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Bovine mammary stem cells: cell biology meets production agriculture

Published online by Cambridge University Press:  03 January 2012

A. V. Capuco*
Affiliation:
Bovine Functional Genomics Laboratory, USDA-ARS, Beltsville, MD 20705, USA Department of Animal and Avian Sciences, University of Maryland, College Park, MD 20742, USA
R. K. Choudhary
Affiliation:
Department of Animal and Avian Sciences, University of Maryland, College Park, MD 20742, USA
K. M. Daniels
Affiliation:
Department of Animal Sciences, The Ohio State University, Wooster, OH 44691, USA
R. W. Li
Affiliation:
Bovine Functional Genomics Laboratory, USDA-ARS, Beltsville, MD 20705, USA
C. M. Evock-Clover
Affiliation:
Bovine Functional Genomics Laboratory, USDA-ARS, Beltsville, MD 20705, USA
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Abstract

Mammary stem cells (MaSC) provide for net growth, renewal and turnover of mammary epithelial cells, and are therefore potential targets for strategies to increase production efficiency. Appropriate regulation of MaSC can potentially benefit milk yield, persistency, dry period management and tissue repair. Accordingly, we and others have attempted to characterize and alter the function of bovine MaSC. In this review, we provide an overview of current knowledge of MaSC gained from studies using mouse and human model systems and present research on bovine MaSC within that context. Recent data indicate that MaSC retain labeled DNA for extended periods because of their selective segregation of template DNA strands during mitosis. Relying on this long-term retention of bromodeoxyuridine-labeled DNA, we identified putative bovine MaSC. These label-retaining epithelial cells (LREC) are in low abundance within mammary epithelium (<1%). They are predominantly estrogen receptor (ER)-negative and localized in a basal or suprabasal layer of the epithelium throughout the gland. Thus, the response of MaSC to estrogen, the major mitogen in mammary gland, is likely mediated by paracrine factors released by cells that are ER-positive. This is consistent with considerable evidence for cross-talk within and between epithelial cells and surrounding stromal cells. Excision of classes of cells by laser microdissection and subsequent microarray analysis will hopefully provide markers for MaSC and insights into their regulation. Preliminary analyses of gene expression in laser-microdissected LREC and non-LREC are consistent with the concept that LREC represent populations of stem cells and progenitor cells that differ with regard to their properties and location within the epithelial layer. We have attempted to modulate the MaSC number by infusing a solution of xanthosine through the teat canal and into the ductal network of the mammary glands of prepubertal heifers. This treatment increased the number of putative stem cells, as evidenced by an increase in the percentage of LREC and increased telomerase activity within the tissue. The exciting possibility that stem cell expansion can influence milk production is currently under investigation.

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Copyright © The Animal Consortium 2011

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References

Akers, RM 2002. Lactation and the mammary gland. Iowa State Press, Ames, IA, USA.Google Scholar
Akers, RM, McFadden, TB, Purup, S, Vestergaard, M, Sejrsen, K, Capuco, AV 2000. Local IGF-I axis in peripubertal ruminant mammary development. Journal of Mammary Gland Biology and Neoplasia 5, 4351.CrossRefGoogle ScholarPubMed
