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Characterization and Classification of Stem Cells

  • Ute Bissels
  • Dominik Eckardt
  • Andreas BosioEmail author
Chapter

Abstract

Starting from a zygote, an organism is made up of thousands, highly organised stem cells, progenitor cells and postmitotic cells which are generated in spatio-temporally coordinated proliferation and differentiation steps. The ongoing advancements in cell culture, isolation techniques, and molecular analyses have driven our basic understanding of different cell types and led to a broad classification of stem cells. This chapter outlines the most prominent techniques used for the characterization and classification of stem cells and provides an overview of many different stem cells, their function and their mRNA, miRNA and protein content.

Keywords

Stem Cell Cancer Stem Cell Neural Stem Cell Pluripotent Stem Cell Spermatogonial Stem Cell 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

ESC

embryonic stem cell

iPSC

induced pluripotent stem cell

HSC

hematopoietic stem cell

TSC

tissue stem cell

CSC

cancer stem cell

EPC

endothelial progenitor cell

SPC

spermtogonial progenitor cell

HpSC

hepatic stem cell

NSC

neural stem cell

BTSC

brain tumor stem cell

MSC

mesenchymal stem cell

LT-HSC

long-term hematopoietic stem cell

ST-HSC

short-term hematopoietic stem cell

MP

multipotent progenitors

CMP

common myeloid progenitor

CLP

common lymphoid progenitor

MEP

megakaryocyte-erythroid progenitor

GMP

granulocyte-macrophage progenitor

ErP

erythroid progenitor

MkP

megakaryocyte progenitor

RBC

red blood cells

NK

natural killer

References

  1. Adewumi O, Aflatoonian B, Ahrlund-Richter L et al (2007) Characterization of human embryonic stem cell lines by the International Stem Cell Initiative. Nat Biotechnol 25:803–816PubMedCrossRefGoogle Scholar
  2. Al-Hajj M, Wicha MS, Benito-Hernandez A et al (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 100:3983–3988PubMedCrossRefGoogle Scholar
  3. Anokye-Danso F, Trivedi CM, Juhr D et al (2011) Highly efficient miRNA-mediated reprogramming of mouse and human somatic cells to pluripotency. Cell Stem Cell 8:376–388PubMedCrossRefGoogle Scholar
  4. Aravin A, Tuschl T (2005) Identification and characterization of small RNAs involved in RNA silencing. FEBS Lett 579:5830–5840PubMedCrossRefGoogle Scholar
  5. Arnold CP, Tan R, Zhou B et al (2011) MicroRNA programs in normal and aberrant stem and progenitor cells. Genome Res 21:798–810PubMedCrossRefGoogle Scholar
  6. Asahara T, Kawamoto A, Masuda H (2011) Concise review: circulating endothelial progenitor cells for vascular medicine. Stem Cells 29:1650–1655PubMedCrossRefGoogle Scholar
  7. Aslan H, Zilberman Y, Kandel L et al (2006) Osteogenic differentiation of noncultured immunoisolated bone marrow-derived CD105+ cells. Stem Cells 24:1728–1737PubMedCrossRefGoogle Scholar
  8. Asselin-Labat ML, Shackleton M, Stingl J et al (2006) Steroid hormone receptor status of mouse mammary stem cells. J Natl Cancer Inst 98:1011–1014PubMedCrossRefGoogle Scholar
  9. Baldus CD, Tanner SM, Kusewitt DF et al (2003) BAALC, a novel marker of human hematopoietic progenitor cells. Exp Hematol 31:1051–1056PubMedGoogle Scholar
  10. Bao S, Wu Q, McLendon RE et al (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756–760PubMedCrossRefGoogle Scholar
  11. Bearzi C, Rota M, Hosoda T et al (2007) Human cardiac stem cells. Proc Natl Acad Sci USA 104:14068–14073PubMedCrossRefGoogle Scholar
