Isolation and characterization of functional mammary gland stem cells

Cell Proliferation, Supplement

Volumn 36, Issue 1, 2003, Pages 17-32

  Welm, Bryan ^a,b   Behbod, Fariba ^b   Goodell, Margaret A ^c   Rosen, J M ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c CENTER FOR CELL AND GENE THERAPY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMICAL MARKER; CELL ANTIGEN; KERATIN; KERATIN 6; STEM CELL ANTIGEN 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL MODEL; BREAST CANCER; BREAST CARCINOGENESIS; CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION; GENETIC ENGINEERING; MAMMARY GLAND; MOUSE; NONHUMAN; REVIEW; STEM CELL; TRANSGENIC MOUSE;

ANIMALIA; MUS MUSCULUS;

EID: 0346244093     PISSN: 14778408     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2184.36.s.1.3.x     Document Type: Review

References (94)

1. AL-HAJJ M, WICHA M, BENITO-HERNANDEZ A, MORRISON SJ, CLARKE MF (2003) Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100, 6980.
2. ALLEN JD, BRINKHUIS RF, WIJNHOLDS J, SCHINKEL AH (1999) The mouse BcrpI/Mxr/Abcp gene: amplification and overexpression in cell lines selected for resistance to topotecan, mitoxantrone, or doxorubicin. Cancer Res. 59, 4237.
3. ALVI AJ, CLAYTON H, JOSHI C, ENVER T, ASHWORTH A, VIVANCO MDM, DALE TC, SMALLEY MJ (2002) Functional and molecular characterisation of mammary side population cells. Breast Cancer Res. 5, R1.
4. ARTAVANIS-TSAKONAS S, RAND MD, LAKE RJ (1999) Notch signaling: cell fate control and signal integration in development. Science. 284, 770.
5. ATTISANO L, WRANA JL, LOPEZ-CASILLAS F, MASSAGUE J (1994) TGF-beta receptors and actions. Biochim. Biophys. Acta 1222, 71.
6. BARBARESCHI M, PECCIARINI L, CANGI MG, MACRI E, RIZZO A, VIALE G, DOGLIONI C (2001) p63, a p53 homologue, is a selective nuclear marker of myoepithelial cells of the human breast. Am. J. Surg. Pathol. 25, 1054.
7. BHARDWAJ G, MURDOCH B, WU D, BAKER DP, WILLIAMS KP, CHADWICK K, LING LE, KARANU FN, BHATIA M (2001) Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat. Immunol. 2, 172.
8. BHATIA M, BONNET D, WU D, MURDOCH B, WRANA J, GALLACHER L, DICK JE (1999) Bone morphogenetic proteins regulate the developmental program of human hematopoietic stem cells. J. Exp. Med. 189, 1139.
9. BORTHWICK DW, SHAHBAZIAN M, KRANTZ QT, DORIN JR, RANDELL SH (2001) Evidence for stem-cell niches in the tracheal epithelium. Am. J. Respir. Cell Mol. Biol. 24, 662.
10. BOULANGER CA, SMITH GH (2001) Reducing mammary cancer risk through premature stem cell senescence. Oncogene. 20, 2264.
11. BRITTAN M, WRIGHT NA (2002) Gastrointestinal stem cells. J. Pathol. 197, 492.
12. CARDIFF RD, ANVER MR, GUSTERSON BA, HENNIGHAUSEN L, JENSEN RA, MERINO MJ, REHM S, RUSSO J, TAVASSOLI FA, WAKEFIELD LM, WARD JM, GREEN JE (2000) The mammary pathology of genetically engineered mice: the consensus report and recommendations from the Annapolis meeting. Oncogene 19, 968.
13. CASHMAN JD, LAPIDOT T, WANG JC, DOEDENS M, SHULTZ LD, LANSDORP P, DICK JE, EAVES CJ (1997) Kinetic evidence of the regeneration of multilineage hematopoiesis from primitive cells in normal human bone marrow transplanted into immunodeficient mice. Blood 89, 4307.
14. CHEN YN, MICKLEY LA, SCHWARTZ AM, ACTON EM, HWANG JL, FOJO AT (1990) Characterization of adriamycin-resistant human breast cancer cells which display overexpression of a novel resistance-related membrane protein. J. Biol. Chem. 265, 10073.
15. CHEPKO G, SMITH GH (1997) Three division-competent, structurally- distinct cell populations contribute to murine mammary epithelial renewal. Tissue Cell. 29, 239.