Anderson, E, Clarke, RB 2004. Steroid receptors and cell cycle in normal mammary epithelium. Journal of Mammary Gland Biology and Neoplasia 9, 313.CrossRefGoogle ScholarPubMed
Annen, EL, Fitzgerald, AC, Gentry, PC, McGuire, MA, Capuco, AV, Baumgard, LH, Collier, RJ 2007. Effect of continuous milking and bovine somatotropin supplementation on mammary epithelial cell turnover. Journal of Dairy Science 90, 165183.CrossRefGoogle ScholarPubMed
Asselin-Labat, ML, Shackleton, M, Stingl, J, Vaillant, F, Forrest, NC, Eaves, CJ, Visvader, JE, Lindeman, GJ 2006. Steroid hormone receptor status of mouse mammary stem cells. Journal of the National Cancer Institute 98, 10111014.CrossRefGoogle ScholarPubMed
Baldwin, RL, Milligan, LP 1966. Enzymatic changes associated with the initiation and maintenance of lactation in the rat. Journal of Biological Chemistry 241, 20582066.CrossRefGoogle ScholarPubMed
Ballagh, K, Korn, N, Riggs, L, Pratt, SL, Dessauge, F, Akers, RM, Ellis, S 2008. Hot topic: prepubertal ovariectomy alters the development of myoepithelial cells in the bovine mammary gland. Journal of Dairy Science 91, 29922995.CrossRefGoogle ScholarPubMed
Bar-Peled, U, Robinzon, B, Maltz, E, Tagari, H, Folman, Y, Bruckental, I, Voet, H, Gacitua, H, Lehrer, AR 1997. Increased weight gain and effects on production parameters of Holstein heifer calves that were allowed to suckle from birth to six weeks of age. Journal of Dairy Science 80, 25232528.CrossRefGoogle ScholarPubMed
Berry, SDK, Jobst, PM, Ellis, SE, Howard, RD, Capuco, AV, Akers, RM 2003. Mammary epithelial proliferation and estrogen receptor alpha expression in prepubertal heifers: effects of ovariectomy and growth hormone. Journal of Dairy Science 86, 20982105.CrossRefGoogle ScholarPubMed
Blanpain, C, Fuchs, E 2009. Epidermal homeostasis: a balancing act of stem cells in the skin. Nature Reviews Molecular Cell Biology 10, 207217.CrossRefGoogle ScholarPubMed
Bocchinfuso, WP, Lindzey, JK, Hewitt, SC, Clark, JA, Myers, PH, Cooper, R, Korach, KS 2000. Induction of mammary gland development in estrogen receptor-alpha knockout mice. Endocrinology 141, 29822994.CrossRefGoogle ScholarPubMed
Booth, BW, Smith, GH 2006. 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 Research 8, R49.CrossRefGoogle ScholarPubMed
Booth, BW, Boulanger, CA, Smith, GH 2007. Alveolar progenitor cells develop in mouse mammary glands independent of pregnancy and lactation. Journal of Cellular Physiology 212, 729736.CrossRefGoogle ScholarPubMed
Booth, BW, Mack, DL, Androutsellis-Theotokis, A, McKay, RD, Boulanger, CA, Smith, GH 2008. The mammary microenvironment alters the differentiation repertoire of neural stem cells. Proceedings of the National Academy of Sciences of the United States of America 105, 1489114896.CrossRefGoogle ScholarPubMed
Booth, BW, Boulanger, CA, Anderson, LH, Jimenez-Rojo, L, Brisken, C, Smith, GH 2010. Amphiregulin mediates self-renewal in an immortal mammary epithelial cell line with stem cell characteristics. Experimental Cell Research 13, 422432.CrossRefGoogle Scholar
Boulanger, CA, Mack, DL, Booth, BW, Smith, GH 2007. Interaction with the mammary microenvironment redirects spermatogenic cell fate in vivo. Proceedings of the National Academy of Sciences of the United States of America 104, 38713876.CrossRefGoogle ScholarPubMed
Boutinaud, M, Guinard-Flamenta, J, Jammes, H 2004. The number and activity of mammary epithelial cells, determining factors for milk production. Reproduction, Nutrition, Development 44, 499508.CrossRefGoogle ScholarPubMed
Brisken, C, Duss, S 2007. Stem cells and the stem cell niche in the breast: an integrated hormonal and developmental perspective. Stem Cell Reviews 3, 147156.CrossRefGoogle ScholarPubMed