  12. Beckervordersandforth R, Tripathi P, Ninkovic J et al (2011) In vivo fate mapping and expression analysis reveals molecular hallmarks of prospectively isolated adult neural stem cells. Cell Stem Cell 7:744–758CrossRefGoogle Scholar
  13. Beltrami AP, Barlucchi L, Torella D et al (2003) Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell 114:763–776PubMedCrossRefGoogle Scholar
  14. Bissels U, Wild S, Tomiuk S et al (2009) Absolute quantification of microRNAs by using a universal reference. RNA 15:2375–2384PubMedCrossRefGoogle Scholar
  15. Bissels U, Bosio A, Wagner W (2011a) MicroRNAs are shaping the hematopoietic landscape. Haematologica 97(2):160–167PubMedCrossRefGoogle Scholar
  16. Bissels U, Wild S, Tomiuk S et al (2011b) Combined characterization of microRNA and mRNA profiles delineates early differentiation pathways of CD133(+) and CD34(+) hematopoietic stem and progenitor cells. Stem Cells 29(5):847–857Google Scholar
  17. Bonnet D, Dick JE (1997) Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 3:730–737PubMedCrossRefGoogle Scholar
  18. Bosio A, Huppert V, Donath S et al (2009) Isolation and enrichment of stem cells. Adv Biochem Eng Biotechnol 114:23–72PubMedGoogle Scholar
  19. Boutin C, Hardt O, de Chevigny A et al (2010) NeuroD1 induces terminal neuronal differentiation in olfactory neurogenesis. Proc Natl Acad Sci USA 107:1201–1206PubMedCrossRefGoogle Scholar
  20. Bruchova H, Yoon D, Agarwal AM et al (2007) Regulated expression of microRNAs in normal and polycythemia vera erythropoiesis. Exp Hematol 35:1657–1667PubMedCrossRefGoogle Scholar
  21. Bu L, Jiang X, Martin-Puig S et al (2009) Human ISL1 heart progenitors generate diverse multipotent cardiovascular cell lineages. Nature 460:113–117PubMedCrossRefGoogle Scholar
  22. Buhring HJ, Seiffert M, Bock TA et al (1999) Expression of novel surface antigens on early hematopoietic cells. Ann N Y Acad Sci 872:25–38; discussion 38–29PubMedCrossRefGoogle Scholar
  23. Buhring HJ, Battula VL, Treml S et al (2007) Novel markers for the prospective isolation of human MSC. Ann N Y Acad Sci 1106:262–271PubMedCrossRefGoogle Scholar
  24. Burns CE, Zon LI (2002) Portrait of a stem cell. Dev Cell 3:612–613PubMedCrossRefGoogle Scholar
  25. Chen CZ, Li L, Lodish HF et al (2004) MicroRNAs modulate hematopoietic lineage differentiation. Science 303:83–86PubMedCrossRefGoogle Scholar
  26. Cheung ST, Cheung PF, Cheng CK et al (2011) Granulin-epithelin precursor and ATP-dependent binding cassette (ABC)B5 regulate liver cancer cell chemoresistance. Gastroenterology 140:344–355PubMedCrossRefGoogle Scholar
  27. Conrad S, Renninger M, Hennenlotter J et al (2008) Generation of pluripotent stem cells from adult human testis. Nature 456:344–349PubMedCrossRefGoogle Scholar
  28. Conti L, Cattaneo E (2010) Neural stem cell systems: physiological players or in vitro entities? Nature Rev 11:176–187Google Scholar
  29. Copland M, Hamilton A, Elrick LJ et al (2006) Dasatinib (BMS-354825) targets an earlier progenitor population than imatinib in primary CML but does not eliminate the quiescent fraction. Blood 107:4532–4539PubMedCrossRefGoogle Scholar
  30. Dalerba P, Dylla SJ, Park IK et al (2007) Phenotypic characterization of human colorectal cancer stem cells. Proc Natl Acad Sci USA 104:10158–10163PubMedCrossRefGoogle Scholar
  31. Dore LC, Amigo JD, Dos Santos CO et al (2008) A GATA-1-regulated microRNA locus essential for erythropoiesis. Proc Natl Acad Sci USA 105:3333–3338PubMedCrossRefGoogle Scholar
  32. Dormeyer W, van Hoof D, Braam SR et al (2008) Plasma membrane proteomics of human embryonic stem cells and human embryonal carcinoma cells. J Proteome Res 7:2936–2951PubMedCrossRefGoogle Scholar
