Side population cells in developing human liver are primarily haematopoietic progenitor cells

Experimental Cell Research

Volumn 315, Issue 13, 2009, Pages 2141-2153

  Terrace, John D ^a   Hay, David C ^a   Samuel, Kay ^a   Payne, Catherine ^a   Anderson, Richard A ^a   Currie, Ian S ^a   Parks, Rowan W ^a   Forbes, Stuart J ^a   Ross, James A ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Development; Human; Liver; Progenitor; Side population

Indexed keywords

CD34 ANTIGEN; FIBRONECTIN; INTEGRIN;

ARTICLE; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CONTROLLED STUDY; EPITHELIUM CELL; FETUS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LIVER DEVELOPMENT; LIVER REGENERATION; PHENOTYPE; PRENATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIDE POPULATION CELL;

EID: 67349263504     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.02.004     Document Type: Article

References (55)

1. Goodell M.A., Brose K., Paradis G., Conner A.S., and Mulligan R.C. Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp.Med. 183 (1996) 1797-1806
2. Goodell M.A., Rosenzweig M., Kim H., Marks D.F., DeMaria M., Paradis G., Grupp S.A., Sieff C.A., Mulligan R.C., and Johnson R.P. Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat.Med. 3 (1997) 1337-1345
3. Goodell M.A., McKinney-Freeman S., and Camargo F.D. Isolation and characterization of side population cells. Methods Mol.Biol. 290 (2005) 343-352
4. Alison M.R. Tissue-based stem cells: ABC transporter proteins take centre stage. J. Pathol. 200 (2003) 547-550
5. Challen G.A., and Ln-Rle M.H. A side order of stem cells: the SP phenotype. Stem Cells 24 (2006) 3-12
6. Nadin B.M., Goodell M.A., and Hirschi K.K. Phenotype and hematopoietic potential of side population cells throughout embryonic development. Blood 102 (2003) 2436-2443
7. Preffer F.I., Dombkowski D., Sykes M., Scadden D., and Yang Y.G. Lineage-negative side-population (SP) cells with restricted hematopoietic capacity circulate in normal human adult blood: immunophenotypic and functional characterization. Stem Cells 20 (2002) 417-427
8. Telford W.G., and Frolova E.G. Discrimination of the Hoechst side population in mouse bone marrow with violet and near-ultraviolet laser diodes. Cytometry Part A 57A (2004) 45-52
9. Telford W.G., Bradford J., Godfrey W., Robey R.W., and Bates S.E. Side population analysis using a violet-excited cell-permeable DNA binding dye. Stem Cells 25 (2007) 1029-1036
10. Uchida N., Dykstra B., Lyons K., Leung F., Kristiansen M., and Eaves C. ABC transporter activities of murine hematopoietic stem cells vary according to their developmental and activation status. Blood 103 (2004) 4487-4495
11. Bunting K.D., Zhou S., Lu T.H., and Sorrentino B.P. Enforced P-glycoprotein pump function in murine bone marrow cells results in expansion of side population stem cells in vitro and repopulating cells in vivo. Blood 96 (2000) 902-909
12. Bunting K.D. ABC transporters as phenotypic markers and functional regulators of stem cells. Stem Cells 20 (2002) 11-20
13. Doyle L.A., and Ross D.D. Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene 22 (2003) 7340-7358
14. Kim M., Turnquist H., Jackson J., Sgagias M., Yan Y., Gong M., Dean M., Sharp J.G., and Cowan K. The multidrug resistance transporter ABCG2 (breast cancer resistance protein 1) effluxes Hoechst 33342 and is overexpressed in hematopoietic stem cells. Clin. Cancer Res. 8 (2002) 22-28
15. Ueda T., Brenner S., Malech H.L., Langemeijer S.M., Perl S., Kirby M., Phang O.A., Krouse A.E., Donahue R.E., Kang E.M., and Tisdale J.F. Cloning and functional analysis of the rhesus macaque ABCG2 gene - forced expression confers an SP phenotype among hematopoietic stem cell progeny in vivo. J. Biol. Chem. 280 (2005) 991-998
16. Zhou S., Schuetz J.D., Bunting K.D., Colapietro A.M., Sampath J., Morris J.J., Lagutina I., Grosveld G.C., Osawa M., Nakauchi H., and Sorrentino B.P. 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 (2001) 1028-1034
