The Concept of Stem Cells
The “stem cell” concept was first proposed by Till and McCulloch following their pioneering studies of the blood system regeneration in vivo. Ten days after transplanting limiting number of syngenic bone marrow (BM) cells into recipient mice, they observed cellular colonies that formed in the spleens of recipient mice. Analysis of these colonies revealed that a very small sub-population of the donor BM cells possessed two remarkable properties: (1) the ability to generate multiple types of myeloerythroid cells, and (2) the ability to self-replicate [5-8]1. These findings introduced the two defining criteria of stem cells i.e. multi-potency and self-renewal. Hematopoietic Stem Cells (HSCs) are the only cells within the hematopoietic system that possess the potential for both multi-potency and self-renewal. In the case of HSC, multi-potency is the ability to differentiate into all functional blood cells, while self-renewal is the ability to give rise to identical daughter HSCs without differentiation.
The field of stem cell research has greatly expanded since the initial studies of Till and McCulloch and now includes stem cells that give rise to specific organs/tissues (collectively termed tissue-specific stem cells) and also embryonic stem (ES) cells which can give rise to every cell type in the adult body. A system of nomenclature has evolved to reflect the differentiation potential of different stem cell populations (summarized in Table 1). It is beyond the scope of this article to discuss non-hematopoietic stem cell populations; excellent reviews of the latter cells are presented elsewhere in this issue.
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In 1988, the initial prospective purification of hematopoietic stem cells from mouse BM was achieved utilizing the relatively new technologies of multi-color fluorescence-activated cell sorting and monoclonal antibodies [10, 11]. The resultant population of enriched mouse HSCs had a surface marker phenotype of Thy-1low Lin (Lineage-markers)− Sca-1+, and represented approximately 0.05% of the mouse adult BM cells. Spangrude and colleagues demonstrated that these were the only cells in mouse BM capable of transferring long-term reconstitution of the entire hematopoietic system (then defined as more than 3 months) when transplanted into lethally irradiated mice [11]. A reductionist approach by Uchida et al showed that Thy1.1low, but not Thy1.1high or Thy1.1− cells could give rise to donor-derived long-term multilineage reconstitution of irradiated hosts; this was true of Sca-1+, but not Sca-1− cells, and of Lin−, but not Lin+ cells [12]. Since these initial studies, mouse HSCs have been more extensively purified by identifying and then utilizing additional cell-surface markers to distinguish them from other cells in BM; these included, but were not exclusively single cells that could self-renew and give long-term multilineage maturation [12-14]. In 1994 the population isolated by Spangrude et al was shown to include at least 3 multipotent populations: Long-Term (LT)-HSC, Short-Term (ST)-HSC, and Multi-Potent Progenitor (MPP, a cell population that has lost the self-renewal capacity of HSC) [15]. In 1996, HSCs from adult mouse BM were sufficiently enriched to conduct single-cell transplantation experiments, and these studies revealed that one in three CD34−/low c-Kit+ Sca-1+ Lin− cells showed myelolymphoid long-term reconstitution in lethally irradiated recipients after a single cell transplant [16]. Despite the fact that hematopoietic tissues contain both stem and progenitor cells, rapid and sustained engraftment of syngenic and even of H2 incompatible allogenic hosts can only be achieved with HSC, the time to engraftment depending on the number of HSC transplanted [17].
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