Skip to main content
SpringerLink
Log in

Genetic deficiency of the tumor suppressor protein p53 influences erythrocyte survival

  • Published:
Apoptosis Aims and scope Submit manuscript

Abstract

The transcription factor p53 suppresses tumor growth by inducing nucleated cell apoptosis and cycle arrest. Because of its influence on primitive erythroid cell differentiation and survival, p53 is an important determinant of erythropoiesis. However, the impact of p53 on the fate of erythrocytes, cells lacking nucleus and mitochondria, during their post-maturation phase in the circulation remained elusive. Erythrocyte survival may be compromised by suicidal erythrocyte death or eryptosis, which is hallmarked by phosphatidylserine translocation and stimulated by increase of cytosolic Ca2+ concentration. Here, we comparatively examined erythrocyte homeostasis in p53-mutant mice (Trp53tm1Tyj/J) and in corresponding WT mice (C57BL/6J) by analyzing eryptosis and erythropoiesis. To this end, spontaneous cell membrane phosphatidylserine exposure and cytosolic Ca2+ concentration were higher in erythrocytes drawn from Trp53tm1Tyj/J mice than from WT mice. Eryptosis induced by glucose deprivation, a pathophysiological cell stressor, was slightly, but significantly more prominent in erythrocytes drawn from Trp53tm1Tyj/J mice as compared to WT mice. The loss of erythrocytes by eryptosis was fully compensated by enhanced erythropoiesis in Trp53tm1Tyj/J mice, as reflected by increased reticulocytosis and abundance of erythroid precursor cells in the bone marrow. Accordingly, erythrocyte number, packed cell volume and hemoglobin were similar in Trp53tm1Tyj/J and WT mice. Taken together, functional p53 deficiency enhances the turnover of circulating erythrocytes by parallel increase of eryptosis and stimulated compensatory erythropoiesis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Ferraiuolo M, Di Agostino S, Blandino G, Strano S (2016) Oncogenic intra-p53 family member interactions in human cancers. Front Oncol 6:77

    Article  Google Scholar 

  2. Pant V, Quintas-Cardama A, Lozano G (2012) The p53 pathway in hematopoiesis: lessons from mouse models, implications for humans. Blood 120:5118–5127

    Article  CAS  Google Scholar 

  3. Beckta JM, Ahmad SF, Yang H, Valerie K (2014) Revisiting p53 for cancer-specific chemo- and radiotherapy: ten years after. Cell Cycle 13:710–713

    Article  Google Scholar 

  4. Feng Z, Hu W, Rajagopal G, Levine AJ (2008) The tumor suppressor p53: cancer and aging. Cell Cycle 7:842–847

    Article  CAS  Google Scholar 

  5. Levine AJ (2017) The p53 protein plays a central role in the mechanism of action of epigentic drugs that alter the methylation of cytosine residues in DNA. Oncotarget 8:7228–7230

    Article  Google Scholar 

  6. Kojima K, Ishizawa J, Andreeff M (2016) Pharmacological activation of wild-type p53 in the therapy of leukemia. Exp Hematol 44:791–798

    Article  CAS  Google Scholar 

  7. Napoli M, Flores ER (2017) The p53 family orchestrates the regulation of metabolism: physiological regulation and implications for cancer therapy. Br J Cancer 116:149–155

    Article  CAS  Google Scholar 

  8. Hientz K, Mohr A, Bhakta-Guha D, Efferth T (2017) The role of p53 in cancer drug resistance and targeted chemotherapy. Oncotarget 8:8921–8946

    Article  Google Scholar 

  9. Reinhardt HC, Schumacher B (2012) The p53 network: cellular and systemic DNA damage responses in aging and cancer. Trends Genet 28:128–136

    Article  CAS  Google Scholar 

  10. Chen J (2016) The cell-cycle arrest and apoptotic functions of p53 in tumor initiation and progression. Cold Spring Harb Perspect Med 6:a026104

