Pregnancy in the mature adult mouse does not alter the proportion of mammary epithelial stem/progenitor cells

Breast Cancer Research

Volumn 11, Issue 2, 2009, Pages

  Britt, Kara L ^a,b   Kendrick, Howard ^a   Regan, Joseph L ^a   Molyneux, Gemma ^a   Magnay, Fiona Ann ^a   Ashworth, Alan ^a   Smalley, Matthew J ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b MONASH MEDICAL CENTRE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA6 INTEGRIN; ATAXIN 1; CD24 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST EPITHELIUM; CELL TRANSPLANTATION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; HEMODILUTION; LACTATION; MOUSE; NONHUMAN; PREGNANCY; PURIFICATION; STEM CELL; ANIMAL; BREEDING; CELL CULTURE; CYTOLOGY; EPITHELIUM CELL; FLUORESCENT ANTIBODY TECHNIQUE; PARITY; PHYSIOLOGY; UDDER;

ANIMALS; CELLS, CULTURED; EPITHELIAL CELLS; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE; LACTATION; MAMMARY GLANDS, ANIMAL; MICE; PARITY; PREGNANCY; PREGNANCY, ANIMAL; STEM CELLS;

EID: 68349118223     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2245     Document Type: Article

References (57)

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 Organ 1970, 43:209-221. 5312521.
2. Britt K, Ashworth A, Smalley M. Pregnancy and the risk of breast cancer. Endocr Relat Cancer 2007, 14:907-933. 10.1677/ERC-07-0137, 18045947.
3. 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, 15597097.
4. Schedin P. Pregnancy-associated breast cancer and metastasis. Nat Rev Cancer 2006, 6:281-291. 10.1038/nrc1839, 16557280.
5. Trichopoulos D, Hsieh CC, MacMahon B, Lin TM, Lowe CR, Mirra AP, Ravnihar B, Salber EJ, Valaoras VG, Yuasa S. Age at any birth and breast cancer risk. Int J Cancer 1983, 31:701-704. 10.1002/ijc.2910310604, 6862681.
6. Russo J, Russo IH. Biological and molecular bases of mammary carcinogenesis. Lab Invest 1987, 57:112-137.
7. Russo J, Tay LK, Russo IH. Differentiation of the mammary gland and susceptibility to carcinogenesis. Breast Cancer Res Treat 1982, 2:5-73. 10.1007/BF01805718, 6216933.
8. Russo J, Gusterson BA, Rogers AE, Russo IH, Wellings SR, van Zwieten MJ. Comparative study of human and rat mammary tumorigenesis. Lab Invest 1990, 62:244-278.
9. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111. 10.1038/35102167, 11689955.
10. Asselin-Labat ML, Shackleton M, Stingl J, Vaillant F, Forrest NC, Eaves CJ, Visvader JE, Lindeman GJ. Steroid hormone receptor status of mouse mammary stem cells. J Natl Cancer Inst 2006, 98:1011-1014.
11. 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. 2063618, 17190790, 10.1083/jcb.200604065.
12. Miura T, Miura C, Ohta T, Nader MR, Todo T, Yamauchi K. Estradiol-17β stimulates the renewal of spermatogonial stem cells in males. Biochem Biophys Res Commun 1999, 264:230-234. 10.1006/bbrc.1999.1494, 10527870.
13. Gargett CE, Chan RW, Schwab KE. Hormone and growth factor signaling in endometrial renewal: role of stem/progenitor cells. Mol Cell Endocrinol 2008, 288:22-29. 10.1016/j.mce.2008.02.026, 18403104.
14. Creighton CJ, Cordero KE, Larios JM, Miller RS, Johnson MD, Chinnaiyan AM, Lippman ME, Rae JM. Genes regulated by estrogen in breast tumor cells in vitro are similarly regulated in vivo in tumor xenografts and human breast tumors. Genome Biol 2006, 7:R28. 1557996, 16606439, 10.1186/gb-2006-7-4-r28.
15. Frasor J, Danes JM, Komm B, Chang KC, Lyttle CR, Katzenellenbogen BS. Profiling of estrogen up- and down-regulated gene expression in human breast cancer cells: insights into gene networks and pathways underlying estrogenic control of proliferation and cell phenotype. Endocrinology 2003, 144:4562-4574. 10.1210/en.2003-0567, 12959972.
16. Rae JM, Johnson MD, Scheys JO, Cordero KE, Larios JM, Lippman ME. GREB 1 is a critical regulator of hormone dependent breast cancer growth. Breast Cancer Res Treat 2005, 92:141-149. 10.1007/s10549-005-1483-4, 15986123.
17. Kendrick H, Regan JL, Magnay FA, Grigoriadis A, Mitsopoulos C, Zvelebil M, Smalley MJ. Transcriptome analysis of mammary epithelial subpopulations identifies novel determinants of lineage commitment and cell fate. BMC Genomics 2008, 9:591. 2629782, 19063729, 10.1186/1471-2164-9-591.