17. Zhou S., Morris J.J., Barnes Y.X., Lan L., Schuetz J.D., and Sorrentino B.P. 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. 99 (2002) 12339-12344
18. Gussoni E., Soneoka Y., Strickland C.D., Buzney E.A., Khan M.K., Flint A.F., Kunkel L.M., and Mulligan R.C. Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401 (1999) 390-394
19. Hoshi N., Kusakabe T., Taylor B.J., and Kimura S. Side population cells in the mouse thyroid exhibit stem/progenitor cell-like characteristics. Endocrinology 148 (2007) 4251-4258
20. Iwatani H., Ito T., Imai E., Matsuzaki Y., Suzuki A., Yamato M., Okabe N., and Hori N. Hematopoietic and nonhematopoietic potentials of Hoechst(low)/side population cells isolated from adult rat kidney. Kidney Int. 65 (2004) 1604-1614
21. Kubota H., Avarbock M.R., and Brinster R.L. Spermatogonial stem cells share some, but not all, phenotypic and functional characteristics with other stem cells. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 6487-6492
22. Montanaro F., Liadaki K., Volinski J., Flint A., and Kunkel L.M. Skeletal muscle engraftment potential of adult mouse skin side population cells. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 9336-9341
23. Murayama A., Matsuzaki Y., Kawaguchi A., Shimazaki T., and Okano H. Flow cytometric analysis of neural stem cells in the developing and adult mouse brain. J. Neurosci. Res. 69 (2002) 837-847
24. Summer R., Kotton D.N., Sun X., Ma B., Fitzsimmons K., and Fine A. Side population cells and Bcrp1 expression in lung. Am. J. Physiol.,Lung Cell. Mol. Physiol. 285 (2003) L97-L104
25. Oh H., Chi X., Bradfute S.B., Mishina Y., Pocius J., Michael L.H., Behringer R.R., Schwartz R.J., Entman M.L., and Schneider M.D. Cardiac muscle plasticity in adult and embryo by heart-derived progenitor cells. Cardiac Engineering: from Genes and Cells to Structure and Function 1015 (2004) 182-189
26. Tsuchiya A., Heike T., Baba S., Fujino H., Umeda K., Matsuda Y., Nomoto M., Ichida T., Aoyagi Y., and Nakahata T. Long-term culture of postnatal mouse hepatic stem/progenitor cells and their relative developmental hierarchy. Stem Cells 25 (2007) 895-902
27. Gajkowska A., Oldak T., Jastrzewska M., Machaj E.K., Walewski J., Kraszewska E., and Pojda Z. Flow cytometric enumeration of CD34(+) hematopoietic stem and progenitor cells in leukapheresis product and bone marrow for clinical transplantation: a comparison of three methods. Folia Histochem. Cytobiol. 44 (2006) 53-60
28. Bird T.G., Lorenzini S., and Forbes S.J. Activation of stem cells in hepatic diseases. Cell Tissue Res. 331 (2008) 283-300
29. Petersen B.E., Zajac V.F., and Michalopoulos G.K. Bile ductular damage induced by methylene dianiline inhibits oval cell activation. Am. J. Pathol. 151 (1997) 905-909
30. Petersen B.E., Zajac V.F., and Michalopoulos G.K. Hepatic oval cell activation in response to injury following chemically induced periportal or pericentral damage in rats. Hepatology 27 (1998) 1030-1038
31. Sell S. Comparison of liver progenitor cells in human atypical ductular reactions with those seen in experimental models of liver injury. Hepatology 27 (1998) 317-331
32. Roskams T., De Vos R., Van Eyken P., Myazaki H., Van Damme B., and Desmet V. Hepatic OV-6 expression in human liver disease and rat experiments: evidence for hepatic progenitor cells in man. J. Hepatol. 29 (1998) 455-463
33. Petersen B.E., Goff J.P., Greenberger J.S., and Michalopoulos G.K. Hepatic oval cells express the hematopoietic stem cell marker Thy-1 in the rat. Hepatology 27 (1998) 433-445
34. Petersen B.E., Grossbard B., Hatch H., Pi L.Y., Deng J., and Scott E.W. Mouse A6-positive hepatic oval cells also express several hematopoietic stem cell markers. Hepatology 37 (2003) 632-640
35. Theise N.D., Saxena R., Portmann B.C., Thung S.N., Yee H., Chiriboga L., Kumar A., and Crawford J.M. The canals of Hering and hepatic stem cells in humans. Hepatology 30 (1999) 1425-1433