    Article  Google Scholar 

  11. Kung CP, Murphy ME (2016) The role of the p53 tumor suppressor in metabolism and diabetes. J Endocrinol 231:R61–R75

    Article  CAS  Google Scholar 

  12. Cooks T, Harris CC, Oren M (2014) Caught in the cross fire: p53 in inflammation. Carcinogenesis 35:1680–1690

    Article  CAS  Google Scholar 

  13. Ganguli G, Back J, Sengupta S, Wasylyk B (2002) The p53 tumour suppressor inhibits glucocorticoid-induced proliferation of erythroid progenitors. EMBO Rep 3:569–574

    Article  CAS  Google Scholar 

  14. Vemula S, Shi J, Mali RS, Ma P, Liu Y, Hanneman P, Koehler KR, Hashino E, Wei L, Kapur R (2012) ROCK1 functions as a critical regulator of stress erythropoiesis and survival by regulating p53. Blood 120:2868–2878

    Article  CAS  Google Scholar 

  15. Caceres G, McGraw K, Yip BH, Pellagatti A, Johnson J, Zhang L, Liu K, Zhang LM, Fulp WJ, Lee JH, Al Ali NH, Basiorka A, Smith LJ, Daugherty FJ, Littleton N, Wells RA, Sokol L, Wei S, Komrokji RS, Boultwood J, List AF (2013) TP53 suppression promotes erythropoiesis in del(5q) MDS, suggesting a targeted therapeutic strategy in lenalidomide-resistant patients. Proc Natl Acad Sci USA 110:16127–16132

    Article  CAS  Google Scholar 

  16. Lang E, Qadri SM, Lang F (2012) Killing me softly—suicidal erythrocyte death. Int J Biochem Cell Biol 44:1236–1243

    Article  CAS  Google Scholar 

  17. Lang F, Qadri SM (2012) Mechanisms and significance of eryptosis, the suicidal death of erythrocytes. Blood Purif 33:125–130

    Article  Google Scholar 

  18. Qadri SM, Bissinger R, Solh Z, Oldenborg PA (2017) Eryptosis in health and disease: a paradigm shift towards understanding the (patho)physiological implications of programmed cell death of erythrocytes. Blood Rev 31:349–361

    Article  CAS  Google Scholar 

  19. Pretorius E, du Plooy JN, Bester J (2016) A comprehensive review on eryptosis. Cell Physiol Biochem 39:1977–2000

    Article  CAS  Google Scholar 

  20. Bissinger R, Bhuyan AAM, Qadri SM, Lang F (2018) Oxidative stress, eryptosis and anemia: a pivotal mechanistic nexus in systemic diseases. FEBS J. https://doi.org/10.1111/febs.14606

    Article  PubMed  Google Scholar 

  21. Jacks T, Remington L, Williams BO, Schmitt EM, Halachmi S, Bronson RT, Weinberg RA (1994) Tumor spectrum analysis in p53-mutant mice. Curr Biol 4:1–7

    Article  CAS  Google Scholar 

  22. Bissinger R, Lang E, Ghashghaeinia M, Singh Y, Zelenak C, Fehrenbacher B, Honisch S, Chen H, Fakhri H, Umbach AT, Liu G, Rexhepaj R, Liu G, Schaller M, Mack AF, Lupescu A, Birnbaumer L, Lang F, Qadri SM (2016) Blunted apoptosis of erythrocytes in mice deficient in the heterotrimeric G-protein subunit Gαi2. Sci Rep 6:30925

    Article  CAS  Google Scholar 

  23. Jemaa M, Fezai M, Bissinger R, Lang F (2017) Methods employed in cytofluorometric assessment of eryptosis, the suicidal erythrocyte death. Cell Physiol Biochem 43:431–444

    Article  CAS  Google Scholar 

  24. Lang E, Bissinger R, Fajol A, Salker MS, Singh Y, Zelenak C, Ghashghaeinia M, Gu S, Jilani K, Lupescu A, Reyskens KM, Ackermann TF, Foller M, Schleicher E, Sheffield WP, Arthur JS, Lang F, Qadri SM (2015) Accelerated apoptotic death and in vivo turnover of erythrocytes in mice lacking functional mitogen- and stress-activated kinase MSK1/2. Sci Rep 5:17316

    Article  CAS  Google Scholar 

  25. Sayed Ael D, Watanabe-Asaka T, Oda S, Mitani H (2016) Apoptosis and morphological alterations after UVA irradiation in red blood cells of p53 deficient Japanese medaka (Oryzias latipes). J Photochem Photobiol B 161:1–8

