Contribution of the ABC transporters Bcrp1 and Mdr1a/1b to the side population phenotype in mammary gland and bone marrow of mice

Stem Cells

Volumn 23, Issue 8, 2005, Pages 1059-1065

  Jonker, Johan W ^a   Freeman, Jamie ^b   Bolscher, Ellen ^a   Musters, Sandra ^a   Alvi, Azra J ^c   Titley, Ian ^c   Schinkel, Alfred H ^a   Dale, Trevor C ^b,c  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

^b CARDIFF UNIVERSITY   (United Kingdom)

^c INSTITUTE OF CANCER RESEARCH   (United Kingdom)

Author keywords

Adult bone marrow stem cells; ATP binding cassette transporter; Progenitor cells fluoresence activated cell sorting analysis

Indexed keywords

ABC TRANSPORTER; HOE 33342; KO 143; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 1A; MULTIDRUG RESISTANCE PROTEIN 1B; PROTEIN BCRP1; PROTEIN BCRP1 INHIBITOR; PROTEIN INHIBITOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL SUBPOPULATION; CELL TRANSPORT; CONTROLLED STUDY; FEMALE; KNOCKOUT MOUSE; MAMMARY GLAND; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; STEM CELL;

ANIMALS; ATP-BINDING CASSETTE TRANSPORTERS; BENZIMIDAZOLES; BONE MARROW CELLS; CELL SURVIVAL; EPITHELIAL CELLS; FEMALE; FLOW CYTOMETRY; GENE SILENCING; HEMATOPOIETIC STEM CELLS; IMMUNOHISTOCHEMISTRY; MAMMARY GLANDS, ANIMAL; MICE; MICE, KNOCKOUT; P-GLYCOPROTEINS; PHENOTYPE;

EID: 25444485195     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2005-0150     Document Type: Article

References (34)

