Mesenchymal stromal cell-derived extracellular vesicles promote myeloid-biased multipotent hematopoietic progenitor expansion via toll-like receptor engagement

Journal of Biological Chemistry

Volumn 291, Issue 47, 2016, Pages 24607-24617

  Goloviznina, Natalya A ^a,b,d   Verghese, Santhosh Chakkaramakkil ^a,b   Yoon, Young Me ^a,b   Taratula, Oleh ^c   Marks, Daniel L ^a,b   Kurre, Peter ^a,b  

^a Department of Pediatrics ^*  (United States)

^b OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^c OREGON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE; CELL CULTURE; CELLS; CHEMICAL ACTIVATION; CROSSTALK; CYTOLOGY; ENZYME ACTIVITY; EXPANSION; FLOWCHARTING; PROTEINS;

ADAPTER PROTEINS; ANGIOGENIC FACTOR; BONE MARROW MICROENVIRONMENT; CELL CROSS TALKS; CO-LOCALIZATIONS; FLUORESCENCE PROTEINS; MESENCHYMAL STROMAL CELLS; TOLL-LIKE RECEPTORS;

STEM CELLS;

HYPOXIA INDUCIBLE FACTOR 1ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; RAB PROTEIN; TOLL LIKE RECEPTOR 4; CCL2 PROTEIN, MOUSE; HIF1A PROTEIN, MOUSE; MYD88 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ADIPOSE DERIVED STEM CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL POPULATION; CONFERENCE PAPER; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENDOSOME; EXOSOME; FLUORESCENCE IMAGING; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MESENCHYMAL STROMA CELL; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; STEM CELL EXPANSION; ANIMAL; CYTOLOGY; MEMBRANE MICROPARTICLE; METABOLISM;

ANIMALS; CELL-DERIVED MICROPARTICLES; CHEMOKINE CCL2; HEMATOPOIETIC STEM CELLS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MESENCHYMAL STROMAL CELLS; MICE; MYELOID DIFFERENTIATION FACTOR 88; RAB5 GTP-BINDING PROTEINS; TOLL-LIKE RECEPTOR 4;

EID: 84995752697     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M116.745653     Document Type: Conference Paper

References (58)