18. Ciarloni L, Mallepell S, Brisken C. Amphiregulin is an essential mediator of estrogen receptor alpha function in mammary gland development. Proc Natl Acad Sci USA 2007, 104:5455-5460. 1838509, 17369357, 10.1073/pnas.0611647104.
19. Kenney NJ, Huang RP, Johnson GR, Wu JX, Okamura D, Matheny W, Kordon E, Gullick WJ, Plowman G, Smith GH, Salomon DS, Adamson ED. Detection and location of amphiregulin and Cripto-1 expression in the developing postnatal mouse mammary gland. Mol Reprod Dev 1995, 41:277-286. 10.1002/mrd.1080410302, 8588926.
20. Lamarca HL, Rosen JM. Estrogen regulation of mammary gland development and breast cancer: amphiregulin takes center stage. Breast Cancer Res 2007, 9:304. 2206713, 17659070, 10.1186/bcr1740.
21. Sternlicht MD, Sunnarborg SW, Kouros-Mehr H, Yu Y, Lee DC, Werb Z. Mammary ductal morphogenesis requires paracrine activation of stromal EGFR via ADAM17-dependent shedding of epithelial amphiregulin. Development 2005, 132:3923-3933. 10.1242/dev.01966, 16079154.
22. Smith GH, Medina D. A morphologically distinct candidate for an epithelial stem cell in mouse mammary gland. J Cell Sci 1988, 90(Pt 1):173-183.
23. 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. 2647777, 18787212, 10.1634/stemcells.2008-0103.
24. 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.
25. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J, Nikolskaya T, Serebryiskaya T, Beroukhim R, Hu M, Halushka MK, Sukumar S, Parker LM, Anderson KS, Harris LN, Garber JE, Richardson AL, Schnitt SJ, Nikolsky Y, Gelman RS, Polyak K. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007, 11:259-273. 10.1016/j.ccr.2007.01.013, 17349583.
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. 1413978, 16417656, 10.1186/bcr1371.
27. 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.
28. Taddei I, Deugnier MA, Faraldo MM, Petit V, Bouvard D, Medina D, Fassler R, Thiery JP, Glukhova MA. β1 integrin deletion from the basal compartment of the mammary epithelium affects stem cells. Nat Cell Biol 2008, 10:716-722. 2659707, 18469806, 10.1038/ncb1734.
29. Matulka LA, Triplett AA, Wagner KU. Parity-induced mammary epithelial cells are multipotent and express cell surface markers associated with stem cells. Dev Biol 2007, 303:29-44. 10.1016/j.ydbio.2006.12.017, 17222404.
30. Smith GH. Experimental mammary epithelial morphogenesis in an in vivo model: evidence for distinct cellular progenitors of the ductal and lobular phenotype. Breast Cancer Res Treat 1996, 39:21-31. 10.1007/BF01806075, 8738603.
31. Wagner KU, Boulanger CA, Henry MD, Sgagias M, Hennighausen L, Smith GH. An adjunct mammary epithelial cell population in parous females: its role in functional adaptation and tissue renewal. Development 2002, 129:1377-1386.
32. Naylor MJ, Li N, Cheung J, Lowe ET, Lambert E, Marlow R, Wang P, Schatzmann F, Wintermantel T, Schuetz G, Clarke AR, Mueller U, Hynes NE, Streuli CH. Ablation of β1 integrin in mammary epithelium reveals a key role for integrin in glandular morphogenesis and differentiation. J Cell Biol 2005, 171:717-728. 2171573, 16301336, 10.1083/jcb.200503144.
33. Booth BW, Smith GH. Estrogen receptor-alpha and progesterone receptor are expressed in label-retaining mammary epithelial cells that divide asymmetrically and retain their template DNA strands. Breast Cancer Res 2006, 8:R49. 1779481, 16882347, 10.1186/bcr1538.
34. Lamarca HL, Rosen JM. Hormones and mammary cell fate: what will I become when I grow up?. Endocrinology 2008, 149:4317-4321. 10.1210/en.2008-0450, 18556345.
35. Tronolab. , http://tronolab.epfl.ch/
36. Welm BE, Dijkgraaf GJ, Bledau AS, Welm AL, Werb Z. Lentiviral transduction of mammary stem cells for analysis of gene function during development and cancer. Cell Stem Cell 2008, 2:90-102. 2276651, 18371425, 10.1016/j.stem.2007.10.002.
