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• W2227902555 abstract "In the 19th century, mammalian tissues were first described to be composed of cells, leading to the claim that cells originate exclusively from other cells (“omnis cellula a cellula”) formulated by Virchow and Schwann, respectively [1Virchow R Editorial.Archiv fuer pathologische Anatomie und Physiologie und fuer klinische Medizin. 1855; 8: 23Google Scholar, 2Schwann T (1847) Microscopical researches into the accordance of structure and growth of animals and plants. London: The Sydenham SocietyGoogle Scholar]. At the beginning of the 20th century, the concept of tissue stem cells as the basis for tissue regeneration was introduced: analyzing the phylogeny of hematopoiesis in the bone marrow solely based on morphological observations, Pappenheim postulated the existence of an undifferentiated stem cell (“gemeinsame Stammzelle”) giving rise to the plethora of blood cells via an intermediate state of progenitor cells (Fig. 1, [3Pappenheim A Prinzipien der neueren morphologischen Haematozytologie nach zytogenetischer Grundlage.Folia haematologica. 1917; 21: 91Google Scholar]). In the 1950s, several groups corroborated the existence of the hematopoietic stem cell in the bone marrow by showing hematopoietic recovery from transplanted bone marrow after irradiation damage [4Lorenz E Uphoff D Reid T.R Shelton E Modification of irradiation injury in mice and guinea pigs by bone marrow injections.J Natl Cancer Inst. 1951; 12: 197PubMed Google Scholar, 5Ford C.E Hamerton J.L Barnes D.W.H Loutit J.F Cytological identification of radiation-chimeras.Nature. 1956; 177: 452Crossref PubMed Scopus (329) Google Scholar, 6Nowell P.C Cole L.J Habermeyer J.G Roan P.L Growth and continued function of rat marrow cells in irradiated mice.Cancer Res. 1956; 16: 258PubMed Google Scholar]. Till and McCulloch later traced hematopoietic repopulation capacity to clonogenic cells establishing spleen colony-forming units [7Till J.E McCulloch E.A A direct measurement of the radiation sensitivity of normal mouse bone marrow cells.Radiat Res. 1961; 14: 213Crossref PubMed Scopus (3180) Google Scholar]. Subsequently, the concept of tissue regeneration from a small population of resident tissue stem cells was generally accepted, was extended to nonhematopoietic tissues such as gut and skin [8Potten C.S Loeffler M Stem cells attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt.Development. 1990; 110: 1001Crossref PubMed Google Scholar], and still is our understanding of adult tissue regeneration today, enriched by an immense body of descriptive data. In parallel, the principle of directed cellular proliferation underlay the understanding of the early stages in embryogenesis and, together with the cellular movement, led to the discovery of morphogenesis via germ layers in the early embryo [9Vogt W Gestaltungsanalyse am Amphibienkeim mit ortlicher Vitalfarbung. II. Teil Gastrulation und Mesodermbildung bei Urodelen und Anuren.Wilhelm Roux Arch Entwicklungsmech Org. 1929; 120: 384Crossref Scopus (221) Google Scholar]. With emerging technologies, it was 33 and 3 years ago that stem cells with the capacity to differentiate into all tissues of the adult organism were functionally isolated from preimplantation embryos in mice and humans, respectively, and were called embryonic stem (ES) cells [10Gardner R.L Edwards R.G Control of the sex ratio at full term in the rabbit by transferring sexed blastocysts.Nature. 1968; 218: 346Crossref PubMed Scopus (148) Google Scholar, 11Evans M.J Kaufman M.H Establishment in culture of pluripotential cells from mouse embryos.Nature. 1981; 292: 154Crossref PubMed Scopus (6249) Google Scholar, 12Martin G.R Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells.Proc Natl Acad Sci U S A. 1981; 78: 7634Crossref PubMed Scopus (4177) Google Scholar, 13Thomson J.A Itskovitz-Eldor J Shapiro S.S et al.Embryonic stem cell lines derived from human blastocysts.Science. 1998; 282: 1145Crossref PubMed Scopus (11907) Google Scholar]. Although the concept of stem cells in embryogenesis and stem cells in adult tissue regeneration were initially pursued in conceptually separate approaches, they merged again with the successful cloning of a mammal from the nucleus of an adult tissue cell 4 years ago [14Wilmut I Schnieke A.E McWhir J Kind A.J Campbell K.H Viable offspring derived from fetal and adult mammalian cells.Nature. 