Identification of a bone marrow-derived mesenchymal progenitor cell subset that can contribute to the gastric epithelium

Laboratory Investigation

Volumn 89, Issue 12, 2009, Pages 1410-1422

  Okumura, Tomoyuki ^a,b   Wang, Sophie Sw ^a,c   Takaishi, Shigeo ^a   Tu, Shui Ping ^a   Ng, Vivian ^a   E Ericksen, Russell ^a   Rustgi, Anil K ^b   Wang, Timothy C ^a  

^a NewYork Presbyterian Hospital   (United States)

^b UNIVERSITY OF TOYAMA   (Japan)

^c KAOHSIUNG MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKERATIN 19; GREEN FLUORESCENT PROTEIN; MESSENGER RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLASTOCYST; CELL CULTURE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HELICOBACTER INFECTION; HEMATOPOIETIC STEM CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN ISOLATION; REAL TIME POLYMERASE CHAIN REACTION; STOMACH EPITHELIUM;

ANIMALS; BLOOD CELLS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; CLONE CELLS; EPITHELIAL CELLS; FEMALE; GASTRIC MUCOSA; HELICOBACTER FELIS; HELICOBACTER INFECTIONS; KERATIN-19; MALE; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PHENOTYPE; TISSUE EXTRACTS; UP-REGULATION;

EID: 70549093266     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2009.88     Document Type: Article

References (66)

