The ability of multipotent mesenchymal stromal cells from the bone marrow of patients with leukemia to maintain normal hematopoietic progenitor cells

European Journal of Haematology

Volumn 97, Issue 3, 2016, Pages 245-252

  Sorokina, Tamara ^a   Shipounova, Irina ^a   Bigildeev, Alexey ^a   Petinati, Nataliya ^a   Drize, Nina ^a   Turkina, Anna ^a   Chelysheva, Ekaterina ^a   Shukhov, Oleg ^a   Kuzmina, Larisa ^a   Parovichnikova, Elena ^a   Savchenko, Valery ^a  

^a NATIONAL RESEARCH CENTER FOR HEMATOLOGY   (Russian Federation)

Author keywords

acute lymphoblastic leukemia; acute myeloid leukemia; chronic myeloid leukemia; cobblestone area forming cells; multipotent mesenchymal stromal cells

Indexed keywords

PROTEIN TYROSINE KINASE INHIBITOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; ACUTE MYELOBLASTIC LEUKEMIA; ADULT; ARTICLE; BONE MARROW; CANCER CHEMOTHERAPY; CHRONIC MYELOID LEUKEMIA; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LEUKEMIA; MALE; MESENCHYMAL STROMA CELL; MULTIPOTENT MESENCHYMAL STROMAL CELL; PRIORITY JOURNAL;

EID: 84982156134     PISSN: 09024441     EISSN: 16000609     Source Type: Journal    
DOI: 10.1111/ejh.12713     Document Type: Article

References (49)

