Stem cells and the developing mammary gland

Journal of Mammary Gland Biology and Neoplasia

Volumn 18, Issue 2, 2013, Pages 209-219

  Makarem, Maisam ^a   Spike, Benjamin T ^b   Dravis, Christopher ^b   Kannan, Nagarajan ^a   Wahl, Geoffrey M ^b   Eaves, Connie J ^a,c  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

^b SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Breast cancer; Development; Fetal; Mammary gland; Progenitors; Stem cells; Transcriptomes

Indexed keywords

TRANSCRIPTOME;

ADULT STEM CELL; BREAST CANCER; CELL DIFFERENTIATION; CELL FUNCTION; CELL GROWTH; CELL LINEAGE; CELL PROLIFERATION; CELL RENEWAL; CLONOGENIC ASSAY; DAUGHTER CELL; FETAL STEM CELL; GENE EXPRESSION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MAMMARY GLAND; MOLECULAR BIOLOGY; MORPHOGENESIS; NONHUMAN; PHENOTYPE; QUANTITATIVE ANALYSIS; REVIEW; STEM CELL;

ANIMALS; FEMALE; HUMANS; MAMMARY GLANDS, ANIMAL; MAMMARY GLANDS, HUMAN; STEM CELLS;

EID: 84879685072     PISSN: 10833021     EISSN: 15737039     Source Type: Journal    
DOI: 10.1007/s10911-013-9284-6     Document Type: Review

References (85)

