Parity induces differentiation and reduces Wnt/Notch signaling ratio and proliferation potential of basal stem/progenitor cells isolated from mouse mammary epithelium

Breast Cancer Research

Volumn 15, Issue 2, 2013, Pages

  Meier Abt, Fabienne ^a,b   Milani, Emanuela ^a,b   Roloff, Tim ^a   Brinkhaus, Heike ^a   Duss, Stephan ^a   Meyer, Dominique S ^a,b   Klebba, Ina ^a   Balwierz, Piotr J ^c   van Nimwegen, Erik ^c   Bentires Alj, Mohamed ^a  

^a FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ESTROGEN RECEPTOR; LYMPHOID ENHANCER FACTOR 1; NOTCH RECEPTOR; PROGESTERONE RECEPTOR; TRANSCRIPTION FACTOR 7 LIKE 1; TRANSCRIPTOME; WNT PROTEIN; WNT4 PROTEIN; BETA CATENIN; LY ANTIGEN; LY6A PROTEIN, MOUSE; MEMBRANE PROTEIN; MESSENGER RNA; TUMOR MARKER;

ANIMAL CELL; ARTICLE; BIOINFORMATICS; BREAST CARCINOGENESIS; BREAST EPITHELIUM; CELL DIFFERENTIATION; CELL ISOLATION; CELL PROLIFERATION; CELL SUBPOPULATION; COLONY FORMATION; DOWN REGULATION; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; GENETIC VARIABILITY; GENOMICS; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MOUSE; MYOEPITHELIUM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PARITY; PROTEIN EXPRESSION; PROTEIN SECRETION; STEM CELL; UPREGULATION; WNT SIGNALING PATHWAY; ANIMAL; CELL CULTURE; CFU COUNTING; CYTOLOGY; DNA MICROARRAY; ENZYME IMMUNOASSAY; EPITHELIUM; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PATHOLOGY; PREGNANCY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; UDDER; WESTERN BLOTTING;

ANIMALS; ANTIGENS, LY; BETA CATENIN; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; COLONY-FORMING UNITS ASSAY; EPITHELIUM; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION PROFILING; IMMUNOENZYME TECHNIQUES; MAMMARY GLANDS, ANIMAL; MEMBRANE PROTEINS; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PARITY; PREGNANCY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, NOTCH; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SIGNAL TRANSDUCTION; STEM CELLS; TUMOR MARKERS, BIOLOGICAL; WNT PROTEINS;

EID: 84876800737     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3419     Document Type: Article

References (64)