  33. Du L, Wang H, He L et al (2008) CD44 is of functional importance for colorectal cancer stem cells. Clin Cancer Res 14:6751–6760PubMedCrossRefGoogle Scholar
  34. Felli N, Fontana L, Pelosi E et al (2005) MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor down-modulation. Proc Natl Acad Sci USA 102:18081–18086PubMedCrossRefGoogle Scholar
  35. Fontana L, Pelosi E, Greco P et al (2007) MicroRNAs 17-5p-20a-106a control monocytopoiesis through AML1 targeting and M-CSF receptor upregulation. Nat Cell Biol 9:775–787PubMedCrossRefGoogle Scholar
  36. Fortunel NO, Otu HH, Ng HH et al (2003) Comment on “ ‘Stemness’: transcriptional profiling of embryonic and adult stem cells” and “a stem cell molecular signature”. Science 302:393; author reply 393PubMedCrossRefGoogle Scholar
  37. Gangaraju VK, Lin H (2009) MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol 10:116–125PubMedCrossRefGoogle Scholar
  38. Georgantas RW 3rd, Tanadve V, Malehorn M et al (2004) Microarray and serial analysis of gene expression analyses identify known and novel transcripts overexpressed in hematopoietic stem cells. Cancer Res 64:4434–4441PubMedCrossRefGoogle Scholar
  39. Georgantas RW 3rd, Hildreth R, Morisot S et al (2007) CD34+ hematopoietic stem-progenitor cell microRNA expression and function: a circuit diagram of differentiation control. Proc Natl Acad Sci USA 104:2750–2755PubMedCrossRefGoogle Scholar
  40. Gerrits A, Dykstra B, Otten M et al (2008) Combining transcriptional profiling and genetic linkage analysis to uncover gene networks operating in hematopoietic stem cells and their progeny. Immunogenetics 60:411–422PubMedCrossRefGoogle Scholar
  41. Giebel B, Zhang T, Beckmann J et al (2006) Primitive human hematopoietic cells give rise to differentially specified daughter cells upon their initial cell division. Blood 107:2146–2152PubMedCrossRefGoogle Scholar
  42. Goodell MA, Brose K, Paradis G et al (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183:1797–1806PubMedCrossRefGoogle Scholar
  43. Gudmundsson KO, Thorsteinsson L, Sigurjonsson OE et al (2007) Gene expression analysis of hematopoietic progenitor cells identifies Dlg7 as a potential stem cell gene. Stem Cells 25:1498–1506PubMedCrossRefGoogle Scholar
  44. Guo S, Lu J, Schlanger R et al (2010) MicroRNA miR-125a controls hematopoietic stem cell number. Proc Natl Acad Sci USA 107:14229–14234PubMedCrossRefGoogle Scholar
  45. Han YC, Park CY, Bhagat G et al (2010) microRNA-29a induces aberrant self-renewal capacity in hematopoietic progenitors, biased myeloid development, and acute myeloid leukemia. J Exp Med 207:475–489PubMedCrossRefGoogle Scholar
  46. Hatfield S, Ruohola-Baker H (2008) microRNA and stem cell function. Cell Tissue Res 331:57–66PubMedCrossRefGoogle Scholar
  47. He X, Gonzalez V, Tsang A et al (2005) Differential gene expression profiling of CD34+ CD133+ umbilical cord blood hematopoietic stem progenitor cells. Stem Cells Dev 14:188–198PubMedCrossRefGoogle Scholar
  48. Hemmoranta H, Hautaniemi S, Niemi J et al (2006) Transcriptional profiling reflects shared and unique characters for CD34+ and CD133+ cells. Stem Cells Dev 15:839–851PubMedCrossRefGoogle Scholar
  49. Huang TS, Hsieh JY, Wu YH et al (2008) Functional network reconstruction reveals somatic stemness genetic maps and dedifferentiation-like transcriptome reprogramming induced by GATA2. Stem Cells 26:1186–1201PubMedCrossRefGoogle Scholar
