Ectopic miR-125a Expression Induces Long-Term Repopulating Stem Cell Capacity in Mouse and Human Hematopoietic Progenitors

Cell Stem Cell

Volumn 19, Issue 3, 2016, Pages 383-396

  Wojtowicz, Edyta E ^a   Lechman, Eric R ^b   Hermans, Karin G ^b   Schoof, Erwin M ^b   Wienholds, Erno ^b   Isserlin, Ruth ^c   van Veelen, Peter A ^d   Broekhuis, Mathilde J C ^a   Janssen, George M C ^d   Trotman Grant, Aaron ^b   Dobson, Stephanie M ^b,c   Krivdova, Gabriela ^b,c   Elzinga, Jantje ^b   Kennedy, James ^b   Gan, Olga I ^b   Sinha, Ankit ^c   Ignatchenko, Vladimir ^c   Kislinger, Thomas ^c   Dethmers Ausema, Bertien ^a   Weersing, Ellen ^a   Alemdehy, Mir Farshid ^e   de Looper, Hans W J ^e   Bader, Gary D ^c   Ritsema, Martha ^a   Erkeland, Stefan J ^f   Bystrykh, Leonid V ^a   Dick, John E ^b,c   de Haan, Gerald ^a   more..

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b PRINCESS MARGARET HOSPITAL   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

^d LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^e ERASMUS MC CANCER INSTITUTE   (Netherlands)

^f ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CD34 ANTIGEN; CD38 ANTIGEN; GAMMA INTERFERON; MICRORNA; MICRORNA 125A; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; MIRN125 MICRORNA, HUMAN; MIRN125 MICRORNA, MOUSE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ECTOPIC EXPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; STEM CELL SELF-RENEWAL; WESTERN BLOTTING; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; CELL PROLIFERATION; CELL SELF-RENEWAL; CYTOLOGY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; ISOTOPE LABELING; MALE; METABOLISM; MULTIPOTENT STEM CELL; REPRODUCIBILITY; TIME FACTOR; TRANSPLANTATION;

ANIMALS; ANTIGENS, CD34; ANTIGENS, CD38; CELL PROLIFERATION; CELL SELF RENEWAL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORKS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; ISOTOPE LABELING; MALE; MICE, INBRED C57BL; MICRORNAS; MODELS, BIOLOGICAL; MULTIPOTENT STEM CELLS; REPRODUCIBILITY OF RESULTS; TIME FACTORS;

EID: 84978857997     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2016.06.008     Document Type: Article

References (46)