36. Zaret K.S. Hepatocyte differentiation: from the endoderm and beyond. Curr. Opin. Genet. Dev. 11 (2001) 568-574
37. Haruna Y., Saito K., Spaulding S., Nalesnik M.A., and Gerber M.A. Identification of bipotential progenitor cells in human liver development. Hepatology 23 (1996) 476-481
38. Van Eyken P., Sciot R., Callea F., van der S.K., Moerman P., and Desmet V.J. The development of the intrahepatic bile ducts in man: a keratin-immunohistochemical study. Hepatology 8 (1988) 1586-1595
39. Tavian M., and Peault B. Embryonic development of the human hematopoietic system. Int. J. Dev. Biol. 49 (2005) 243-250
40. Terrace J.D., Currie I.S., Hay D.C., Masson N.M., Anderson R.A., Forbes S.J., Parks R.W., and Ross J.A. Progenitor cell characterization and location in the developing human liver. Stem Cells Dev. 16 (2007) 771-778
41. Wulf G.G., Luo K.L., Jackson K.A., Brenner M.K., and Goodell M.A. Cells of the hepatic side population contribute to liver regeneration and can be replenished by bone marrow stem cells. Haematologica 88 (2003) 368-378
42. Uchida N., Fujisaki T., Eaves A.C., and Eaves C.J. Transplantable hematopoietic stem cells in human fetal liver have a CD34(+) side population (SP) phenotype. J. Clin. Invest. 108 (2001) 1071-1077
43. Kotton D.N., Fabian A.J., and Mulligan R.C. A novel stem-cell population in adult liver with potent hematopoietic-reconstitution activity. Blood 106 (2005) 1574-1580
44. Tsamandas A.C., Jain A.B., Raikow R.B., Demetris A.J., Nalesnik M.A., and Randhawa P.S. Extramedullary hematopoiesis in the allograft liver. Mod. Path. 8 (1995) 671-674
45. Omori M., Omori N., Evarts R.P., Teramoto T., and Thorgeirsson S.S. Coexpression of flt-3 ligand flt-3 and SCF/c-kit signal transduction systems in bile-duct-ligated sl and w mice. Am. J. Pathol. 150 (1997) 1179-1187
46. Theise N.D., Nimmakayalu M., Gardner R., Illei P.B., Morgan G., Teperman L., Henegariu O., and Kruse D.S. Liver from bone marrow in humans. Hepatology 32 (2000) 11-16
47. Alison M.R., Poulsom R., Jeffery R., Dhillon A.P., Quaglia A., Jacob J., Novelli M., Prentice G., Williamson J., and Wright N.A. Cell differentiation - hepatocytes from nonhepatic adult stem cells. Nature 406 (2000) 257
48. Hussain S.Z., Strom S.C., Kirby M.R., Burns S., Langemeijer S., Ueda T., Hsieh M., and Tisdale J.F. Side population cells derived from adult human liver generate hepatocyte-like cells in vitro. Dig. Dis. Sci. 50 (2005) 1755-1763
49. Shimano K., Satake M., Okaya A., Kitanaka J., Kitanaka N., Takemura M., Sakagami M., Terada N., and Tsujimura T. Hepatic oval cells have the side population phenotype defined by expression of ATP-binding cassette transporter ABCG2/BCRP1. Am. J. Path. 163 (2003) 3-9
50. Suzuki A., Zheng Y., Kondo R., Kusakabe M., Takada Y., Fukao K., Nakauchi H., and Taniguchi H. Flow-cytometric separation and enrichment of hepatic progenitor cells in the developing mouse liver. Hepatology 32 (2000) 1230-1239
51. Suzuki A., Zheng Y.W., Kaneko S., Onodera M., Fukao K., Nakauchi H., and Taniguchi H. Clonal identification and characterization of self-renewing pluripotent stem cells in the developing liver. J. Cell Biol. 156 (2002) 173-184
52. Potocnik A.J., Brakebusch C., and Fassler R. Fetal and adult hematopoietic stem cells require beta1 integrin function for colonizing fetal liver, spleen, and bone marrow. Immunity 12 (2000) 653-663
53. ffrench-Constant C., and Hynes R.O. Alternative splicing of fibronectin is temporally and spatially regulated in the chicken embryo. Development 106 (1989) 375-388
54. ffrench-Constant C. Alternative splicing of fibronectin-many different proteins but few different functions. Exp.Cell Res. 221 (1995) 261-271
55. Hay D.C., Zhao D., Fletcher J., Hewitt Z.A., McLean D., Urruticoechea-Uriguen A., Black J.R., Elcombe C., Ross J.A., Wolf R., and Cui W. Efficient differentiation of hepatocytes from human embryonic stem cells exhibiting markers recapitulating liver development in vivo. Stem Cells 26 (2008) 894-902