DOI: 10.1182/blood.v100.10.3553. Characterization of gene expression of CD34+ cells from normal and myelodysplastic bone marrow

Characterization of gene expression of CD34+ cells from normal and myelodysplastic bone marrow

10.1182/blood.v100.10.3553

Crossref journal-article

American Society of Hematology

Blood (234)

Abstract

Gene patterns of expression in purified CD34+ bone marrow cells from 7 patients with low-risk myelodysplastic syndrome (MDS) and 4 patients with high-risk MDS were compared with expression data from CD34+ bone marrow cells from 4 healthy control subjects. CD34+ cells were isolated by magnetic cell separation, and high-density oligonucleotide microarray analysis was performed. For confirmation, the expression of selected genes was analyzed by real-time polymerase chain reaction. Class membership prediction analysis selected 11 genes. Using the expression profile of these genes, we were able to discriminate patients with low-risk from patients with high-risk MDS and both patient groups from the control group by hierarchical clustering (Spearman confidence). The power of these 11 genes was verified by applying the algorithm to an unknown test set containing expression data from 8 additional patients with MDS (3 at low risk, 5 at high risk). Patients at low risk could be distinguished from those at high risk by clustering analysis. In low-risk MDS, we found that the retinoic-acid–induced gene (RAI3), the radiation-inducible, immediate-early response gene (IEX1), and the stress-induced phosphoprotein 1 (STIP1) were down-regulated. These data suggest that CD34+cells from patients with low-risk MDS lack defensive proteins, resulting in their susceptibility to cell damage. In summary, we propose that gene expression profiling may have clinical relevance for risk evaluation in MDS at the time of initial diagnosis. Furthermore, this study provides evidence that in MDS, hematopoietic stem cells accumulate defects that prevent normal hematopoiesis.

Bibliography

Hofmann, W.-K., de Vos, S., Komor, M., Hoelzer, D., Wachsman, W., & Koeffler, H. P. (2002). Characterization of gene expression of CD34+ cells from normal and myelodysplastic bone marrow. Blood, 100(10), 3553â3560.

Authors 6

Wolf-K. Hofmann (first)
Sven de Vos (additional)
Martina Komor (additional)
Dieter Hoelzer (additional)
William Wachsman (additional)
H. Phillip Koeffler (additional)

