Synergistic Effect of Human Chorionic Gonadotropin and Granulocyte Colony Stimulating Factor in the Mobilization of HSPCs Improves Overall Survival After PBSCT in a Preclinical Murine Model. Are We Far Enough for Therapy?
HCG
HSPCs
Hematopoiesis
MSCs
PBSCT
Journal
Stem cell reviews and reports
ISSN: 2629-3277
Titre abrégé: Stem Cell Rev Rep
Pays: United States
ID NLM: 101752767
Informations de publication
Date de publication:
03 Nov 2023
03 Nov 2023
Historique:
accepted:
19
10
2023
medline:
3
11
2023
pubmed:
3
11
2023
entrez:
3
11
2023
Statut:
aheadofprint
Résumé
Strategies to improve hematopoietic stem and progenitor cell (HSPC) mobilization from the bone marrow can have a pivotal role in addressing iatrogenic bone-marrow insufficiency from chemo(radio)therapy and overcoming peripheral blood stem cell transplantation (PBSCT) limitations such as insufficient mobilization. Granulocyte-colony stimulating factor (G-CSF) represents the standard mobilization strategy for HSPC and has done so for more than three decades since its FDA approval. Its association with non-G-CSF agents is often employed for difficult HSPC mobilization. However, obtaining a synergistic effect between the two classes is limited by different timing and mechanisms of action. Based on our previous in vitro results, we tested the mobilization potential of human chorionic gonadotropin (HCG), alone and in combination with G-CSF in vivo in a murine study. Our results show an improved mobilization capability of the combination, which seems to act synergistically in stimulating hematopoiesis. With the current understanding of the dynamics of HSPCs and their origins in more primitive cells related to the germline, new strategies to employ the mobilization of hematopoietic progenitors using chorionic gonadotropins could soon become clinical practice.
Identifiants
pubmed: 37922107
doi: 10.1007/s12015-023-10648-5
pii: 10.1007/s12015-023-10648-5
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Unitatea Executiva pentru Finantarea Invatamantului Superior, a Cercetarii, Dezvoltarii si Inovarii
ID : PN-III-P1-1.1-PD-2019-1095
Organisme : Unitatea Executiva pentru Finantarea Invatamantului Superior, a Cercetarii, Dezvoltarii si Inovarii
ID : PD 202 ⁄ 2020
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Jagannathan-Bogdan, M., & Zon, L. I. (2013). Hematopoiesis. Development, 140, 2463. https://doi.org/10.1242/DEV.083147
doi: 10.1242/DEV.083147
pubmed: 23715539
pmcid: 3666375
Kim, C. H. (2010). Homeostatic and pathogenic extramedullary hematopoiesis. Journal of Blood Medicine, 1, 13. https://doi.org/10.2147/JBM.S7224
doi: 10.2147/JBM.S7224
pubmed: 22282679
pmcid: 3262334
Crawford, J., Caserta, C., Roila, F. (2010). Hematopoietic growth factors: ESMO clinical practice guidelines for the applications. Annals of Oncology, 21(Suppl 5). https://doi.org/10.1093/ANNONC/MDQ195
Snowden, J. A., Sánchez-Ortega, I., Corbacioglu, S., et al. (2022). Indications for haematopoietic cell transplantation for haematological diseases, solid tumours and immune disorders: Current practice in Europe, 2022. Bone Marrow Transplantation, 57, 1217. https://doi.org/10.1038/S41409-022-01691-W
doi: 10.1038/S41409-022-01691-W
pubmed: 35589997
pmcid: 9119216
Wuchter, P., Ran, D., Bruckner, T., et al. (2010). Poor mobilization of hematopoietic stem cells-definitions, incidence, risk factors, and impact on outcome of autologous transplantation. Biology of Blood and Marrow Transplantation, 16, 490–499. https://doi.org/10.1016/J.BBMT.2009.11.012
doi: 10.1016/J.BBMT.2009.11.012
pubmed: 19925876
