Mammary stem cells: expansion and animal productivity

Journal of Animal Science and Biotechnology

Ratan K Choudhary¹ 

[1] School of Animal Biotechnology, Guru Angad Dev Veterinary and Animal Science University, Ludhiana, Punjab 141004, India

关键词: Xanthosine;    Ruminant;    Milk production;    Manipulation;    Mammary stem cell;    Hormones;   

Others  :  1139240
DOI  :  10.1186/2049-1891-5-36

 received in 2014-01-12, accepted in 2014-07-04,  发布年份 2014

【 摘 要 】

Identification and characterization of mammary stem cells and progenitor cells from dairy animals is important in the understanding of mammogenesis, tissue turnover, lactation persistency and regenerative therapy. It has been realized by many investigators that altered lactation, long dry periods (non-milking period between two consecutive lactation cycles), abrupt cessation of lactation (common in water buffaloes) and disease conditions like mastitis, greatly reduce milk yield thus render huge financial losses within the dairy sector. Cellular manipulation of specialized cell types within the mammary gland, called mammary stem cells (MaSCs)/progenitor cells, might provide potential solutions to these problems and may improve milk production. In addition, MaSCs/progenitor cells could be used in regenerative therapy against tissue damage caused by mastitis. This review discusses methods of MaSC/progenitor cell manipulation and their mechanisms in bovine and caprine animals. Author believes that intervention of MaSCs/progenitor cells could lessen the huge financial losses to the dairy industry globally.