1. MacMahon B, Cole P, Lin TM, Lowe CR, Mirra AP, Ravnihar B, Salber EJ, Valaoras VG, Yuasa S. Age at first birth and breast cancer risk. Bull World Health Org 1970, 43:209-221. 2427645, 5312521.
2. Albrektsen G, Heuch I, Hansen S, Kvale G. Breast cancer risk by age at birth, time since birth and time intervals between births: exploring interaction effects. Br J Cancer 2005, 92:167-175. 10.1038/sj.bjc.6602302, 2361726, 15597097.
3. Medina D. Mammary developmental fate and breast cancer risk. Endocr Relat Cancer 2005, 12:483-495. 10.1677/erc.1.00804, 16172188.
4. Rajkumar L, Kittrell FS, Guzman RC, Brown PH, Nandi S, Medina D. Hormone-induced protection of mammary tumorigenesis in genetically engineered mouse models. Breast Cancer Res 2007, 9:R12. 10.1186/bcr1645, 1851398, 17257424.
5. Thordarson G, Jin E, Guzman RC, Swanson SM, Nandi S, Talamantes F. Refractoriness to mammary tumorigenesis in parous rats: is it caused by persistent changes in the hormonal environment or permanent biochemical alterations in the mammary epithelia?. Carcinogenesis 1995, 16:2847-2853. 10.1093/carcin/16.11.2847, 7586208.
6. Schedin P, Mitrenga T, McDaniel S, Kaeck M. Mammary ECM composition and function are altered by reproductive state. Mol Carcinog 2004, 41:207-220. 10.1002/mc.20058, 15468292.
7. Russo J, Moral R, Balogh GA, Mailo D, Russo IH. The protective role of pregnancy in breast cancer. Breast Cancer Res 2005, 7:131-142. 10.1186/bcr1029, 1143568, 15987443.
8. Russo J, Balogh GA, Russo IH. Full-term pregnancy induces a specific genomic signature in the human breast. Cancer Epidemiol Biomarkers Prev 2008, 17:51-66. 10.1158/1055-9965.EPI-07-0678, 18199711.
9. D'Cruz CM, Moody SE, Master SR, Hartman JL, Keiper EA, Imielinski MB, Cox JD, Wang JY, Ha SI, Keister BA, Chodosh LA. Persistent parity-induced changes in growth factors, TGF-beta3, and differentiation in the rodent mammary gland. Mol Endocrinol 2002, 16:2034-2051. 10.1210/me.2002-0073, 12198241.
10. Blakely CM, Stoddard AJ, Belka GK, Dugan KD, Notarfrancesco KL, Moody SE, D'Cruz CM, Chodosh LA. Hormone-induced protection against mammary tumorigenesis is conserved in multiple rat strains and identifies a core gene expression signature induced by pregnancy. Cancer Res 2006, 66:6421-6431. 10.1158/0008-5472.CAN-05-4235, 16778221.
11. Lindeman GJ, Visvader JE. Insights into the cell of origin in breast cancer and breast cancer stem cells. Asia Pac J Clin Oncol 2010, 6:89-97. 10.1111/j.1743-7563.2010.01279.x, 20565420.
12. Deome KB, Faulkin LJ, Bern HA, Blair PB. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Res 1959, 19:515-520.
13. Bruno RD, Smith GH. Functional characterization of stem cell activity in the mouse mammary gland. Stem Cell Rev 2011, 7:238-247. 10.1007/s12015-010-9191-9, 3492888, 20853073.
14. Van Keymeulen A, Rocha AS, Ousset M, Beck B, Bouvencourt G, Rock J, Sharma N, Dekoninck S, Blanpain C. Distinct stem cells contribute to mammary gland development and maintenance. Nature 2011, 479:189-193. 10.1038/nature10573, 21983963.
15. van Amerongen R, Bowman AN, Nusse R. Developmental stage and time dictate the fate of Wnt/beta-catenin-responsive stem cells in the mammary gland. Cell Stem Cell 2012, 11:387-400. 10.1016/j.stem.2012.05.023, 22863533.
16. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, Li HI, Eaves CJ. Purification and unique properties of mammary epithelial stem cells. Nature 2006, 439:993-997.