1997; 385: 810Crossref PubMed Scopus (3956) Google Scholar]. These experiments established that the nuclei of at least some adult cells were capable of being reprogrammed and spurred several groups to reevaluate the differentiation capacity of adult tissue stem cells, leading to a number of reports on somatic stem cell plasticity over the last 3 years. Here, we will review the current evidence for stem cell plasticity. Following the chronology of discoveries, we will start from the broadening developmental potential of bone marrow–derived stem cells leading to the differentiation capacities of stem cells from nonhematopoietic tissues. We will discuss some of the potential caveats to the current work, and finally will speculate about the potential underlying mechanisms of transdifferentiation. Donor-derived cells have recently been found integrated in the parenchyma of several nonhematopoietic tissues after whole bone marrow transplantation (Table 1). One of the earliest and most convincing examples came from the groups of Mavilio and Cossu [15Ferrari G Cusella-De Angelis G Coletta M et al.Muscle regeneration by bone marrow–derived myogenic progenitors.Science. 1998; 279: 1528Crossref PubMed Scopus (2419) Google Scholar], who transplanted bone marrow from transgenic mice expressing the lacZ-gene under the control of a muscle-specific promoter into wild-type recipients. Several months after transplantation, a lower hind-limb muscle was injured by the injection of cobra venom, causing inflammation followed by the regeneration of skeletal muscle. Analyzing the repaired muscle two to three weeks after the injury, they observed a significant number of lacZ+ muscle fibers. This group also observed lacZ+ muscle fibers following the direct injection of donor cells into the injured skeletal muscle. These landmark experiments, in accordance with reports from other groups [16Bittner R.E Schofer C Weipoltshammer K et al.Recruitment of bone-marrow–derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice.Anat Embryol (Berl). 1999; 199: 391Crossref PubMed Scopus (380) Google Scholar], clearly showed that adult murine bone marrow contained cells capable of differentiation into skeletal muscle, although the cell type(s) responsible remained largely unexplored. Interestingly, such activity had been first proposed more than 30 years ago [17Bateson R.G Woodrow D.F Sloper J.C Circulating cells as a source of myoblasts in regenerating injured mammalian skeletal muscle.Nature. 1967; 213: 1035Crossref Scopus (39) Google Scholar] but was disputed [18Grounds M.D Skeletal muscle precursors do not arise from bone marrow cells.Cell Tissue Res. 1983; 234: 713Crossref PubMed Scopus (35) Google Scholar].Table 1Donor cell contribution to nonhematopoietic tissues after whole bone marrow transplantationReferenceTarget TissueSpeciesApproximate frequencyEglitis et al., 1997 25Eglitis M.A Mezey E Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice.Proc Natl Acad Sci U S A. 1997; 94: 4080Crossref PubMed Scopus (943) Google Scholarmacro and microgliaMouse0.5–2%Ferrari et al., 1998 15Ferrari G Cusella-De Angelis G Coletta M et al.Muscle regeneration by bone marrow–derived myogenic progenitors.Science. 1998; 279: 1528Crossref PubMed Scopus (2419) Google Scholarskeletal muscleMouseMinimalShi et al., 1998 20Shi Q Rafii S Wu M.H et al.Evidence for circulating bone marrow–derived endothelial cells.Blood. 1998; 92: 362Crossref PubMed Google Scholarendothelial cellsDogN/APetersen et al., 1999 28Petersen B.E Bowen W.C Patrene K.D et al.Bone marrow as a potential source of hepatic oval cells.Science. 1999; 284: 1168Crossref PubMed Scopus (2168) Google Scholaroval cells/hepatocytesRat0.14%Horwitz et al., 1999 24Horwitz E.M Prockop D.J Fitzpatrick L.A et al.Transplantability and therapeutic effects of bone marrow–derived mesenchymal cells in children with osteogenesis imperfecta.Nat Med. 1999; 5: 309Crossref PubMed Scopus (1586) Google ScholarosteoblastsHuman1.5–2%Bittner et al., 1999 16Bittner R.E Schofer C Weipoltshammer K et al.Recruitment of bone-marrow–derived cells by skeletal and cardiac muscle in adult dystrophic mdx mice.Anat Embryol (Berl). 