1. Goodell MA, Brose K, Paradis G et al. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 1996;183:1797-1806.
2. Zhou S, Schuetz JD, Bunting KD et al. The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 2001;7:1028-1034.
3. Zhou S, Morris JJ, Barnes Y et al. Bcrp1 gene expression is required for normal numbers of side population stem cells in mice, and confers relative protection to mitoxantrone in hematopoietic cells in vivo. Proc Natl Acad Sci U S A 2002;99:12339-12344.
4. Zhou S, Zong Y, Lu T et al. Hematopoietic cells from mice that are deficient in both Bcrp1/Abcg2 and Mdr1a/1b develop normally but are sensitized to mitoxantrone. Biotechniques 2003;35:1248-1252.
5. Scharenberg CW, Harkey MA, Torok-Storb B. The ABCG2 transporter is an efficient Hoechst 33342 efflux pump and is preferentially expressed by immature human hematopoietic progenitors. Blood 2002;99:507-512.
6. Kim M, Turnquist H, Jackson J et al. The multidrug resistance transporter ABCG2 (breast cancer resistance protein 1) effluxes Hoechst 33342 and is overexpressed in hematopoietic stem cells. Clin Cancer Res 2002;8:22-28.
7. Alvi AJ, Clayton H, Joshi C et al. Functional and molecular characterisation of mammary side population cells. Breast Cancer Res 2002;5:R1-R8.
8. Welm BE, Tepera SB, Venezia T et al. Sca-1(pos) cells in the mouse mammary gland represent an enriched progenitor cell population. Dev Biol 2002;245:42-56.
9. Clayton H, Titley I, Vivanco M. Growth and differentiation of progenitor/stem cells derived from the human mammary gland. Exp Cell Res 2004;297:444-460.
10. Asakura A, Seale P, Girgis-Gabardo A et al. Myogenic specification of side population cells in skeletal muscle. J Cell Biol 2002;159:123-134.
11. Lechner A, Leech CA, Abraham EJ et al. Nestin-positive progenitor cells derived from adult human pancreatic islets of Langerhans contain side population (SP) cells defined by expression of the ABCG2 (BCRP1) ATP-binding cassette transporter. Biochem Biophys Res Commun 2002;293:670-674.
12. Summer R, Kotton DN, Sun X et al. Side population cells and Bcrp1 expression in lung. Am J Physiol Lung Cell Mol Physiol 2003;285:L97-104.
13. Bhattacharya S, Jackson JD, Das AV et al. Direct identification and enrichment of retinal stem cells/progenitors by Hoechst dye efflux assay. Invest Ophthalmol Vis Sci 2003;44:2764-2773.
14. Shimano K, Satake M, Okaya A et al. Hepatic oval cells have the side population phenotype defined by expression of ATP-binding cassette transporter ABCG2/BCRP1. Am J Pathol 2003;163:3-9.
15. Lassalle B, Bastos H, Louis JP et al. "Side population" cells in adult mouse testis express Bcrp1 gene and are enriched in spermatogonia and germinal stem cells. Development 2003;131:479-487.
16. Martin CM, Meeson AP, Robertson SM et al. Persistent expression of the ATP-binding cassette transporter, Abcg2, identifies cardiac SP cells in the developing and adult heart. Dev Biol 2004;265:262-275.
17. Triel C, Vestergaard ME, Bolund L et al. Side population cells in human and mouse epidermis lack stem cell characteristics. Exp Cell Res 2004;295:79-90.
18. Kondo T, Setoguchi T, Taga T. Persistence of a small subpopulation of cancer stem-like cells in the C6 glioma cell line. Proc Natl Acad Sci U S A 2004;101:781-786.
19. Setoguchi T, Taga T, Kondo T. Cancer stem cells persist in many cancer cell lines. Cell Cycle 2004;3:414-415.
20. Hirschmann-Jax C, Foster AE, Wulf GG et al. A distinct "side population" of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci U S A 2004;101:14228-14233.
21. Krishnamurthy P, Ross DD, Nakanishi T et al. The stem cell marker Bcrp/ABCG2 enhances hypoxic cell survival through interactions with heme. J Biol Chem 2004;279:24218-24225.
22. Jonker JW, Buitelaar M, Wagenaar E et al. The breast cancer resistance protein protects against a major chlorophyll-derived dietary phototoxin and protoporphyria. Proc Natl Acad Sci U S A 2002;99:15649-15654.
23. Schinkel AH, Smit JJ, Van Tellingen O et al. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 1994;77:491-502.
24. 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.
25. Naylor S, Smalley MJ, Robertson D et al. Retroviral expression of Wnt-1 and Wnt-7b produces different effects in mouse mammary epithelium. J Cell Sci 2000;113:2129-2138.
26. Schinkel AH, Mayer U, Wagenaar E et al. Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins. Proc Natl Acad Sci U S A 1997;94:4028-4033.
27. Allen JD, Van Loevezijn A, Lakhai JM et al. Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Mol Cancer Ther 2002;1:417-425.
28. Welm B, Behbod F, Goodell MA et al. Isolation and characterization of functional mammary gland stem cells. Cell Prolif 2003;36(suppl 1):17-32.
29. Triel C, Vestergaard ME, Bolund L et al. Side population cells in human and mouse epidermis lack stem cell characteristics. Exp Cell Res 2004;295:79-90.
30. Montanaro F, Liadaki K, Schienda J et al. Demystifying SP cell purification: viability, yield, and phenotype are defined by isolation parameters. Exp Cell Res 2004;298:144-154.
31. Jonker JW, Merino G, Musters S et al. The breast cancer resistance protein BCRP (ABCG2) concentrates drugs and carcinogenic xenotoxins into milk. Nat Med 2005;11:127-129.
32. Petersen OW, Gudjonsson T, Villadsen R et al. Epithelial progenitor cell lines as models of normal breast morphogenesis and neoplasia. Cell Prolif 2003;36(suppl 1):33-44.
33. Clarke RB, Smith GH. Stem cells and tissue homeostasis in mammary glands. J Mammary Gland Biol Neoplasia 2005;10:1-3.
34. Morroni M, Giordano A, Zingaretti MC et al. Reversible transdifferentiation of secretory epithelial cells into adipocytes in the mammary gland. Proc Natl Acad Sci U S A 2004;101:16801-16806.