16. COTSARELIS G, CHENG SZ, DONG G, SUN TT, LAVKER RM (1989) Existence of slow-cycling limbal epithelial basal cells that can be preferentially stimulated to proliferate: implications on epithelial stem cells. Cell 57, 201.
17. COTSARELIS G, SUN TT, LAVKER RM (1990) Label-retaining cells reside in the bulge area of pilosebaceous unit: implications for follicular stem cells, hair cycle, and skin carcinogenesis. Cell 61, 1329.
18. DANIEL CW, DE OME KB, YOUNG JT, BLAIR PB, FAULKIN LJ, JR (1968) The in vivo life span of normal and preneoplastic mouse mammary glands: a serial transplantation study. Proc. Natl Acad. Sci. USA 61, 53.
19. DANIEL CW, SILBERSTEIN GB (1987) Postnatal development of the rodent mammary gland. In: Neville MC, Daniel CW, eds. The Mammary Gland. New York: Plenum Press, p. 3.
20. DEOME KB FI, BERN HA, BLAIR PB (1959) Development of mammary tumors from hyperplastic alveolar nodules transplanted into gland free mammary fat pads of female C3H mice. J. Natl Cancer Inst. 78, 751.
21. DESAI KV, XIAO N, WANG W, GANGI L, GREENE J, POWELL JI, DICKSON R, FURTH P, HUNTER K, KUCHERLAPATI R, SIMON R, LIU ET, GREEN JE (2002) Initiating oncogenic event determines gene-expression patterns of human breast cancer models. Proc. Natl Acad. Sci. USA 99, 6967.
22. DULBECCO R, ALLEN WR, BOLOGNA M, BOWMAN M (1986) Marker evolution during the development of the rat mammary gland: stem cells identified by markers and the role of myoepithelial cells. Cancer Res. 46, 2449.
23. DULBECCO R, ARMSTRONG B, ALLEN WR, BOWMAN M (1986) Distribution of developmental markers in rat mammary tumors induced by N-nitrosomethylurea. Cancer Res. 46, 5144.
24. DULBECCO R, HENAHAN M, ARMSTRONG B (1982) Cell types and morphogenesis in the mammary gland. Proc. Natl Acad. Sci. USA 79, 7346.
25. EAVES AC, EAVES CJ (1988) Maintenance and proliferation control of primitive hemopoietic progenitors in long-term cultures of human marrow cells. Blood Cells 14, 355.
26. FARALDO MM, DEUGNIER MA, LUKASHEV M, THIERY JP, GLUKHOVA MA (1998) Perturbation of beta1-integrin function alters the development of murine mammary gland. EMBO J. 17, 2139.
27. GOODELL MA, BROSE K, PARADIS G, CONNER AS, MULLIGAN RC (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 183, 1797.
28. GRIMM SL, SEAGROVES TN, KABOTYANSKI EB, HOVEY RC, VONDERHAAR BK, LYDON JP, MIYOSHI K, HENNIGHAUSEN L, ORMANDY CJ, LEE AV, STULL MA, WOOD TL, ROSEN JM (2002) Disruption of steroid and prolactin receptor patterning in the mammary gland correlates with a block in lobuloalveolar development. Mol. Endocrinol. 16, 2675.
29. GUDJONSSON T, VILLADSEN R, NIELSEN HL, RONNOV-JESSEN L, BISSELL MJ, PETERSEN OW (2002) Isolation, immortalization, and characterization of a human breast epithelial cell line with stem cell properties. Genes Dev. 16, 693.
30. HASLAM SZ, BERN HA (1977) Histopathogenesis of 7,12-diemthylbenz (a) anthracene-induced rat mammary tumors. Proc. Natl Acad. Sci. USA 74, 4020.
31. HATZFELD J, LI ML, BROWN EL, SOOKDEO H, LEVESQUE JP, O'TOOLE T, GURNEY C, CLARK SC, HATZFELD A (1991) Release of early human hematopoietic progenitors from quiescence by antisense transforming growth factor beta 1 or Rb oligonucleotides. J. Exp. Med. 174, 925.
32. HENNIGHAUSEN L (2000) Mouse models for breast cancer. Breast Cancer Res. 2, 2.
33. HENNIGHAUSEN L, ROBINSON GW (2001) Signaling pathways in mammary gland development. Dev. Cell. 1, 467.
34. HOCKFIELD S, MCKAY RD (1985) Identification of major cell classes in the developing mammalian nervous system. J. Neurosci. 5, 3310.