17. Sleeman KE, Kendrick H, Robertson D, Isacke CM, Ashworth A, Smalley MJ. Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. J Cell Biol 2007, 176:19-26. 10.1083/jcb.200604065, 2063618, 17190790.
18. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, Wu L, Lindeman GJ, Visvader JE. Generation of a functional mammary gland from a single stem cell. Nature 2006, 439:84-88. 10.1038/nature04372, 16397499.
19. Smalley MJ, Kendrick H, Sheridan JM, Regan JL, Prater MD, Lindeman GJ, Watson CJ, Visvader JE, Stingl J. Isolation of mouse mammary epithelial subpopulations: a comparison of leading methods. J Mammary Gland Biol Neoplasia 2012, 17:91-97. 10.1007/s10911-012-9257-1, 22644112.
20. Siwko SK, Dong J, Lewis MT, Liu H, Hilsenbeck SG, Li Y. Evidence that an early pregnancy causes a persistent decrease in the number of functional mammary epithelial stem cells: implications for pregnancy-induced protection against breast cancer. Stem Cells 2008, 26:3205-3209. 10.1634/stemcells.2008-0103, 2647777, 18787212.
21. Britt KL, Kendrick H, Regan JL, Molyneux G, Magnay FA, Ashworth A, Smalley MJ. Pregnancy in the mature adult mouse does not alter the proportion of mammary epithelial stem/progenitor cells. Breast Cancer Res 2009, 11:R20. 10.1186/bcr2245, 2688949, 19386118.
22. Smalley MJ, Titley J, O'Hare MJ. Clonal characterization of mouse mammary luminal epithelial and myoepithelial cells separated by fluorescence-activated cell sorting. Vitro Cell Dev Biol Anim 1998, 34:711-721.
23. Stingl J, Eaves CJ, Zandieh I, Emerman JT. Characterization of bipotent mammary epithelial progenitor cells in normal adult human breast tissue. Breast Cancer Res Treat 2001, 67:93-109. 10.1023/A:1010615124301, 11519870.
24. Roarty K, Rosen JM. Wnt and mammary stem cells: hormones cannot fly wingless. Curr Opin Pharmacol 2010, 10:643-649. 10.1016/j.coph.2010.07.004, 2981611, 20810315.
25. Many AM, Brown AM. Mammary stem cells and cancer: roles of Wnt signaling in plain view. Breast Cancer Res 2010, 12:313. 3096951, 20887643.
26. Sleeman KE, Kendrick H, Ashworth A, Isacke CM, Smalley MJ. CD24 staining of mouse mammary gland cells defines luminal epithelial, myoepithelial/basal and non-epithelial cells. Breast Cancer Res 2006, 8:R7. 10.1186/bcr1371, 1413978, 16417656.
27. Smalley MJ. Isolation, culture and analysis of mouse mammary epithelial cells. Methods Mol Biol 2010, 633:139-170. 10.1007/978-1-59745-019-5_11, 20204626.
28. GSEA homepage. http://www.broadinstitute.org/gsea
29. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA 2005, 102:15545-15550. 10.1073/pnas.0506580102, 1239896, 16199517.
30. Edgar R, Domrachev M, Lash AE. Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210. 10.1093/nar/30.1.207, 99122, 11752295.
31. Gonzalez RC, Woods RE, Eddins SL. Digital Image Processing using MATLAB 2009, Knoxville, TN: Gatesmark Publishing.
32. ISMARA. http://www.mara.unibas.ch
33. Palmer HG, Anjos-Afonso F, Carmeliet G, Takeda H, Watt FM. The vitamin D receptor is a Wnt effector that controls hair follicle differentiation and specifies tumor type in adult epidermis. PLoS One 2008, 3:e1483. 10.1371/journal.pone.0001483, 2198947, 18213391.
34. Oikonomopoulos A, Sereti KI, Conyers F, Bauer M, Liao A, Guan J, Crapps D, Han JK, Dong H, Bayomy AF, Fine GC, Westerman K, Biechele TL, Moon RT, Force T, Liao R. Wnt signaling exerts an antiproliferative effect on adult cardiac progenitor cells through IGFBP3. Circ Res 2011, 109:1363-1374. 10.1161/CIRCRESAHA.111.250282, 3384997, 22034491.