1999; 199: 391Crossref PubMed Scopus (380) Google Scholarskeletal, cardiac muscleMouseNot givenAsahara et al., 1999 95Asahara T Masuda H Takahashi T et al.Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization.Circ Res. 1999; 85: 221Crossref PubMed Scopus (2883) Google Scholarendothelial cellsMouseNot givenTheise et al., 2000 29Theise N.D Badve S Saxena R et al.Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation.Hepatology. 2000; 31: 235Crossref PubMed Scopus (891) Google Scholar, 31Theise N.D Nimmakayalu M Gardner R et al.Liver from bone marrow in humans.Hepatology. 2000; 32: 11Crossref PubMed Scopus (1148) Google ScholarhepatocytesMouse and human2.2%Brazelton et al., 2000 27Brazelton T.R Rossi F.M Keshet G.I Blau H.M From marrow to brain expression of neuronal phenotypes in adult mice.Science. 2000; 290: 1775Crossref PubMed Scopus (1573) Google ScholarneuronsMouse0.2–0.3%Mezey et al., 2000 26Mezey E Chandross K.J Harta G Maki R.A McKercher S.R Turning blood into brain cells bearing neuronal antigens generated in vivo from bone marrow.Science. 2000; 290: 1779Crossref PubMed Scopus (1678) Google ScholarneuronsMouse0.3–2.3% Open table in a new tab Given the close relationship of hematopoiesis and vasculogenesis during embryogenesis (reviewed in [19Hirschi K.K Goodell M.A Common origins of blood and blood vessels in adults?.Differentiation. 2001; In PressGoogle Scholar]), several groups examined the bone marrow for the presence of a precursor population with vasculogenic potential. Shi et al. found donor-derived vascular endothelial cells after bone marrow transplantation in dogs [20Shi Q Rafii S Wu M.H et al.Evidence for circulating bone marrow–derived endothelial cells.Blood. 1998; 92: 362Crossref PubMed Google Scholar]. In these experiments, a Dacron graft was inserted into the descending thoracic aorta 6 to 8 months after bone marrow transplantation and was shown to be populated by donor endothelial cells 12 weeks later. Bone marrow–derived endothelial progenitors were also found to be recruitable into the blood stream by cytokines and ischemic stress, contributing to neovascularization in vitro [21Asahara T Murohara T Sullivan A et al.Isolation of putative progenitor endothelial cells for angiogenesis.Science. 1997; 275: 964Crossref PubMed Scopus (7553) Google Scholar, 22Takahashi T Kalka C Masuda H et al.Ischemia- and cytokine-induced mobilization of bone marrow–derived endothelial progenitor cells for neovascularization.Nat Med. 1999; 5: 434Crossref PubMed Scopus (46) Google Scholar]. Analogously, the long-standing evidence of bone marrow as an ample source of cells with the capacity for mesenchymal differentiation (reviewed in [23Devine S.M Hoffman R Role of mesenchymal stem cells in hematopoietic stem cell transplantation.Curr Opin Hematol. 2000; 7: 358Crossref PubMed Scopus (151) Google Scholar]) encouraged Horwitz et al. to transplant whole bone marrow in order to repopulate the osteoblast lineage in patients with osteogenesis imperfecta [24Horwitz E.M Prockop D.J Fitzpatrick L.A et al.Transplantability and therapeutic effects of bone marrow–derived mesenchymal cells in children with osteogenesis imperfecta.Nat Med. 1999; 5: 309Crossref PubMed Scopus (1586) Google Scholar]. In three patients transplanted, bone density and growth rate improved, and donor-derived osteoblasts were found to participate in bone formation. Even more surprising have been experiments showing the integration of bone marrow–derived cells into nonmesodermal-derived parenchyma. In the brain of mice, Eglitis and Mezey discovered a continuous influx of bone marrow–derived cells which differentiated into microglia and astroglia, a neuroectodermal cell type, after bone marrow transplantation [25Eglitis M.A Mezey E Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice.Proc Natl Acad Sci U S A. 1997; 94: 4080Crossref PubMed Scopus (943) Google Scholar]. Further characterization of this phenomenon demonstrated a neuronal phenotype of some marrow-derived cells and gave a first insight in their transcriptional repertoire [26Mezey E Chandross K.J Harta G Maki R.A McKercher S.R Turning blood into brain cells bearing neuronal antigens generated in vivo from bone marrow.Science. 