Widespread nonhematopoietic tissue distribution by transplanted human progenitor cells with high aldehyde dehydrogenase activity

Stem Cells

Volumn 26, Issue 3, 2008, Pages 611-620

  Hess, David A ^a,c   Craft, Timothy P ^a   Wirthlin, Louisa ^a   Hohm, Sarah ^a   Zhou, Ping ^a   Eades, William C ^a   Creer, Michael H ^b   Sands, Mark S ^a   Nolta, Jan A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ROBARTS RESEARCH INSTITUTE   (Canada)

Author keywords

Aldehyde dehydrogenase; CD133; NOD SCID model; Transplantation; Umbilical cord blood

Indexed keywords

ALDEHYDE DEHYDROGENASE; BETA GLUCURONIDASE; CD133 ANTIGEN; CD45 ANTIGEN; HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; BIOLOGICAL MARKER;

ANIMAL EXPERIMENT; ARTICLE; CELLULAR DISTRIBUTION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; STEM CELL; TISSUE DISTRIBUTION; XENOTRANSPLANTATION; ANIMAL; CELL SEPARATION; CYTOLOGY; DONOR; ENZYMOLOGY; FLOW CYTOMETRY; HEMATOPOIETIC SYSTEM; LIVER; METABOLISM; MOUSE MUTANT; MUCOPOLYSACCHARIDOSIS TYPE 7; NONOBESE DIABETIC MOUSE; PANCREAS ISLET; PATHOLOGY; STEM CELL TRANSPLANTATION;

MUS;

ALDEHYDE DEHYDROGENASE; ANIMALS; BIOLOGICAL MARKERS; CELL SEPARATION; FLOW CYTOMETRY; GLUCURONIDASE; HEMATOPOIETIC SYSTEM; HUMANS; ISLETS OF LANGERHANS; LIVER; MICE; MICE, INBRED NOD; MICE, SCID; MUCOPOLYSACCHARIDOSIS VII; STEM CELL TRANSPLANTATION; STEM CELLS; TISSUE DONORS;

EID: 43049150840     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1634/stemcells.2007-0429     Document Type: Article

References (55)