  50. Hubin F, Humblet C, Belaid Z et al (2005) Murine bone marrow stromal cells sustain in vivo the survival of hematopoietic stem cells and the granulopoietic differentiation of more mature progenitors. Stem Cells 23:1626–1633PubMedCrossRefGoogle Scholar
  51. Huss R, Moosmann S (2002) The co-expression of CD117 (c-kit) and osteocalcin in activated bone marrow stem cells in different diseases. Br J Haematol 118:305–312PubMedCrossRefGoogle Scholar
  52. Iozzo RV (1998) Matrix proteoglycans: from molecular design to cellular function. Annu Rev Biochem 67:609–652PubMedCrossRefGoogle Scholar
  53. Ivanova NB, Dimos JT, Schaniel C et al (2002) A stem cell molecular signature. Science 298:601–604PubMedCrossRefGoogle Scholar
  54. Jaatinen T, Hemmoranta H, Hautaniemi S et al (2006) Global gene expression profile of human cord blood-derived CD133+ cells. Stem Cells 24:631–641PubMedCrossRefGoogle Scholar
  55. Jin P, Wang E, Ren J et al (2008) Differentiation of two types of mobilized peripheral blood stem cells by microRNA and cDNA expression analysis. J Transl Med 6:39PubMedCrossRefGoogle Scholar
  56. Jones R, Barber J, Vala M (1995) Assessment of aldehyde dehydrogenase in viable cells. Blood 85:2742–2746PubMedGoogle Scholar
  57. Jones EA, Kinsey SE, English A et al (2002) Isolation and characterization of bone marrow multipotential mesenchymal progenitor cells. Arthritis Rheum 46:3349–3360PubMedCrossRefGoogle Scholar
  58. Jungblut M, Oeltze K, Zehnter I et al (2008) Preparation of single-cell suspensions from mouse spleen with the gentleMACS Dissociator. J Vis Exp 2008 Dec 11, 22(2):1029. doi: 10.3791/1029 Google Scholar
  59. Jungblut M, Oeltze K, Zehnter I et al (2009) Standardized preparation of single-cell suspensions from mouse lung tissue using the gentleMACS Dissociator. J Vis Exp 29:e1266Google Scholar
  60. Kanatsu-Shinohara M, Takashima S, Ishii K et al (2011) Dynamic changes in EPCAM expression during spermatogonial stem cell differentiation in the mouse testis. PLoS One 6:e23663PubMedCrossRefGoogle Scholar
  61. Kiel MJ, Yilmaz OH, Iwashita T et al (2005) SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell 121:1109–1121PubMedCrossRefGoogle Scholar
  62. Kubota H, Avarbock MR, Brinster RL (2004) Growth factors essential for self-renewal and expansion of mouse spermatogonial stem cells. Proc Natl Acad Sci USA 101:16489–16494PubMedCrossRefGoogle Scholar
  63. Landgraf P, Rusu M, Sheridan R et al (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129:1401–1414PubMedCrossRefGoogle Scholar
  64. Li C, Heidt DG, Dalerba P et al (2007) Identification of pancreatic cancer stem cells. Cancer Res 67:1030–1037PubMedCrossRefGoogle Scholar
  65. Liao R, Sun J, Zhang L et al (2008) MicroRNAs play a role in the development of human hematopoietic stem cells. J Cell Biochem 104:805–817PubMedCrossRefGoogle Scholar
  66. Lu J, Guo S, Ebert BL et al (2008) MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Dev Cell 14:843–853PubMedCrossRefGoogle Scholar
  67. Majumdar MK, Keane-Moore M, Buyaner D et al (2003) Characterization and functionality of cell surface molecules on human mesenchymal stem cells. J Biomed Sci 10:228–241PubMedCrossRefGoogle Scholar
  68. Mallanna SK, Rizzino A (2010) Emerging roles of microRNAs in the control of embryonic stem cells and the generation of induced pluripotent stem cells. Dev Biol 344:16–25PubMedCrossRefGoogle Scholar
  69. Merkerova M, Vasikova A, Belickova M et al (2009) MicroRNA expression profiles in umbilical cord blood cell lineages. Stem Cells Dev 19(1):17–26CrossRefGoogle Scholar
  70. Merkle FT, Alvarez-Buylla A (2006) Neural stem cells in mammalian development. Curr Opin Cell Biol 18:704–709PubMedCrossRefGoogle Scholar