Menendez-Gonzalez, J. B., & Hoggatt, J. (2021). Hematopoietic stem cell mobilization: current collection approaches, stem cell heterogeneity, and a proposed new method for stem cell transplant conditioning. Stem Cell Reviews and Reports, 176(17), 1939–1953. https://doi.org/10.1007/S12015-021-10272-1
doi: 10.1007/S12015-021-10272-1
Hoggatt, J., & Pelus, L. M. (2012). Hematopoietic stem cell mobilization with agents other than G-CSF. Methods in Molecular Biology, 904, 49–67. https://doi.org/10.1007/978-1-61779-943-3_4/COVER
doi: 10.1007/978-1-61779-943-3_4/COVER
pubmed: 22890921
Van Overstraeten-Schlögel, N., Beguin, Y., & Gothot, A. (2006). Role of stromal-derived factor-1 in the hematopoietic-supporting activity of human mesenchymal stem cells. European Journal of Haematology, 76, 488–493. https://doi.org/10.1111/J.1600-0609.2006.00633.X
doi: 10.1111/J.1600-0609.2006.00633.X
pubmed: 16494621
Fajardo-Orduña, G. R., Mayani, H., & Montesinos, J. J. (2015). Hematopoietic support capacity of mesenchymal stem cells: biology and clinical potential. Archives of Medical Research, 46, 589–596. https://doi.org/10.1016/J.ARCMED.2015.10.001
doi: 10.1016/J.ARCMED.2015.10.001
pubmed: 26522615
De Luca, L., Trino, S., Laurenzana, I., et al. (2016). MiRNAs and piRNAs from bone marrow mesenchymal stem cell extracellular vesicles induce cell survival and inhibit cell differentiation of cord blood hematopoietic stem cells: a new insight in transplantation. Oncotarget, 7, 6676–6692. https://doi.org/10.18632/ONCOTARGET.6791
doi: 10.18632/ONCOTARGET.6791
pubmed: 26760763
Aqmasheh, S., Shamsasanjan, K., Akbarzadehlaleh, P., et al. (2017). Effects of mesenchymal stem cell derivatives on hematopoiesis and hematopoietic stem cells. Advanced Pharmaceutical Bulletin, 7, 165. https://doi.org/10.15171/APB.2017.021
doi: 10.15171/APB.2017.021
pubmed: 28761818
pmcid: 5527230
Nancarrow-Lei, R., Mafi, P., Mafi, R., Khan, W. (2017). A systemic review of adult mesenchymal stem cell sources and their multilineage differentiation potential relevant to musculoskeletal tissue repair and regeneration. Current Stem Cell Research & Therapy, 12. https://doi.org/10.2174/1574888X12666170608124303
Rossi, L., Challen, G. A., Sirin, O., et al. (2011). Hematopoietic stem cell characterization and isolation. Methods in Molecular Biology, 750, 47. https://doi.org/10.1007/978-1-61779-145-1_3
doi: 10.1007/978-1-61779-145-1_3
pubmed: 21618082
Saleh, M., Shamsasanjan, K., Movassaghpourakbari, A., et al. (2015). The impact of mesenchymal stem cells on differentiation of hematopoietic stem cells. Advanced Pharmaceutical Bulletin, 5, 299. https://doi.org/10.15171/APB.2015.042
doi: 10.15171/APB.2015.042
pubmed: 26504750
pmcid: 4616896
Abdelbaset-Ismail, A., Suszynska, M., Borkowska, S. J., et al. (2015). Human hematopoietic stem/progenitor cells (HSPCs) and mesenchymal stromal cells (MSCs) express several functional pituitary and gonadal sex hormone receptors - identification of follicle stimulating hormone (FSH) and luteinizing hormone (LH) as new growth factors for HSPCs and MSCs. Blood, 126, 2393–2393. https://doi.org/10.1182/BLOOD.V126.23.2393.2393
doi: 10.1182/BLOOD.V126.23.2393.2393
Shahidi, N. T., Diamond, L. K. (2010). Testosterone-induced remission in aplastic anemia of both acquired and congenital types. 264, 953–967. https://doi.org/10.1056/NEJM196105112641901
Seip, M. (1961). Aplastic anemia treated with anabolic steroids and corticosteroidsl. Acta Paediatrica, 50, 561–564. https://doi.org/10.1111/J.1651-2227.1961.TB08046.X
doi: 10.1111/J.1651-2227.1961.TB08046.X
pubmed: 13910347
Coletta, A., Esposito, L., & Palomby, L. (1961). On several recent therapeutic trends in hypoplastic pancytopenia: Testosterone and anabolic steroids. La Pediatria, 69, 413–421.