    Article  Google Scholar 

  26. Lang E, Bissinger R, Qadri SM, Lang F (2017) Suicidal death of erythrocytes in cancer and its chemotherapy: a potential target in the treatment of tumor-associated anemia. Int J Cancer 141:1522–1528

    Article  CAS  Google Scholar 

  27. Qadri SM, Mahmud H, Lang E, Gu S, Bobbala D, Zelenak C, Jilani K, Siegfried A, Foller M, Lang F (2012) Enhanced suicidal erythrocyte death in mice carrying a loss-of-function mutation of the adenomatous polyposis coli gene. J Cell Mol Med 16:1085–1093

    Article  CAS  Google Scholar 

  28. Bissinger R, Schumacher C, Qadri SM, Honisch S, Malik A, Gotz F, Kopp HG, Lang F (2016) Enhanced eryptosis contributes to anemia in lung cancer patients. Oncotarget 7:14002–14014

    Article  Google Scholar 

  29. Bissinger R, Artunc F, Qadri SM, Lang F (2016) Reduced erythrocyte survival in uremic patients under hemodialysis or peritoneal dialysis. Kidney Blood Press Res 41:966–977

    Article  CAS  Google Scholar 

  30. Lang E, Gatidis S, Freise NF, Bock H, Kubitz R, Lauermann C, Orth HM, Klindt C, Schuier M, Keitel V, Reich M, Liu G, Schmidt S, Xu HC, Qadri SM, Herebian D, Pandyra AA, Mayatepek E, Gulbins E, Lang F, Haussinger D, Lang KS, Foller M, Lang PA (2015) Conjugated bilirubin triggers anemia by inducing erythrocyte death. Hepatology 61:275–284

    Article  CAS  Google Scholar 

  31. Lang E, Pozdeev VI, Gatidis S, Qadri SM, Haussinger D, Kubitz R, Herebian D, Mayatepek E, Lang F, Lang KS, Lang PA (2016) Bile acid-induced suicidal erythrocyte death. Cell Physiol Biochem 38:1500–1509

    Article  CAS  Google Scholar 

  32. Kempe-Teufel DS, Bissinger R, Qadri SM, Wagner R, Peter A, Lang F (2018) Cellular markers of eryptosis are altered in type 2 diabetes. Clin Chem Lab Med 56:e177–e180. https://doi.org/10.1515/cclm-2017-1058

    Article  CAS  PubMed  Google Scholar 

  33. Bissinger R, Kempe-Teufel DS, Honisch S, Qadri SM, Randrianarisoa E, Haring HU, Henes J, Lang F (2016) Stimulated suicidal erythrocyte death in arteritis. Cell Physiol Biochem 39:1068–1077

    Article  CAS  Google Scholar 

  34. Qadri SM, Donkor DA, Bhakta V, Eltringham-Smith LJ, Dwivedi DJ, Moore JC, Pepler L, Ivetic N, Nazi I, Fox-Robichaud AE, Liaw PC, Sheffield WP (2016) Phosphatidylserine externalization and procoagulant activation of erythrocytes induced by Pseudomonas aeruginosa virulence factor pyocyanin. J Cell Mol Med 20:710–720

    Article  CAS  Google Scholar 

  35. Jiang P, Bian M, Ma W, Liu C, Yang P, Zhu B, Xu Y, Zheng M, Qiao J, Shuai Z, Zhou X, Huang D (2016) Eryptosis as an underlying mechanism in systemic lupus erythematosus-related anemia. Cell Physiol Biochem 40:1391–1400

    Article  CAS  Google Scholar 

  36. Shan F, Yang R, Ji T, Jiao F (2016) Vitamin C inhibits aggravated eryptosis by hydrogen peroxide in glucose-6-phosphated dehydrogenase deficiency. Cell Physiol Biochem 39:1453–1462

    Article  CAS  Google Scholar 

  37. Bartolmas T, Mayer B, Balola AH, Salama A (2017) Eryptosis in autoimmune haemolytic anaemia. Eur J Haematol 100:36–44