1. Aljurf, M., Rizzo, J.D., Mohty, M., Hussain, F., Madrigal, A., Pasquini, M.C., Passweg, J., Chaudhri, N., Ghavamzadeh, A., Solh, H.E., et al. Challenges and opportunities for HSCT outcome registries: perspective from international HSCT registries experts. Bone Marrow Transplant. 49 (2014), 1016–1021.
2. Ballen, K.K., Gluckman, E., Broxmeyer, H.E., Umbilical cord blood transplantation: the first 25 years and beyond. Blood 122 (2013), 491–498.
3. Balmain, A., Harris, C.C., Carcinogenesis in mouse and human cells: parallels and paradoxes. Carcinogenesis 21 (2000), 371–377.
4. Barker, J.N., Weisdorf, D.J., Wagner, J.E., Creation of a double chimera after the transplantation of umbilical-cord blood from two partially matched unrelated donors. N. Engl. J. Med. 344 (2001), 1870–1871.
5. Bartel, D.P., MicroRNAs: target recognition and regulatory functions. Cell 136 (2009), 215–233.
6. Baudet, A., Karlsson, C., Safaee Talkhoncheh, M., Galeev, R., Magnusson, M., Larsson, J., RNAi screen identifies MAPK14 as a druggable suppressor of human hematopoietic stem cell expansion. Blood 119 (2012), 6255–6258.
7. Boitano, A.E., Wang, J., Romeo, R., Bouchez, L.C., Parker, A.E., Sutton, S.E., Walker, J.R., Flaveny, C.A., Perdew, G.H., Denison, M.S., et al. Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 329 (2010), 1345–1348.
8. Bousquet, M., Harris, M.H., Zhou, B., Lodish, H.F., MicroRNA miR-125b causes leukemia. Proc. Natl. Acad. Sci. USA 107 (2010), 21558–21563.
9. Buckley, D.A., Cheng, A., Kiely, P.A., Tremblay, M.L., O'Connor, R., Regulation of insulin-like growth factor type I (IGF-I) receptor kinase activity by protein tyrosine phosphatase 1B (PTP-1B) and enhanced IGF-I-mediated suppression of apoptosis and motility in PTP-1B-deficient fibroblasts. Mol. Cell. Biol. 22 (2002), 1998–2010.
10. Chaudhuri, A.A., So, A.Y., Mehta, A., Minisandram, A., Sinha, N., Jonsson, V.D., Rao, D.S., O'Connell, R.M., Baltimore, D., Oncomir miR-125b regulates hematopoiesis by targeting the gene Lin28A. Proc. Natl. Acad. Sci. USA 109 (2012), 4233–4238.
11. Cox, J., Mann, M., MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat. Biotechnol. 26 (2008), 1367–1372.
12. Doulatov, S., Notta, F., Eppert, K., Nguyen, L.T., Ohashi, P.S., Dick, J.E., Revised map of the human progenitor hierarchy shows the origin of macrophages and dendritic cells in early lymphoid development. Nat. Immunol. 11 (2010), 585–593.
13. Dubé, N., Cheng, A., Tremblay, M.L., The role of protein tyrosine phosphatase 1B in Ras signaling. Proc. Natl. Acad. Sci. USA 101 (2004), 1834–1839.
14. Dubé, N., Bourdeau, A., Heinonen, K.M., Cheng, A., Loy, A.L., Tremblay, M.L., Genetic ablation of protein tyrosine phosphatase 1B accelerates lymphomagenesis of p53-null mice through the regulation of B-cell development. Cancer Res. 65 (2005), 10088–10095.
15. Fares, I., Chagraoui, J., Gareau, Y., Gingras, S., Ruel, R., Mayotte, N., Csaszar, E., Knapp, D.J., Miller, P., Ngom, M., et al. Cord blood expansion. Pyrimidoindole derivatives are agonists of human hematopoietic stem cell self-renewal. Science 345 (2014), 1509–1512.
16. Filipowicz, W., Bhattacharyya, S.N., Sonenberg, N., Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?. Nat. Rev. Genet. 9 (2008), 102–114.
17. Gentner, B., Visigalli, I., Hiramatsu, H., Lechman, E., Ungari, S., Giustacchini, A., Schira, G., Amendola, M., Quattrini, A., Martino, S., et al. Identification of hematopoietic stem cell-specific miRNAs enables gene therapy of globoid cell leukodystrophy. Sci. Transl. Med., 2, 2010, 58ra84.
18. Gerrits, A., Walasek, M.A., Olthof, S., Weersing, E., Ritsema, M., Zwart, E., van Os, R., Bystrykh, L.V., de Haan, G., Genetic screen identifies microRNA cluster 99b/let-7e/125a as a regulator of primitive hematopoietic cells. Blood 119 (2012), 377–387.
19. Guo, S., Scadden, D.T., A microRNA regulating adult hematopoietic stem cells. Cell Cycle 9 (2010), 3637–3638.
20. Guo, S., Bai, H., Megyola, C.M., Halene, S., Krause, D.S., Scadden, D.T., Lu, J., Complex oncogene dependence in microRNA-125a-induced myeloproliferative neoplasms. Proc. Natl. Acad. Sci. USA 109 (2012), 16636–16641.
21. Helgason, C.D., Damen, J.E., Rosten, P., Grewal, R., Sorensen, P., Chappel, S.M., Borowski, A., Jirik, F., Krystal, G., Humphries, R.K., Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev. 12 (1998), 1610–1620.
22. Hu, Y., Smyth, G.K., ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol. Methods. 347 (2009), 70–78.
23. Ito, K., Hirao, A., Arai, F., Takubo, K., Matsuoka, S., Miyamoto, K., Ohmura, M., Naka, K., Hosokawa, K., Ikeda, Y., Suda, T., Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat. Med. 12 (2006), 446–451.