1. Howard BA. In the beginning: the establishment of the mammary lineage during embryogenesis. Semin Cell Dev Biol. 2012;23(5):574-82.
2. Brisken C, O'Malley B. Hormone action in the mammary gland. Cold Spring Harb Perspect Biol. 2010;2(12):a003178.
3. Richert MM, Schwertfeger KL, Ryder JW, Anderson SM. An atlas of mouse mammary gland development. J Mammary Gland Biol Neoplasia. 2000;5(2):227-41.
4. Fata JE, Chaudhary V, Khokha R. Cellular turnover in the mammary gland is correlated with systemic levels of progesterone and not 17beta-estradiol during the estrous cycle. Biol Reprod. 2001;65(3):680-8.
5. Kannan N, Huda N, Tu L, Droumeva R, Aubert G, Chavez E, et al. The luminal progenitor compartment of the human mammary gland constitutes a unique site of telomere dysfunction. 2013. Stem Cell Reports (in press).
6. 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(1):19-26.
7. Shehata M, Teschendorff A, Sharp G, Novcic N, Russell A, Avril S, et al. Phenotypic and functional characterization of the luminal cell hierarchy of the mammary gland. Breast Cancer Res. 2012;14(5):R134.
8. Stingl J, Eirew P, Ricketson I, Shackleton M, Vaillant F, Choi D, et al. Purification and unique properties of mammary epithelial stem cells. Nature. 2006;439(7079):993-7.
9. Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat ML, et al. Generation of a functional mammary gland from a single stem cell. Nature. 2006;439(7072):84-8.
10. Deugnier MA, Teuliere J, Faraldo MM, Thiery JP, Glukhova MA. The importance of being a myoepithelial cell. Breast Cancer Res. 2002;4(6):224-30.
11. Visvader JE. Keeping abreast of the mammary epithelial hierarchy and breast tumorigenesis. Genes Dev. 2009;23(22):2563-77.
12. Mikaelian I, Hovick M, Silva KA, Burzenski LM, Shultz LD, Ackert-Bicknell CL, et al. Expression of terminal differentiation proteins defines stages of mouse mammary gland development. Vet Pathol. 2006;43(1):36-49.
13. Sun P, Yuan Y, Li A, Li B, Dai X. Cytokeratin expression during mouse embryonic and early postnatal mammary gland development. Histochem Cell Biol. 2010;133(2):213-21.
14. Spike BT, Engle DD, Lin JC, Cheung SK, La J, Wahl GM. A mammary stem cell population identified and characterized in late embryogenesis reveals similarities to human breast cancer. Cell Stem Cell. 2012;10(2):183-97.
15. Van Keymeulen A, Rocha AS, Ousset M, Beck B, Bouvencourt G, Rock J, et al. Distinct stem cells contribute to mammary gland development and maintenance. Nature. 2011;479(7372):189-93.
16. Sakakura T, Nishizuka Y, Dawe CJ. Capacity of mammary fat pads of adult C3H/HeMs mice to interact morphogenetically with fetal mammary epithelium. J Natl Cancer Inst. 1979;63(3):733-6.
17. Till JE, Mc CE. A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res. 1961;14:213-22.
18. Siminovitch L, McCulloch EA, Till JE. The distribution of colony-forming cells among spleen colonies. J Cell Physiol. 1963;62:327-36.
19. Doulatov S, Notta F, Laurenti E, Dick JE. Hematopoiesis: a human perspective. Cell Stem Cell. 2012;10(2):120-36.
20. Ang YS, Gaspar-Maia A, Lemischka IR, Bernstein E. Stem cells and reprogramming: breaking the epigenetic barrier? Trends Pharmacol Sci. 2011;32(7):394-401.
21. Margueron R, Reinberg D. The polycomb complex PRC2 and its mark in life. Nature. 2011;469(7330):343-9.
22. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J, et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell. 2006;125(2):315-26.
23. Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH. Viable offspring derived from fetal and adult mammalian cells. Nature. 1997;385(6619):810-3.
24. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell. 2006;126(4):663-76.
25. Graf T. Historical origins of transdifferentiation and reprogramming. Cell Stem Cell. 2011;9(6):504-16.
26. Deome KB, Faulkin Jr 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(5):515-20.
27. Hoshino K, Gardner WU. Transplantability and life span of mammary gland during serial transplantation in mice. Nature. 1967;213(5072):193-4.
28. Young LJ, Medina D, DeOme KB, Daniel CW. The influence of host and tissue age on life span and growth rate of serially transplanted mouse mammary gland. Exp Gerontol. 1971;6(1):49-56.
29. Daniel CW, De Ome KB, Young JT, Blair PB, Faulkin Jr LJ. The in vivo life span of normal and preneoplastic mouse mammary glands: a serial transplantation study. Proc Natl Acad Sci U S A. 1968;61(1):53-60.
30. Kordon EC, Smith GH. An entire functional mammary gland may comprise the progeny from a single cell. Development. 1998;125(10):1921-30.
31. Tsai YC, Lu Y, Nichols PW, Zlotnikov G, Jones PA, Smith HS. Contiguous patches of normal human mammary epithelium derived from a single stem cell: implications for breast carcinogenesis. Cancer Res. 1996;56(2):402-4.
32. Gossen M, Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci U S A. 1992;89(12):5547-51.
