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MYELODYSPLASTIC NEOPLASM

CAR virus receptor mediates erythroid differentiation and migration and is downregulated in MDS

Leukemia volume 37, pages 2250–2260 (2023)Cite this article

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Abstract

Myelodysplastic syndromes (MDS) are myeloid neoplasms presenting with dysplasia in the bone marrow (BM) and peripheral cytopenia. In most patients anemia develops. We screened for genes that are expressed abnormally in erythroid progenitor cells (EP) and contribute to the pathogenesis of MDS. We found that the Coxsackie-Adenovirus receptor (CAR = CXADR) is markedly downregulated in CD45low/CD105+ EP in MDS patients compared to control EP. Correspondingly, the erythroblast cell lines HEL, K562, and KU812 stained negative for CAR. Lentiviral transduction of the full-length CXADR gene into these cells resulted in an increased expression of early erythroid antigens, including CD36, CD71, and glycophorin A. In addition, CXADR-transduction resulted in an increased migration against a serum protein gradient, whereas truncated CXADR variants did not induce expression of erythroid antigens or migration. Furthermore, conditional knock-out of Cxadr in C57BL/6 mice resulted in anemia and erythroid dysplasia. Finally, decreased CAR expression on EP was found to correlate with high-risk MDS and decreased survival. Together, CAR is a functionally relevant marker that is down-regulated on EP in MDS and is of prognostic significance. Decreased CAR expression may contribute to the maturation defect and altered migration of EP and thus their pathologic accumulation in the BM in MDS.

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Fig. 1: mRNA expression profiles of EP in MDS compared to EP of patients with reactive anemia and schematic presentation of the marker profile of human erythropoiesis.
Fig. 2: Expression of CAR on EP of MDS patients.
Fig. 3: Effect of CXADR transduction on expression of erythroid differentiation antigens in HEL cells, K562 cells and KU812 cells.
Fig. 4: Effects of CXADR transduction on migration of erythroid progenitor cells.
Fig. 5: Conditional knock out of Cxadr in C57BL/6 mice results in anemia and a MDS-like phenotype.

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Acknowledgements

We like to thank Nadine Witzeneder, Barbara Peter, Martin Danzer, Harald Herrmann, and Hans-Ulrich Klein for their skillful technical assistance.

Funding

This study was supported by The Austrian Science Fund (FWF) SFB grants F4701-B20, F4704-B20, P30625-B28, by a grant of the Upper Austrian Cancer Aid Fund and by a stem cell grant of the Medical University of Vienna, Austria.

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Author notes

  1. These authors contributed equally: Karin Bauer, Sigrid Machherndl-Spandl, Lukas Kazianka.

Authors and Affiliations

  1. Department of Internal Medicine I, Division of Hematology and Hemostaseology, Medical University of Vienna, Vienna, Austria

    Karin Bauer, Lukas Kazianka, Irina Sadovnik, Sinan Gültekin, Gregor Eisenwort, Ann-Sofie Schmolke, Emiel van der Kouwe, Wolfgang R. Sperr, Philipp B. Staber & Peter Valent

  2. Ludwig Boltzmann Institute for Hematology and Oncology, Medical University of Vienna, Vienna, Austria

    Karin Bauer, Irina Sadovnik, Gregor Hoermann, Gregor Eisenwort, Wolfgang R. Sperr, Philipp B. Staber & Peter Valent