【 授权许可】

   
2014 Choudhary; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Akers RM, Capuco AV, Keys JE: Mammary histology and alveolar cell differentiation during late gestation and early lactation in mammary tissue of beef and dairy heifers. Livest Sci 2006, 105:44-49.
• [2]Safayi S, Theil PK, Hou L, Engbaek M, Nørgaard JV, Sejrsen K, Nielsen MO: Continuous lactation effects on mammary remodeling during late gestation and lactation in dairy goats. J Dairy Sci 2010, 93:203-17.
• [3]Visvader JE, Lindeman GJ: Mammary stem cells and mammopoiesis. Cancer Res 2006, 66:9798-9801.
• [4]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.
• [5]Esmailpour T, Huang T: Advancement in mammary stem cell research. Pathology 2008, 4:131-138.
• [6]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.
• [7]Capuco AV, Wood DL, Baldwin R, Mcleod K, Paape MJ: Mammary cell number, proliferation, and apoptosis during a bovine lactation: relation to milk production and effect of bST. J Dairy Sci 2001, 84:2177-87.
• [8]Wall EH, Auchtung TL, Dahl GE, Ellis SE, McFadden TB: Exposure to short day photoperiod during the dry period enhances mammary growth in dairy cows. J Dairy Sci 2005, 88:1994-2003.
• [9]Capuco AV, Evock-Clover CM, Minuti A, Wood DL: In vivo expansion of the mammary stem/ progenitor cell population by xanthosine infusion. Exp Biol Med (Maywood) 2009, 234:475-482.
• [10]Capuco AV, Ellis SE, Hale SA, Long E, Erdman RA, Zhao X, Paape MJ: Lactation persistency: Insights from mammary cell proliferation studies. J Anim Sci 2003, 81:18-31.
• [11]Borena BM, Bussche L, Burvenich C, Duchateau L, Van de Walle GR: Mammary stem cell research in veterinary science: an update. Stem Cells Dev 2013, 22:1743-1751.
• [12]Capuco AV, Ellis SE: Comparative Aspects of Mammary Gland Development and Homeostasis. Annu Rev Anim Biosci 2013, 1:179-202.
• [13]Kordon EC, Smith GH: An entire functional mammary gland may comprise the progeny from a single cell. Development 1998, 125:1921-1930.
• [14]Prpar S, Martignani E, Dovc P, Baratta M: Identification of goat mammary stem/progenitor cells. Biol Reprod 2012, 86:117.
• [15]Kaimala S, Bisana S, Kumar S: Mammary gland stem cells: more puzzles than explanations. J Biosci 2012, 37:349-358.
• [16]Joshi PA, Khokha R: The mammary stem cell conundrum: is it unipotent or multipotent? Breast Cancer Res 2012, 14:305.
• [17]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.
• [18]Shackleton M, Vaillant F, Simpson KJ, Stingl J, Smyth GK, Asselin-Labat M-L, Wu L, Lindeman GJ, Visvader JE: Generation of a functional mammary gland from a single stem cell. Nature 2006, 439:84-88.
• [19]Dey D, Saxena M, Paranjape AN, Krishnan V, Giraddi R, Kumar MV, Mukherjee G, Rangarajan A: Phenotypic and functional characterization of human mammary stem/progenitor cells in long term culture. PLoS One 2009, 4:e5329.
• [20]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 Cell Dev Biol Anim 1998, 34:711-721.
• [21]Stingl J, Raouf A, Emerman JT, Eaves CJ: Epithelial progenitors in the normal human mammary gland. J Mammary Gland Biol Neoplasia 2005, 10:49-59.
• [22]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.
• [23]Choudhary RK, Choudhary S: Ruminant mammary stem cells: Methods of identification and status. Rumin Sci 2012, 1:101-108.
• [24]Eirew P, Stingl J, Raouf A, Turashvili G, Aparicio S, Emerman JT, Eaves CJ: A method for quantifying normal human mammary epithelial stem cells with in vivo regenerative ability. Nat Med 2008, 14:1384-1389.
• [25]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.
• [26]Meier-Abt F, Milani E, Roloff T, Brinkhaus H, Duss S, Meyer DS, Klebba I, Balwierz PJ, van Nimwegen E, Bentires-Alj M: Parity induces differentiation and reduces Wnt/Notch signaling ratio and proliferation potential of basal stem/progenitor cells isolated from mouse mammary epithelium. Breast Cancer Res 2013, 15:R36.
• [27]Rauner G, Barash I: Cell hierarchy and lineage commitment in the bovine mammary gland. PLoS One 2012, 7:e30113.
• [28]Capuco AV: Identification of putative bovine mammary epithelial stem cells by their retention of labeled DNA strands. Exp Biol Med (Maywood) 2007, 232:1381-1390.
• [29]Smith GH: Label-retaining epithelial cells in mouse mammary gland divide asymmetrically and retain their template DNA strands. Development 2005, 132:681-687.
• [30]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.
