45. Lord JD, McIntosh BC, Greenberg PD, Nelson BH. 2000. The IL-2 receptor promotes lymphocyte proliferation and induction of the c-myc, bcl-2, and bcl-x genes through the trans-activation domain of Stat5. The Journal of Immunology 164:2533-2541.
46. Lowe SW, Cepero E, Evan G. 2004. Intrinsic tumour suppression. Nature 432:307-315. doi: 10.1038/nature03098.
47. Lynch M. 2010. Rate, molecular spectrum, and consequences of human mutation. Proceedings of the National Academy of Sciences of the United States of America 107:961-968. doi: 10.1073/pnas.0912629107.
48. Lyons TR, O'Brien J, Borges VF, Conklin MW, Keely PJ, Eliceiri KW, Marusyk A, Tan AC, Schedin P. 2011. Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nature medicine 17:1109-1115. doi: 10.1038/nm.2416.
49. MacMahon B, Cole P, Lin TM, Lowe CR, Mirra AP, Ravnihar B, Salber EJ, Valaoras VG, Yuasa S. 1970. Age at first birth and breast cancer risk. Bulletin of the World Health Organization 43:209-221.
50. Matsumura I, Kitamura T, Wakao H, Tanaka H, Hashimoto K, Albanese C, Downward J, Pestell RG, Kanakura Y. 1999. Transcriptional regulation of the cyclin D1 promoter by STAT5: its involvement in cytokine-dependent growth of hematopoietic cells. The EMBO Journal 18:1367-1377. doi: 10.1093/emboj/18.5.1367.
51. Medina D. 2004. Breast cancer: the protective effect of pregnancy. Clinical Cancer Research 10:380S-384S. doi: 10.1158/1078-0432.CCR-031211.
52. Medina D, Sivaraman L, Hilsenbeck SG, Conneely O, Ginger M, Rosen J, Omalle BW. 2001. Mechanisms of hormonal prevention of breast cancer. Annals of the New York Academy of Sciences 952:23-35. doi: 10.1111/j.1749-6632.2001.tb02725.x.
53. Moraes RC, Zhang X, Harrington N, Fung JY, Wu MF, Hilsenbeck SG, Allred DC, Lewis MT. 2007. Constitutive activation of smoothened (SMO) in mammary glands of transgenic mice leads to increased proliferation, altered differentiation and ductal dysplasia. Development 134:1231-1242. doi: 10.1242/dev.02797.
54. Nevalainen MT, Xie J, Torhorst J, Bubendorf L, Haas P, Kononen J, Sauter G, Rui H. 2004. Signal transducer and activator of transcription-5 activation and breast cancer prognosis. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology 22:2053-2060. doi: 10.1200/JCO.2004.11.046.
55. Nielsen M, Thomsen JL, Primdahl S, Dyreborg U, Andersen JA. 1987. Breast cancer and atypia among young and middle-aged women: a study of 110 medicolegal autopsies. British Journal of Cancer 56:814-819. doi: 10.1038/bjc.1987.296.
56. Peck AR, Witkiewicz AK, Liu C, Stringer GA, Klimowicz AC, Pequignot E, Freydin B, Tran TH, Yang N, Rosenberg AL, Hooke JA, Kovatich AJ, Nevalainen MT, Shriver CD, Hyslop T, Sauter G, Rimm DL, Magliocco AM, Rui H. 2011. Loss of nuclear localized and tyrosine phosphorylated Stat5 in breast cancer predicts poor clinical outcome and increased risk of antiestrogen therapy failure. Journal of Clinical Oncology: Official Journal of the American Society of Clinical Oncology 29:2448-2458. doi: 10.1200/JCO.2010.30.3552.
57. Plotnikov A, Li Y, Tran TH, Tang W, Palazzo JP, Rui H, Fuchs SY. 2008. Oncogene-mediated inhibition of glycogen synthase kinase 3 beta impairs degradation of prolactin receptor. Cancer Research 68:1354-1361. doi: 10.1158/0008-5472.CAN-07-6094.