2000; 290: 1779Crossref PubMed Scopus (1678) Google Scholar, 27Brazelton T.R Rossi F.M Keshet G.I Blau H.M From marrow to brain expression of neuronal phenotypes in adult mice.Science. 2000; 290: 1775Crossref PubMed Scopus (1573) Google Scholar]. In addition, the bone marrow has been found to contribute to endoderm-derived tissues: mature liver cells as well as hepatic oval cells, a common stem cell of hepatocytes and biliary epithelium, were partially donor-derived after bone marrow transplantation in rodents [28Petersen B.E Bowen W.C Patrene K.D et al.Bone marrow as a potential source of hepatic oval cells.Science. 1999; 284: 1168Crossref PubMed Scopus (2168) Google Scholar, 29Theise N.D Badve S Saxena R et al.Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation.Hepatology. 2000; 31: 235Crossref PubMed Scopus (891) Google Scholar] and humans [30Alison M.R Poulsom R Jeffery R et al.Hepatocytes from non-hepatic adult stem cells.Nature. 2000; 406: 257Crossref PubMed Scopus (944) Google Scholar, 31Theise N.D Nimmakayalu M Gardner R et al.Liver from bone marrow in humans.Hepatology. 2000; 32: 11Crossref PubMed Scopus (1148) Google Scholar]. Collectively, these striking observations indicated that there are bone marrow cells that can migrate to distant sites and participate in the repair of tissues across germ layer boundaries. However, bone marrow is a composite tissue that contains hematopoietic parenchyma and a stroma of different cell types, such as fibroblasts, endothelial, fat, and smooth muscle cells [32Clark B.R Keating A Biology of bone marrow stroma.Ann N Y Acad Sci. 1995; 770: 70Crossref PubMed Scopus (171) Google Scholar]. The cell populations involved in bone marrow–derived distal tissue repair are just beginning to be characterized. Below, we will focus on those reports in which purified (or enriched) bone marrow hematopoietic stem cells (HSC) had been transplanted (Table 2).Table 2Engraftment of purified or enriched hematopoietic stem cells into nonhematopoietic tissueReferenceHSCTarget TissueCell No.PurityInjury induced*Engraftment (%)Gussoni et al., 1999 33Gussoni E Soneoka Y Strickland C.D et al.Dystrophin expression in the mdx mouse restored by stem cell transplantation.Nature. 1999; 401: 390Crossref PubMed Scopus (1619) Google ScholarSP(1)Skeletal muscle2–5000NSTBI + genetic deficiency (mdx mouse)1–10Lagasse et al., 2000 37Lagasse E Connors H Al-Dhalimy M et al.Purified hematopoietic stem cells can differentiate into hepatocytes in vivo.Nat Med. 2000; 6: 1229Crossref PubMed Scopus (2118) Google ScholarKTSL(2)Liver50–100095–98%TBI + genetic deficiency (FAH)Very rareOrlic et al., 2001 35Orlic D Kajstura J Chimenti S et al.Bone marrow cells regenerate infarcted myocardium.Nature. 2001; 410: 701Crossref PubMed Scopus (4632) Google ScholarLin− c-Kithi (3)Cardiac muscle3–20,000NSCoronary artery ligation54% of new tissueVasculatureKocher et al., 2001 36Kocher A.A Schuster M.D Szabolcs M.J et al.Neovascularization of ischemic myocardium by human bone-marrow–derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function.Nat Med. 2001; 7: 430Crossref PubMed Scopus (2312) Google ScholarCD34+(3)Vasculature2 × 10698%Coronary artery ligation20–25Jackson et al., 2001 34Jackson K.A Majka S.M Wang H et al.Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells.J Clin Invest. 2001; 107: 1395Crossref PubMed Scopus (1754) Google ScholarSP1Cardiac muscle200092%TBI + coronary artery ligation0.02Endothelial cells2–4Krause et al., 2001 38Krause D.S Theise N.D Collector M.I et al.Multi-organ, multi-lineage engraftment by a single bone marrow–derived stem cell.Cell. 2001; 105: 369Abstract Full Text Full Text PDF PubMed Scopus (2434) Google Scholar“homed” HSC(4)Lung alveoli1—TBI20Lung bronchiTBI3.7EsophagusTBI1.81StomachTBI0.52Small bowelTBI0.87Large bowelTBI0.19Bile ductTBI0.84SkinTBI3.39*TBI: Total-body irradiation (lethal dose in all cases). NS: not stated/determined. (1) The HSC were purified as “side population” or “SP” cells that efflux the fluorescent dye, Hoechst 33342 44Goodell M.A Brose K Paradis G Conner