Difference in gene expression between human fetal liver and adult bone marrow mesenchymal stem cells

Haematologica

Volumn 90, Issue 8, 2005, Pages 1017-1026

  Götherström, Cecilia ^a   West, Anne ^b   Liden, Johan ^c   Uzunel, Mehmet ^a   Lahesmaa, Riitta ^b   Le Blanc, Katarina ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b UNIVERSITY OF TURKU   (Finland)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Fetal stem cells; Gene expression and development; Hematopoiesis; Mesenchymal stem cells

Indexed keywords

DNA; HLA ANTIGEN CLASS 1; HLA ANTIGEN CLASS 2; HLA G ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; VASCULAR CELL ADHESION MOLECULE 1;

ARTICLE; BONE MARROW CELL; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; CELL PROLIFERATION; CHROMATIN STRUCTURE; DNA REPAIR; ENZYME LINKED IMMUNOSORBENT ASSAY; FETUS; FETUS LIVER; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPHENOTYPING; IMMUNOSUPPRESSIVE TREATMENT; MESENCHYMAL STEM CELL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SERIAL ANALYSIS OF GENE EXPRESSION; SMOOTH MUSCLE; TRANSCRIPTION REGULATION; VALIDATION PROCESS;

ADULT; ALGORITHMS; ANTIGENS, CD; BONE MARROW CELLS; DNA PRIMERS; FETUS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GESTATIONAL AGE; HUMANS; MALE; MESODERM; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; STEM CELLS;

EID: 24944494021     PISSN: 03906078     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (78)