pubmed: 13694633
Calado, R. T., & Clé, D. V. (2017). Treatment of inherited bone marrow failure syndromes beyond transplantation. Hematology: the American Society of Hematology Education Program, 2017, 96. https://doi.org/10.1182/ASHEDUCATION-2017.1.96
doi: 10.1182/ASHEDUCATION-2017.1.96
Selleri, C., Catalano, L., De Rosa, G., et al. (1991). Danazol: In vitro effects on human hemopoiesis and in vivo activity in hypoplastic and myelodysplastic disorders. European Journal of Haematology, 47, 197–203. https://doi.org/10.1111/J.1600-0609.1991.TB01555.X
doi: 10.1111/J.1600-0609.1991.TB01555.X
pubmed: 1915803
Nakada, D., Oguro, H., Levi, B. P., et al. (2014). Estrogen increases haematopoietic stem cell self-renewal in females and during pregnancy. Nature, 505, 555. https://doi.org/10.1038/NATURE12932
doi: 10.1038/NATURE12932
pubmed: 24451543
pmcid: 4015622
Maggio, M., Snyder, P. J., Ceda, G. P., et al. (2013). Is the haematopoietic effect of testosterone mediated by erythropoietin? The results of a clinical trial in older men. Andrology, 1, 24–28. https://doi.org/10.1111/J.2047-2927.2012.00009.X
doi: 10.1111/J.2047-2927.2012.00009.X
pubmed: 23258626
Ascoli, M., Fanelli, F., & Segaloff, D. L. (2002). The Lutropin/choriogonadotropin receptor, a 2002 perspective. Endocrine Reviews, 23, 141–174. https://doi.org/10.1210/EDRV.23.2.0462
doi: 10.1210/EDRV.23.2.0462
pubmed: 11943741
Mierzejewska, K., Borkowska, S., Suszynska, E., et al. (2015). Hematopoietic stem/progenitor cells express several functional sex hormone receptors—novel evidence for a potential developmental link between hematopoiesis and primordial germ cells. Stem Cells and Development, 24, 927. https://doi.org/10.1089/SCD.2014.0546
doi: 10.1089/SCD.2014.0546
pubmed: 25607657
pmcid: 4390002
Edgar, R., Mazor, Y., Rinon, A., et al. (2013). LifeMap discovery™: The embryonic development, stem cells, and regenerative medicine research portal. PLoS One, 8, 66629. https://doi.org/10.1371/JOURNAL.PONE.0066629
doi: 10.1371/JOURNAL.PONE.0066629
Tourkova, I. L., Witt, M. R., Li, L., et al. (2015). Follicle stimulating hormone receptor in mesenchymal stem cells integrates effects of glycoprotein reproductive hormones. Annals of the New York Academy of Sciences, 1335, 100–109. https://doi.org/10.1111/NYAS.12502
doi: 10.1111/NYAS.12502
pubmed: 25118101
Ratajczak, M. Z., & Suszynska, M. (2016). Emerging strategies to enhance homing and engraftment of hematopoietic stem cells. Stem Cell Reviews and Reports, 12, 121–128. https://doi.org/10.1007/S12015-015-9625-5/FIGURES/1
doi: 10.1007/S12015-015-9625-5/FIGURES/1
pubmed: 26400757
Rahman, N. A., & Rao, C. V. (2009). Recent progress in luteinizing hormone/human chorionic gonadotrophin hormone research. Molecular Human Reproduction, 15, 703–711. https://doi.org/10.1093/MOLEHR/GAP067
doi: 10.1093/MOLEHR/GAP067
pubmed: 19710244