A.S Mulligan R.C Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo.J Exp Med. 1996; 183: 1797Crossref PubMed Scopus (2440) Google Scholar. (2) The HSC were purified as so called “KTSL” cells that are c-kit+, Thy-1low, Sca-1+, and lineage marker−/low 96Uchida N Weissman I.L Searching for hematopoietic stem cells evidence that Thy-1.1loLin−Sca-1+ cells are the only stem cells in C57BL/Ka-Thy-1.1 bone marrow.J Exp Med. 1992; 175: 175Crossref PubMed Scopus (305) Google Scholar. (3) Lin− c-kithi cells and CD34+ cells would be considered enriched for HSC, but these populations also contain a variety of other uncharacterized progenitors. (4) The HSC were obtained by initial transplantation of lineageneg Fraction 25 PKH26-labeled cells into an irradiated host, and 48 hours later, harvesting of the labeled cells that had homed to the bone marrow and not divided. Single “homed” HSC (cell number based on limiting dilution) were transplanted along with helper cells into lethally irradiated hosts. Open table in a new tab In experiments by Gussoni et al. [33Gussoni E Soneoka Y Strickland C.D et al.Dystrophin expression in the mdx mouse restored by stem cell transplantation.Nature. 1999; 401: 390Crossref PubMed Scopus (1619) Google Scholar], 2000–5000 highly purified male murine hematopoietic stem cells were transplanted into lethally irradiated female mdx mice, a mouse model of muscular dystrophy. In this model, the dystrophin gene is mutated by a single point mutation for which a relatively high reversion rate is known (around 1%). Four to six weeks after transplantation with purified stem cells, muscle fibers from the hind limb of the recipients were examined for dystrophin expression in conjunction with the presence of a Y-chromosome. The group found that between 1 and 10% of fibers were dystrophin positive, and a portion of these were marker chromosome positive. Since this mouse model does not exhibit a severe muscular dystrophy, unlike the phenotype of mutations in the human gene, the authors were not able to determine the functional significance of the engraftment. Nevertheless, this was the first good evidence that purified HSC could regenerate the hematopoietic system and also generate progeny that could differentiate into a nonhematopoietic cell type, in this case, skeletal muscle. In our laboratory, we have shown that the progeny of 2000 HSC transplanted into the bone marrow can generate cardiomyocytes and, far more frequently, endothelial cells after severe injury by coronary artery ligation [34Jackson K.A Majka S.M Wang H et al.Regeneration of ischemic cardiac muscle and vascular endothelium by adult stem cells.J Clin Invest. 2001; 107: 1395Crossref PubMed Scopus (1754) Google Scholar]. The generation of capillary endothelium of the peri-infarct region from purified HSC likely reflects the close relationship between endothelial and hematopoietic progenitors and may suggest the existence of an adult “hemangioblast” (reviewed in [19Hirschi K.K Goodell M.A Common origins of blood and blood vessels in adults?.Differentiation. 2001; In PressGoogle Scholar]). Similarly, Orlic and colleagues [35Orlic D Kajstura J Chimenti S et al.Bone marrow cells regenerate infarcted myocardium.Nature. 2001; 410: 701Crossref PubMed Scopus (4632) Google Scholar] as well as Kocher and colleagues [36Kocher A.A Schuster M.D Szabolcs M.J et al.Neovascularization of ischemic myocardium by human bone-marrow–derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function.Nat Med. 2001; 7: 430Crossref PubMed Scopus (2312) Google Scholar] injected bone marrow populations enriched for HSC directly into the damaged myocardium or into the bloodstream 48 hours after ischemic damage, respectively. After local injection, Orlic et al. observed transplanted cells near the site of injection exhibiting the markers and morphology of immature cardiomyocytes, endothelial cells, and smooth muscle cells. After systemic infusion, Kocher et al. saw an engraftment in the neovasculature of the repairing myocardium. Both studies reported the improvement of post-infarct cardiac function as a result of the engraftment from transplanted cells. In the most definitive study for nonhematopoietic differentiation of