Brown, EG, Vandehaar, MJ, Daniels, KM, Liesman, JS, Chapin, LT, Forrest, JW, Akers, RM, Pearson, RE, Nielsen, MS 2005. Effect of increasing energy and protein intake on mammary development in heifer calves. Journal of Dairy Science 88, 595603.CrossRefGoogle ScholarPubMed
Capuco, AV 2007. Identification of putative bovine mammary epithelial stem cells by their retention of labeled DNA strands. Experimental Biology and Medicine (Maywood) 232, 13811390.CrossRefGoogle ScholarPubMed
Capuco, AV, Akers, RM 1999. Mammary involution in dairy animals. Journal of Mammary Gland Biology and Neoplasia 4, 137144.CrossRefGoogle ScholarPubMed
Capuco, AV, Ellis, S 2005. Bovine mammary progenitor cells: current concepts and future directions. Journal of Mammary Gland Biology and Neoplasia 10, 515.CrossRefGoogle ScholarPubMed
Capuco, AV, Akers, RM, Smith, JJ 1997. Mammary growth in Holstein cows during the dry period: quantification of nucleic acids and histology. Journal of Dairy Science 80, 477487.CrossRefGoogle ScholarPubMed
Capuco, AV, Evock-Clover, CM, Minuti, A, Wood, DL 2009. In vivo expansion of the mammary stem/progenitor cell population by xanthosine infusion. Experimental Biology and Medicine (Maywood) 234, 475482.CrossRefGoogle ScholarPubMed
Capuco, AV, Wood, DL, Baldwin, R, McLeod, K, Paape, MJ 2001. Mammary cell number, proliferation, and apoptosis during a bovine lactation: relation to milk production and effect of bST. Journal of Dairy Science 84, 21772187.CrossRefGoogle ScholarPubMed
Capuco, AV, Annen, E, Fitzgerald, AC, Ellis, SE, Collier, RJ 2006. Mammary cell turnover: relevance to lactation persistency and dry period management. In Ruminant physiology: digestion, metabolism and impact of nutrition on gene expression, immunology and stress (ed. K Sejrsen, T Hvelplund and MO Nielsen), pp. 363388. Wageningen Academic Publishers, Wageningen, the Netherlands.Google Scholar
Capuco, AV, Ellis, S, Wood, DL, Akers, RM, Garrett, W 2002a. Postnatal mammary ductal growth: three-dimensional imaging of cell proliferation, effects of estrogen treatment, and expression of steroid receptors in prepubertal calves. Tissue and Cell 34, 143154.CrossRefGoogle ScholarPubMed
Capuco, AV, Li, M, Long, E, Ren, S, Hruska, KS, Schorr, K, Furth, PA 2002b. Concurrent pregnancy retards mammary involution: effects on apoptosis and proliferation of the mammary epithelium after forced weaning of mice. Biology of Reproduction 66, 14711476.CrossRefGoogle ScholarPubMed
Capuco, AV, Ellis, SE, Hale, SA, Long, E, Erdman, RA, Zhao, X, Paape, MJ 2003. Lactation persistency: insights from mammary cell proliferation studies. Journal of Animal Science 81 (suppl. 3), 1831.CrossRefGoogle ScholarPubMed
Chepko, G, Smith, GH 1997. Three division-competent, structurally-distinct cell populations contribute to murine mammary epithelial renewal. Tissue and Cell 29, 239253.CrossRefGoogle ScholarPubMed
Chepko, G, Dickson, RB 2003. Ultrastructure of the putative stem cell niche in rat mammary epithelium. Tissue and Cell 35, 8393.CrossRefGoogle ScholarPubMed
Choudhary, RK, Daniels, KM, Evock-Clover, CM, Garrett, W, Capuco, AV 2010a. Technical note: a rapid method for 5-bromo-2′-deoxyuridine (BrdU) immunostaining in bovine mammary cryosections that retains RNA quality. Journal of Dairy Science 93, 25742579.CrossRefGoogle ScholarPubMed
Choudhary, RK, Li, RW, Evock-Clover, CM, Capuco, AV 2010b. Bovine mammary stem cells: transcriptome profiling and the stem cell niche. Journal of Dairy Science 93 (E-suppl. 1), ii–iii.Google Scholar