1. Taichman RS. Blood and bone: two tissues whose fates are intertwined to create the hematopoietic stem-cell niche. Blood 2005;105:2631–9.
2. Doan PL, Chute JP. The vascular niche: home for normal and malignant hematopoietic stem cells. Leukemia 2012;26:54–62.
3. Pinho S, Lacombe J, Hanoun M, Mizoguchi T, Bruns I, Kunisaki Y, Frenette PS. PDGFRα and CD51 mark human nestin+ sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion. J Exp Med 2013;210:1351–67.
4. Park D, Spencer JA, Koh BI, Kobayashi T, Fujisaki J, Clemens TL, et al. Endogenous bone marrow MSCs are dynamic, fate-restricted participants in bone maintenance and regeneration. Cell Stem Cell 2012;10:259–72.
5. 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.
6. Rodríguez-Pardo VM, Vernot JP. Mesenchymal stem cells promote a primitive phenotype CD34 + c-kit+ in human cord blood-derived hematopoietic stem cells during ex vivo expansion. Cell Mol Biol Lett 2013;18:11–33.
7. Cheng H, Hao S, Liu Y, Pang Y, Ma S, Dong F, et al. Leukemic marrow infiltration reveals a novel role for Egr3 as a potent inhibitor of normal hematopoietic stem cell proliferation. Blood 2015;126:1302–13.
8. Schepers K, Pietras EM, Reynaud D, Flach J, Binnewies M, Garg T, et al. Myeloproliferative neoplasia remodels the endosteal bone marrow niche into a self-reinforcing leukemic niche. Cell Stem Cell 2013;13:285–99.
9. Schepers K, Campbell TB, Passegué E. Normal and leukemic stem cell niches: insights and therapeutic opportunities. Cell Stem Cell 2015;16:254–67.
10. Krevvata M, Silva BC, Manavalan JS, Galan-Diez M, Kode A, Matthews BG, et al. Inhibition of leukemia cell engraftment and disease progression in mice by osteoblasts. Blood 2014;124:2834–46.
11. Lu M, Xia L, Liu Y-C, Hochman T, Bizzari L, Aruch D, et al. Lipocalin produced by myelofibrosis cells affects the fate of both hematopoietic and marrow microenvironmental cells. Blood 2015;126:972–82.
12. Paggetti J, Haderk F, Seiffert M, Janji B, Distler U, Ammerlaan W, et al. Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts. Blood 2015;126:1106–17.
13. Devine SM, Hoffman R. Role of mesenchymal stem cells in hematopoietic stem cell transplantation. Curr Opin Hematol 2000;7:358–63.
14. Frisch BJ, Ashton JM, Xing L, Becker MW, Jordan CT, Calvi LM. Functional inhibition of osteoblastic cells in an in vivo mouse model of myeloid leukemia. Blood 2012;119:540–50.
15. Lopez-Villar O, Garcia JL, Sanchez-Guijo FM, Robledo C, Villaron EM, Hernández-Campo P, et al. Both expanded and uncultured mesenchymal stem cells from MDS patients are genomically abnormal, showing a specific genetic profile for the 5q- syndrome. Leukemia 2009;23:664–72.
16. Vicente López Á, Vázquez García MN, Melen GJ, Entrena Martínez A, Cubillo Moreno I, García-Castro J, et al. Mesenchymal stromal cells derived from the bone marrow of acute lymphoblastic leukemia patients show altered BMP4 production: correlations with the course of disease. PLoS One 2014;9:e84496.
17. Zhao Z, Sun L, Wang X, Zhang Y, Yu Y, Yang H. et al. [Immunomodulatory effects of mesenchymal stem cells derived from the bone marrow in acute leukemia patients]. Zhonghua Zhong Liu Za Zhi 2011;33:105–9.
18. Zhao Z-G, Liang Y, Li K, Li W-M, Li Q-B, Chen Z-C, et al. Phenotypic and functional comparison of mesenchymal stem cells derived from the bone marrow of normal adults and patients with hematologic malignant diseases. Stem Cells Dev 2007;16:637–48.
19. Visconte V, Tiu RV, Rogers HJ. Pathogenesis of myelodysplastic syndromes: an overview of molecular and non-molecular aspects of the disease. Blood Res 2014;49:216–27.
20. Medyouf H, Mossner M, Jann J-C, Nolte F, Raffel S, Herrmann C, et al. Myelodysplastic cells in patients reprogram mesenchymal stromal cells to establish a transplantable stem cell niche disease unit. Cell Stem Cell 2014;14:824–37.
21. Blau O, Baldus CD, Hofmann W-K, Thiel G, Nolte F, Burmeister T, et al. Mesenchymal stromal cells of myelodysplastic syndrome and acute myeloid leukemia patients have distinct genetic abnormalities compared with leukemic blasts. Blood 2011;118:5583–92.
22. Estrada-González PK, Gómez-Ceja L, Montesinos JJ, Mayani H, Chávez-González A, Meillón L, et al. Decreased frequency, but normal functional integrity of mesenchymal stromal cells derived from untreated and Imatinib-treated chronic myeloid leukemia patients. Leuk Res 2014a;38:594–600.
23. Fecteau J-F, Kipps TJ. Structure and function of the hematopoietic cancer niche: focus on chronic lymphocytic leukemia. Front Biosci (Schol Ed) 2012;4:61–73.
24. Janel A, Dubois-Galopin F, Bourgne C, Berger J, Tarte K, Boiret-Dupré N, et al. The chronic lymphocytic leukemia clone disrupts the bone marrow microenvironment. Stem Cells Dev 2014;23:2972–82.