1. Purton, L. E., and Scadden, D. T. (2008) The hematopoietic stem cell niche. in StemBook, Harvard Stem Cell Institute, Cambridge, MA, 10.3824/stembook.1.28.1
2. Cabezas-Wallscheid, N., Klimmeck, D., Hansson, J., Lipka, D. B., Reyes, A., Wang, Q., Weichenhan, D., Lier, A., von Paleske, L., Renders, S., Wünsche, P., Zeisberger, P., Brocks, D., Gu, L., Herrmann, C., et al. (2014) Identification of regulatory networks in HSCs and their immediate progeny via integrated proteome, transcriptome, and DNA methylome analysis. Cell Stem Cell 15, 507-522
3. Cosgun, K. N., Rahmig, S., Mende, N., Reinke, S., Hauber, I., Schäfer, C., Petzold, A., Weisbach, H., Heidkamp, G., Purbojo, A., Cesnjevar, R., Platz, A., Bornhäuser, M., Schmitz, M., Dudziak, D., Hauber, J., Kirberg, J., and Waskow, C. (2014) Kit regulates HSC engraftment across the humanmouse species barrier. Cell Stem Cell 15, 227-238
4. Greenbaum, A., Hsu, Y. M., Day, R. B., Schuettpelz, L. G., Christopher, M. J., Borgerding, J. N., Nagasawa, T., and Link, D. C. (2013) CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495, 227-230
5. Morrison, S. J., and Scadden, D. T. (2014) The bone marrow niche for haematopoietic stem cells. Nature 505, 327-334
6. Zhou, B. O., Ding, L., and Morrison, S. J. (2015) Hematopoietic stem and progenitor cells regulate the regeneration of their niche by secreting Angiopoietin-1. Elife 4, e05521
7. King, K. Y., and Goodell, M. A. (2011) Inflammatory modulation of HSCs: viewing the HSC as a foundation for the immune response. Nat. Rev. Immunol. 11, 685-692
8. Baldridge, M. T., King, K. Y., and Goodell, M. A. (2011) Inflammatory signals regulate hematopoietic stem cells. Trends Immunol. 32, 57-65
9. Espín-Palazón, R., Stachura, D. L., Campbell, C. A., García-Moreno, D., Del Cid, N., Kim, A. D., Candel, S., Meseguer, J., Mulero, V., and Traver, D. (2014) Proinflammatory signaling regulates hematopoietic stem cell emergence. Cell 159, 1070-1085
10. Sawamiphak, S., Kontarakis, Z., and Stainier, D. Y. (2014) Interferon γ signaling positively regulates hematopoietic stem cell emergence. Dev. Cell 31, 640-653
11. Boettcher, S., Gerosa, R. C., Radpour, R., Bauer, J., Ampenberger, F., Heikenwalder, M., Kopf, M., and Manz, M. G. (2014) Endothelial cells translate pathogen signals into G-CSF-driven emergency granulopoiesis. Blood 124, 1393-1403
12. Boiko, J. R., and Borghesi, L. (2012) Hematopoiesis sculpted by pathogens: Toll-like receptors and inflammatory mediators directly activate stem cells. Cytokine 57, 1-8
13. He, Q., Zhang, C., Wang, L., Zhang, P., Ma, D., Lv, J., and Liu, F. (2015) Inflammatory signaling regulates hematopoietic stem and progenitor cell emergence in vertebrates. Blood 125, 1098-1106
14. Nagai, Y., Garrett, K. P., Ohta, S., Bahrun, U., Kouro, T., Akira, S., Takatsu, K., and Kincade, P. W. (2006) Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24, 801-812
15. Schuettpelz, L. G., Borgerding, J. N., Christopher, M. J., Gopalan, P. K., Romine, M. P., Herman, A. C., Woloszynek, J. R., Greenbaum, A. M., and Link, D. C. (2014) G-CSF regulates hematopoietic stem cell activity, in part, through activation of Toll-like receptor signaling. Leukemia 28, 1851-1860
16. Takeuchi, O., and Akira, S. (2010) Pattern recognition receptors and inflammation. Cell 140, 805-820
17. Fiedler, K., Kokai, E., Bresch, S., and Brunner, C. (2013) MyD88 is involved in myeloid as well as lymphoid hematopoiesis independent of the presence of a pathogen. Am. J. Blood Res. 3, 124-140
18. Grassinger, J., Williams, B., Olsen, G. H., Haylock, D. N., and Nilsson, S. K. (2012) Granulocyte colony stimulating factor expands hematopoietic stem cells within the central but not endosteal bone marrow region. Cytokine 58, 218-225
19. Mirantes, C., Passegué, E., and Pietras, E. M. (2014) Pro-inflammatory cytokines: emerging players regulating HSC function in normal and diseased hematopoiesis. Exp. Cell Res. 329, 248-254
20. Zhao, J. L., Ma, C., O'Connell, R. M., Mehta, A., DiLoreto, R., Heath, J. R., and Baltimore, D. (2014) Conversion of danger signals into cytokine signals by hematopoietic stem and progenitor cells for regulation of stressinduced hematopoiesis. Cell Stem Cell 14, 445-459
21. Pietras, E. M., Mirantes-Barbeito, C., Fong, S., Loeffler, D., Kovtonyuk, L. V., Zhang, S., Lakshminarasimhan, R., Chin, C. P., Techner, J. M., Will, B., Nerlov, C., Steidl, U., Manz, M. G., Schroeder, T., and Passegué, E. (2016) Chronic interleukin-1 exposure drives haematopoietic stem cells towards precocious myeloid differentiation at the expense of self-renewal. Nat. Cell Biol. 18, 607-618
22. Colombo, M., Raposo, G., and Théry, C. (2014) Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30, 255-289
23. Costa-Silva, B., Aiello, N. M., Ocean, A. J., Singh, S., Zhang, H., Thakur, B. K., Becker, A., Hoshino, A., Mark, M. T., Molina, H., Xiang, J., Zhang, T., Theilen, T. M., García-Santos, G., Williams, C., et al. (2015) Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat. Cell Biol. 17, 816-826
24. Peinado, H., Alečković, M., Lavotshkin, S., Matei, I., Costa-Silva, B., Moreno-Bueno, G., Hergueta-Redondo, M., Williams, C., García-Santos, G., Ghajar, C., Nitadori-Hoshino, A., Hoffman, C., Badal, K., Garcia, B. A., Callahan, M. K., et al. (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 18, 883-891