58. Plotnikov A, Varghese B, Tran TH, Liu C, Rui H, Fuchs SY. 2009. Impaired turnover of prolactin receptor contributes to transformation of human breast cells. Cancer Research 69:3165-3172. doi: 10.1158/0008-5472.CAN-08-4033.
59. Polyak K. 2006. Pregnancy and breast cancer: the other side of the coin. Cancer Cell 9:151-153. doi: 10.1016/j.ccr.2006.02.026.
60. Quintas-Cardama A, Vaddi K, Liu P, Manshouri T, Li J, Scherle PA, Caulder E, Wen X, Li Y, Waeltz P, Rupar M, Burn T, Lo Y, Kelley J, Covington M, Shepard S, Rodgers JD, Haley P, Kantarjian H, Fridman JS, Verstovsek S. 2010. Preclinical characterization of the selective JAK1/2 inhibitor INCB018424: therapeutic implications for the treatment of myeloproliferative neoplasms. Blood 115:3109-3117. doi: 10.1182/blood-2009-04-214957.
61. Reddy JP, Peddibhotla S, Bu W, Zhao J, Haricharan S, Du YC, Podsypanina K, Rosen JM, Donehower LA, Li Y. 2010. Defining the ATM-mediated barrier to tumorigenesis in somatic mammary cells following ErbB2 activation. Proceedings of the National Academy of Sciences of the United States of America 107:3728-3733. doi: 10.1073/pnas.0910665107.
62. Redell MS, Ruiz MJ, Alonzo TA, Gerbing RB, Tweardy DJ. 2011. Stat3 signaling in acute myeloid leukemia: ligand-dependent and-independent activation and induction of apoptosis by a novel small-molecule Stat3 inhibitor. Blood 117:5701-5709. doi: 10.1182/blood-2010-04-280123.
63. Ren S, Cai HR, Li M, Furth PA. 2002. Loss of Stat5a delays mammary cancer progression in a mouse model. Oncogene 21:4335-4339. doi: 10.1038/sj.onc.1205484.
64. Schedin P. 2006. Pregnancy-associated breast cancer and metastasis. Nature Reviews Cancer 6:281-291. doi: 10.1038/nrc1839.
65. Socolovsky M, Nam H, Fleming MD, Haase VH, Brugnara C, Lodish HF. 2001. Ineffective erythropoiesis in Stat5a(-/-)5b(-/-) mice due to decreased survival of early erythroblasts. Blood 98:3261-3273. doi: 10.1182/blood.V98.12.3261.
66. Toneff MJ, Du Z, Dong J, Huang J, Sinai P, Forman J, Hilsenbeck S, Schiff R, Huang S, Li Y. 2010. Somatic expression of PyMT or activated ErbB2 induces estrogen-independent mammary tumorigenesis. Neoplasia 12:718-726.
67. Vafaizadeh V, Klemmt PA, Groner B. 2012. Stat5 assumes distinct functions in mammary gland development and mammary tumor formation. Frontiers in Bioscience: a Journal and Virtual Library 17:1232-1250. doi: 10.2741/3983.
68. Vargo-Gogola T, Rosen JM. 2007. Modelling breast cancer: one size does not fit all. Nature Reviews Cancer 7:659-672. doi: 10.1038/nrc2193.
69. Wagner KU, Rui H. 2008. Jak2/Stat5 signaling in mammogenesis, breast cancer initiation and progression. Journal of Mammary Gland Biology and Neoplasia 13:93-103. doi: 10.1007/s10911-008-9062-z.
70. Watson CJ. 2001. Stat transcription factors in mammary gland development and tumorigenesis. Journal of Mammary Gland Biology and Neoplasia 6:115-127. doi: 10.1023/A:1009524817155.
71. Welch HG, Black WC. 1997. Using autopsy series to estimate the disease "reservoir" for ductal carcinoma in situ of the breast: how much more breast cancer can we find? Annals of Internal Medicine 127:1023-1028. doi: 10.7326/0003-4819-127-11-199712010-00014.
72. Xu X, Kasembeli MM, Jiang X, Tweardy BJ, Tweardy DJ. 2009. Chemical probes that competitively and selectively inhibit Stat3 activation. PLOS ONE 4:e4783. doi: 10.1371/journal.pone.0004783.