Ciarloni, L, Mallepell, S, Brisken, C 2007. Amphiregulin is an essential mediator of estrogen receptor alpha function in mammary gland development. Proceedings of the National Academy of Sciences of the United States of America 104, 54555460.CrossRefGoogle ScholarPubMed
Clarke, RB, Anderson, E, Howell, A, Potten, CS 2003. Regulation of human breast epithelial stem cells. Cell Proliferation 36 (suppl. 1), 4558.CrossRefGoogle ScholarPubMed
Clarke, RB, Spence, K, Anderson, E, Howell, A, Okano, H, Potten, CS 2005. A putative human breast stem cell population is enriched for steroid receptor-positive cells. Developmental Biology 277, 443456.CrossRefGoogle ScholarPubMed
Cohen, AR, Gomes, FL, Roysam, B, Cayouette, M 2010. Computational prediction of neural progenitor cell fates. Nature Methods 7, 213218.CrossRefGoogle ScholarPubMed
Connor, EE, Meyer, MJ, Li, RW, Van Amburgh, ME, Boisclair, YR, Capuco, AV 2007. Regulation of gene expression in the bovine mammary gland by ovarian steroids. Journal of Dairy Science 90 (suppl. 1), E55E65.CrossRefGoogle ScholarPubMed
Cosentino, L, Shaver-Walker, P, Heddle, JA 1996. The relationships among stem cells, crypts, and villi in the small intestine of mice as determined by mutation tagging. Developmental Dynamics 207, 420428.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
Daniel, CW, Young, LJ, Medina, D, DeOme, KB 1971. The influence of mammogenic hormones on serially transplanted mouse mammary gland. Experimental Gerontology 6, 95101.CrossRefGoogle ScholarPubMed
Daniel, CW, Aidells, BD, Medina, D, Faulkin, LJ Jr 1975. Unlimited division potential of precancerous mouse mammary cells after spontaneous or carcinogen-induced transformation. Federation Proceedings 34, 6467.Google ScholarPubMed
Daniels, KM, Capuco, AV, McGilliard, ML, James, RE, Akers, RM 2009. Effects of milk replacer formulation on measures of mammary growth and composition in Holstein heifers. Journal of Dairy Science 92, 59375950.CrossRefGoogle ScholarPubMed
DeOme, KB, Faulkin, LJ Jr, Bern, HA, Blair, PB 1959. Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland-free mammary fat pads of female C3H mice. Cancer Research 19, 515520.Google ScholarPubMed
Desponts, C, Ding, S 2010. Using small molecules to improve generation of induced pluripotent stem cells from somatic cells. Methods in Molecular Biology 636, 207218.CrossRefGoogle ScholarPubMed
Dontu, G, El-Ashry, D, Wicha, MS 2004. Breast cancer, stem/progenitor cells and the estrogen receptor. Trends in Endocrinology and Metabolism 15, 193197.CrossRefGoogle ScholarPubMed
Dontu, G, Abdallah, WM, Foley, JM, Jackson, KW, Clarke, MF, Kawamura, MJ, Wicha, MS 2003a. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes and Development 17, 12531270.CrossRefGoogle ScholarPubMed
Dontu, G, Al-Hajj, M, Abdallah, WM, Clarke, MF, Wicha, MS 2003b. Stem cells in normal breast development and breast cancer. Cell Proliferation 36 (suppl. 1), 5972.CrossRefGoogle ScholarPubMed
Ellis, S, Capuco, AV 2002. Cell proliferation in bovine mammary epithelium: identification of the primary proliferative cell population. Tissue and Cell 34, 155163.CrossRefGoogle ScholarPubMed
Ellis, S, Edwards, FG, Akers, RM 1995. Morphological and histological analysis of the prepubertal ovine mammary gland. Journal of Dairy Science 78 (suppl. 1), 157.Google Scholar
Ellis, S, Purup, S, Sejrsen, K, Akers, RM 2000. Growth and morphogenesis of epithelial cell organoids from peripheral and medial mammary parenchyma of prepubertal heifers. Journal of Dairy Science 83, 952961.CrossRefGoogle ScholarPubMed
Esmailpour, T, Huang, T 2008. Advancement in mammary stem cell research. Journal of Cancer Molecules 4, 131138.Google Scholar