33. 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(3):387-400.
34. Smalley MJ, Kendrick H, Sheridan JM, Regan JL, Prater MD, Lindeman GJ, et al. Isolation of mouse mammary epithelial subpopulations: a comparison of leading methods. J Mammary Gland Biol Neoplasia. 2012.
35. Gyorki DE, Asselin-Labat ML, van Rooijen N, Lindeman GJ, Visvader JE. Resident macrophages influence stem cell activity in the mammary gland. Breast Cancer Res. 2009;11(4):R62.
36. Vaillant F, Lindeman GJ, Visvader JE. Jekyll or Hyde: does Matrigel provide a more or less physiological environment in mammary repopulating assays? Breast Cancer Res. 2011;13(3):108.
37. Badders NM, Goel S, Clark RJ, Klos KS, Kim S, Bafico A, et al. The Wnt receptor, Lrp5, is expressed by mouse mammary stem cells and is required to maintain the basal lineage. PLoS One. 2009;4(8):e6594.
38. Regan JL, Kendrick H, Magnay FA, Vafaizadeh V, Groner B, Smalley MJ. c-Kit is required for growth and survival of the cells of origin of Brca1-mutation-associated breast cancer. Oncogene. 2012;31(7):869-83.
39. Joshi PA, Jackson HW, Beristain AG, Di Grappa MA, Mote PA, Clarke CL, et al. Progesterone induces adult mammary stem cell expansion. Nature. 2010;465(7299):803-7.
40. Eirew P, Stingl J, Raouf A, Turashvili G, Aparicio S, Emerman JT, et al. A method for quantifying normal human mammary epithelial stem cells with in vivo regenerative ability. Nat Med. 2008;14(12):1384-9.
41. Lim E, Vaillant F, Wu D, Forrest NC, Pal B, Hart AH, et al. Aberrant luminal progenitors as the candidate target population for basal tumor development in BRCA1 mutation carriers. Nat Med. 2009;15(8):907-13.
42. Emerman JT, Stingl J, Petersen A, Shpall EJ, Eaves CJ. Selective growth of freshly isolated human breast epithelial cells cultured at low concentrations in the presence or absence of bone marrow cells. Breast Cancer Res Treat. 1996;41(2):147-59.
43. Dundas SR, Ormerod MG, Gusterson BA, O'Hare MJ. Characterization of luminal and basal cells flow-sorted from the adult rat mammary parenchyma. J Cell Sci. 1991;100(Pt 3):459-71.
44. 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(2):93-109.
45. Stingl J, Eaves CJ, Emerman JT. Characterization of normal human breast epithelial cell subpopulations isolated by flourescence-activated cell sorting and their clonogenic growth in vitro. In: Ip MM, Asch BB, editors. Methods in mammary gland biology & breast cancer research. Kluwer Academic/Plenum Publishers: New York pp. 177-193.
46. Smalley MJ, Titley J, O'Hare MJ. Clonal characterization of mouse mammary luminal epithelial and myoepithelial cells separated by fluorescence-activated cell sorting. In vitro cellular & developmental biology. Animal. 1998;34(9):711-21.
47. Makarem M, Kannan N, Nguyen LV, Knapp DJHF, Balani S, Prater MD, et al. Developmental changes in the in vitro activated regenerative activity of primitive mammary epithelial cells. Submitted. 2013.
48. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, et al. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev. 2003;17(10):1253-70.
49. 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(6):568-77.
50. Sakakura T, Nishizuka Y, Dawe CJ. Mesenchyme-dependent morphogenesis and epithelium-specific cytodifferentiation in mouse mammary gland. Science. 1976;194(4272):1439-41.
51. Narod SA, Foulkes WD. BRCA1 and BRCA2: 1994 and beyond. Nat Rev Cancer. 2004;4(9):665-76.
52. Roy R, Chun J, Powell SN. BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nat Rev Cancer. 2012;12(1):68-78.
53. Luo W, Semenza GL. Pyruvate kinase M2 regulates glucose metabolism by functioning as a coactivator for hypoxia-inducible factor 1 in cancer cells. Oncotarget. 2011;2(7):551-6.
54. Eirew P, Kannan N, Knapp DJ, Vaillant F, Emerman JT, Lindeman GJ, et al. Aldehyde dehydrogenase activity is a biomarker of primitive normal human mammary luminal cells. Stem Cells. 2012;30(2):344-8.
55. Wansbury O, Panchal H, James M, Parry S, Ashworth A, Howard B. Dynamic expression of Erbb pathway members during early mammary gland morphogenesis. J Investig Dermatol. 2008;128(4):1009-21.
56. Howard B, Panchal H, McCarthy A, Ashworth A. Identification of the scaramanga gene implicates Neuregulin3 in mammary gland specification. Genes Dev. 2005;19(17):2078-90.
57. Panchal H, Wansbury O, Parry S, Ashworth A, Howard B. Neuregulin3 alters cell fate in the epidermis and mammary gland. BMC Dev Biol. 2007;7:105.
58. Mailleux AA, Spencer-Dene B, Dillon C, Ndiaye D, Savona-Baron C, Itoh N, et al. Role of FGF10/FGFR2b signaling during mammary gland development in the mouse embryo. Development. 2002;129(1):53-60.
59. Greco V, Chen T, Rendl M, Schober M, Pasolli HA, Stokes N, et al. A two-step mechanism for stem cell activation during hair regeneration. Cell Stem Cell. 2009;4(2):155-69.