1. Haynesworth SE, Goshima J, Goldberg VM, Caplan AI. Characterization or cells with osteogenic potential from human marrow. Bone 1992;13:81-8.
2. Pereira RF, Halford KW, O'Hara MD, Leeper DB, Sokolov BP, Pollard MD, et al. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci USA 1995;92:4857-61.
3. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999;284:143-7.
4. Liechty KW, MacKenzie TC, Shaaban AF, Radu A, Moseley AM, Deans R, et al. Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 2000;6:1282-6.
5. Friedenstein AJ, Deriglasova UF, Kulagina NN, Panasuk AF, Rudakowa SF, Luria EA, 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.
6. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ, et al. Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 2001;7:211-28.
7. Nakahara H, Dennis JE, Bruder SP, Haynesworth SE, Lennon DP, Caplan AI. In vitro differentiation of bone and hypertrophic cartilage from periosteal-derived cells. Exp Cell Res 1991;195:492-503.
8. Nathanson MA. Bone matrix-directed chondrogenesis of muscle in vitro. Clin Orthop Relat Res 1985:142-58.
9. Tremain N, Korkko J, Ibberson D, Kopen GC, DiGirolamo C, Phinney DG. MicroSAGE analysis of 2,353 expressed genes in a single cell-derived colony of undifferentiated human mesenchymal stem cells reveals mRNAs of multiple cell lineages. Stem Cells 2001;19:408-18.
10. D'Ippolito G, Schiller PC, Ricordi C, Roos BA, Howard GA. Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow. J Bone Miner Res 1999;14:1115-22.
11. In't Anker PS, Scherjon SA, Kleijburgvan der Keur C, de Groot-Swings GM, Claas FH, Fibbe WE, et al. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 2004;22:1338-45.
12. Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 2000;109:235-42.
13. Panepucci RA, Siufi JL, Silva WA Jr, Proto-Siquiera R, Neder L, Orellana M, et al. Comparison of gene expression of umbilical cord vein and bone marrow-derived mesenchymal stem cells. Stem Cells 2004;22:1263-78.
14. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM. Identification of mesenchymal stem/ progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001;98:2396-402.
15. Gotherstrom C, Ringden O, Westgren M, Tammik C, Le Blanc K. Immunomodulatory effects of human foetal liver-derived mesenchymal stem cells. Bone Marrow Transplant 2003;32:265-72.
16. in't Anker PS, Noort WA, Scherjon SA, Kleijburg-van der Keur C, Kruisselbrink AB, van Bezooijen RL, et al. Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 2003;88:845-52.
17. Mendes SC, Robin C, Dzierzak E. Mesenchymal progenitor cells localize within hematopoietic sites throughout ontogeny. Development 2005;132:1127-36.
18. +) hematopoietic progenitor cells. J Cell Physiol 2000;184:58-69.
19. Majumdar MK, Thiede MA, Haynesworth SE, Bruder SP, Gerson SL. Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J Hematother Stem Cell Res 2000;9:841-8.
20. Almeida-Porada G, Flake AW, Glimp HA, Zanjani ED. Cotransplantation of stroma results in enhancement of engraftment and early expression of donor hematopoietic stem cells in utero. Exp Hematol 1999;27:1569-75.
21. Almeida-Porada G, Porada CD, Tran N, Zanjani ED. Cotransplantation of human stromal cell progenitors into preimmune fetal sheep results in early appearance of human donor cells in circulation and boosts cell levels in bone marrow at later time points after transplantation. Blood 2000;95:3620-7.
22. Noort WA, Kruisselbrink AB, in't Anker PS, Kruger M, van Bezooijen RL, de Paus RA, et al. Mesenchymal stem cells promote engraftment of human umbilical cord blood-derived CD34(+) cells in NOD/SCID mice. Exp Hematol 2002;30:870-8.
23. +) cells in NOD/SCID mice. Exp Hematol 2003;31:881-9.
24. Maitra B, Szekely E, Gjini K, Laughlin MJ, Dennis J, Haynesworth SE, et al. Human mesenchymal stem cells support unrelated donor hematopoietic stem cells and suppress T-cell activation. Bone Marrow Transplant 2004;33:597-604.
25. Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O. Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 2003;57:11-20.
26. Tse WT, Pendleton JD, Beyer WM, Egalka MC, Guinan EC. Suppression of allogeneic T-cell proliferation by human marrow stromal cells: implications in transplantation. Transplantation 2003;75:389-97.
27. Rasmusson I, Ringden O, Sundberg B, Le Blanc K. Mesenchymal stem cells inhibit the formation of cytotoxic T lymphocytes, but not activated cytotoxic T lymphocytes or natural killer cells. Transplantation 2003;76:1208-13.
28. Le Blanc K, Rasmusson I, Sundberg B, Gotherstrom C, Hassan M, Uzunel M, et al. Treatment of severe acute graft-versus-host disease with third party haploidentical mesenchymal stem cells. Lancet 2004;363:1439-41.