1. Theise ND, Badve S, Saxena R, et al. Derivation of hepatocytes from bone marrow cells in mice after radiation-induced myeloablation. Hepatology 2000;31:235-240.
2. Spencer H, Rampling D, Aurora P, et al. Transbronchial biopsies provide longitudinal evidence for epithelial chimerism in children following sex mismatched lung transplantation. Thorax 2005;60:60-62.
3. Suratt BT, Cool CD, Serls AE, et al. Human pulmonary chimerism after hematopoietic stem cell transplantation. Am J Respir Crit Care Med 2003;168:318-322.
4. Korbling M, Katz RL, Khanna A, et al. Hepatocytes and epithelial cells of donor origin in recipients of peripheral-blood stem cells. N Engl J Med 2002;346:738-746.
5. Okamoto R, Yajima T, Yamazaki M, et al. Damaged epithelia regenerated by bone marrow-derived cells in the human gastrointestinal tract. Nat Med 2002;8:1011-1017.
6. Ishikawa F, Yasukawa M, Yoshida S, et al. Human cord blood-and bone marrow-derived CD34+ cells regenerate gastrointestinal epithelial cells. FASEB J 2004;18:1958-1960.
7. Matsumoto T, Okamoto R, Yajima T, et al. Increase of bone marrow-derived secretory lineage epithelial cells during regeneration in the human intestine. Gastroenterology 2005;128:1851-1867.
8. Spyridonidis A, Schmitt-Graff A, Tomann T, et al. Epithelial tissue chimerism after human hematopoietic cell transplantation is a real phenomenon. Am J Pathol 2004;164:1147-1155.
9. Petersen BE, Bowen WC, Patrene KD, et al. Bone marrow as a potential source of hepatic oval cells. Science 1999;284:1168-1170.
10. Krause DS, Theise ND, Collector MI, et al. Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 2001;105:369-377.
11. Lagasse E, Connors H, Al-Dhalimy M, et al. Purified hematopoietic stem cells can differentiate into hepatocytes in vivo. Nat Med 2000;6: 1229-1234.
12. Poulsom R, Forbes SJ, Hodivala-Dilke K, et al. Bone marrow contributes to renal parenchymal turnover and regeneration. J Pathol 2001;195:229-235.
13. Bruscia EM, Ziegler EC, Price JE, et al. Engraftment of donor-derived epithelial cells in multiple organs following bone marrow transplantation into newborn mice. Stem Cells 2006;24: 2299-2308.
14. Houghton J, Stoicov C, Nomura S, et al. Gastric cancer originating from bone marrow-derived cells. Science 2004;306:1568-1571.
15. Chakraborty A, Lazova R, Davies S, et al. Donor DNA in a renal cell carcinoma metastasis from a bone marrow transplant recipient. Bone Marrow Transplant 2004;34:183-186.
16. Cogle CR, Theise ND, Fu D, et al. Bone marrow contributes to epithelial cancers in mice and humans as developmental mimicry. Stem Cells 2007;25:1881-1887.
17. Avital I, Moreira A, Downey RJ. The origin of epithelial neoplasms after allogeneic stem cell transplantation. Haematologica 2006;91:ELT07; author reply ELT06.
18. Herzog EL, Krause DS. Engraftment of marrow-derived epithelial cells: the role of fusion. Proc Am Thorac Soc 2006;3:691-695.
19. Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 1970;3:393-403.
20. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-147.
21. Friedenstein AJ, Chailakhyan RK, Latsinik NV, et al. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation 1974;17:331-340.
22. Friedenstein AJ, Deriglasova UF, Kulagina NN, et al. Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol 1974; 2:83-92.
23. Ferrari G, Cusella-De Angelis G, Coletta M, et al. Muscle regeneration by bone marrow-derived myogenic progenitors. Science 1998;279:1528-1530.
24. Rojas M, Xu J, Woods CR, et al. Bone marrow-derived mesenchymal stem cells in repair of the injured lung. Am J Respir Cell Mol Biol 2005;33:145-152.
25. Mackenzie TC, Shaaban AF, Radu A, et al. Engraftment of bone marrow and fetal liver cells after in utero transplantation in MDX mice. J Pediatr Surg 2002;37:1058-1064.
26. Cho KJ, Trzaska KA, Greco SJ, et al. Neurons derived from human mesenchymal stem cells show synaptic transmission and can be induced to produce the neurotransmitter substance P by interleukin-1 alpha. Stem Cells 2005;23:383-391.
27. Pittenger MF, Martin BJ. Mesenchymal stem cells and their potential as cardiac therapeutics. Circ Res 2004;95:9-20. Review.
28. Mackenzie TC, Flake AW. Multilineage differentiation of human MSC after in utero transplantation. Cytotherapy 2001;3: 403-405.
29. Anjos-Afonso F, Bonnet D. Nonhematopoietic/endothelial SSEA-1+ cells define the most primitive progenitors in the adult murine bone marrow mesenchymal compartment. Blood 2007;109: 1298-1306.
30. Jiang Y, Jahagirdar BN, Reinhardt RL, et al. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002;418:41-49.
31. Nadri S, Soleimani M, Kiani J, et al. Multipotent mesenchymal stem cells from adult human eye conjunctiva stromal cells. Differentiation 2007;76:223-231.
32. D'Ippolito G, Diabira S, Howard GA, et al. Marrow-isolated adult multilineage inducible (MIAMI) cells, a unique population of postnatal young and old human cells with extensive expansion and differentiation potential. J Cell Sci 2004;117:2971-2981.
33. Moll R, Franke WW, Schiller DL, et al. The catalog of human cytokeratins: patterns of expression in normal epithelia, tumors and cultured cells. Cell 1982;31:11-24.
34. Michel M, Torok N, Godbout MJ, et al. Keratin 19 as a biochemical marker of skin stem cells in vivo and in vitro: keratin 19 expressing cells are differentially localized in function of anatomic sites, and their number varies with donor age and culture stage. J Cell Sci 1996;109:1017-1028.