Handschuh, K., Guibourdenche, J., Tsatsaris, V., et al. (2007). Human chorionic gonadotropin produced by the invasive trophoblast but not the villous trophoblast promotes cell invasion and is down-regulated by peroxisome proliferator-activated receptor-gamma. Endocrinology, 148, 5011–5019. https://doi.org/10.1210/EN.2007-0286
doi: 10.1210/EN.2007-0286
pubmed: 17628005
Canfield, R. E., O’Connor, J. F., Birken, S., et al. (1987). Development of an assay for a biomarker of pregnancy and early fetal loss. Environmental Health Perspectives, 74, 57–66. https://doi.org/10.1289/EHP.877457
doi: 10.1289/EHP.877457
pubmed: 3319556
pmcid: 1474496
Lapthorn, A. J., Harris, D. C., Littlejohn, A., et al. (1994). Crystal structure of human chorionic gonadotropin. Nature, 369, 455–461. https://doi.org/10.1038/369455A0
doi: 10.1038/369455A0
pubmed: 8202136
Lee, J. A., & Ramasamy, R. (2018). Indications for the use of human chorionic gonadotropic hormone for the management of infertility in hypogonadal men. Translational Andrology and Urology, 7, S348. https://doi.org/10.21037/TAU.2018.04.11
doi: 10.21037/TAU.2018.04.11
pubmed: 30159241
pmcid: 6087849
Gao, X., Lee, H. Y., Li, W. et al. (2017). Thyroid hormone receptor beta and NCOA4 regulate terminal erythrocyte differentiation. Proceedings of the National Academy of Sciences, 114:10107–10112. https://doi.org/10.1073/PNAS.1711058114
Arnold, R., Schmeiser, T., Heit, W., et al. (1986). Hemopoietic reconstitution after bone marrow transplantation. Experimental Hematology, 14, 271–277.
pubmed: 2870935
Domenech, J., Linassier, C., Gihana, E., et al. (1995). Prolonged impairment of hematopoiesis after high-dose therapy followed by autologous bone marrow transplantation. Blood, 85, 3320–3327. https://doi.org/10.1182/BLOOD.V85.11.3320.BLOODJOURNAL85113320
doi: 10.1182/BLOOD.V85.11.3320.BLOODJOURNAL85113320
pubmed: 7756665
Cismaru, A. C., Soritau, O., Jurj, A. M., et al. (2020). Human chorionic gonadotropin improves the proliferation and regenerative potential of bone marrow adherent stem cells and the immune tolerance of fetal microchimeric stem cells in vitro. Stem Cell Reviews and Reports, 163(16), 524–540. https://doi.org/10.1007/S12015-020-09957-W
doi: 10.1007/S12015-020-09957-W
Nair, A. B., & Jacob, S. (2016). A simple practice guide for dose conversion between animals and human. Journal of Basic and Clinical Pharmacy, 7, 27. https://doi.org/10.4103/0976-0105.177703
doi: 10.4103/0976-0105.177703
pubmed: 27057123
pmcid: 4804402
Morley, A., & Blake, J. (1974). Haemopoietic precursor cells in experimental hypoplastic marrow failure. Australian Journal of Experimental Biology and Medical Science, 52, 909–914. https://doi.org/10.1038/ICB.1974.90
doi: 10.1038/ICB.1974.90
pubmed: 4462526
Boime, I., & Ben-Menahem, D. (1999). Glycoprotein hormone structure-function and analog design. Recent Progress in Hormone Research, 54, 271–289.