    Article  Google Scholar 

  38. Lang E, Jilani K, Bissinger R, Rexhepaj R, Zelenak C, Lupescu A, Lang F, Qadri SM (2015) Vitamin D-rich diet in mice modulates erythrocyte survival. Kidney Blood Press Res 40:403–412

    Article  CAS  Google Scholar 

  39. Lupescu A, Bissinger R, Goebel T, Salker MS, Alzoubi K, Liu G, Chirigiu L, Mack AF, Qadri SM, Lang F (2015) Enhanced suicidal erythrocyte death contributing to anemia in the elderly. Cell Physiol Biochem 36:773–783

    Article  CAS  Google Scholar 

  40. Lang F, Bissinger R, Abed M, Artunc F (2017) Eryptosis—the neglected cause of anemia in end stage renal disease. Kidney Blood Press Res 42:749–760

    Article  CAS  Google Scholar 

  41. Al Mamun Bhuyan A, Bissinger R, Cao H, Lang F (2017) Triggering of suicidal erythrocyte death by exemestane. Cell Physiol Biochem 42:1–12

    Article  CAS  Google Scholar 

  42. Al Mamun Bhuyan A, Cao H, Lang F (2017) Triggering of eryptosis, the suicidal erythrocyte death by mammalian target of rapamycin (mTOR) inhibitor temsirolimus. Cell Physiol Biochem 42:1575–1591

    Article  CAS  Google Scholar 

  43. Al Mamun Bhuyan A, Nguyen MT, Bissinger R, Gotz F, Lang F (2017) Lipopeptide-induced suicidal erythrocyte death correlates with the degree of acylation. Cell Physiol Biochem 41:296–309

    Article  CAS  Google Scholar 

  44. Qadri SM, Donkor DA, Nazy I, Branch DR, Sheffield WP (2018) Bacterial neuraminidase-mediated erythrocyte desialylation provokes cell surface aminophospholipid exposure. Eur J Haematol 100:502–510

    Article  CAS  Google Scholar 

  45. Ghashghaeinia M, Wesseling MC, Ramos E, Petkova-Kirova P, Waibel S, Lang E, Bissinger R, Alzoubi K, Edelmann B, Hosseinzadeh Z, Dreischer P, Shahvaroughi-Farahani A, Mrowietz U, Koberle M, Kaestner L, Bernhardt I, Martinez-Ruiz A, Wieder T, Lang F (2017) Trifluoperazine-induced suicidal erythrocyte death and S-nitrosylation inhibition, reversed by the nitric oxide donor sodium nitroprusside. Cell Physiol Biochem 42:1985–1998

    Article  CAS  Google Scholar 

  46. Signoretto E, Zierle J, Bissinger R, Castagna M, Bossi E, Lang F (2016) Triggering of suicidal erythrocyte death by pazopanib. Cell Physiol Biochem 38:926–938

    Article  CAS  Google Scholar 

  47. Mischitelli M, Jemaaa M, Fezai M, Almasry M, Lang F, Faggio C (2017) Stimulation of erythrocyte cell membrane scrambling by adarotene. Cell Physiol Biochem 41:519–529

    Article  CAS  Google Scholar 

  48. Almasry M, Jemaa M, Mischitelli M, Faggio C, Lang F (2016) Stimulation of suicidal erythrocyte death by phosphatase inhibitor calyculin A. Cell Physiol Biochem 40:163–171

    Article  CAS  Google Scholar 

  49. Jemaa M, Mischitelli M, Fezai M, Almasry M, Faggio C, Lang F (2016) Stimulation of suicidal erythrocyte death by the CDC25 inhibitor NSC-95397. Cell Physiol Biochem 40:597–607

    Article  CAS  Google Scholar 

  50. Mischitelli M, Jemaa M, Almasry M, Faggio C, Lang F (2016) Triggering of erythrocyte cell membrane scrambling by emodin. Cell Physiol Biochem 40:91–103

    Article  CAS  Google Scholar 

  51. Al Mamun Bhuyan A, Wagner T, Cao H, Lang F (2017) Triggering of suicidal erythrocyte death by gefitinib. Cell Physiol Biochem 41:1697–1708