60. Wansbury O, Mackay A, Kogata N, Mitsopoulos C, Kendrick H, Davidson K, et al. Transcriptome analysis of embryonic mammary cells reveals insights into mammary lineage establishment. Breast Cancer Res. 2011;13(4):R79.
61. Vogel WF, Aszodi A, Alves F, Pawson T. Discoidin domain receptor 1 tyrosine kinase has an essential role in mammary gland development. Mol Cell Biol. 2001;21(8):2906-17.
62. Kruger GM, Mosher JT, Bixby S, Joseph N, Iwashita T, Morrison SJ. Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron. 2002;35(4):657-69.
63. Kim I, Saunders TL, Morrison SJ. Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell. 2007;130(3):470-83.
64. Nishino J, Kim I, Chada K, Morrison SJ. Hmga2 promotes neural stem cell self-renewal in young but not old mice by reducing p16Ink4a and p19Arf expression. Cell. 2008;135(2):227-39.
65. Mochizuki-Kashio M, Mishima Y, Miyagi S, Negishi M, Saraya A, Konuma T, et al. Dependency on the polycomb gene Ezh2 distinguishes fetal from adult hematopoietic stem cells. Blood. 2011;118(25):6553-61.
66. Bruggeman SW, Valk-Lingbeek ME, van der Stoop PP, Jacobs JJ, Kieboom K, Tanger E, et al. Ink4a and Arf differentially affect cell proliferation and neural stem cell self-renewal in Bmi1-deficient mice. Genes Dev. 2005;19(12):1438-43.
67. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ. Bmi-1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature. 2003;425(6961):962-7.
68. Pietersen AM, Evers B, Prasad AA, Tanger E, Cornelissen-Steijger P, Jonkers J, et al. Bmi1 regulates stem cells and proliferation and differentiation of committed cells in mammary epithelium. Curr Biol. 2008;18(14):1094-9.
69. Shah SN, Kerr C, Cope L, Zambidis E, Liu C, Hillion J, et al. HMGA1 reprograms somatic cells into pluripotent stem cells by inducing stem cell transcriptional networks. PLoS One. 2012;7(11):e48533.
70. Blenkiron C, Goldstein LD, Thorne NP, Spiteri I, Chin SF, Dunning MJ, et al. MicroRNA expression profiling of human breast cancer identifies new markers of tumor subtype. Genome Biol. 2007;8(10):R214.
71. Pietersen AM, Horlings HM, Hauptmann M, Langerod A, Ajouaou A, Cornelissen-Steijger P, et al. EZH2 and BMI1 inversely correlate with prognosis and TP53 mutation in breast cancer. Breast Cancer Res. 2008;10(6):R109.
72. Mills AA, Zheng B, Wang XJ, Vogel H, Roop DR, Bradley A. p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature. 1999;398(6729):708-13.
73. Blanpain C, Fuchs E. p63: revving up epithelial stem-cell potential. Nat Cell Biol. 2007;9(7):731-3.
74. Nekulova M, Holcakova J, Coates P, Vojtesek B. The role of p63 in cancer, stem cells and cancer stem cells. Cell Mol Biol Lett. 2011;16(2):296-327.
75. Asselin-Labat ML, Shackleton M, Stingl J, Vaillant F, Forrest NC, Eaves CJ, et al. Steroid hormone receptor status of mouse mammary stem cells. J Natl Cancer Inst. 2006;98(14):1011-4.
76. Asselin-Labat ML, Sutherland KD, Barker H, Thomas R, Shackleton M, Forrest NC, et al. Gata-3 is an essential regulator of mammary-gland morphogenesis and luminal-cell differentiation. Nat Cell Biol. 2007;9(2):201-9.
77. Kouros-Mehr H, Slorach EM, Sternlicht MD, Werb Z. GATA-3 maintains the differentiation of the luminal cell fate in the mammary gland. Cell. 2006;127(5):1041-55.
78. Chakrabarti R, Wei Y, Romano RA, DeCoste C, Kang Y, Sinha S. Elf5 regulates mammary gland stem/progenitor cell fate by influencing notch signaling. Stem Cells. 2012;30(7):1496-508.
79. Guo W, Keckesova Z, Donaher JL, Shibue T, Tischler V, Reinhardt F, et al. Slug and Sox9 cooperatively determine the mammary stem cell state. Cell. 2012;148(5):1015-28.
80. Ito M, Yang Z, Andl T, Cui C, Kim N, Millar SE, et al. Wnt-dependent de novo hair follicle regeneration in adult mouse skin after wounding. Nature. 2007;447(7142):316-20.
81. Levy V, Lindon C, Zheng Y, Harfe BD, Morgan BA. Epidermal stem cells arise from the hair follicle after wounding. FASEB J. 2007;21(7):1358-66.
82. van Es JH, Sato T, van de Wetering M, Lyubimova A, Nee AN, Gregorieff A, et al. Dll1+ secretory progenitor cells revert to stem cells upon crypt damage. Nat Cell Biol. 2012;14(10):1099-104.
83. Tian H, Biehs B, Warming S, Leong KG, Rangell L, Klein OD, et al. A reserve stem cell population in small intestine renders Lgr5-positive cells dispensable. Nature. 2011;478(7368):255-9.
84. Gastaldi S, Sassi F, Accornero P, Torti D, Galimi F, Migliardi G, et al. Met signaling regulates growth, repopulating potential and basal cell-fate commitment of mammary luminal progenitors: implications for basal-like breast cancer. Oncogene. 2012.
85. Moraes RC, Zhang X, Harrington N, Fung JY, Wu MF, Hilsenbeck SG, et al. Constitutive activation of smoothened (SMO) in mammary glands of transgenic mice leads to increased proliferation, altered differentiation and ductal dysplasia. Development. 2007;134(6):1231-42.