Evans, MJ, Kaufman, MH 1981. Establishment in culture of pluripotential cells from mouse embryos. Nature 292, 154156.CrossRefGoogle ScholarPubMed
Faulkin, LJ Jr, DeOme, KB 1960. Regulation of growth and spacing of gland elements in the mammary fat pad of the C3H mouse. Journal of the National Cancer Institute 24, 953969.Google ScholarPubMed
Ferguson, DJ 1985. Ultrastructural characterisation of the proliferative (stem?) cells within the parenchyma of the normal ‘resting’ breast. Virchows Archiv A, Pathological Anatomy and Histopathology 407, 379385.CrossRefGoogle ScholarPubMed
Fliedner, TM 1998. The role of blood stem cells in hematopoietic cell renewal. Stem Cells 16 (suppl. 1), 1329.CrossRefGoogle ScholarPubMed
Ginestier, C, Hur, MH, Charafe-Jauffret, E, Monville, F, Dutcher, J, Brown, M, Jacquemier, J, Viens, P, Kleer, CG, Liu, S, Schott, A, Hayes, D, Birnbaum, D, Wicha, MS, Dontu, G 2007. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1, 555567.CrossRefGoogle Scholar
Heng, JC, Feng, B, Han, J, Jiang, J, Kraus, P, Ng, JH, Orlov, YL, Huss, M, Yang, L, Lufkin, T, Lim, B, Ng, HH 2010. The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell 6, 167174.CrossRefGoogle ScholarPubMed
Holland, MS, Holland, RE 2005. The cellular perspective on mammary gland development: stem/progenitor cells and beyond. Journal of Dairy Science 88 (suppl. 1), E1E8.CrossRefGoogle ScholarPubMed
Holland, MS, Stasko, JA, Holland, RE 2007. Influence of extracellular matrix on bovine mammary gland progenitor cell growth and differentiation. American Journal of Veterinary Research 68, 476482.CrossRefGoogle ScholarPubMed
Holland, MS, Tai, MH, Trosko, JE, Griffin, LD, Stasko, JA, Cheville, NC, Holland, RE 2003. Isolation and differentiation of bovine mammary gland progenitor cell populations. American Journal of Veterinary Research 64, 396403.CrossRefGoogle ScholarPubMed
Hovey, RC, Aimo, L 2010. Diverse and active roles for adipocytes during mammary gland growth and function. Journal of Mammary Gland Biology and Neoplasia 15, 279290.CrossRefGoogle Scholar
Hovey, RC, McFadden, TB, Akers, RM 1999. Regulation of mammary gland growth and morphogenesis by the mammary fat pad: a species comparison. Journal of Mammary Gland Biology and Neoplasia 4, 5368.CrossRefGoogle ScholarPubMed
Jia, F, Wilson, KD, Sun, N, Gupta, DM, Huang, M, Li, Z, Panetta, NJ, Chen, ZY, Robbins, RC, Kay, MA, Longaker, MT, Wu, JC 2010. A nonviral minicircle vector for deriving human iPS cells. Nature Methods 7, 197199.CrossRefGoogle ScholarPubMed
Jones, P, Simons, BD 2008. Epidermal homeostasis: do committed progenitors work while stem cells sleep? Nature Reviews Molecular Cell Biology 9, 8288.CrossRefGoogle ScholarPubMed
Jones, PH, Watt, FM 1993. Separation of human epidermal stem cells from transit amplifying cells on the basis of differences in integrin function and expression. Cell 73, 713724.CrossRefGoogle ScholarPubMed
Jonker, JW, Merino, G, Musters, S, van Herwaarden, AE, Bolscher, E, Wagenaar, E, Mesman, E, Dale, TC, Schinkel, AH 2005. The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nature Medicine 11, 127129.CrossRefGoogle ScholarPubMed
Joshi, PA, Jackson, HW, Beristain, AG, Di Grappa, MA, Mote, PA, Clarke, CL, Stingl, J, Waterhouse, PD, Khokha, R 2010. Progesterone induces adult mammary stem cell expansion. Nature 465, 803807.CrossRefGoogle ScholarPubMed
Kenney, NJ, Smith, GH, Lawrence, E, Barrett, JC, Salomon, DS 2001. Identification of stem cell units in the terminal end bud and duct of the mouse mammary gland. Journal of Biomedicine and Biotechnology 1, 133143.CrossRefGoogle ScholarPubMed