29. Gotherstrom C, Ringden O, Tammik C, Zetterberg E, Westgren M, Le Blanc K. Immunologic properties of human fetal mesenchymal stem cells. Am J Obstet Gynecol 2004;190:239-45.
30. Le Blanc K, Tammik L, Zetterberg E, Ringden O. HLA expression and immunologic properties of differentiated and undifferentiated mesenchymal stem cells. Exp Haematol 2003;31:890-6.
31. Djouad F, Plence P, Bony C, Tropel P, Apparailly F, Sany J, et al. Immunosuppressive effect of mesenchymal stem cells favors tumor growth in allogeneic animals. Blood 2003;102:3837-44.
32. Le Blanc K, Gotherstrom C, Ringdén O, Hassan M, McMahon R, Horwitz E, et al. Fetal mesenchymal stem cell engraftment in bone following in utero transplantation in a patient with severe osteogenesis imperfecta. Transplantation 2005;79:1607-14.
33. Monticone M, Liu Y, Tonachini L, Mastrogiacomo M, Parodi S, Quarto R, et al. Gene expression profile of human bone marrow stromal cells determined by restriction fragment differential display analysis. J Cell Biochem 2004;92:733-44.
34. Doi M, Nagano A, Nakamura Y. Genome-wide screening by cDNA microarray of genes associated with matrix mineralization by human mesenchymal stem cells in vitro. Biochem Biophys Res Commun 2002;290:381-90.
35. Lee RH, Kim B, Choi I, Kim H, Choi HS, Suh K, et al. Characterization and expression analysis of mesenchymal stem cells from human bone marrow and adipose tissue. Cell Physiol Biochem 2004;14:311-24.
36. Silva WA Jr, Covas DT, Panepucci RA, Proto-Siqueira R, Siufi JL, Zanette DL, et al. The profile of gene expression of human marrow mesenchymal stem cells. Stem Cells 2003;21:661-9.
37. Jia L, Young MF, Powell J, Yang L, Ho NC, Hotchkiss R, et al. Gene expression profile of human bone marrow stromal cells: high-throughput expressed sequence tag sequencing analysis. Genomics 2002;79:7-17.
38. Qi H, Aguiar DJ, Williams SM, La Pean A, Pan W, Verfaillie CM. Identification of genes responsible for osteoblast differentiation from human mesodermal Crogenitor cells. Proc Natl Acad Sci USA 2003;100:3305-10.
39. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 2001;98:5116-21.
40. Uzunel M, Ringden O. Poor correlation of kinetics between BCR-ABL and WT1 transcript levels after allogeneic stem cell transplantation. Bone Marrow Transplant 2004;33:47-52.
41. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004;5: R80.
42. Richards M, Tan SP, Tan JH, Chan WK, Bongso A. The transcriptome profile of human embryonic stem cells as defined by SAGE. Stem Cells 2004;22:51-64.
43. Bhattacharya B, Miura T, Brandenberger R, Mejido J, Luo Y, Yang AX, et al. Gene expression in human embryonic stem cell lines: unique molecular signature. Blood 2004;103:2956-64.
44. Zhou G, Wang J, Zhang Y, Zhong C, Ni J, Wang L, et al. Cloning, expression and subcellular localization of HN1 and HN1L genes, as well as characterization of their orthologs, defining an evolutionarily conserved gene family. Gene 2004;331:115-23.
45. Zhao XF, Nowak NJ, Shows TB, Aplan PD. MAGOH interacts with a novel RNA-binding protein. Genomics 2000;63:145-8.
46. Lappin DW, McMahon R, Murphy M, Brady HR. Gremlin: an example of the re-emergence of developmental programmes in diabetic nephropathy. Nephrol Dial Transplant 2002;17 Suppl 9:65-7.
47. Abouzied MM, Baader SL, Dietz F, Kappler J, Gieselmann V, Franken S. Expression patterns and different subcellular localization of the growth factors HDGF (hepatoma-derived growth factor) and HRP-3 (HDGF-related protein-3) suggest functions in addition to their mitogenic activity. Biochem J 2004;378:169-76.
48. Stumpo DJ, Eddy RL, Jr., Haley LL, Sait S, Shows TB, Lai WS, et al. Promoter sequence, expression, and fine chromosomal mapping of the human gene (MLP) encoding the MARCKS-like protein: identification of neighboring and linked polymorphic loci for MLP and MACS and use in the evaluation of human neural tube defects. Genomics 1998;49:253-64.
49. Miano JM, Thomas S, Disteche CM. Expression and chromosomal mapping of the mouse smooth muscle calponin gene. Mamm Genome 2001;12:187-91.
50. Chang DF, Belaguli NS, Iyer D, Roberts WB, Wu SP, Dong XR, et al. Cysteine-rich LIM-only proteins CRP1 and CRP2 are potent smooth muscle differentiation cofactors. Dev Cell 2003;4:107-18.
51. Takahashi H, Asano K, Kinouchi M, Ishida-Yamamoto A, Wuepper KD, Iizuka H. Structure and transcriptional regulation of the human cystatin A gene. The 12-O-tetradecanoylphorbol-13-acetate (TPA) responsive element-2 site (-272 to -278) on cystatin A gene is critical for TPA-dependent regulation. J Biol Chem 1998;270:17375-80.