35. Brembeck FH, Moffett J, Wang TC, et al. The keratin 19 promoter is potent for cell-specific targeting of genes in transgenic mice. Gastroenterology 2001;120:1720-1728.
36. Calnek D, Quaroni A. Changes in keratin expression during fetal and postnatal development of intestinal epithelial cells. Biochem J 1992;285(Part 3):939-946.
37. Calnek D, Quaroni A. Differential localization by in situ hybridization of distinct keratin mRNA species during intestinal epithelial cell development and differentiation. Differentiation 1993;53: 95-104.
38. Quaroni A, Calnek D, Quaroni E, et al. Keratin expression in rat intestinal crypt and villus cells. Analysis with a panel of monoclonal antibodies. J Biol Chem 1991;266:11923-11931.
39. Chun-mao H, Su-yi W, Ping-ping L, et al. Human bone marrow-derived mesenchymal stem cells differentiate into epidermal-like cells in vitro. Differentiation 2007;75:292-298.
40. Digirolamo CM, Stokes D, Colter D, et al. Propagation and senescence of human marrow stromal cells in culture: a simple colony-forming assay identifies samples with the greatest potential to propagate and differentiate. Br J Haematol 1999;107:275-281.
41. Colter DC, Class R, DiGirolamo CM, et al. Rapid expansion of recycling stem cells in cultures of plastic-adherent cells from human bone marrow. Proc Natl Acad Sci USA 2000;97:3213-3218.
42. Javazon EH, Colter DC, Schwarz EJ, et al. Rat marrow stromal cells are more sensitive to plating density and expand more rapidly from single-cell-derived colonies than human marrow stromal cells. Stem Cells 2001;19:219-225.
43. Phinney DG, Kopen G, Isaacson RL, et al. Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: variations in yield, growth, and differentiation. J Cell Biochem 1999;72:570-585.
44. Kadiyala S, Young RG, Thiede MA, et al. Culture expanded canine mesenchymal stem cells possess osteochondrogenic potential in vivo and in vitro. Cell Transplant 1997;6:125-134.
45. Martin DR, Cox NR, Hathcock TL, et al. Isolation and characterization of multipotential mesenchymal stem cells from feline bone marrow. Exp Hematol 2002;30:879-886.
46. Javazon EH, Beggs KJ, Flake AW. Mesenchymal stem cells: paradoxes of passaging. Exp Hematol 2004;32:414-425.
47. Owen M, Friedenstein AJ. Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found Symp 1988;136:42-60.
48. Houghton J, Wang TC. Role of bone marrow-derived cells in gastro adenocarcinoma. In: Wang TC, Fox J, Giraud A (eds). The Biology of Gastric Cancers. Springer Science Press: New York, NY, 2009, pp 561-586.
49. Yoon YS, Wecker A, Heyd L, et al. Clonally expanded novel multipotent stem cells from human bone marrow regenerate myocardium after myocardial infarction. J Clin Invest 2005;115:326-338.
50. Reyes M, Lund T, Lenvik T, et al. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 2001;98:2615-2625.
51. Li H, Fan X, Kovi RC, et al. Spontaneous expression of embryonic factors and p53 point mutations in aged mesenchymal stem cells: A model of age-related tumorigenesis in mice. Cancer Res 2007;67:10889-10898.
52. Kuznetsov SA, Mankani MH, Gronthos S, et al. Circulating skeletal stem cells. J Cell Biol 2001;153:1133-1140.
53. Metcalf D. Formation in agar of fibroblast-like colonies by cells from the mouse pleural cavity and other sources. J Cell Physiol 1972;80: 409-419.
54. Piersma AH, Ploemacher RE, Brockbank KG, et al. Migration of fibroblastoid stromal cells in murine blood. Cell Tissue Kinet 1985;18:589-595.
55. Rochefort GY, Delorme B, Lopez A, et al. Multipotential mesenchymal stem cells are mobilized into peripheral blood by hypoxia. Stem Cells 2006;24:2202-2208.
56. Kassis I, Zangi L, Rivkin R, et al. Isolation of mesenchymal stem cells from G-CSF-mobilized human peripheral blood using fibrin microbeads. Bone Marrow Transplant 2006;37:967-976. (Pubitemid 43792558)
57. Juliano RL, Haskill S. Signal transduction from the extracellular matrix. J Cell Biol. 1993;120:577-585.
58. van den Brink GR, Hardwick JC, Tytgat GN, et al. Sonic hedgehog regulates gastric gland morphogenesis in man and mouse. Gastroenterology. 2001;121:317-328.
59. Halttunen T, Marttinen A, Rantala I, et al. Fibroblasts and transforming growth factor beta induce organization and differentiation of T84 human epithelial cells. Gastroenterology 1996;111:1252-1262.
60. Dignass AU, Tsunekawa S, Podolsky DK. Fibroblast growth factors modulate intestinal epithelial cell growth and migration. Gastroenterology 1994;106:1254-1262.
61. Fritsch C, Swietlicki EA, Lefebvre O, et al. Epimorphin expression in intestinal myofibroblasts induces epithelial morphogenesis. J Clin Invest 2002;110:1629-1641.
62. Montesano R, Matsumoto K, Nakamura T, et al. Identification of a fibroblast-derived epithelial morphogen as hepatocyte growth factor. Cell. 1991;67:901-908.
63. Narita T, Saitoh K, Kameda T, et al. BMPs are necessary for stomach gland formation in the chicken embryo: a study using virally induced BMP-2 and Noggin expression. Development. 2000;127: 981-988.
64. Swenson ES, Price JG, Brazelton T, et al. Limitations of green fluorescent protein as a cell lineage marker. Stem Cells 2007;25: 2593-2600.
65. Okabe M, Ikawa M, Kominami K, et al. Green mice' as a source of ubiquitous green cells. FEBS Lett 1997;407:313-319.
66. Fox JG, Blanco M, Murphy JC, et al. Local and systemic immune responses in murine Helicobacter felis active chronic gastritis. Infect Immun 1993;61:2309-2315.