Keys, JE, Capuco, AV, Akers, RM, Djiane, J 1989. Comparative study of mammary gland development and differentiation between beef and dairy heifers. Domestic Animal Endocrinology 6, 311319.CrossRefGoogle ScholarPubMed
Kordon, EC, Smith, GH 1998. An entire functional mammary gland may comprise the progeny from a single cell. Development 125, 19211930.CrossRefGoogle ScholarPubMed
Kuperwasser, C, Chavarria, T, Wu, M, Magrane, G, Gray, JW, Carey, L, Richardson, A, Weinberg, RA 2004. Reconstruction of functionally normal and malignant human breast tissues in mice. Proceedings of the National Academy of Sciences of the United States of America 101, 49664971.CrossRefGoogle ScholarPubMed
Lagarkova, MA, Shutova, MV, Bogomazova, AN, Vassina, EM, Glazov, EA, Zhang, P, Rizvanov, AA, Chestkov, IV, Kiselev, SL 2010. Induction of pluripotency in human endothelial cells resets epigenetic profile on genome scale. Cell Cycle 9, 937946.CrossRefGoogle ScholarPubMed
Lamarca, HL, Rosen, JM 2008. Hormones and mammary cell fate – what will I become when I grow up? Endocrinology 149, 43174321.CrossRefGoogle Scholar
Lee, HS, Crane, GG, Merok, JR, Tunstead, JR, Hatch, NL, Panchalingam, K, Powers, MJ, Griffith, LG, Sherley, JL 2003. Clonal expansion of adult rat hepatic stem cell lines by suppression of asymmetric cell kinetics (SACK). Biotechnology and Bioengineering 83, 760777.CrossRefGoogle ScholarPubMed
Li, P, Wilde, CJ, Finch, LM, Fernig, DG, Rudland, PS 1999. Identification of cell types in the developing goat mammary gland. Histochemical Journal 31, 379393.CrossRefGoogle ScholarPubMed
Li, JX, Zhang, Y, Ma, LB, Sun, JH, Yin, BY 2009. Isolation and culture of bovine mammary epithelial stem cells. Journal of Veterinary Medical Science 71, 1519.CrossRefGoogle ScholarPubMed
Li, RW, Meyer, MJ, Van Tassell, CP, Sonstegard, TS, Connor, EE, Van Amburgh, ME, Boisclair, YR, Capuco, AV 2006. Identification of estrogen-responsive genes in the parenchyma and fat pad of the bovine mammary gland by microarray analysis. Physiological Genomics 27, 4253.CrossRefGoogle ScholarPubMed
Lindvall, C, Evans, NC, Zylstra, CR, Li, Y, Alexander, CM, Williams, BO 2006. The Wnt signaling receptor Lrp5 is required for mammary ductal stem cell activity and Wnt1-induced tumorigenesis. Journal of Biological Chemistry 281, 3508135087.CrossRefGoogle ScholarPubMed
Liu, S, Ginestier, C, Charafe-Jauffret, E, Foco, H, Kleer, CG, Merajver, SD, Dontu, G, Wicha, MS 2008. BRCA1 regulates human mammary stem/progenitor cell fate. Proceedings of the National Academy of Sciences of the United States of America 105, 16801685.CrossRefGoogle ScholarPubMed
Mallepell, S, Krust, A, Chambon, P, Brisken, C 2006. Paracrine signaling through the epithelial estrogen receptor alpha is required for proliferation and morphogenesis in the mammary gland. Proceedings of the National Academy of Sciences of the United States of America 103, 21962201.CrossRefGoogle ScholarPubMed
Martignani, E, Eirew, P, Eaves, C, Baratta, M 2009. Functional identification of bovine mammary epithelial stem/progenitor cells. Veterinary Research Communications 33 (suppl. 1), 101103.CrossRefGoogle ScholarPubMed
Martin, GR 1981. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proceedings of the National Academy of Sciences of the United States of America 78, 76347648.CrossRefGoogle ScholarPubMed
Meyer, MJ, Capuco, AV, Ross, DA, Lintault, LM, Van Amburgh, ME 2006a. Developmental and nutritional regulation of the prepubertal bovine mammary gland: II. Epithelial cell proliferation, parenchymal accretion rate, and allometric growth. Journal of Dairy Science 89, 42984304.CrossRefGoogle ScholarPubMed