    Article  CAS  Google Scholar 

  52. Al Mamun Bhuyan A, Signoretto E, Bissinger R, Lang F (2016) Enhanced eryptosis following exposure to dolutegravir. Cell Physiol Biochem 39:639–650

    Article  CAS  Google Scholar 

  53. Lupescu A, Shaik N, Jilani K, Zelenak C, Lang E, Pasham V, Zbidah M, Plate A, Bitzer M, Foller M, Qadri SM, Lang F (2012) Enhanced erythrocyte membrane exposure of phosphatidylserine following sorafenib treatment: an in vivo and in vitro study. Cell Physiol Biochem 30:876–888

    Article  CAS  Google Scholar 

  54. Lang E, Pozdeev VI, Xu HC, Shinde PV, Behnke K, Hamdam JM, Lehnert E, Scharf RE, Lang F, Haussinger D, Lang KS, Lang PA (2016) Storage of erythrocytes induces suicidal erythrocyte death. Cell Physiol Biochem 39:668–676

    Article  CAS  Google Scholar 

  55. Qadri SM, Chen D, Schubert P, Devine DV, Sheffield WP (2017) Early gamma-irradiation and subsequent storage of red cells in SAG-M additive solution potentiate energy imbalance, microvesiculation and susceptibility to stress-induced apoptotic cell death. Vox Sang 112:480–483

    Article  CAS  Google Scholar 

  56. Qadri SM, Chen D, Schubert P, Perruzza DL, Bhakta V, Devine DV, Sheffield WP (2017) Pathogen inactivation by riboflavin and ultraviolet light illumination accelerates the red blood cell storage lesion and promotes eryptosis. Transfusion 57:661–673

    Article  CAS  Google Scholar 

  57. Zelenak C, Foller M, Velic A, Krug K, Qadri SM, Viollet B, Lang F, Macek B (2011) Proteome analysis of erythrocytes lacking AMP-activated protein kinase reveals a role of PAK2 kinase in eryptosis. J Proteome Res 10:1690–1697

    Article  CAS  Google Scholar 

  58. Gatidis S, Zelenak C, Fajol A, Lang E, Jilani K, Michael D, Qadri SM, Lang F (2011) p38 MAPK activation and function following osmotic shock of erythrocytes. Cell Physiol Biochem 28:1279–1286

    Article  CAS  Google Scholar 

  59. Zelenak C, Eberhard M, Jilani K, Qadri SM, Macek B, Lang F (2012) Protein kinase CK1α regulates erythrocyte survival. Cell Physiol Biochem 29:171–180

    Article  CAS  Google Scholar 

  60. Kucherenko Y, Zelenak C, Eberhard M, Qadri SM, Lang F (2012) Effect of casein kinase 1α activator pyrvinium pamoate on erythrocyte ion channels. Cell Physiol Biochem 30:407–417

    Article  CAS  Google Scholar 

  61. Lang E, Zelenak C, Eberhard M, Bissinger R, Rotte A, Ghashghaeinia M, Lupescu A, Lang F, Qadri SM (2015) Impact of cyclin-dependent kinase CDK4 inhibition on eryptosis. Cell Physiol Biochem 37:1178–1186

    Article  CAS  Google Scholar 

  62. Qadri SM, Bauer J, Zelenak C, Mahmud H, Kucherenko Y, Lee SH, Ferlinz K, Lang F (2011) Sphingosine but not sphingosine-1-phosphate stimulates suicidal erythrocyte death. Cell Physiol Biochem 28:339–346

    Article  CAS  Google Scholar 

  63. Lang E, Lang PA, Shumilina E, Qadri SM, Kucherenko Y, Kempe DS, Foller M, Capasso A, Wieder T, Gulbins E, Clemen CS, Herr C, Noegel AA, Huber SM, Lang F (2010) Enhanced eryptosis of erythrocytes from gene-targeted mice lacking annexin A7. Pflugers Arch 460:667–676

    Article  CAS  Google Scholar 

  64. Borst O, Abed M, Alesutan I, Towhid ST, Qadri SM, Foller M, Gawaz M, Lang F (2012) Dynamic adhesion of eryptotic erythrocytes to endothelial cells via CXCL16/SR-PSOX. Am J Physiol Cell Physiol 302:C644–C651