  71. Miyoshi N, Ishii H, Nagano H et al (2011) Reprogramming of mouse and human cells to pluripotency using mature microRNAs. Cell Stem Cell 8:633–638PubMedCrossRefGoogle Scholar
  72. Mori T, Buffo A, Gotz M (2005) The novel roles of glial cells revisited: the contribution of radial glia and astrocytes to neurogenesis. Curr Top Dev Biol 69:67–99PubMedCrossRefGoogle Scholar
  73. Ng YY, van Kessel B, Lokhorst HM et al (2004) Gene-expression profiling of CD34+ cells from various hematopoietic stem-cell sources reveals functional differences in stem-cell activity. J Leukoc Biol 75:314–323PubMedCrossRefGoogle Scholar
  74. Niehage C, Steenblock C, Pursche T et al (2011) The cell surface proteome of human mesenchymal stromal cells. PLoS One 6:e20399PubMedCrossRefGoogle Scholar
  75. Nijnik A, Woodbine L, Marchetti C et al (2007) DNA repair is limiting for haematopoietic stem cells during ageing. Nature 447:686–690PubMedCrossRefGoogle Scholar
  76. Novershtern N, Subramanian A, Lawton LN et al (2011) Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell 144:296–309PubMedCrossRefGoogle Scholar
  77. Nunomura K, Nagano K, Itagaki C et al (2005) Cell surface labeling and mass spectrometry reveal diversity of cell surface markers and signaling molecules expressed in undifferentiated mouse embryonic stem cells. Mol Cell Proteomics 4:1968–1976PubMedCrossRefGoogle Scholar
  78. O’Brien CA, Pollett A, Gallinger S et al (2007) A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445:106–110PubMedCrossRefGoogle Scholar
  79. O’Connell RM, Chaudhuri AA, Rao DS et al (2010) MicroRNAs enriched in hematopoietic stem cells differentially regulate long-term hematopoietic output. Proc Natl Acad Sci USA 107:14235–14240PubMedCrossRefGoogle Scholar
  80. Ogawa M (2002) Changing phenotypes of hematopoietic stem cells. Exp Hematol 30:3–6PubMedCrossRefGoogle Scholar
  81. Oh H, Bradfute SB, Gallardo TD et al (2003) Cardiac progenitor cells from adult myocardium: homing, differentiation, and fusion after infarction. Proc Natl Acad Sci USA 100:12313–12318PubMedCrossRefGoogle Scholar
  82. Ooi AG, Sahoo D, Adorno M et al (2010) MicroRNA-125b expands hematopoietic stem cells and enriches for the lymphoid-balanced and lymphoid-biased subsets. Proc Natl Acad Sci USA 107:21505–21510PubMedCrossRefGoogle Scholar
  83. Orkin SH, Zon LI (2008) Hematopoiesis: an evolving paradigm for stem cell biology. Cell 132:631–644PubMedCrossRefGoogle Scholar
  84. Pang R, Law WL, Chu AC et al (2010) A subpopulation of CD26+ cancer stem cells with metastatic capacity in human colorectal cancer. Cell Stem Cell 6:603–615PubMedCrossRefGoogle Scholar
  85. Pastrana E, Cheng LC, Doetsch F (2009) Simultaneous prospective purification of adult subventricular zone neural stem cells and their progeny. Proc Natl Acad Sci USA 106:6387–6392PubMedGoogle Scholar
  86. Pennartz S, Belvindrah R, Tomiuk S et al (2004) Purification of neuronal precursors from the adult mouse brain: comprehensive gene expression analysis provides new insights into the control of cell migration, differentiation, and homeostasis. Mol Cell Neurosci 25:692–706PubMedCrossRefGoogle Scholar
  87. Pennartz S, Reiss S, Biloune R et al (2009) Generation of single-cell suspensions from mouse neural tissue. J Vis Exp 2009 Jul 7, 29(2):1267. doi: 10.3791/1267 Google Scholar
  88. Petriv OI, Kuchenbauer F, Delaney AD et al (2010) Comprehensive microRNA expression profiling of the hematopoietic hierarchy. Proc Natl Acad Sci USA 107:15443–15448PubMedCrossRefGoogle Scholar