37. Smalley MJ, Titley J, Paterson H, Perusinghe N, Clarke C, O'Hare MJ. Differentiation of separated mouse mammary luminal epithelial and myoepithelial cells cultured on EHS matrix analyzed by indirect immunofluorescence of cytoskeletal antigens. J Histochem Cytochem 1999, 47:1513-1524.
38. Lindeman GJ, Visvader JE, Smalley MJ, Eaves CJ. The future of mammary stem cell biology: the power of in vivo transplants. Breast Cancer Res 2008, 10:402. author reply 403., 2481484, 18522763, 10.1186/bcr1986.
39. 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. 2481490, 18471300, 10.1186/bcr2094.
40. Cumming G, Fidler F, Vaux DL. Error bars in experimental biology. J Cell Biol 2007, 177:7-11. 2064100, 17420288, 10.1083/jcb.200611141.
41. Alvi AJ, Clayton H, Joshi C, Enver T, Ashworth A, Vivanco MM, Dale TC, Smalley MJ. Functional and molecular characterisation of mammary side population cells. Breast Cancer Res 2003, 5:R1-R8. 154129, 12559051, 10.1186/bcr563.
42. Smalley MJ, Clarke RB. The mammary gland 'side population': a putative stem/progenitor cell marker?. J Mammary Gland Biol Neoplasia 2005, 10:37-47. 10.1007/s10911-005-2539-0, 15886885.
43. Barroca V, Lassalle B, Coureuil M, Louis JP, Le Page F, Testart J, Allemand I, Riou L, Fouchet P. Mouse differentiating spermatogonia can generate germinal stem cells in vivo. Nat Cell Biol 2009, 11:190-196. 10.1038/ncb1826, 19098901.
44. Li N, Zhang Y, Naylor MJ, Schatzmann F, Maurer F, Wintermantel T, Schuetz G, Mueller U, Streuli CH, Hynes NE. β1 integrins regulate mammary gland proliferation and maintain the integrity of mammary alveoli. EMBO J 2005, 24:1942-1953. 1142608, 15889143, 10.1038/sj.emboj.7600674.
45. Dontu G, Al-Hajj M, Abdallah WM, Clarke MF, Wicha MS. Stem cells in normal breast development and breast cancer. Cell Prolif 2003, 36(Suppl 1):59-72. 10.1046/j.1365-2184.36.s.1.6.x, 14521516.
46. Molyneux G, Regan J, Smalley MJ. Mammary stem cells and breast cancer. Cell Mol Life Sci 2007, 64:3248-3260. 10.1007/s00018-007-7391-5, 17955177.
47. Melchor L, Benitez J. An integrative hypothesis about the origin and development of sparadic and familial breast cancer subtypes. Carcinogenesis 2008, 29:1475-1482. 10.1093/carcin/bgn157, 18596026.
48. 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.
49. Yang J, Yoshizawa K, Nandi S, Tsubura A. Protective effects of pregnancy and lactation against N-methyl-N-nitrosourea-induced mammary carcinomas in female Lewis rats. Carcinogenesis 1999, 20:623-628. 10.1093/carcin/20.4.623, 10223190.
50. Kass L, Durando M, Ramos JG, Varayoud J, Powell CE, Luque EH, Munoz-de-Toro M. Association of increased estrogen receptor β2 expression with parity-induced alterations in the rat mammary gland. J Steroid Biochem Mol Biol 2004, 91:29-39. 10.1016/j.jsbmb.2004.02.001, 15261305.
51. Ginger MR, Gonzalez-Rimbau MF, Gay JP, Rosen JM. Persistent changes in gene expression induced by estrogen and progesterone in the rat mammary gland. Mol Endocrinol 2001, 15:1993-2009. 10.1210/me.15.11.1993, 11682629.
52. 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-β3, and differentiation in the rodent mammary gland. Mol Endocrinol 2002, 16:2034-2051. 10.1210/me.2002-0073, 12198241.
53. 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.
54. Abrams TJ, Guzman RC, Swanson SM, Thordarson G, Talamantes F, Nandi S. Changes in the parous rat mammary gland environment are involved in parity-associated protection against mammary carcinogenesis. Anticancer Res 1998, 18:4115-4121.
55. 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. 26817, 10051675, 10.1073/pnas.96.5.2520.
56. Wagner KU, Smith GH. Pregnancy and stem cell behavior. J Mammary Gland Biol Neoplasia 2005, 10:25-36. 10.1007/s10911-005-2538-1, 15886884.
57. Thordarson G, Slusher N, Leong H, Ochoa D, Rajkumar L, Guzman R, Nandi S, Talamantes F. Insulin-like growth factor (IGF)-I obliterates the pregnancy-associated protection against mammary carcinogenesis in rats: evidence that IGF-I enhances cancer progression through estrogen receptor-alpha activation via the mitogen-activated protein kinase pathway. Breast Cancer Res 2004, 6:R423-R436. 468665, 15217511, 10.1186/bcr812.