pubmed: 10548880
Menzies, B. R., Pask, A. J., & Renfree, M. B. (2011). Placental expression of pituitary hormones is an ancestral feature of therian mammals. EvoDevo, 2, 1–9. https://doi.org/10.1186/2041-9139-2-16/FIGURES/4
doi: 10.1186/2041-9139-2-16/FIGURES/4
Valassi, E. (2021). Pituitary disease and pregnancy. : Endocrinología, Diabetes y Nutrición (English ed), 68, 184–195. https://doi.org/10.1016/J.ENDIEN.2020.07.002
doi: 10.1016/J.ENDIEN.2020.07.002
Ueland, K. (1976). Maternal cardiovascular dynamics: VII. Intrapartum blood volume changes. American Journal of Obstetrics and Gynecology, 126, 671–677. https://doi.org/10.1016/0002-9378(76)90517-2
doi: 10.1016/0002-9378(76)90517-2
pubmed: 984141
Chandra, S., Tripathi, A. K., Mishra, S., et al. (2012). Physiological changes in hematological parameters during pregnancy. Indian Journal of Hematology and Blood Transfusion, 28, 144. https://doi.org/10.1007/S12288-012-0175-6
doi: 10.1007/S12288-012-0175-6
pubmed: 23997449
pmcid: 3422383
Karalis, I., Nadar, S. K., Al Yemeni, E., et al. (2005). Platelet activation in pregnancy-induced hypertension. Thrombosis Research, 116, 377–383. https://doi.org/10.1016/J.THROMRES.2005.01.009
doi: 10.1016/J.THROMRES.2005.01.009
pubmed: 16122550
Luo, C., Wang, L., Wu, G., et al. (2021). (2021) Comparison of the efficacy of hematopoietic stem cell mobilization regimens: A systematic review and network meta-analysis of preclinical studies. Stem Cell Research & Therapy, 121(12), 1–19. https://doi.org/10.1186/S13287-021-02379-6
doi: 10.1186/S13287-021-02379-6
Kuan, J. W., Su, A. T., & Leong, C. F. (2017). Pegylated granulocyte-colony stimulating factor versus non-pegylated granulocyte-colony stimulating factor for peripheral blood stem cell mobilization: A systematic review and meta-analysis. Journal of Clinical Apheresis, 32, 517–542. https://doi.org/10.1002/JCA.21550
doi: 10.1002/JCA.21550
pubmed: 28485020
Thakkar, D., Tiwari, A. K., Pabbi, S., et al. (2021). Peripheral blood stem cell mobilization with pegylated granulocyte colony stimulating factor in children. Cancer Reports, 4, e1408. https://doi.org/10.1002/CNR2.1408
doi: 10.1002/CNR2.1408
pubmed: 34245131
pmcid: 8714533
Li, L., Yin, J., Li, Y., et al. (2021). Allogeneic hematopoietic stem cell transplantation mobilized with pegylated granulocyte colony-stimulating factor ameliorates severe acute graft-versus-host disease through enrichment of monocytic myeloid-derived suppressor cells in the graft: a real world experience. Frontiers in Immunology, 12, 1. https://doi.org/10.3389/FIMMU.2021.621935/FULL
doi: 10.3389/FIMMU.2021.621935/FULL
Wright, D. E., Cheshier, S. H., Wagers, A. J., et al. (2001). Cyclophosphamide/granulocyte colony-stimulating factor causes selective mobilization of bone marrow hematopoietic stem cells into the blood after M phase of the cell cycle. Blood, 97, 2278–2285. https://doi.org/10.1182/BLOOD.V97.8.2278
doi: 10.1182/BLOOD.V97.8.2278
pubmed: 11290588
Devine, S. M., Vij, R., Rettig, M., et al. (2008). Rapid mobilization of functional donor hematopoietic cells without G-CSF using AMD3100, an antagonist of the CXCR4/SDF-1 interaction. Blood, 112, 990–998. https://doi.org/10.1182/BLOOD-2007-12-130179
doi: 10.1182/BLOOD-2007-12-130179
pubmed: 18426988
DiPersio, J. F., Stadtmauer, E. A., Nademanee, A., et al. (2009). Plerixafor and G-CSF versus placebo and G-CSF to mobilize hematopoietic stem cells for autologous stem cell transplantation in patients with multiple myeloma. Blood, 113, 5720–5726. https://doi.org/10.1182/BLOOD-2008-08-174946
doi: 10.1182/BLOOD-2008-08-174946
pubmed: 19363221
Attolico, I., Pavone, V., Ostuni, A., et al. (2012). Plerixafor added to chemotherapy plus G-CSF is safe and allows adequate PBSC collection in predicted poor mobilizer patients with multiple myeloma or lymphoma. Biology of Blood and Marrow Transplantation, 18, 241–249. https://doi.org/10.1016/J.BBMT.2011.07.014