35. Yao HH, Matzuk MM, Jorgez CJ, Menke DB, Page DC, Swain A, Capel B. Follistatin operates downstream of Wnt4 in mammalian ovary organogenesis. Dev Dyn 2004, 230:210-215. 10.1002/dvdy.20042, 15162500.
36. Willert J, Epping M, Pollack JR, Brown PO, Nusse R. A transcriptional response to Wnt protein in human embryonic carcinoma cells. BMC Dev Biol 2002, 2:8. 10.1186/1471-213X-2-8, 117803, 12095419.
37. Borggrefe T, Oswald F. The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell Mol Life Sci 2009, 66:1631-1646. 10.1007/s00018-009-8668-7, 19165418.
38. Suzuki H, Forrest AR, van Nimwegen E, Daub CO, Balwierz PJ, Irvine KM, Lassmann T, Ravasi T, Hasegawa Y, de Hoon MJ, Katayama S, Schroder K, Carninci P, Tomaru Y, Kanamori-Katayama M, Kubosaki A, Akalin A, Ando Y, Arner E, Asada M, Asahara H, Bailey T, Bajic VB, Bauer D, Beckhouse AG, Bertin N, Björkegren J, Brombacher F, Bulger E, et al. FANTOM Consortium The transcriptional network that controls growth arrest and differentiation in a human myeloid leukemia cell line. Nat Genet 2009, 41:553-562. 10.1038/ng.375, 19377474, FANTOM Consortium.
39. Sivaraman L, Conneely OM, Medina D, O'Malley BW. p53 is a potential mediator of pregnancy and hormone-induced resistance to mammary carcinogenesis. Proc Natl Acad Sci USA 2001, 98:12379-12384. 10.1073/pnas.221459098, 60062, 11606748.
40. Ingenuity Systems. http://www.ingenuity.com
41. Yi F, Pereira L, Hoffman JA, Shy BR, Yuen CM, Liu DR, Merrill BJ. Opposing effects of Tcf3 and Tcf1 control Wnt stimulation of embryonic stem cell self-renewal. Nat Cell Biol 2011, 13:762-770. 10.1038/ncb2283, 3129424, 21685894.
42. Cowling VH, Cole MD. Turning the tables: Myc activates Wnt in breast cancer. Cell Cycle 2007, 6:2625-2627. 10.4161/cc.6.21.4880, 17726380.
43. Zeng YA, Nusse R. Wnt proteins are self-renewal factors for mammary stem cells and promote their long-term expansion in culture. Cell Stem Cell 2010, 6:568-577. 10.1016/j.stem.2010.03.020, 2917779, 20569694.
44. Bouras T, Pal B, Vaillant F, Harburg G, Asselin-Labat ML, Oakes SR, Lindeman GJ, Visvader JE. Notch signaling regulates mammary stem cell function and luminal cell-fate commitment. Cell Stem Cell 2008, 3:429-441. 10.1016/j.stem.2008.08.001, 18940734.
45. Visvader JE, Smith GH. Murine mammary epithelial stem cells: discovery, function, and current status. Cold Spring Harb Perspect Biol 2011, 3:a004879. 10.1101/cshperspect.a004879, 3039534,3039534, 20926515.
46. Brisken C, Heineman A, Chavarria T, Elenbaas B, Tan J, Dey SK, McMahon JA, McMahon AP, Weinberg RA. Essential function of Wnt-4 in mammary gland development downstream of progesterone signaling. Genes Dev 2000, 14:650-654. 316462, 10733525.
47. Rajaram RD, Brisken C. Role of canonical Wnt signaling in mammary gland development. PhD Thesis. ISREC, School of Life Sciences Ecole Polytechnique Federal (EPFL) 2009,
48. Plaks V, Brenot A, Lawson DA, Linnemann JR, Van Kappel EC, Wong KC, de Sauvage F, Klein OD, Werb Z. Lgr5-expressing cells are sufficient and necessary for postnatal mammary gland organogenesis. Cell Rep 2013, 3:70-78. 10.1016/j.celrep.2012.12.017, 3563842, 23352663.
49. Raouf A, Zhao Y, To K, Stingl J, Delaney A, Barbara M, Iscove N, Jones S, McKinney S, Emerman J, Aparicio S, Marra M, Eaves C. Transcriptome analysis of the normal human mammary cell commitment and differentiation process. Cell Stem Cell 2008, 3:109-118. 10.1016/j.stem.2008.05.018, 18593563.