35. HOGAN CJ, SHPALL EJ, MCNULTY O, MCNIECE I, DICK JE, SHULTZ LD, KELLER G (1997) Engraftment and development of human CD34(+)-enriched cells from umbilical cord blood in NOD/LtSz-scid/scid mice. Blood 90, 85.
36. HUMPHREYS RC, LYDON JP, O'MALLEY BW, ROSEN JM (1997) Use of PRKO mice to study the role of progesterone in mammary gland development. J. Mammary Gland Biol. Neoplasia 2, 343.
37. IVANOVA NB, DIMOS JT, SCHANIEL C, HACKNEY JA, MOORE KA, LEMISCHKA IR (2002) A stem cell molecular signature. Science 298, 601.
38. JACKSON KA, MAJKA SM, WULF GG, GOODELL MA (2002) Stem cells: a minireview. J. Cell Biochem. Suppl. Suppl. 38, 1.
39. 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, 713.
40. KANEKO Y, SAKAKIBARA S, IMAI T, SUZUKI A, NAKAMURA Y, SAWAMOTO K, OGAWA Y, TOYAMA Y, MIYATA T, OKANO H (2000) Musashi-1: an evolutionally conserved marker for CNS progenitor cells including neural stem cells. Dev. Neurosci. 22, 139.
41. KARANU FN, MURDOCH B, GALLACHER L, WU DM, KOREMOTO M, SAKANO S, BHATIA M (2000) The notch ligand jagged-1 represents a novel growth factor of human hematopoietic stem cells. J. Exp. Med. 192, 1365.
42. KORDON EC, MCKNIGHT RA, JHAPPAN C, HENNIGHAUSEN L, MERLINO G, SMITH GH (1995) Ectopic TGF beta 1 expression in the secretory mammary epithelium induces early senescence of the epithelial stem cell population. Dev. Biol. 168, 47.
43. KORDON EC, SMITH GH (1998) An entire functional mammary gland may comprise the progeny from a single cell. Development 125, 1921.
44. LAND CE, MCGREGOR DH (1979) Breast cancer incidence among atomic bomb survivors: implications for radiobiologic risk at low doses. J. Natl Cancer Inst. 62, 17.
45. LENDAHL U, ZIMMERMAN LB, MCKAY RD (1990) CNS stem cells express a new class of intermediate filament protein. Cell. 60, 585.
46. LI Y, WELM B, PODSYPANINA K, HUANG S, CHAMORRO M, ZHANG X, ROWLANDS T, EGEBLAD M, COWIN P, WERB Z, TAN LK, ROSEN JM, VARMUS HE (2003) Differential expression of developmental markers in transgene-induced mouse mammary cancers correlates with activation of different signaling pathways. Genes Develop. Submitted.
47. LOWELL S, JONES P, LE ROUX I, DUNNE J, WATT FM (2000) Stimulation of human epidermal differentiation by delta-notch signalling at the boundaries of stem-cell clusters. Curr. Biol. 10, 491.
48. MACKENZIE IC, BICKENBACH JR (1985) Label-retaining keratinocytes and Langerhans cells in mouse epithelia. Cell Tissue Res. 242, 551.
49. MAENO M, MEAD PE, KELLEY C, XU RH, KUNG HF, SUZUKI A, UENO N, ZON LI (1996) The role of BMP-4 and GATA-2 in the induction and differentiation of hematopoietic mesoderm in Xenopus laevis. Blood 88, 1965.
50. MASSAGUE J (1996) TGFbeta signaling: receptors, transducers, and Mad proteins. Cell 85, 947.
51. MELTZER H, HATTON JD, SANG UH (1998) Cell type-specific development of rodent central nervous system progenitor cells in culture. J. Neurosurg. 88, 93.
52. MILLS AA, ZHENG B, WANG XJ, VOGEL H, ROOP DR, BRADLEY A (1999) p63 is a p53 homologue required for limb and epidermal morphogenesis. Nature 398, 708.
53. MIYOSHI K, SHILLINGFORD JM, SMITH GH, GRIMM SL, WAGNER KU, OKA T, ROSEN JM, ROBINSON GW, HENNIGHAUSEN L (2001) Signal transducer and activator of transcription (Stat) 5 controls the proliferation and differentiation of mammary alveolar epithelium. J. Cell Biol. 155, 531.