52. Zeeuwen PL, Dale BA, de Jongh GJ, van Vlijmen-Willems IM, Fleckman P, Kimball JR, et al. The human cystatin M/E gene (CST6): exclusion candidate gene for harlequin ichthyosis. J Invest Dermatol 2003;121:65-8.
53. Qu X, Zhang C, Zhai Y, Xing G, Wei H, Yu Y, et al. Characterization and tissue expression of a novel human gene npdc1. Gene 2001;264:37-44.
54. Akbas GE, Taylor HS. HOXC and HOXD gene expression in human endometrium: lack of redundancy with HOXA paralogs. Biol Reprod 2004-70:39-45.
55. Simons-Evelyn M, Bailey-Dell K, Toretsky JA, Ross DD, Fenton R, Kalvakolanu D, et al. PBK/TOPK is a novel mitotic kinase which is upregulated in Burkitt's lymphoma and other highly proliferative malignant cells. Blood Cells Mol Dis 2001;27:825-9.
56. Raabe EH, Abdurrahman L, Behbehani G, Arceci RJ. An SNF2 factor involved in mammalian development and cellular proliferation. Dev Dyn 2001;221:92-105.
57. Okabe H, Satoh S, Furukawa Y, Kato T, Hasegawa S, Nakajima Y, et al. Involvement of PEG10 in human hepatocellular carcinogenesis through interaction with SIAH1. Cancer Res 2003;63:3043-8.
58. Davenport JW, Fernandes ER, Harris LD, Neale GA, Goorha R. The mouse mitotic checkpoint gene bub1b, a novel bub1 family member, is expressed in a cell cycle-dependent manner. Genomics 1999;55:113-7.
59. Moncrieff CL, Bailey ME, Morrison N, Johnson KJ. Cloning and chromosomal localization of human Cdc42-binding protein kinase β. Genomics 1999;57:297-300.
60. rd, Drubin DG, Barnes G. Architecture of the budding yeast kinetochore reveals a conserved molecular core. J Cell Biol 2003;163:215-22.
61. Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, Bonner W. Histone H2A variants H2AX and H2AZ. Curr Opin Genet Dev 2002;12:162-9.
62. McDonald WH, Pavlova Y, Yates JR, 3rd, Boddy MN. Novel essential DNA repair proteins Nse1 and Nse2 are subunits of the fission yeast Smc5-Smc6 complex. J Biol Chem 2003;278:45460.
63. Kimura K, Cuvier O, Hirano T. Chromosome condensation by a human condensin complex in Xenopus egg extracts. J Biol Chem 2001;276:5417-20.
64. Tresini M, Pignolo RJ, Allen RG, Cristofalo VJ. Effects of donor age on the expression of a marker of replicative senescence (EPC-1) in human dermal fibroblasts. J Cell Physiol 1999;179:11-7.
65. Di Bacco A, Gill G. The secreted glycoprotein CREG inhibits cell growth dependent on the mannose-6-phosphate/insulin-like growth factor II receptor. Oncogene 2003;22:5436-45.
66. Grellier P, Yee D, Gonzalez M, Abboud SL. Characterization of insulin-like growth factor binding proteins (IGFBP) and regulation of IGFBP-4 in bone marrow row stromal cells. Br J Haematol 1995;90:249-57.
67. Nagy B, Lundan T, Larramendy ML, Aalto Y, Zhu Y, Niini T, et al. Abnormal expression of apoptosis-related genes in haematological malignancies: overexpression of MYC is poor prognostic sign in mantle cell lymphoma. Br J Haematol 2003;120:434-41.
68. Valverde P, Obin MS, Taylor A. Role of Gas6/Axl signaling in lens epithelial cell proliferation and survival. Exp Eye Res 1 2004;78:27-37.
69. Shirane M, Nakayama KI. Inherent calcineurin inhibitor FKBP38 targets Bcl-2 to mitochondria and inhibits apoptosis. Nat Cell Biol 2003;5:28-37.
70. Llano M, Lee N, Navarro F, Garcia P, Albar JP, Geraghty DE, et al. HLA-E-bound peptides influence recognition by inhibitory and triggering CD94/NKG2 receptors: preferential response to an HLA-G-derived nonamer. Eur J Immunol 1998;28:2854-63.
71. Le Bouteiller P, Blaschitz A. The functionality of HLA-G is emerging. Immunol Rev 1999;167:233-44.
72. De Ugarte DA, Morizono K, Elbarbary A, Alfonso Z, Zuk PA, Zhu M, et al. Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 2003;174:101-9.
73. van de Stolpe A, van der Saag PT. Intercellular adhesion molecule-1. J Mol Med 1996;74:13-33.
74. Chirathaworn C, Kohlmeier JE, Tibbetts SA, Rumsey LM, Chan MA, Benedict SH. Stimulation through intercellular adhesion molecule-1 provides a second signal for T cell activation. J Immunol 2002;168:5530-7.
75. Funk PE, Kincade PW, Witte PL. Native associations of early hematopoietic stem cells and stromal cells isolated in bone marrow cell aggregates. Blood 1994;83:361-9.
76. + hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J Exp Med 1997;185:111-20.
77. Wynn RF, Hart CA, Corradi-Perini C, O'Neill L, Evans CA, Wraith JE, et al. A small proportion of mesenchymal stem cells strongly expresses functionally active CXCR4 receptor capable of promoting migration to bone marrow. Blood 2004;104:2643-5.
78. Rasmusson I, Ringden O, Sundberg B, Le Blanc K. Mesenchymal stem cells inhibit lymphocyte proliferation by mitogens and alloantigens by different mechanisms. Exp Cell Res 2005;305:33-41.