50. Munoz-Descalzo S, de Navascues J, Arias AM. Wnt-Notch signalling: an integrated mechanism regulating transitions between cell states. Bioessays 2012, 34:110-118. 10.1002/bies.201100102, 22215536.
51. Taylor D, Pearce CL, Hovanessian-Larsen L, Downey S, Spicer DV, Bartow S, Pike MC, Wu AH, Hawes D. Progesterone and estrogen receptors in pregnant and premenopausal non-pregnant normal human breast. Breast Cancer Res Treat 2009, 118:161-168. 10.1007/s10549-009-0322-4, 19205874.
52. Wu CI, Hoffman JA, Shy BR, Ford EM, Fuchs E, Nguyen H, Merrill BJ. Function of Wnt/beta-catenin in counteracting Tcf3 repression through the Tcf3-beta-catenin interaction. Development 2012, 139:2118-2129. 10.1242/dev.076067, 3357906, 22573616.
53. Visvader JE, Lindeman GJ. Cancer stem cells: current status and evolving complexities. Cell Stem Cell 2012, 10:717-728. 10.1016/j.stem.2012.05.007, 22704512.
54. Visvader JE. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev 2009, 23:2563-2577. 10.1101/gad.1849509, 2779757, 19933147.
55. Gauger KJ, Hugh JM, Troester MA, Schneider SS. Down-regulation of sfrp1 in a mammary epithelial cell line promotes the development of a cd44high/cd24low population which is invasive and resistant to anoikis. Cancer Cell Int 2009, 9:11. 10.1186/1475-2867-9-11, 2687411, 19422694.
56. Du WW, Yang BB, Shatseva TA, Yang BL, Deng Z, Shan SW, Lee DY, Seth A, Yee AJ. Versican G3 promotes mouse mammary tumor cell growth, migration, and metastasis by influencing EGF receptor signaling. PLoS One 2010, 5:e13828. 10.1371/journal.pone.0013828, 2974650, 21079779.
57. 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. Evidence that transgenes encoding components of the Wnt signaling pathway preferentially induce mammary cancers from progenitor cells. Proc Natl Acad Sci USA 2003, 100:15853-15858. 10.1073/pnas.2136825100, 307657, 14668450.
58. Medina D, Kittrell FS. p53 function is required for hormone-mediated protection of mouse mammary tumorigenesis. Cancer Res 2003, 63:6140-6143.
59. Dunphy KA, Blackburn AC, Yan H, O'Connell LR, Jerry DJ. Estrogen and progesterone induce persistent increases in p53-dependent apoptosis and suppress mammary tumors in BALB/c-Trp53+/- mice. Breast Cancer Res 2008, 10:R43. 10.1186/bcr2094, 2481490, 18471300.
60. Colditz GA, Rosner BA, Chen WY, Holmes MD, Hankinson SE. Risk factors for breast cancer according to estrogen and progesterone receptor status. J Natl Cancer Inst 2004, 96:218-228. 10.1093/jnci/djh025, 14759989.
61. Guzman RC, Yang J, Rajkumar L, Thordarson G, Chen X, Nandi S. Hormonal prevention of breast cancer: mimicking the protective effect of pregnancy. Proc Natl Acad Sci USA 1999, 96:2520-2525. 10.1073/pnas.96.5.2520, 26817, 10051675.
62. Smith GH, Salomon DS, Vonderhar BK. Re: "Evidence that an early pregnancy causes a persistent decrease in the number of functional mammary epithelial stem cells-implications for pregnancy-induced protection against breast cancer" by Siwko et al Stem Cells 2009, 27:1223. author reply 1224-1225, 10.1002/stem.19, 19418459.
63. Han LQ, Yang GY, Zhu HS, Wang YY, Wang LF, Guo YJ, Lu WF, Li HJ, Wang YL. Selection and use of reference genes in mouse mammary glands. Genet Mol Res 2010, 9:449-456. 10.4238/vol9-1gmr724, 20391330.
64. Wnt homepage. http://www.wnt.stanford.edu