doi: 10.1016/J.BBMT.2011.07.014
pubmed: 21791194
Duarte, R. F., & Frank, D. A. (2002). The synergy between stem cell factor (SCF) and granulocyte colony-stimulating factor (G-CSF): Molecular basis and clinical relevance. Leukaemia & Lymphoma, 43, 1179–1187. https://doi.org/10.1080/10428190290026231
doi: 10.1080/10428190290026231
Turan, R. D. (2021). Pluripotin facilitates the expansion of hematopoietic stem cells, but restricts the growth of fibroblasts and the proliferation of mesenchymal stem cells from the bone marrow. https://doi.org/10.21203/RS.3.RS-250861/V1
AbuSamra, D. B., Aleisa, F. A., Al-Amoodi, A. S., et al. (2017). Not just a marker: CD34 on human hematopoietic stem/progenitor cells dominates vascular selectin binding along with CD44. Blood Advances, 1, 2799. https://doi.org/10.1182/BLOODADVANCES.2017004317
doi: 10.1182/BLOODADVANCES.2017004317
pubmed: 29296932
pmcid: 5745127
Reyes-Reyes, M., Mora, N., Gonzalez, G., & Rosales, C. (2002). beta1 and beta2 integrins activate different signalling pathways in monocytes. The Biochemical Journal, 363, 273. https://doi.org/10.1042/0264-6021:3630273
doi: 10.1042/0264-6021:3630273
pubmed: 11931654
pmcid: 1222475
Kim, M. Y., & Cho, J. Y. (2016). Molecular association of CD98, CD29, and CD147 critically mediates monocytic U937 cell adhesion. The Korean Journal of Physiology & Pharmacology, 20, 515. https://doi.org/10.4196/KJPP.2016.20.5.515
doi: 10.4196/KJPP.2016.20.5.515
Pilarski, L. M., Yacyshyn, B. R., Jensen, G. S., et al. (1991). Beta 1 integrin (CD29) expression on human postnatal T cell subsets defined by selective CD45 isoform expression. The Journal of Immunology, 147, 830–837. https://doi.org/10.4049/JIMMUNOL.147.3.830
doi: 10.4049/JIMMUNOL.147.3.830
pubmed: 1830599
Maleki, M., Ghanbarvand, F., Behvarz, M. R., et al. (2014). Comparison of mesenchymal stem cell markers in multiple human adult stem cells. International Journal of Stem Cells, 7, 118. https://doi.org/10.15283/IJSC.2014.7.2.118
doi: 10.15283/IJSC.2014.7.2.118
pubmed: 25473449
pmcid: 4249894
Sierra-Parraga, J. M., Merino, A., Eijken, M., et al. (2020). Reparative effect of mesenchymal stromal cells on endothelial cells after hypoxic and inflammatory injury. Stem Cell Research & Therapy, 11, 1–11. https://doi.org/10.1186/S13287-020-01869-3/FIGURES/5
doi: 10.1186/S13287-020-01869-3/FIGURES/5
Lin, C. S., Ning, H., Lin, G., & Lue, T. F. (2012). Is CD34 truly a negative marker for mesenchymal stromal cells? Cytotherapy, 14, 1159–1163. https://doi.org/10.3109/14653249.2012.729817
doi: 10.3109/14653249.2012.729817
pubmed: 23066784
Stroncek, D. F., Matthews, C. L., Follmann, D., & Leitman, S. F. (2002). Kinetics of G-CSF-induced granulocyte mobilization in healthy subjects: Effects of route of administration and addition of dexamethasone. Transfusion, 42, 597–602. https://doi.org/10.1046/J.1537-2995.2002.00091.X
doi: 10.1046/J.1537-2995.2002.00091.X
pubmed: 12084168
Filgrastim Side Effects: Common, Severe, Long Term - Drugs.com. https://www.drugs.com/sfx/filgrastim-side-effects.html . Accessed 8 Jun 2023
Tavian, M., & Péault, B. (2005). Embryonic development of the human hematopoietic system. International Journal of Developmental Biology, 49, 243–250. https://doi.org/10.1387/IJDB.041957MT
doi: 10.1387/IJDB.041957MT
pubmed: 15906238
Pereda Tapiol, J., & Niimi, G. (2008). Embryonic erythropoiesis in human yolk sac: Two different compartments for two different processes. Microscopy Research and Technique, 71, 856–862. https://doi.org/10.1002/JEMT.20627
doi: 10.1002/JEMT.20627
Sabin, F. R. (1920). Studies on the origin of blood-vessels and of red blood-corpuscles as seen in the living blastoderm of chicks during the second day of incubation | WorldCat.org. Contrib Embryol, 1, 213–262.