• [31]Choudhary RK, Li RW, Evock-Clover CM, Capuco AV: Comparison of the transcriptomes of long-term label retaining-cells and control cells microdissected from mammary epithelium: an initial study to characterize potential stem/progenitor cells. Front Oncol 2013, 3:21.
• [32]Vogel A, Horneffer V, Lorenz K, Linz N, Hüttmann G, Gebert A: Principles of laser microdissection and catapulting of histologic specimens and live cells. Methods Cell Biol 2007, 82:153-205.
• [33]Legres LG, Janin A, Masselon C, Bertheau P: Beyond laser microdissection technology: follow the yellow brick road for cancer research. Am J Cancer Res 2014, 4:1-28.
• [34]Choudhary RK, Daniels KM, Evock-Clover CM, Garrett W, Capuco AV: Technical note: A rapid method for 5-bromo-2’-deoxyuridine (BrdU) immunostaining in bovine mammary cryosections that retains RNA quality. J Dairy Sci 2010, 93:2574-2579.
• [35]Ellis S, Capuco AV: Cell proliferation in bovine mammary epithelium: identification of the primary proliferative cell population. Tissue Cell 2002, 34:155-163.
• [36]Epting CL, King FW, Pedersen A, Zaman J, Ritner C, Bernstein HS: Stem cell antigen-1 localizes to lipid microdomains and associates with insulin degrading enzyme in skeletal myoblasts. J Cell Physiol 2008, 217:250-260.
• [37]Motyl T, Bierła JB, Kozłowski M, Gajewska M, Gajkowska B, Koronkiewicz M: Identification, quantification and transcriptional profile of potential stem cells in bovine mammary gland. Livest Sci 2011, 136:136-149.
• [38]Heng J-CD, Feng B, Han J, Jiang J, Kraus P, Ng J-H, Orlov YL, Huss M, Yang L, Lufkin T, Lim B, Ng H-H: The nuclear receptor Nr5a2 can replace Oct4 in the reprogramming of murine somatic cells to pluripotent cells. Cell Stem Cell 2010, 6:167-174.
• [39]Navarro P, Chambers I, Karwacki-Neisius V, Chureau C, Morey C, Rougeulle C, Avner P: Molecular coupling of Xist regulation and pluripotency. Science 2008, 321:1693-1695.
• [40]Li H, Cherukuri P, Li N, Cowling V, Spinella M, Cole M, Godwin AK, Wells W, DiRenzo J: Nestin is expressed in the basal/myoepithelial layer of the mammary gland and is a selective marker of basal epithelial breast tumors. Cancer Res 2007, 67:501-510.
• [41]Simões BM, Piva M, Iriondo O, Comaills V, López-Ruiz JA, Zabalza I, Mieza JA, Acinas O, Vivanco MDM: Effects of estrogen on the proportion of stem cells in the breast. Breast Cancer Res Treat 2011, 129:23-35.
• [42]Lengerke C, Fehm T, Kurth R, Neubauer H, Scheble V, Müller F, Schneider F, Petersen K, Wallwiener D, Kanz L, Fend F, Perner S, Bareiss PM, Staebler A: Expression of the embryonic stem cell marker SOX2 in early-stage breast carcinoma. BMC Cancer 2011, 11:42.
• [43]Hassiotou F, Beltran A, Chetwynd E, Stuebe AM, Twigger A-J, Metzger P, Trengove N, Lai CT, Filgueira L, Blancafort P, Hartmann PE: Breastmilk is a novel source of stem cells with multilineage differentiation potential. Stem Cells 2012, 30:2164-2174.
• [44]Li P, Wilde CJ, Finch LM, Fernig DG, Rudland PS: Identification of cell types in the developing goat mammary gland. Histochem J 1999, 31:379-393.
• [45]Capuco AV, Ellis S: Bovine mammary progenitor cells: current concepts and future directions. J Mammary Gland Biol Neoplasia 2005, 10:5-15.
• [46]Capuco AV, Choudhary RK, Daniels KM, Li RW, Evock-Clover CM: Bovine mammary stem cells: cell biology meets production agriculture. Animal 2012, 6:382-393.
• [47]Rios AC, Fu NY, Lindeman GJ, Visvader JE: In situ identification of bipotent stem cells in the mammary gland. Nature 2014, 506:322-327.
• [48]Boutinaud M, Guinard-Flamenta J, Jammes H: The number and activity of mammary epithelial cells, determining factors for milk production. Reprod Nutr Dev 2004, 44:499-508.
• [49]Joshi PA, Jackson HW, Beristain AG, Di Grappa MA, Mote PA, Clarke CL, Stingl J, Waterhouse PD, Khokha R: Progesterone induces adult mammary stem cell expansion. Nature 2010, 465:803-807.
• [50]Rahal OM, Simmen RCM: Paracrine-acting adiponectin promotes mammary epithelial differentiation and synergizes with genistein to enhance transcriptional response to estrogen receptor β signaling. Endocrinology 2011, 152:3409-3421.
• [51]Baldassarre H, Deslauriers J, Neveu N, Bordignon V: Detection of endoplasmic reticulum stress markers and production enhancement treatments in transgenic goats expressing recombinant human butyrylcholinesterase. Transgenic Res 2011, 20:1265-1272.