Meyer, MJ, Capuco, AV, Ross, DA, Lintault, LM, Van Amburgh, ME 2006b. Developmental and nutritional regulation of the prepubertal heifer mammary gland: I. Parenchyma and fat pad mass and composition. Journal of Dairy Science 89, 42894297.CrossRefGoogle ScholarPubMed
Mimeault, M, Hauke, R, Batra, SK 2007. Stem cells: a revolution in therapeutics – recent advances in stem cell biology and their therapeutic applications in regenerative medicine and cancer therapies. Clinical Pharmacology and Therapeutics 82, 252264.CrossRefGoogle ScholarPubMed
Niku, M, Ilmonen, L, Pessa-Morikawa, T, Iivanainen, A 2004. Limited contribution of circulating cells to the development and maintenance of nonhematopoietic bovine tissues. Stem Cells 22, 1220.CrossRefGoogle Scholar
Pacini, S, Spinabella, S, Trombi, L, Fazzi, R, Galimberti, S, Dini, F, Carlucci, F, Petrini, M 2007. Suspension of bone marrow-derived undifferentiated mesenchymal stromal cells for repair of superficial digital flexor tendon in race horses. Tissue Engineering 13, 29492955.CrossRefGoogle ScholarPubMed
Rambhatla, L, Ram-Mohan, S, Cheng, JJ, Sherley, JL 2005. Immortal DNA strand cosegregation requires p53/IMPDH-dependent asymmetric self-renewal associated with adult stem cells. Cancer Research 65, 31553161.CrossRefGoogle ScholarPubMed
Ribitsch, I, Burk, J, Delling, U, Geissler, C, Gittel, C, Julke, H, Brehm, W 2010. Basic science and clinical application of stem cells in veterinary medicine. Advances in Biochemical Engineering/Biotechnology 23, 219263.Google Scholar
Savarese, F, Flahndorfer, K, Jaenisch, R, Busslinger, M, Wutz, A 2006. Hematopoietic precursor cells transiently reestablish permissiveness for X inactivation. Molecular and Cellular Biology 26, 71677177.CrossRefGoogle ScholarPubMed
Sejrsen, K, Purup, S 1997. Influence of prepubertal feeding level on milk yield potential of dairy heifers: a review. Journal of Animal Science 75, 828835.CrossRefGoogle ScholarPubMed
Sejrsen, K, Huber, JT, Tucker, HA, Akers, RM 1982. Influence of nutrition on mammary development in pre- and postpubertal heifers. Journal of Dairy Science 65, 793800.CrossRefGoogle ScholarPubMed
Shackleton, M, Vaillant, F, Simpson, KJ, Stingl, J, Smyth, GK, Asselin-Labat, ML, Wu, L, Lindeman, GJ, Visvader, JE 2006. Generation of a functional mammary gland from a single stem cell. Nature 439, 8488.CrossRefGoogle ScholarPubMed
Sherley, JL 2002. Asymmetric cell kinetics genes: the key to expansion of adult stem cells in culture. Stem Cells 20, 561572.CrossRefGoogle ScholarPubMed
Sherley, JL, Stadler, PB, Johnson, DR 1995. Expression of the wild-type p53 antioncogene induces guanine nucleotide-dependent stem cell division kinetics. Proceedings of the National Academy of Sciences of the United States of America 92, 136140.CrossRefGoogle ScholarPubMed
Sinha, YN, Tucker, HA 1969. Mammary development and pituitary prolactin level of heifers from birth through puberty and during the estrous cycle. Journal of Dairy Science 52, 507512.CrossRefGoogle ScholarPubMed
Sleeman, KE, Kendrick, H, Ashworth, A, Isacke, CM, Smalley, MJ 2006. CD24 staining of mouse mammary gland cells defines luminal epithelial, myoepithelial/basal and non-epithelial cells. Breast Cancer Research 8, R7.CrossRefGoogle ScholarPubMed
Sleeman, KE, Kendrick, H, Robertson, D, Isacke, CM, Ashworth, A, Smalley, MJ 2007. Dissociation of estrogen receptor expression and in vivo stem cell activity in the mammary gland. Journal of Cell Biology 176, 1926.CrossRefGoogle ScholarPubMed
Smith, GH 1996. Experimental mammary epithelial morphogenesis in an in vivo model: evidence for distinct cellular progenitors of the ductal and lobular phenotype. Breast Cancer Research and Treatment 39, 2131.CrossRefGoogle Scholar