References 31 Referenced 192

10.1182/blood.V96.12.3932 / Blood. / The role of apoptosis, proliferation, and the Bcl-2–related proteins in the myelodysplastic syndromes and acute myeloid leukemia secondary to MDS. by Parker (2000)
10.1016/S0301-472X(98)00077-0 / Exp Hematol. / Characterization of defective megakaryocytic development in patients with myelodysplastic syndromes. by Hofmann (1999)
10.1016/S0301-472X(00)00527-0 / Exp Hematol. / Alteration of c-mpl–mediated signal transduction in CD34(+) cells from patients with myelodysplastic syndromes. by Kalina (2000)
10.1038/sj.leu.2402211 / Leukemia. / P15INK4B gene methylation and expression in normal, myelodysplastic, and acute myelogenous leukemia cells and in the marrow cells of cured lymphoma patients. by Preisler (2001)
10.1182/blood.V89.6.2079 / Blood. / International scoring system for evaluating prognosis in myelodysplastic syndromes. by Greenberg (1997)
{'key': '2019111900193297300_B6', 'first-page': '131', 'article-title': 'World Health Organization classification of the acute leukemias and myelodysplastic syndrome.', 'volume': '72', 'author': 'Bennett', 'year': '2000', 'journal-title': 'Int J Hematol.'} / Int J Hematol. / World Health Organization classification of the acute leukemias and myelodysplastic syndrome. by Bennett (2000)
10.1073/pnas.97.6.2680 / Proc Natl Acad Sci U S A. / Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis. by Voehringer (2000)
10.1109/TIT.1967.1053964 / IEEE Trans Information Theory. / Nearest neighbor pattern classification. by Cover (1967)
10.1126/science.286.5439.531 / Science. / Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. by Golub (1999)
10.1056/NEJM200102223440801 / N Engl J Med. / Gene-expression profiles in hereditary breast cancer. by Hedenfalk (2001)
10.1182/blood.V98.3.787 / Blood. / Altered apoptosis pathways in mantle cell lymphoma detected by oligonucleotide microarray. by Hofmann (2001)
{'key': '2019111900193297300_B12', 'first-page': '4233', 'article-title': 'Distinct expression patterns of the p53-homologue p73 in malignant and normal hematopoiesis assessed by a novel real-time reverse transcription-polymerase chain reaction assay and protein analysis.', 'volume': '59', 'author': 'Peters', 'year': '1999', 'journal-title': 'Cancer Res.'} / Cancer Res. / Distinct expression patterns of the p53-homologue p73 in malignant and normal hematopoiesis assessed by a novel real-time reverse transcription-polymerase chain reaction assay and protein analysis. by Peters (1999)
10.1677/jme.0.0250169 / J Mol Endocrinol. / Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. by Bustin (2000)
10.1182/blood.V98.2.422 / Blood. / Identification of myelodysplastic syndrome-specific genes by DNA microarray analysis with purified hematopoietic stem cell fraction. by Miyazato (2001)
10.1073/pnas.96.6.2907 / Proc Natl Acad Sci U S A. / Interpreting patterns of gene expression with self-organizing maps: methods and application to hematopoietic differentiation. by Tamayo (1999)
10.1073/pnas.96.23.13264 / Proc Natl Acad Sci U S A. / cDNA microarrays detect activation of a myogenic transcription program by the PAX3-FKHR fusion oncogene. by Khan (1999)
10.1016/S0014-5793(00)01294-1 / FEBS Lett. / Genome microarray analysis of transcriptional activation in multidrug resistance yeast mutants. by DeRisi (2000)
10.1073/pnas.97.4.1778 / Proc Natl Acad Sci U S A. / Global analysis of gene expression in pulmonary fibrosis reveals distinct programs regulating lung inflammation and fibrosis. by Kaminski (2000)
10.1182/blood.V98.3.771 / Blood. / Identifying intercellular signaling genes expressed in malignant plasma cells by using complementary DNA arrays. by De Vos (2001)
10.1073/pnas.111144898 / Proc Natl Acad Sci U S A. / Analysis of gene expression during myc oncogene-induced lymphomagenesis in the bursa of Fabricius. by Neiman (2001)
10.1182/blood.V98.6.1914 / Blood. / Transcription patterning of uncoupled proliferation and differentiation in myelodysplastic bone marrow with erythroid-focused arrays. by Lee (2001)
10.1101/gad.14.8.981 / Genes Dev. / Analysis of p53-regulated gene expression patterns using oligonucleotide arrays. by Zhao (2000)
10.1073/pnas.091062498 / Proc Natl Acad Sci U S A. / Significance analysis of microarrays applied to the ionizing radiation response. by Tusher (2001)
10.1073/pnas.111163698 / Proc Natl Acad Sci U S A. / Exploring the DNA-binding specificities of zinc fingers with DNA microarrays. by Bulyk (2001)
10.1046/j.1365-2141.1998.00708.x / Br J Haematol. / Ineffective haemopoiesis and apoptosis in myelodysplastic syndromes. by Parker (1998)
10.1182/blood.V96.4.1388 / Blood. / Intramedullary apoptosis of hematopoietic cells in myelodysplastic syndrome patients can be massive: apoptotic cells recovered from high-density fraction of bone marrow aspirates. by Shetty (2000)
10.1016/S0301-472X(00)00489-6 / Exp Hematol. / Increased apoptosis of bone marrow cells and preserved proliferative capacity of selected progenitors predict for clinical response to anti-inflammatory therapy in myelodysplastic syndromes. by Novitzky (2000)
{'key': '2019111900193297300_B28', 'first-page': '1498', 'article-title': 'Identification and characterization of a radiation-inducible glycosylated human early-response gene.', 'volume': '56', 'author': 'Kondratyev', 'year': '1996', 'journal-title': 'Cancer Res.'} / Cancer Res. / Identification and characterization of a radiation-inducible glycosylated human early-response gene. by Kondratyev (1996)
10.1038/sj.leu.2400844 / Leukemia. / Overexpression of tumor necrosis factor (TNF)-alpha and interferon (IFN)-gamma by bone marrow cells from patients with myelodysplastic syndromes. by Kitagawa (1997)
10.1126/science.281.5379.998 / Science. / IEX-1L, an apoptosis inhibitor involved in NF-κB–mediated cell survival. by Wu (1998)
10.1101/gad.14.16.1997 / Genes Dev. / The Dlk1 and Gtl2 genes are linked and reciprocally imprinted. by Schmidt (2000)

Dates

Type	When
Created	22 years, 9 months ago (Oct. 30, 2002, 2:43 p.m.)
Deposited	2 years, 4 months ago (April 25, 2023, 1:15 a.m.)
Indexed	11 months, 3 weeks ago (Sept. 5, 2024, 10 a.m.)
Issued	22 years, 9 months ago (Nov. 15, 2002)
Published	22 years, 9 months ago (Nov. 15, 2002)
Published Print	22 years, 9 months ago (Nov. 15, 2002)

Funders 0

None

BibTeX

@article{Hofmann_2002, title={Characterization of gene expression of CD34+ cells from normal and myelodysplastic bone marrow}, volume={100}, ISSN={0006-4971}, url={http://dx.doi.org/10.1182/blood.v100.10.3553}, DOI={10.1182/blood.v100.10.3553}, number={10}, journal={Blood}, publisher={American Society of Hematology}, author={Hofmann, Wolf-K. and de Vos, Sven and Komor, Martina and Hoelzer, Dieter and Wachsman, William and Koeffler, H. Phillip}, year={2002}, month=nov, pages={3553–3560} }

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      "author": "Preisler",
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      "author": "Peters",
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      "volume": "96",
      "author": "Khan",
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      "volume": "470",
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      "year": "2000",
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      "author": "Kaminski",
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