  3. Department of Internal Medicine I, Ordensklinikum, Linz, Austria

    Sigrid Machherndl-Spandl & Ansgar Weltermann

  4. Medical Faculty, Johannes Kepler University, Linz, Austria

    Sigrid Machherndl-Spandl & Johannes Proell

  5. Department of Molecular Biology, Transfusion Service of Upper Austria, Linz, Austria

    Johannes Proell & Christian Gabriel

  6. Labor Europaplatz, Linz, Austria

    Jeroen Lauf & Peter Bettelheim

  7. MLL Munich Leukemia Laboratory, Munich, Germany

    Gregor Hoermann

  8. Department of Gynaecology and Obstetrics, Jena University Hospital, Jena, Germany

    Norman Häfner

  9. Laboratory for Molecular and Genetic Diagnostics, Ordensklinikum, Linz, Austria

    Mathilde Födermayr-Mayrleitner, Otto Zach, Gerald Webersinke & Peter Bettelheim

  10. Division of Hematology, University of Dresden, Dresden, Germany

    Uwe Platzbecker

  11. Medical Clinic and Polyclinic I, Hematology and Cellular Therapy, University Hospital Leipzig, Leipzig, Germany

    Uwe Platzbecker

  12. Children´s Cancer Research Institute Vienna und Department of Pediatrics, Medical University of Vienna, Vienna, Austria

    Thomas Lion

  13. Department of Hematology, Oncology and Clinical Immunology, Medical University of Düsseldorf, Düsseldorf, Germany

    Ulrich Germing

  14. Hematology Laboratory, CHU de Nantes, Nantes, France

    Marie C. Béné

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  1. Karin Bauer
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Contributions

KB and SMS designed the study and performed key laboratory experiments. LK, SG, AS and EK performed mouse experiments. WRS provided patients and statistical analyses. HUK contributed bioinformatics. SS, MD, and JP performed molecular and gene array studies. JL performed flow cytometry experiments. GE and IS performed transduction- and cell sorting experiments. GH provided laboratory data and molecular studies. NH provided modified pBK-CMV vectors containing different CXADR splice variants. MCB, UP, OZ, and AW contributed patients and logistic support. CG and GW performed molecular studies and provided logistic support. TL performed the adenovirus peptide-binding assay. UG contributed patients and logistic support. PV, PBS and PB designed the study and wrote the manuscript. All authors contributed by writing parts of the manuscript and by critically reading the paper. All authors approved the final version of the document.

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Correspondence to Peter Valent.

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Competing interests

The authors declare no completing interests in this study. Conflict of interest outside the study are: P.V. received research grants from Celgene, Novartis, Incyte, Pfizer, and AOP Orphan, and honoraria from Celgene, Novartis, Pfizer, Incyte, and AOP Orphan. S.M.S received honoraria from Celgene, Novartis, Pfizer, Abbvie, Amgen, Jazz, Gilead, Servier and Incyte. P.B. was supported by Alexion outside the study. T.L. received research grants from Incyte and Novartis, and honoraria from Incyte, Pfizer, Angelini, Amgen and Chimerix. O.Z. was supported by Pfizer, Takeda, Amgen, Novartis, BMS, Genzyme, Sanofi, Pierre Fabre and Roche, and he is part of advisory boards of Amgen, Pfizer and Novartis. U.G. received research support from Novartis and Celgene, and honoraria from Celgene, Jazz, Novartis and Jansen. G.W. received research grants from Abbvie, Amgen, AstraZeneca, BMS, Böhringer Ingelheim, Gilead, Incyte, Lilly, Mundipharma, Novartis, Pfizer, Roche and Tesaro. G.H. received research grants from Novartis, he received honoraria and he is part of advisory boards of Novartis, Roche, Beckman Coulter, Pfizer, Celgene, Bristol-Myers Squibb. L.K. was supported by a DOCmed Fellowship of the Austrian Academy of Sciences (OeAW) and a research grant of the Vienna Comprehensive Cancer Center (CCC). P.B.S. reports grants and personal fees from Roche, Celgene, and AbbVie; and personal fees from Amgen, Takeda, AbbVie, and Janssen Cilag outside the submitted work.The other authors declare that they have no conflicts of interest.

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Bauer, K., Machherndl-Spandl, S., Kazianka, L. et al. CAR virus receptor mediates erythroid differentiation and migration and is downregulated in MDS. Leukemia 37, 2250–2260 (2023). https://doi.org/10.1038/s41375-023-02015-7

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