• [52]Choudhary RK, Capuco AV: In vitro expansion of the mammary stem/progenitor cell population by xanthosine treatment. BMC Cell Biol 2012, 13:14.
• [53]Lee H-S, Crane GG, Merok JR, Tunstead JR, Hatch NL, Panchalingam K, Powers MJ, Griffith LG, Sherley JL: Clonal expansion of adult rat hepatic stem cell lines by suppression of asymmetric cell kinetics (SACK). Biotechnol Bioeng 2003, 83:760-771.
• [54]Matulka LA, Triplett AA, Wagner K-U: Parity-induced mammary epithelial cells are multipotent and express cell surface markers associated with stem cells. Dev Biol 2007, 303:29-44.
• [55]Boulanger CA, Wagner K-U, Smith GH: Parity-induced mouse mammary epithelial cells are pluripotent, self-renewing and sensitive to TGF-beta1 expression. Oncogene 2005, 24:552-560.
• [56]Booth BW, Boulanger CA, Smith GH: Alveolar progenitor cells develop in mouse mammary glands independent of pregnancy and lactation. J Cell Physiol 2007, 212:729-736.
• [57]Wagner K-U, Smith GH: Pregnancy and stem cell behavior. J Mammary Gland Biol Neoplasia 2005, 10:25-36.
• [58]Choudhary RK, Evock-Clover CM, Capuco AV: Expression of noval, putative mammary stem markers in prepubertal and lactating bovine mammary glands. J Dairy Sci 2011, 94:180.
• [59]Sherley JL: Guanine nucleotide biosynthesis is regulated by the cellular p53 concentration. J Biol Chem 1991, 266:24815-28428.
• [60]Sherley JL: Asymmetric cell kinetics genes: The key to expansion of adult stem cells in culture. Stem Cells 2002, 20:561-572.
• [61]Asselin-Labat M-L, Vaillant F, Sheridan JM, Pal B, Wu D, Simpson ER, Yasuda H, Smyth GK, Martin TJ, Lindeman GJ, Visvader JE: Control of mammary stem cell function by steroid hormone signalling. Nature 2010, 465:798-802.
• [62]Dou X, Zhang B, Liu R, Li J, Shi D, Lu C, Zhu X, Liao L, Du Z, Zhao RC: Expanding Sca-1(+) mammary stem cell in the presence of oestrogen and growth hormone. Clin Transl Oncol 2012, 14:444-451.
• [63]Graham JD, Mote PA, Salagame U, van Dijk JH, Balleine RL, Huschtscha LI, Reddel RR, Clarke CL: DNA replication licensing and progenitor numbers are increased by progesterone in normal human breast. Endocrinology 2009, 150:3318-3326.
• [64]Beleut M, Rajaram RD, Caikovski M, Ayyanan A, Germano D, Choi Y, Schneider P, Brisken C: Two distinct mechanisms underlie progesterone-induced proliferation in the mammary gland. Proc Natl Acad Sci U S A 2010, 107:2989-2994.
• [65]Schams D, Kohlenberg S, Amselgruber W, Berisha B, Pfaffl MW, Sinowatz F: Expression and localisation of oestrogen and progesterone receptors in the bovine mammary gland during development, function and involution. J Endocrinol 2003, 177:305-317.
• [66]Roarty K, Rosen JM: Wnt and mammary stem cells: hormones cannot fly wingless. Curr Opin Pharmacol 2010, 10:643-649.
• [67]Wood CE, Branstetter D, Jacob AP, Cline JM, Register TC, Rohrbach K, Huang L-Y, Borgerink H, Dougall WC: Progestin effects on cell proliferation pathways in the postmenopausal mammary gland. Breast Cancer Res 2013, 15:R62.
• [68]Collier RJ, Annen-Dawson EL, Pezeshki A: Effects of continuous lactation and short dry periods on mammary function and animal health. Animal 2012, 6:403-414.
• [69]Annen EL, Collier RJ, Mcguire MA, Vicini JL, Ballam JM, Lormore MJ: Effects of Dry Period Length on Milk Yield and Mammary Epithelial Cells *. J Dairy Sci 2004, 87(June 2003):66-76.
• [70]Annen EL, Collier RJ, McGuire MA, Vicini JL, Ballam JM, Lormore MJ: Effect of modified dry period lengths and bovine somatotropin on yield and composition of milk from dairy cows. J Dairy Sci 2004, 87:3746-3761.
• [71]Annen EL, Stiening CM, Crooker BA, Fitzgerald AC, Collier RJ: Effect of continuous milking and prostaglandin E2 on milk production and mammary epithelial cell turnover, ultrastructure, and gene expression. J Anim Sci 2008, 86:1132-1144.
• [72]Caja G, Salama AAK, Such X: Omitting the dry-off period negatively affects colostrum and milk yield in dairy goats. J Dairy Sci 2006, 89:4220-4228.
• [73]Safayi S, Theil PK, Elbrønd VS, Hou L, Engbaek M, Nørgaard JV, Sejrsen K, Nielsen MO: Mammary remodeling in primiparous and multiparous dairy goats during lactation. J Dairy Sci 2010, 93:1478-1490.
• [74]Baldassarre H, Schirm M, Deslauriers J, Turcotte C, Bordignon V: Protein profile and alpha-lactalbumin concentration in the milk of standard and transgenic goats expressing recombinant human butyrylcholinesterase. Transgenic Res 2009, 18:621-632.