purified hematopoietic stem cells, Lagasse and coworkers rescued mice from an otherwise lethal liver defect by transplantation of as few as 50 purified HSC [37Lagasse E Connors H Al-Dhalimy M et al.Purified hematopoietic stem cells can differentiate into hepatocytes in vivo.Nat Med. 2000; 6: 1229Crossref PubMed Scopus (2118) Google Scholar]. In the fumarylacetoacetate hydrolase (FAH) knockout mouse, a model of fatal hereditary tyrosinemia, the authors compared the ability of different cell populations purified from mouse bone marrow to regenerate the liver following engraftment into the bone marrow. The only population capable of contributing to liver regeneration were those with a hematopoietic stem cell phenotype, namely the so-called KTSL population defined by expression of c-kithigh, ThylowSca1+Lin−/lo. Hepatic repair was only seen in conjunction with long-term hematopoietic engraftment. The transfer of such small numbers of cells and their stringent phenotypic characterization, as well as the acquisition of a novel function, as demonstrated by several liver function tests in addition to rigorous histology, constitutes an almost unequivocal demonstration of “transdifferentiation.” In this and all studies described above, multiple purified stem cells were introduced, from 50 to several thousand. Since some impurities are always contained within flow-sorted cell populations, the possibility remains that the novel activities apparently displayed by purified “HSC” were due to contaminants in the purified or enriched cell populations (Table 2). Therefore, ultimate proof of bipotentiality will require the demonstration that a single HSC is capable of regenerating both hematopoiesis and a novel cell type, such as hepatocytes or cardiomyocytes. This will likely be done by transplantation of single cells, or by lineage tracking using retroviral marking. The recent work by Krause et al. [38Krause D.S Theise N.D Collector M.I et al.Multi-organ, multi-lineage engraftment by a single bone marrow–derived stem cell.Cell. 2001; 105: 369Abstract Full Text Full Text PDF PubMed Scopus (2434) Google Scholar] went some distance toward addressing this clonality issue: the authors transplanted single cells—as determined by limiting dilution—in a murine hematopoietic transplantation assay and looked for engraftment in different epithelial tissues 11 months later (Table 2). They reported engraftment in all epithelial tissues examined, ranging up to nearly 20% in the lung pneumocytes of one animal. In contrast to most other studies in which severe tissue injury or genetic deficiency were a requirement for nonhematopoietic engraftment, Krause et al. observed HSC-derived epithelial cells after total-body irradiation with 10.5 to 11 Gy alone. However, the exceptionally long interval between transplantation and examination (one year), or some particular features of the epithelial tissues examined, might have contributed to the high levels of engraftment in this situation. Indeed, Krause et al. noted that the tissues exhibiting high engraftment were also those that are targets of graft-vs-host disease. One of the first reports that launched this fervent area of research was that of turning “brain into blood” (Table 3 and [39Bjornson C.R.R Rietze R.L Reynolds B.A Magli M.C Vescovi A.L Turning brain into blood A hematopoietic fate adopted by adult neural stem cells in vivo.Science. 1999; 283: 534Crossref PubMed Scopus (1284) Google Scholar]). Cultured neural stem cells (NSC) and clonal neural stem cell lines derived from lacZ transgenic mice were transplanted into the bone marrow of sublethally irradiated allogeneic recipients. Over time, both whole and clonal NSC populations contributed to all blood lineages of the host animals. However, several unusual features of these experiments, especially the considerable engraftment across major histocompatibility complex (MHC) barriers and the significantly delayed engraftment observed in this model, put this work in the position of an isolated finding at this point in time.Table 3Plasticity from neural and muscle stem cells?ReferenceCells→TissuePrecultured?Population descriptionBjornson et al., 1999 39Bjornson C.R.R Rietze R.L Reynolds B.A Magli M.C Vescovi A.L Turning brain into blood A hematopoietic fate adopted by adult neural stem cells in vivo.Science. 