25. André T, Najar M, Stamatopoulos B, Pieters K, Pradier O, Bron D, et al. Immune impairments in multiple myeloma bone marrow mesenchymal stromal cells. Cancer Immunol Immunother 2015;64:213–24.
26. Garayoa M, Garcia JL, Santamaria C, Garcia-Gomez A, Blanco JF, Pandiella A, et al. Mesenchymal stem cells from multiple myeloma patients display distinct genomic profile as compared with those from normal donors. Leukemia 2009;23:1515–27.
27. van Os RP, Dethmers-Ausema B, de Haan G. In vitro assays for cobblestone area-forming cells, LTC-IC, and CFU-C. Methods Mol Biol 2008;430:143–57.
28. de Haan G, Ploemacher R. The cobblestone-area-forming cell assay. Methods Mol Med 2002;63:143–51.
29. Ploemacher RE, van der Sluijs JP, Voerman JS, Brons NH. An in vitro limiting-dilution assay of long-term repopulating hematopoietic stem cells in the mouse. Blood 1989;74:2755–63.
30. Ploemacher RE, van der Sluijs JP, van Beurden CA, Baert MR, Chan PL. Use of limiting-dilution type long-term marrow cultures in frequency analysis of marrow-repopulating and spleen colony-forming hematopoietic stem cells in the mouse. Blood 1991;78:2527–33.
31. Nifontova IN, Ershler MA, Drize NI. Abnormalities in long-term bone culture from mice deficient in tumor necrosis factor: Induction of apoptosis and cell proliferation. Bull Exp Biol Med 2002;133:386–8.
32. Breems DA, Blokland EAW, Neben S, Ploemacher RE. Frequency analysis of human primitive haematopoietic stem cell subsets using a cobblestone area forming cell assay. Leukemia 1994;8:1095–104.
33. Van Os RP, Dethmers-Ausema B, De Haan G. In vitro assays for cobblestone area-forming cells, LTC-IC, and CFU-C. Methods Mol Biol 2007;430:143–57.
34. Klein C, Strobel J, Zingsem J, Richter RH, Goecke TW, Beckmann MW, et al. Ex vivo expansion of hematopoietic stem- and progenitor cells from cord blood in coculture with mesenchymal stroma cells from amnion, chorion, Wharton's jelly, amniotic fluid, cord blood, and bone marrow. Tissue Eng Part A 2013;19:2577–85.
35. Van Overstraeten-Schlögel N, Beguin Y, Gothot A. Role of stromal-derived factor-1 in the hematopoietic-supporting activity of human mesenchymal stem cells. Eur J Haematol 2006;76:488–93.
36. Parovichnikova EN, Kliasova GA, Isaev VG, Sokolov AN, Kokhno AV, Troitskaia VV. et al. [First results of Ph-negative acute lymphoblastic leukemia therapy of adults according to the protocol of Research Group of Russian Hematological Centers ALL-2009]. Ter Arkh 2011;83:11–7.
37. Parovichnikova EN, Troitskaia VV, Kliasova GA, Kuz'mina LA, Sokolov AN, Paramonova EV, et al. [Treating patients with acute myeloid leukemias (AML) according to the protocol of the AML-01.10 Russian multicenter randomized trial: the coordinating center's results]. Ter Arkh 2014;86:14–23.
38. Kobari L, Dubart A, Le Pesteur F, Vainchenker W, Sainteny F. Hematopoietic-promoting activity of the murine stromal cell line MS-5 is not related to the expression of the major hematopoietic cytokines. J Cell Physiol 1995;163:295–304.
39. Fazekas de St Groth. The evaluation of limiting dilution assays. J Immunol Methods 1982;49:R11–23.
40. Nifontova IN, Ershler MA, Drize NI. Dynamics of precursor cell composition in bone marrow culture derived from mice deficient by tumor necrosis factor. Bull Exp Biol Med 2003;135:285–8.
41. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 1987;162:156–9.
42. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc 2008;3:1101–8.
43. Boyd AL, Campbell CJ V, Hopkins CI, Fiebig-Comyn A, Russell J, Ulemek J, et al. Niche displacement of human leukemic stem cells uniquely allows their competitive replacement with healthy HSPCs. J Exp Med 2014;211:1925–35.
44. Miraki-Moud F, Anjos-Afonso F, Hodby KA, Griessinger E, Rosignoli G, Lillington D, et al. Acute myeloid leukemia does not deplete normal hematopoietic stem cells but induces cytopenias by impeding their differentiation. Proc Natl Acad Sci USA 2013;110:13576–81.
45. Bigildeev AE, Zhironkina OA, Lubkova ON, Drize NJ. Interleukin-1 beta is an irradiation-induced stromal growth factor. Cytokine 2013;64:131–7.
46. Shipounova IN, Petrova TV, Svinareva DA, Momotuk KS, Mikhailova EA, Drize NI. Alterations in hematopoietic microenvironment in patients with aplastic anemia. Clin Transl Sci 2009;2:67–74.
47. Ding L, Morrison SJ. Haematopoietic stem cells and early lymphoid progenitors occupy distinct bone marrow niches. Nature 2013;495:231–5.
48. Carrara RCV, Orellana MD, Fontes AM, Palma PVB, Kashima S, Mendes MR, et al. Mesenchymal stem cells from patients with chronic myeloid leukemia do not express BCR-ABL and have absence of chimerism after allogeneic bone marrow transplant. Braz J Med Biol Res 2007;40:57–67.
49. Kuzmina LA, Petinati NA, Shipounova IN, Sats NV, Bigildeev AE, Zezina EA, et al. Analysis of multipotent mesenchymal stromal cells used for acute graft-versus-host disease prophylaxis. Eur J Haematol 2015;20 JUL 2015, doi: 10.1111/ejh.12613.