1. Jiang Y, Jahagirdar BN, Reinhardt RL et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41-49.
2. Reyes M, Dudek A, Jahagirdar B et al. Origin of endothelial progenitors in human postnatal bone marrow. J Clin Invest 2002;109:337-346.
3. Schwartz RE, Reyes M, Koodie L et al. Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J Clin Invest 2002;109:1291-1302.
4. Kondo M, Wagers AJ, Manz MG et al. Biology of hematopoietic stem cells and progenitors: Implications for clinical application. Annu Rev Immunol 2003;21:759-806.
5. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997;276:71-74.
6. Asahara T, Murohara T, Sullivan A et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997;275:964-967.
7. Bhatia M, Wang JC, Kapp U et al. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci U S A 1997;94:5320-5325.
8. Murohara T, Ikeda H, Duan J et al. Transplanted cord blood-derived endothelial precursor cells augment postnatal neovascularization. J Clin Invest 2000;105:1527-1536.
9. Peichev M, Naiyer AJ, Pereira D et al. Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000;95:952-958.
10. Romanov YA, Svintsitskaya VA, Smirnov VN. Searching for alternative sources of postnatal human mesenchymal stem cells: Candidate MSC-like cells from umbilical cord. STEM CELLS 2003;21:105-110.
11. Ourednik J, Ourednik V, Lynch WP et al. Neural stem cells display an inherent mechanism for rescuing dysfunctional neurons. Nat Biotechnol 2002;20:1103-1110.
12. Park KI, Teng YD, Snyder EY. The injured brain interacts reciprocally with neural stem cells supported by scaffolds to reconstitute lost tissue. Nat Biotechnol 2002;20:1111-1117.
13. Fazel S, Cimini M, Chen L et al. Cardioprotective c-kit+ cells are from the bone marrow and regulate the myocardial balance of angiogenic cytokines. J Clin Invest 2006;116:1865-1877.
14. Kocher AA, Schuster MD, Szabolcs MJ et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 2001;7:430-436.
15. Miyahara Y, Nagaya N, Kataoka M et al. Monolayered mesenchymal stem cells repair scarred myocardium after myocardial infarction. Nat Med 2006;12:459-465.
16. Hess D, Li L, Martin M et al. Bone marrow-derived stem cells initiate pancreatic regeneration. Nat Biotechnol 2003;21:763-770.
17. Lee RH, Seo MJ, Reger RL et al. Multipotent stromal cells from human marrow home to and promote repair of pancreatic islets and renal glomeruli in diabetic NOD/scid mice. Proc Natl Acad Sci U S A 2006;103:17438-17443.
18. Capoccia BJ, Shepherd RM, Link DC. G-CSF and AMD3100 mobilize monocytes into the blood that stimulate angiogenesis in vivo through a paracrine mechanism. Blood 2006;108:2438-2445.
19. Jin DK, Shido K, Kopp HG et al. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4+ hemangiocytes. Nat Med 2006;12:557-567.
20. Schatteman GC, Hanlon HD, Jiao C et al. Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J Clin Invest 2000;106:571-578.
21. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 2004;95:9-20.
22. Yoder MC, Mead LE, Prater D et al. Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals. Blood 2007;109:1801-1809.
23. Hess DA, Meyerrose TE, Wirthlin L et al. Functional characterization of highly purified human hematopoietic repopulating cells isolated according to aldehyde dehydrogenase activity. Blood 2004;104:1648-1655.
24. Hess DA, Wirthlin L, Craft TP et al. Selection based on CD133 and high aldehyde dehydrogenase activity isolates long-term reconstituting human hematopoietic stem cells. Blood 2006;107:2162-2169.
25. Storms RW, Green PD, Safford KM et al. Distinct hematopoietic progenitor compartments are delineated by the expression of aldehyde dehydrogenase and CD34. Blood 2005;106:95-102.
26. Storms RW, Trujillo AP, Springer JB et al. Isolation of primitive human hematopoietic progenitors on the basis of aldehyde dehydrogenase activity. Proc Natl Acad Sci U S A 1999;96:9118-9123.
27. Sahovic EA, Colvin M, Hilton J et al. Role for aldehyde dehydrogenase in survival of progenitors for murine blast cell colonies after treatment with 4-hydroperoxycyclophosphamide in vitro. Cancer Res 1988;48:1223-1226.
28. Sly WS, Quinton BA, McAlister WH et al. Beta glucuronidase deficiency: Report of clinical, radiologic, and biochemical features of a new mucopolysaccharidosis. J Pediatr 1973;82:249-257.
29. Birkenmeier EH, Davisson MT, Beamer WG et al. Murine mucopolysaccharidosis type VII. Characterization of a mouse with beta-glucuronidase deficiency. J Clin Invest 1989;83:1258-1266.