1999; 283: 534Crossref PubMed Scopus (1284) Google ScholarNeural stem cells→bloodYesClonally derived neural stem cellsGalli et al., 2000 97Galli R Borello U Gritti A et al.Skeletal myogenic potential of human and mouse neural stem cells.Nat Neurosci. 2000; 3: 986Crossref PubMed Scopus (416) Google ScholarNeural stem cells→muscleYesClonally derived neural stem cellsClarke et al., 2000 40Clarke D.L Johansson C.B Wilbertz J et al.Generalized potential of adult neural stem cells.Science. 2000; 288: 1660Crossref PubMed Scopus (911) Google ScholarNeural stem cells→multiple embryonic tissuesYesClonal and mixed neural stem cellsGussoni et al., 1999 33Gussoni E Soneoka Y Strickland C.D et al.Dystrophin expression in the mdx mouse restored by stem cell transplantation.Nature. 1999; 401: 390Crossref PubMed Scopus (1619) Google ScholarSkeletal muscle→bloodNoSP population from skeletal muscleJackson et al., 1999 42Jackson K.A Mi T Goodell M.A Hematopoietic potential of stem cells isolated from murine skeletal muscle.Proc Natl Acad Sci U S A. 1999; 96: 14482Crossref PubMed Scopus (872) Google ScholarSkeletal muscle→bloodYesMuscle enriched for satellite cellsPang 2000 43Pang W Role of muscle-derived cells in hematopoietic reconstitution of irradiated mice.Blood. 2000; 95: 1106PubMed Google ScholarSkeletal muscle→bloodYes/noMuscle-derived mononuclear cells Open table in a new tab Subsequently, Clarke et al. [40Clarke D.L Johansson C.B Wilbertz J et al.Generalized potential of adult neural stem cells.Science. 2000; 288: 1660Crossref PubMed Scopus (911) Google Scholar] tested the regenerative abilities of NSC outside the neural system by injection of NSC from lacZ-transgenic mice into either chick or mouse embryos. In these experiments, NSC contributed to multiple lineages of the developing embryos, encompassing a wide variety of tissues of all three germ layers. Interestingly, contribution to hematopoiesis was not seen. In similar experiments, Geiger et al. [41Geiger H Sick S Bonifer C Muller A.M Globin gene expression is reprogrammed in chimeras generated by injecting adult hematopoietic stem cells into mouse blastocysts.Cell. 1998; 93: 1055Abstract Full Text Full Text PDF PubMed Scopus (112) Google Scholar] tested the differentiation capacity of purified hematopoietic stem cells after injection into the blastocyst. The adult-derived HSC were marked with a transgenic human globin locus, which remarkably underwent a switch of adult to fetal globin expression when injected in the embryos. However, this reprogramming was limited to hematopoietic development and the human transgene was detected at a low level. Hematopoietic activity from cells in the skeletal muscle were first described in 1999 by our group [42Jackson K.A Mi T Goodell M.A Hematopoietic potential of stem cells isolated from murine skeletal muscle.Proc Natl Acad Sci U S A. 1999; 96: 14482Crossref PubMed Scopus (872) Google Scholar] and those of Mulligan and Kunkel [33Gussoni E Soneoka Y Strickland C.D et al.Dystrophin expression in the mdx mouse restored by stem cell transplantation.Nature. 1999; 401: 390Crossref PubMed Scopus (1619) Google Scholar], followed by Pang [43Pang W Role of muscle-derived cells in hematopoietic reconstitution of irradiated mice.Blood. 2000; 95: 1106PubMed Google Scholar]. Transplanting crude mixtures of precultured skeletal muscle cells, we found that high levels of T, B, and myeloid cells were generated in a competitive transplantation assay after lethal total-body irradiation. Unlike the report with NSC, the kinetics of hematopoietic engraftment were indistinguishable from those of bone marrow–derived HSC. Bone marrow from primary recipients rescued and engrafted secondary recipients at reasonable levels, although the lineage engraftment was somewhat skewed. Gussoni et al. [33Gussoni E Soneoka Y Strickland C.D et al.Dys" @default.
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• W2227902555 date "2001-12-01" @default.
• W2227902555 modified "2023-10-15" @default.
• W2227902555 title "Somatic stem cell plasticity" @default.
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