  89. Pfister O, Mouquet F, Jain M et al (2005) CD31- but Not CD31+ cardiac side population cells exhibit functional cardiomyogenic differentiation. Circ Res 97:52–61PubMedCrossRefGoogle Scholar
  90. Piccirillo SG, Vescovi AL (2006) Bone morphogenetic proteins regulate tumorigenicity in human glioblastoma stem cells. Ernst Schering Found Symp Proc 5:59–81PubMedGoogle Scholar
  91. Pontier SM, Muller WJ (2009) Integrins in mammary-stem-cell biology and breast-cancer progression–a role in cancer stem cells? J Cell Sci 122:207–214PubMedCrossRefGoogle Scholar
  92. Quirici N, Soligo D, Bossolasco P et al (2002) Isolation of bone marrow mesenchymal stem cells by anti-nerve growth factor receptor antibodies. Exp Hematol 30:783–791PubMedCrossRefGoogle Scholar
  93. Rafii S, Lyden D (2003) Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 9:702–712PubMedCrossRefGoogle Scholar
  94. Ramalho-Santos M, Yoon S, Matsuzaki Y et al (2002) “Stemness”: transcriptional profiling of embryonic and adult stem cells. Science 298:597–600PubMedCrossRefGoogle Scholar
  95. Ricci-Vitiani L, Lombardi DG, Pilozzi E et al (2007) Identification and expansion of human colon-cancer-initiating cells. Nature 445:111–115PubMedCrossRefGoogle Scholar
  96. Rossi DJ, Bryder D, Zahn JM et al (2005) Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci USA 102:9194–9199PubMedCrossRefGoogle Scholar
  97. Schiedlmeier B, Santos AC, Ribeiro A et al (2007) HOXB4’s road map to stem cell expansion. Proc Natl Acad Sci USA 104:16952–16957PubMedCrossRefGoogle Scholar
  98. Schmelzer E, Reid LM (2008) EpCAM expression in normal, non-pathological tissues. Front Biosci 13:3096–3100PubMedCrossRefGoogle Scholar
  99. Schmelzer E, Zhang L, Bruce A et al (2007) Human hepatic stem cells from fetal and postnatal donors. J Exp Med 204:1973–1987PubMedCrossRefGoogle Scholar
  100. Seandel M, James D, Shmelkov SV et al (2007) Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 449:346–350PubMedCrossRefGoogle Scholar
  101. Seidenfaden R, Desoeuvre A, Bosio A et al (2006) Glial conversion of SVZ-derived committed neuronal precursors after ectopic grafting into the adult brain. Mol Cell Neurosci 32:187–198PubMedCrossRefGoogle Scholar
  102. Shackleton M, Vaillant F, Simpson KJ et al (2006) Generation of a functional mammary gland from a single stem cell. Nature 439:84–88PubMedCrossRefGoogle Scholar
  103. Shi S, Gronthos S (2003) Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18:696–704PubMedCrossRefGoogle Scholar
  104. Shimono Y, Zabala M, Cho RW et al (2009) Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells. Cell 138:592–603PubMedCrossRefGoogle Scholar
  105. Singh SK, Clarke ID, Terasaki M et al (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:5821–5828PubMedGoogle Scholar
  106. Singh SK, Clarke ID, Hide T et al (2004a) Cancer stem cells in nervous system tumors. Oncogene 23:7267–7273PubMedCrossRefGoogle Scholar
  107. Singh SK, Hawkins C, Clarke ID et al (2004b) Identification of human brain tumour initiating cells. Nature 432:396–401PubMedCrossRefGoogle Scholar
  108. Smith RR, Barile L, Cho HC, Leppo MK, Hare JM, Messina E, Giacomello A, Abraham MR, Marbán E (2007) Regenerative potential of cardiosphere-derived cells expanded from percutaneous endomyocardial biopsy specimens. Circulation 115(7):896–908Google Scholar
  109. Son MJ, Woolard K, Nam DH et al (2009) SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 4:440–452PubMedCrossRefGoogle Scholar