Murray, P. D. F. (1932). The development in vitro of the blood of the early chick embryo.Proceedings of the Royal Society of London. Series B, Containing Papers of a Biological Character, 111:497–521. https://doi.org/10.1098/RSPB.1932.0070
Tavian, M., Hallais, M. F., & Péault, B. (1999). Emergence of intraembryonic hematopoietic precursors in the pre-liver human embryo. Development, 126, 793–803. https://doi.org/10.1242/DEV.126.4.793
doi: 10.1242/DEV.126.4.793
pubmed: 9895326
Zovein, A. C., Hofmann, J. J., Lynch, M., et al. (2008). Fate tracing reveals the endothelial origin of hematopoietic stem cells. Cell Stem Cell, 3, 625. https://doi.org/10.1016/J.STEM.2008.09.018
doi: 10.1016/J.STEM.2008.09.018
pubmed: 19041779
pmcid: 2631552
Ratajczak, M. Z., Ratajczak, J., & Kucia, M. (2019). Very small embryonic-like stem cells (VSELs) – an update and future directions. Circulation Research, 124, 208. https://doi.org/10.1161/CIRCRESAHA.118.314287
doi: 10.1161/CIRCRESAHA.118.314287
pubmed: 30653438
pmcid: 6461217
Virant-Klun, I. (2016). Very small embryonic-like stem cells: a potential developmental link between germinal lineage and hematopoiesis in humans. Stem Cells and Development, 25, 101–113. https://doi.org/10.1089/SCD.2015.0275
doi: 10.1089/SCD.2015.0275
pubmed: 26494182
Ratajczak, M. Z., Zuba-Surma, E., Wojakowski, W., et al. (2013). Very small embryonic-like stem cells (VSELs) represent a real challenge in stem cell biology: Recent pros and cons in the midst of a lively debate. Leukemia 2014, 283(28), 473–484. https://doi.org/10.1038/leu.2013.255
doi: 10.1038/leu.2013.255
Migliaccio, G., Migliaccio, A. R., Petti, S., et al. (1986). Human embryonic hemopoiesis. Kinetics of progenitors and precursors underlying the yolk sac––liver transition. The Journal of Clinical Investigation, 78, 51–60. https://doi.org/10.1172/JCI112572
doi: 10.1172/JCI112572
pubmed: 3722384
pmcid: 329530
Cismaru, C. A., Pirlog, R., Calin, G. A., & Berindan-Neagoe, I. (2022). Stem cells in the tumor immune microenvironment –part of the cure or part of the disease? Ontogeny and dichotomy of stem and immune cells has led to better understanding. Stem Cell Reviews and Reports, 1, 1–17. https://doi.org/10.1007/S12015-022-10428-7
doi: 10.1007/S12015-022-10428-7
Ratajczak, M. Z. (2017). Why are hematopoietic stem cells so “sexy”? – on a search for developmental explanation. Leukemia, 31, 1671. https://doi.org/10.1038/LEU.2017.148
doi: 10.1038/LEU.2017.148
pubmed: 28502982
pmcid: 5540746
Ratajczak, M. Z. (2015). A novel view of the adult bone marrow stem cell hierarchy and stem cell trafficking. Leukemia, 29, 776. https://doi.org/10.1038/LEU.2014.346
doi: 10.1038/LEU.2014.346
pubmed: 25486871
pmcid: 4396402