    Article  CAS  Google Scholar 

  65. Larsson A, Hult A, Nilsson A, Olsson M, Oldenborg PA (2016) Red blood cells with elevated cytoplasmic Ca(2+) are primarily taken up by splenic marginal zone macrophages and CD207 + dendritic cells. Transfusion 56:1834–1844

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors thank Prof. Lars Zender, Dr. Tae-Won Kang and their laboratory members (Department of Vegetative & Clinical Physiology, University of Tübingen, Germany) for their valuable suggestions and for providing samples from Trp53tm1Tyj/J mice. The study was supported by the Deutsche Forschungsgemeinschaft (DFG) to FL, EU Systems Biology to Identify Molecular Targets for Vascular Disease Treatment (SysVasc), HEALTH-2013 603288 to LP, and the Open Access Publishing Fund of the University of Tuebingen. Work of RB is supported by the Institutional Strategy of the University of Tuebingen (Deutsche Forschungsgemeinschaft, ZUK63). SMQ was supported by resources from Canadian Blood Services. As a condition of Canadian government funding, this report must contain the statement, “The views expressed herein do not necessarily represent the view of the federal government of Canada.”

Author information

Author notes

  1. Syed M. Qadri and Florian Lang have contributed equally and thus share the corresponding authorship.

Authors and Affiliations

  1. Department of Internal Medicine III, Eberhard-Karls University Tübingen, Tübingen, Germany

    Rosi Bissinger & Florian Lang

  2. Department of Molecular Medicine II, Heinrich-Heine University, Düsseldorf, Germany

    Elisabeth Lang & Florian Lang

  3. Institute of Pathology and Neuropathology, Eberhard-Karls University Tübingen, Tübingen, Germany

    Irene Gonzalez-Menendez & Leticia Quintanilla-Martinez

  4. Comprehensive Cancer Center, University Hospital Tübingen, Tübingen, Germany

    Irene Gonzalez-Menendez & Leticia Quintanilla-Martinez

  5. Psoriasis Center, Department of Dermatology, University Medical Center Schleswig-Holstein, Campus Kiel, Kiel, Germany

    Mehrdad Ghashghaeinia

  6. Department of Vegetative & Clinical Physiology, Institute of Physiology, Eberhard Karls University Tübingen, Wilhelmstraße 56, 72074, Tübingen, Germany

    Mehrdad Ghashghaeinia, Lisann Pelzl, Basma Sukkar, Abdulla Al Mamun Bhuyan, Hajar Fakhri, Anja T. Umbach & Florian Lang

  7. Research Institute for Women’s Health, University Hospital Tübingen, Tübingen, Germany

    Madhuri S. Salker

  8. Institute of Medical Genetics and Applied Genomics, Eberhard-Karls University Tübingen, Tübingen, Germany

    Yogesh Singh

  9. Department of Dermatology, Eberhard-Karls University Tübingen, Tübingen, Germany

    Birgit Fehrenbacher & Martin Schaller

  10. Department of Pathology and Molecular Medicine, McMaster University, 1280 Main Street West, Hamilton, ON, L8S 4K1, Canada

    Syed M. Qadri

  11. Centre for Innovation, Canadian Blood Services, Hamilton, ON, Canada

    Syed M. Qadri

Authors
  1. Rosi Bissinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elisabeth Lang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Irene Gonzalez-Menendez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Leticia Quintanilla-Martinez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mehrdad Ghashghaeinia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Lisann Pelzl
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Basma Sukkar
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Abdulla Al Mamun Bhuyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Madhuri S. Salker
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yogesh Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Birgit Fehrenbacher
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Hajar Fakhri
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Anja T. Umbach
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Martin Schaller
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Syed M. Qadri
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Florian Lang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Syed M. Qadri or Florian Lang.

Ethics declarations

Conflict of interest

The authors declare no potential conflicts of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bissinger, R., Lang, E., Gonzalez-Menendez, I. et al. Genetic deficiency of the tumor suppressor protein p53 influences erythrocyte survival. Apoptosis 23, 641–650 (2018). https://doi.org/10.1007/s10495-018-1481-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10495-018-1481-8

Keywords

Search

Navigation