24. Lechman, E.R., Gentner, B., van Galen, P., Giustacchini, A., Saini, M., Boccalatte, F.E., Hiramatsu, H., Restuccia, U., Bachi, A., Voisin, V., et al. Attenuation of miR-126 activity expands HSC in vivo without exhaustion. Cell Stem Cell 11 (2012), 799–811.
25. Meenhuis, A., van Veelen, P.A., de Looper, H., van Boxtel, N., van den Berge, I.J., Sun, S.M., Taskesen, E., Stern, P., de Ru, A.H., van Adrichem, A.J., et al. MiR-17/20/93/106 promote hematopoietic cell expansion by targeting sequestosome 1-regulated pathways in mice. Blood 118 (2011), 916–925.
26. Metcalf, D., Hematopoietic cytokines. Blood 111 (2008), 485–491.
27. North, T.E., Goessling, W., Walkley, C.R., Lengerke, C., Kopani, K.R., Lord, A.M., Weber, G.J., Bowman, T.V., Jang, I.H., Grosser, T., et al. Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447 (2007), 1007–1011.
28. Notta, F., Doulatov, S., Laurenti, E., Poeppl, A., Jurisica, I., Dick, J.E., Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 333 (2011), 218–221.
29. O'Connell, R.M., Rao, D.S., Chaudhuri, A.A., Boldin, M.P., Taganov, K.D., Nicoll, J., Paquette, R.L., Baltimore, D., Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J. Exp. Med. 205 (2008), 585–594.
30. O'Connell, R.M., Chaudhuri, A.A., Rao, D.S., Gibson, W.S., Balazs, A.B., Baltimore, D., MicroRNAs enriched in hematopoietic stem cells differentially regulate long-term hematopoietic output. Proc. Natl. Acad. Sci. USA 107 (2010), 14235–14240.
31. Ogawa, M., Differentiation and proliferation of hematopoietic stem cells. Blood 81 (1993), 2844–2853.
32. Ong, S.E., Blagoev, B., Kratchmarova, I., Kristensen, D.B., Steen, H., Pandey, A., Mann, M., Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 1 (2002), 376–386.
33. Ooi, A.G., Sahoo, D., Adorno, M., Wang, Y., Weissman, I.L., Park, C.Y., MicroRNA-125b expands hematopoietic stem cells and enriches for the lymphoid-balanced and lymphoid-biased subsets. Proc. Natl. Acad. Sci. USA 107 (2010), 21505–21510.
34. Oran, B., Shpall, E., Umbilical cord blood transplantation: a maturing technology. Hematology (Am Soc Hematol Educ Program) 2012 (2012), 215–222.
35. Peng, X., Mandal, P.K., Kaminskyy, V.O., Lindqvist, A., Conrad, M., Arnér, E.S., Sec-containing TrxR1 is essential for self-sufficiency of cells by control of glucose-derived H2O2. Cell Death Dis., 5, 2014, e1235.
36. Pineault, N., Abu-Khader, A., Advances in umbilical cord blood stem cell expansion and clinical translation. Exp. Hematol. 43 (2015), 498–513.
37. Rangarajan, A., Hong, S.J., Gifford, A., Weinberg, R.A., Species- and cell type-specific requirements for cellular transformation. Cancer Cell 6 (2004), 171–183.
38. Sauvageau, G., Iscove, N.N., Humphries, R.K., In vitro and in vivo expansion of hematopoietic stem cells. Oncogene 23 (2004), 7223–7232.
39. Uren, A.G., Mikkers, H., Kool, J., van der Weyden, L., Lund, A.H., Wilson, C.H., Rance, R., Jonkers, J., van Lohuizen, M., Berns, A., Adams, D.J., A high-throughput splinkerette-PCR method for the isolation and sequencing of retroviral insertion sites. Nat. Protoc. 4 (2009), 789–798.
40. Verovskaya, E., Broekhuis, M.J., Zwart, E., Ritsema, M., van Os, R., de Haan, G., Bystrykh, L.V., Heterogeneity of young and aged murine hematopoietic stem cells revealed by quantitative clonal analysis using cellular barcoding. Blood 122 (2013), 523–532.
41. Wagner, J.E. Jr., Eapen, M., Carter, S., Wang, Y., Schultz, K.R., Wall, D.A., Bunin, N., Delaney, C., Haut, P., Margolis, D., et al., Blood and Marrow Transplant Clinical Trials Network. One-unit versus two-unit cord-blood transplantation for hematologic cancers. N. Engl. J. Med. 371 (2014), 1685–1694.
42. Wang, Y., Kellner, J., Liu, L., Zhou, D., Inhibition of p38 mitogen-activated protein kinase promotes ex vivo hematopoietic stem cell expansion. Stem Cells Dev. 20 (2011), 1143–1152.
43. Ward, A.C., Smith, L., de Koning, J.P., van Aesch, Y., Touw, I.P., Multiple signals mediate proliferation, differentiation, and survival from the granulocyte colony-stimulating factor receptor in myeloid 32D cells. J. Biol. Chem. 274 (1999), 14956–14962.
44. Wojtowicz, E.E., Walasek, M.A., Broekhuis, M.J., Weersing, E., Ritsema, M., Ausema, A., Bystrykh, L.V., de Haan, G., MicroRNA-125 family members exert a similar role in the regulation of murine hematopoiesis. Exp. Hematol., 42, 2014, 909-18.e1.
45. Yagishita, N., Ohneda, K., Amano, T., Yamasaki, S., Sugiura, A., Tsuchimochi, K., Shin, H., Kawahara, K., Ohneda, O., Ohta, T., et al. Essential role of synoviolin in embryogenesis. J. Biol. Chem. 280 (2005), 7909–7916.
46. Zhang, J., Grindley, J.C., Yin, T., Jayasinghe, S., He, X.C., Ross, J.T., Haug, J.S., Rupp, D., Porter-Westpfahl, K.S., Wiedemann, L.M., et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 441 (2006), 518–522.