Smith, GH 2005. Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development 132, 681687.CrossRefGoogle ScholarPubMed
Smith, GH, Chepko, G 2001. Mammary epithelial stem cells. Microscopy Research and Technique 52, 190203.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Smith, GH, Medina, D 1988. A morphologically distinct candidate for an epithelial stem cell in mouse mammary gland. Journal of Cell Science 90, 173184.CrossRefGoogle ScholarPubMed
Smith, GH, Medina, D 2008. Re-evaluation of mammary stem cell biology based on in vivo transplantation. Breast Cancer Research 10, 203.CrossRefGoogle ScholarPubMed
Stingl, J, Eirew, P, Ricketson, I, Shackleton, M, Vaillant, F, Choi, D, Li, HI, Eaves, CJ 2006. Purification and unique properties of mammary epithelial stem cells. Nature 439, 993997.CrossRefGoogle ScholarPubMed
Takahashi, K, Yamanaka, S 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126, 663676.CrossRefGoogle ScholarPubMed
Takahashi, K, Okita, K, Nakagawa, M, Yamanaka, S 2007. Induction of pluripotent stem cells from fibroblast cultures. Nature Protocols 2, 30813089.CrossRefGoogle ScholarPubMed
Traurig, HH 1967. A radioautographic study of cell proliferation in the mammary gland of the pregnant mouse. Anatomical Record 159, 239247.CrossRefGoogle ScholarPubMed
Tucker, HA, Paape, MJ, Sinha, YN 1967. Ovariectomy and suckling intensity effects on mammary nucleic acid, prolactin, and ACTH. American Journal of Physiology 213, 262266.CrossRefGoogle ScholarPubMed
Vaillant, F, Asselin-Labat, ML, Shackleton, M, Lindeman, GJ, Visvader, JE 2007. The emerging picture of the mouse mammary stem cell. Stem Cell Reviews 3, 114123.CrossRefGoogle ScholarPubMed
Villadsen, R, Fridriksdottir, AJ, Ronnov-Jessen, L, Gudjonsson, T, Rank, F, LaBarge, MA, Bissell, MJ, Petersen, OW 2007. Evidence for a stem cell hierarchy in the adult human breast. Journal of Cell Biology 177, 87101.CrossRefGoogle ScholarPubMed
Visvader, JE, Lindeman, GJ 2006. Mammary stem cells and mammopoiesis. Cancer Research 66, 97989801.CrossRefGoogle ScholarPubMed
Wagner, KU, Boulanger, CA, Henry, MD, Sgagias, M, Hennighausen, L, Smith, GH 2002. An adjunct mammary epithelial cell population in parous females: its role in functional adaptation and tissue renewal. Development 129, 13771386.CrossRefGoogle ScholarPubMed
Welm, BE, Tepera, SB, Venezia, T, Graubert, TA, Rosen, JM, Goodell, MA 2002. Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Developmental Biology 245, 4256.CrossRefGoogle ScholarPubMed
Wilmut, I, Schnieke, AE, McWhir, J, Kind, AJ, Campbell, KH 1997. Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810813.CrossRefGoogle ScholarPubMed
Woodward, WA, Chen, MS, Behbod, F, Rosen, JM 2005. On mammary stem cells. Journal of Cell Science 118, 35853594.CrossRefGoogle ScholarPubMed
Yu, J, Vodyanik, MA, Smuga-Otto, K, Antosiewicz-Bourget, J, Frane, JL, Tian, S, Nie, J, Jonsdottir, GA, Ruotti, V, Stewart, R, Slukvin, II, Thomson, JA 2007. Induced pluripotent stem cell lines derived from human somatic cells. Science 318, 19171920.CrossRefGoogle ScholarPubMed
Zeps, N, Bentel, JM, Papadimitriou, JM, D'Antuono, MF, Dawkins, HJS 1998. Estrogen receptor-negative epithelial cells in mouse mammary gland development and growth. Differentiation 62, 221226.CrossRefGoogle ScholarPubMed
Zhou, H, Wu, S, Joo, JY, Zhu, S, Han, DW, Lin, T, Trauger, S, Bien, G, Yao, S, Zhu, Y, Siuzdak, G, Scholer, HR, Duan, L, Ding, S 2009. Generation of induced pluripotent stem cells using recombinant proteins. Cell Stem Cell 4, 381384.CrossRefGoogle ScholarPubMed