30. Young PP, Hofling AA, Sands MS. VEGF increases engraftment of bone marrow-derived endothelial progenitor cells (EPCs) into vasculature of newborn murine recipients. Proc Natl Acad Sci U S A 2002;99:11951-11956.
31. Freeman BJ, Roberts MS, Vogler CA et al. Behavior and therapeutic efficacy of beta-glucuronidase-positive mononuclear phagocytes in a murine model of mucopolysaccharidosis type VII. Blood 1999;94:2142-2150.
32. Snyder EY, Taylor RM, Wolfe JH. Neural progenitor cell engraftment corrects lysosomal storage throughout the MPS VII mouse brain. Nature 1995;374:367-370.
33. Soper BW, Lessard MD, Vogler CA et al. Nonablative neonatal marrow transplantation attenuates functional and physical defects of beta-glucuronidase deficiency. Blood 2001;97:1498-1504.
34. Soper BW, Duffy TM, Vogler CA et al. A genetically myeloablated MPS VII model detects the expansion and curative properties of as few as 100 enriched murine stem cells. Exp Hematol 1999;27:1691-1704.
35. Hofling AA, Vogler C, Creer MH et al. Engraftment of human CD34+ cells leads to widespread distribution of donor-derived cells and correction of tissue pathology in a novel murine xenotransplantation model of lysosomal storage disease. Blood 2003;101:2054-2063.
36. Sands MS, Birkenmeier EH. A single-base-pair deletion in the beta-glucuronidase gene accounts for the phenotype of murine mucopolysaccharidosis type VII. Proc Natl Acad Sci U S A 1993;90:6567-6571.
37. Meyerrose TE, De Ugarte DA, Hofling AA et al. In vivo distribution of human adipose-derived MSC. STEM CELLS 2007;25:220-227.
38. Hofling AA, Devine S, Vogler C et al. Human CD34+ hematopoietic progenitor cell-directed lentiviral-mediated gene therapy in a xenotransplantation model of lysosomal storage disease. Mol Ther 2004;9:856-865.
39. Wolfe JH, Sands MS, Barker JE et al. Reversal of pathology in murine mucopolysaccharidosis type VII by somatic cell gene transfer. Nature 1992;360:749-753.
40. Cai J, Cheng A, Luo Y et al. Membrane properties of rat embryonic multipotent neural stem cells. J Neurochem 2004;88:212-226.
41. Corti S, Locatelli F, Papadimitriou D et al. Identification of a primitive brain-derived neural stem cell population based on aldehyde dehydrogenase activity. STEM CELLS 2006;24:975-985.
42. Ishikawa M, Asahara T. Endothelial progenitor cell culture for vascular regeneration. Stem Cells Dev 2004;13:344-349.
43. Gallacher L, Murdoch B, Wu DM et al. Isolation and characterization of human CD34(-)Lin(-) and CD34(+)Lin(-) hematopoietic stem cells using cell surface markers AC133 and CD7. Blood 2000;95:2813-2820.
44. Miraglia S, Godfrey W, Yin AH et al. A novel five-transmembrane hematopoietic stem cell antigen: Isolation, characterization, and molecular cloning. Blood 1997;90:5013-5021.
45. Yin AH, Miraglia S, Zanjani ED et al. AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 1997;90:5002-5012.
46. Bonnet D, Bhatia M, Wang JC et al. Cytokine treatment or accessory cells are required to initiate engraftment of purified primitive human hematopoietic cells transplanted at limiting doses into NOD/SCID mice. Bone Marrow Transplant 1999;23:203-209.
47. Adams GB, Chabner KT, Alley IR et al. Stem cell engraftment at the endosteal niche is specified by the calcium-sensing receptor. Nature 2006;439:599-603.
48. Calvi LM, Adams GB, Weibrecht KW et al. Osteoblastic cells regulate the haematopoietic stem cell niche. Nature 2003;425:841-846.
49. Danet GH, Luongo JL, Butler G et al. C1qRp defines a new human stem cell population with hematopoietic and hepatic potential. Proc Natl Acad Sci U S A 2002;99:10441-10445.
50. Wang X, Willenbring H, Akkari Y et al. Cell fusion is the principal source of bone-marrow-derived hepatocytes. Nature 2003;422:897-901.
51. Bhatia M, Bonnet D, Murdoch B et al. A newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nat Med 1998;4:1038-1045.
52. Willenbring H, Bailey AS, Foster M et al. Myelomonocytic cells are sufficient for therapeutic cell fusion in liver. Nat Med 2004;10:744-748.
53. Kashofer K, Siapati EK, Bonnet D. In vivo formation of unstable heterokaryons after liver damage and hematopoietic stem cell/progenitor transplantation. STEM CELLS 2006;24:1104-1112.
54. Quintana-Bustamante O, Alvarez-Barrientos A, Kofman AV et al. Hematopoietic mobilization in mice increases the presence of bone marrow-derived hepatocytes via in vivo cell fusion. Hepatology 2006;43:108-116.
55. Gentry T, Foster S, Winstead L et al. Simultaneous isolation of human BM hematopoietic, endothelial and mesenchymal progenitor cells by flow sorting based on aldehyde dehydrogenase activity: Implications for cell therapy. Cytotherapy 2007;9:259-274.