  110. Steidl U, Kronenwett R, Rohr UP et al (2002) Gene expression profiling identifies significant differences between the molecular phenotypes of bone marrow-derived and circulating human CD34+ hematopoietic stem cells. Blood 99:2037–2044PubMedCrossRefGoogle Scholar
  111. Stingl J, Eirew P, Ricketson I et al (2006) Purification and unique properties of mammary epithelial stem cells. Nature 439:993–997PubMedGoogle Scholar
  112. Storms R, Trujillo A, Springer J (1999) Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci USA 96:9118–9123PubMedCrossRefGoogle Scholar
  113. Sturzu AC, Wu SM (2011) Developmental and regenerative biology of multipotent cardiovascular progenitor cells. Circ Res 108:353–364PubMedCrossRefGoogle Scholar
  114. Suh MR, Lee Y, Kim JY et al (2004) Human embryonic stem cells express a unique set of microRNAs. Dev Biol 270:488–498PubMedCrossRefGoogle Scholar
  115. Sun S, Guo Z, Xiao X et al (2003) Isolation of mouse marrow mesenchymal progenitors by a novel and reliable method. Stem Cells 21:527–535PubMedCrossRefGoogle Scholar
  116. Tang C, Ang BT, Pervaiz S (2007) Cancer stem cell: target for anti-cancer therapy. FASEB J 21:3777–3785PubMedCrossRefGoogle Scholar
  117. Timmermans F, Plum J, Yoder MC et al (2009) Endothelial progenitor cells: identity defined? J Cell Mol Med 13:87–102PubMedCrossRefGoogle Scholar
  118. Tondreau T, Meuleman N, Delforge A et al (2005) Mesenchymal stem cells derived from CD133-positive cells in mobilized peripheral blood and cord blood: proliferation, Oct4 expression, and plasticity. Stem Cells 23:1105–1112PubMedCrossRefGoogle Scholar
  119. Toren A, Bielorai B, Jacob-Hirsch J et al (2005) CD133-positive hematopoietic stem cell “stemness” genes contain many genes mutated or abnormally expressed in leukemia. Stem Cells 23:1142–1153PubMedCrossRefGoogle Scholar
  120. Wagner W, Ansorge A, Wirkner U et al (2004) Molecular evidence for stem cell function of the slow-dividing fraction among human hematopoietic progenitor cells by genome-wide analysis. Blood 104:675–686PubMedCrossRefGoogle Scholar
  121. Wilson KD, Venkatasubrahmanyam S, Jia F et al (2009) MicroRNA profiling of human-induced pluripotent stem cells. Stem Cells Dev 18:749–758PubMedCrossRefGoogle Scholar
  122. Wollscheid B, Bausch-Fluck D, Henderson C et al (2009) Mass-spectrometric identification and relative quantification of N-linked cell surface glycoproteins. Nat Biotechnol 27:378–386PubMedCrossRefGoogle Scholar
  123. Xiao C, Calado DP, Galler G et al (2007) MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell 131:146–159PubMedCrossRefGoogle Scholar
  124. Yang ZF, Ho DW, Ng MN et al (2008) Significance of CD90+ cancer stem cells in human liver cancer. Cancer Cell 13(2):153–166Google Scholar
  125. Yovchev MI, Grozdanov PN, Joseph B et al (2007) Novel hepatic progenitor cell surface markers in the adult rat liver. Hepatology 45:139–149PubMedCrossRefGoogle Scholar
  126. Yovchev MI, Grozdanov PN, Zhou H et al (2008) Identification of adult hepatic progenitor cells capable of repopulating injured rat liver. Hepatology 47:636–647PubMedCrossRefGoogle Scholar
  127. Zhan M, Miller CP, Papayannopoulou T et al (2007) MicroRNA expression dynamics during murine and human erythroid differentiation. Exp Hematol 35:1015–1025PubMedCrossRefGoogle Scholar
  128. Zhou B, Wang S, Mayr C et al (2007) miR-150, a microRNA expressed in mature B and T cells, blocks early B cell development when expressed prematurely. Proc Natl Acad Sci USA 104:7080–7085PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  1. 1.Miltenyi Biotec GmbHBergisch GladbachGermany

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