Ratajczak, M. Z., Ratajczak, J., & Kucia, M. (2019). Very small embryonic-like stem cells (VSELs). Circulation Research, 124, 208–210. https://doi.org/10.1161/CIRCRESAHA.118.314287
doi: 10.1161/CIRCRESAHA.118.314287
pubmed: 30653438
pmcid: 6461217
Rich, I. N. (1995). Primordial germ cells are capable of producing cells of the hematopoietic system in vitro. Blood, 86, 463–472. https://doi.org/10.1182/BLOOD.V86.2.463.BLOODJOURNAL862463
doi: 10.1182/BLOOD.V86.2.463.BLOODJOURNAL862463
pubmed: 7541662
Cismaru, C. A., Pop, L., & Berindan-Neagoe, I. (2018). Incognito: Are microchimeric fetal stem cells that cross placental barrier real emissaries of peace? Stem Cell Reviews and Reports, 145(14), 632–641. https://doi.org/10.1007/S12015-018-9834-9
doi: 10.1007/S12015-018-9834-9
Cismaru, C. A., Soritau, O., Jurj, A.-M., et al. (2019). Isolation and Characterization of a Fetal-Maternal Microchimeric Stem Cell Population in Maternal Hair Follicles Long after Parturition. Stem Cell Reviews and Reports, 154(15), 519–529. https://doi.org/10.1007/S12015-019-09885-4
doi: 10.1007/S12015-019-09885-4
Ratajczak, M. Z., Ratajczak, J., Suszynska, M., et al. (2017). A novel view of the adult stem cell compartment from the perspective of a quiescent population of very small embryonic-like stem cells. Circulation Research, 120, 166–178. https://doi.org/10.1161/CIRCRESAHA.116.309362
doi: 10.1161/CIRCRESAHA.116.309362
pubmed: 28057792
pmcid: 5221475
Shaikh, A., Anand, S., Kapoor, S., et al. (2017). Mouse bone marrow VSELs exhibit differentiation into three embryonic germ lineages and germ & hematopoietic cells in culture. Stem Cell Reviews and Reports, 13, 202–216. https://doi.org/10.1007/S12015-016-9714-0/FIGURES/6
doi: 10.1007/S12015-016-9714-0/FIGURES/6
pubmed: 28070859
Caplan, A. I., & Correa, D. (2011). The MSC: An injury drugstore. Cell Stem Cell, 9, 11. https://doi.org/10.1016/J.STEM.2011.06.008
doi: 10.1016/J.STEM.2011.06.008
pubmed: 21726829
pmcid: 3144500
Caplan, A. I., & Hariri, R. (2015). Body management: Mesenchymal stem cells control the internal regenerator. Stem Cells Translational Medicine, 4, 695–701. https://doi.org/10.5966/SCTM.2014-0291
doi: 10.5966/SCTM.2014-0291
pubmed: 26019227
pmcid: 4479626
Rühle, A., Lopez Perez, R., Zou, B., et al. (2019). The therapeutic potential of mesenchymal stromal cells in the treatment of chemotherapy-induced tissue damage. Stem Cell Reviews and Reports, 153(15), 356–373. https://doi.org/10.1007/S12015-019-09886-3
doi: 10.1007/S12015-019-09886-3
Wang, L., Zhu, C.-y, Ma, D.-x, et al. (2018). Efficacy and safety of mesenchymal stromal cells for the prophylaxis of chronic graft-versus-host disease after allogeneic hematopoietic stem cell transplantation: a meta-analysis of randomized controlled trials. Annals of Hematology, 97, 1941–1950. https://doi.org/10.1007/S00277-018-3384-8
doi: 10.1007/S00277-018-3384-8
pubmed: 29947972