54. OKANO H (2002) Stem cell biology of the central nervous system. J. Neurosci. Res. 69, 698.
55. OKANO H, IMAI T, OKABE M (2002) Musashi: a translational regulator of cell fate. J. Cell Sci. 115, 1355.
56. PECHOUX C, GUDJONSSON T, RONNOV-JESSEN L, BISSELL MJ, PETERSEN OW (1999) Human mammary luminal epithelial cells contain progenitors to myoepithelial cells. Dev. Biol. 206, 88.
57. PEVNY LH, SOCKANATHAN S, PLACZEK M, LOVELL-BADGE R (1998) A role for SOX1 in neural determination. Development 125, 1967.
58. PFLUMIO F, IZAC B, KATZ A, SHULTZ LD, VAINCHENKER W, COULOMBEL L (1996) Phenotype and function of human hematopoietic cells engrafting immune-deficient CB17-severe combined immunodeficiency mice and nonobese diabetic-severe combined immunodeficiency mice after transplantation of human cord blood mononuclear cells. Blood 88, 3731.
59. POTTEN CS, MORRIS RJ (1988) Epithelial stem cells in vivo. J. Cell Sci. Suppl 10, 45.
60. RAMALHO-SANTOS M, YOON S, MATSUZAKI Y, MULLIGAN RC, MELTON DA (2002) 'Stemness': transcriptional profiling of embryonic and adult stem cells. Science 298, 597.
61. REYA T, MORRISON SJ, CLARKE MF, WEISSMAN IL (2001) Stem cells, cancer, and cancer stem cells. Nature 414, 105.
62. ROBEY RW, HONJO Y, VAN DE LAAR A, MIYAKE K, REGIS JT, LITMAN T, BATES SE (2001) A functional assay for detection of the mitoxantrone resistance protein, MXR (ABCG2). Biochim. Biophys. Acta 1512, 171.
63. ROCK KL, REISER H, BAMEZAI A, MCGREW J, BENACERRAF B (1989) The LY-6 locus: a multigene family encoding phosphatidylinositol-anchored membrane proteins concerned with T-cell activation. Immunol. Rev. 111, 195.
64. ROSEN PP, GROSHEN S, SAIGO PE, KINNE DW, HELLMAN S (1989) Pathological prognostic factors in stage I (T1N0M0) and stage II (T1N1M0): breast carcinoma: a study of 644 patients with median follow-up of 18 years. J. Clin. Oncol. 7, 1239.
65. ROSNER A, MIYOSHI K, LANDESMAN-BOLLAG E, XU X, SELDIN DC, MOSER AR, MACLEOD CL, SHYAMALA G, GILLGRASS AE, CARDIFF RD (2002) Pathway pathology: histological differences between ErbB/Ras and Wnt pathway transgenic mammary tumors. Am. J. Pathol. 161, 1087.
66. RUSSO IH, RUSSO J (1978) Developmental stage of the rat mammary gland as determinant of its susceptibility to 7,12-dimethylbenz[a]anthracene. J. Natl Cancer Inst. 61, 1439.
67. +c-kit-cells: correlation between long-term culture-initiating cells and telomerase expression. Leukemia 12, 728.
68. SAKAKIBARA S, IMAI T, HAMAGUCHI K, OKABE M, ARUGA J, NAKAJIMA K, YASUTOMI D, NAGATA T, KURIHARA Y, UESUGI S, MIYATA T, OGAWA M, MIKOSHIBA K, OKANO H (1996) Mouse Musashi-1, a neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev. Biol. 176, 230.
69. SAKAKIBARA S, OKANO H (1997) Expression of neural RNA-binding proteins in the postnatal CNS: implications of their roles in neuronal and glial cell development. J. Neurosci. 17, 8300.
70. SEAGROVES TN, LYDON JP, HOVEY RC, VONDERHAAR BK, ROSEN JM (2000) C/EBPbeta (CCAAT/enhancer binding protein) controls cell fate determination during mammary gland development. Mol. Endocrinol. 14, 359.
71. SELL S, PIERCE GB (1994) Maturation arrest of stem cell differentiation is a common pathway for the cellular origin of teratocarcinomas and epithelial cancers. Lab. Invest. 70, 6.
72. SHILLINGFORD JM, MIYOSHI K, FLAGELLA M, SHULL GE, HENNIGHAUSEN L (2002a) Mouse Mammary epithelial cells express the NaKCl cotransporter, NKCCl. Characterization, localization, and involvement in ductal development and morphogenesis. Mol. Endocrinol. 16, 1309.
73. SHILLINGFORD JM, MIYOSHI K, ROBINSON GW, GRIMM SL, ROSEN JM, NEUBAUER H, PFEFFER K, HENNIGHAUSEN L (2002b) Jak2 is an essential tyrosine kinase involved in pregnancy-mediated development of mammary secretory epithelium. Mol. Endocrinol. 16, 563.
74. SMALLEY MJ, TITLEY J, PATERSON H, PERUSINGHE N, CLARKE C, O'HARE MJ (1999) Differentiation of separated mouse mammary luminal epithelial and myoepithelial cells cultured on EHS matrix analyzed by indirect immunofluorescence of cytoskeletal antigens. J. Histochem. Cytochem. 47, 1513.
75. 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 Res. Treat. 39, 21.
76. SMITH GH, CHEPKO G (2001) Mammary epithelial stem cells. Microsc. Res. Techn. 52, 190.
77. SMITH GH, MEDINA D (1988) A morphologically distinct candidate for an epithelial stem cell in mouse mammary gland. J. Cell Sci. 90, 173.
78. SMITH GH, MEHREL T, ROOP DR (1990) Differential keratin gene expression in developing, differentiating, preneoplastic, and neoplastic mouse mammary epithelium. Cell Growth Differ. 1, 161.
79. SONNENBERG A, DAAMS H, VAN DER VALK MA, HILKENS J, HILGERS J (1986) Development of mouse mammary gland: identification of stages in differentiation of luminal and myoepithelial cells using monoclonal antibodies and polyvalent antiserum against keratin. J. Histochem. Cytochem. 34, 1037.
80. SOYAL S, ISMAIL PM, LI J, MULAC-JERICEVIC B, CONNEELY OM, LYDON JP (2002) Progesterone receptors - animal models and cell signaling in breast cancer: Progesterone's role in mammary gland development and tumorigenesis as disclosed by experimental mouse genetics. Breast Cancer Res. 4, 191.
81. STINGL JEC, EMERMAN JT (2000) Characterization of Normal Human Breast Epithelial Cell Subpopulations Isolated by Fluorescence Activated Cell Sorting and Their Clonogenic Growth in vitro. New York: Kluwer Academic/Plenum Publishers.
82. TAIPALE J, BEACHY PA (2001) The Hedgehog and Wnt signalling pathways in cancer. Nature 411, 349.
83. TAYLOR G, LEHRER MS, JENSEN PJ, SUN TT, LAVKER RM (2000) Involvement of follicular stem cells in forming not only the follicle but also the epidermis. Cell 102, 451.
84. TSAI YC, LU Y, NICHOLS PW, ZLOTNIKOV G, JONES PA, SMITH HS (1996) Contiguous patches of normal human mammary epithelium derived from a single stem cell: implications for breast carcinogenesis. Cancer Res. 56, 402.
85. TULINA N, MATUNIS E (2001) Control of stem cell self-renewal in Drosophila spermatogenesis by JAK-STAT signaling. Science 294, 2546.
86. VARNUM-FINNEY B, XU L, BRASHEM-STEIN C, NOURIGAT C, FLOWERS D, BAKKOUR S, PEAR WS, BERNSTEIN ID (2000) Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat. Med. 6, 1278.
87. VORMOOR J, LAPIDOT T, PFLUMIO F, RISDON G, PATTERSON B, BROXMEYER HE, DICK JE (1994) Immature human cord blood progenitors engraft and proliferate to high levels in severe combined immunodeficient mice. Blood 83, 2489.
88. 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, 1377.
89. 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. Dev. Biol. 245, 42.
90. YANG A, SCHWEITZER R, SUN D, KAGHAD M, WALKER N, BRONSON RT, TABIN C, SHARPE A, CAPUT D, CRUM C, MCKEON F (1999) p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development. Nature 398, 714.
91. ZEPS N, BENTEL JM, PAPADIMITRIOU JM, D'ANTUONO MF, DAWKINS HJ (1998) Estrogen receptor-negative epithelial cells in mouse mammary gland development and growth. Differentiation 62, 221.
92. ZHANG Y, KALDERON D (2001) Hedgehog acts as a somatic stem cell factor in the Drosophila ovary. Nature 410, 599.
93. ZHOU S, SCHUETZ JD, BUNTING KD, COLAPIETRO AM, SAMPATH J, MORRIS JJ, LAGUTINA I, GROSVELD GC, OSAWA M, NAKAUCHI H, SORRENTINO BP (2001) 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. 7, 1028.
94. ZHU AJ, WATT FM (1999) Beta-catenin signalling modulates proliferative potential of human epidermal keratinocytes independently of intercellular adhesion. Development 126, 2285.