25. Huan, J., Hornick, N. I., Goloviznina, N. A., Kamimae-Lanning, A. N., David, L. L., Wilmarth, P. A., Mori, T., Chevillet, J. R., Narla, A., Roberts, C. T., Jr., Loriaux, M. M., Chang, B. H., and Kurre, P. (2015) Coordinate regulation of residual bone marrow function by paracrine trafficking of AML exosomes. Leukemia 29, 2285-2295
26. Huan, J., Hornick, N. I., Shurtleff, M. J., Skinner, A. M., Goloviznina, N. A., Roberts, C. T., Jr, and Kurre, P. (2013) RNA trafficking by acute myelogenous leukemia exosomes. Cancer Res. 73, 918-929
27. Lai, R. C., Yeo, R. W., and Lim, S. K. (2015) Mesenchymal stem cell exosomes. Semin. Cell Dev. Biol. 40, 82-88
28. Frenette, P. S., Pinho, S., Lucas, D., and Scheiermann, C. (2013) Mesenchymal stem cell: keystone of the hematopoietic stem cell niche and a stepping-stone for regenerative medicine. Annu. Rev. Immunol. 31, 285-316
29. Platt, M. O., Roman, A. J., Wells, A., Lauffenburger, D. A., and Griffith, L. G. (2009) Sustained epidermal growth factor receptor levels and activation by tethered ligand binding enhances osteogenic differentiation of multi-potent marrow stromal cells. J. Cell. Physiol. 221, 306-317
30. Zielske, S. P., Livant, D. L., and Lawrence, T. S. (2009) Radiation increases invasion of gene-modified mesenchymal stem cells into tumors. Int. J. Radiat. Oncol. Biol. Phys. 75, 843-853
31. Peister, A., Mellad, J. A., Larson, B. L., Hall, B. M., Gibson, L. F., and Prockop, D. J. (2004) Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103, 1662-1668
32. Soleimani, M., and Nadri, S. (2009) A protocol for isolation and culture of mesenchymal stem cells from mouse bone marrow. Nat. Protoc 4, 102-106
33. Pietras, E. M., Reynaud, D., Kang, Y. A., Carlin, D., Calero-Nieto, F. J., Leavitt, A. D., Stuart, J. M., Göttgens, B., and Passegué, E. (2015) Functionally distinct subsets of lineage-biased multipotent progenitors control blood production in normal and regenerative conditions. Cell Stem Cell 17, 35-46
34. Oguro, H., Ding, L., and Morrison, S. J. (2013) SLAM family markers resolve functionally distinct subpopulations of hematopoietic stem cells and multipotent progenitors. Cell Stem Cell 13, 102-116
35. Muzumdar, M. D., Tasic, B., Miyamichi, K., Li, L., and Luo, L. (2007) A global double-fluorescent Cre reporter mouse. Genesis 45, 593-605
36. Lai, C. P., Kim, E. Y., Badr, C. E., Weissleder, R., Mempel, T. R., Tannous, B. A., and Breakefield, X. O. (2015) Visualization and tracking of tumour extracellular vesicle delivery and RNA translation using multiplexed reporters. Nat. Commun. 6, 7029
37. Burberry, A., Zeng, M. Y., Ding, L., Wicks, I., Inohara, N., Morrison, S. J., and Núñez, G. (2014) Infection mobilizes hematopoietic stem cells through cooperative NOD-like receptor and Toll-like receptor signaling. Cell Host Microbe 15, 779-791
38. Shi, C., Jia, T., Mendez-Ferrer, S., Hohl, T. M., Serbina, N. V., Lipuma, L., Leiner, I., Li, M. O., Frenette, P. S., and Pamer, E. G. (2011) Bone marrow mesenchymal stem and progenitor cells induce monocyte emigration in response to circulating Toll-like receptor ligands. Immunity 34, 590-601
39. Buza-Vidas, N., Duarte, S., Luc, S., Bouriez-Jones, T., Woll, P. S., and Jacobsen, S. E. (2011) GATA3 is redundant for maintenance and selfrenewal of hematopoietic stem cells. Blood 118, 1291-1293
40. Mercier, F. E., Sykes, D. B., and Scadden, D. T. (2016) Single targeted exon mutation creates a true congenic mouse for competitive hematopoietic stem cell transplantation: the C57BL/6-CD45.1STEM mouse. Stem Cell Reports 6, 985-992
41. Zhang, H., Rodriguez, S., Wang, L., Wang, S., Serezani, H., Kapur, R., Cardoso, A. A., and Carlesso, N. (2016) Sepsis induces hematopoietic stem cell exhaustion and myelosuppression through distinct contributions of TRIF and MYD88. Stem Cell Reports 6, 940-956
42. Cantaluppi, V., Gatti, S., Medica, D., Figliolini, F., Bruno, S., Deregibus, M. C., Sordi, A., Biancone, L., Tetta, C., and Camussi, G. (2012) Microvesicles derived from endothelial progenitor cells protect the kidney from ischemia-reperfusion injury by microRNA-dependent reprogramming of resident renal cells. Kidney Int. 82, 412-427
43. Vicencio, J. M., Yellon, D. M., Sivaraman, V., Das, D., Boi-Doku, C., Arjun, S., Zheng, Y., Riquelme, J. A., Kearney, J., Sharma, V., Multhoff, G., Hall, A. R., and Davidson, S. M. (2015) Plasma exosomes protect the myocardium from ischemia-reperfusion injury. J. Am. Coll. Cardiol. 65, 1525-1536
44. Anderson, P., Carrillo-Gálvez, A. B., García-Pérez, A., Cobo, M., and Martín, F. (2013) CD105 (endoglin)-negative murine mesenchymal stromal cells define a new multipotent subpopulation with distinct differentiation and immunomodulatory capacities. PLoS ONE 8, e76979
45. Zhang, B., Yin, Y., Lai, R. C., Tan, S. S., Choo, A. B., and Lim, S. K. (2014) Mesenchymal stem cells secrete immunologically active exosomes. Stem Cells Dev. 23, 1233-1244
46. Zhu, Y. G., Feng, X. M., Abbott, J., Fang, X. H., Hao, Q., Monsel, A., Qu, J. M., Matthay, M. A., and Lee, J. W. (2014) Human mesenchymal stem cell microvesicles for treatment of Escherichia coli endotoxin-induced acute lung injury in mice. Stem Cells 32, 116-125
47. Pinho, S., Lacombe, J., Hanoun, M., Mizoguchi, T., Bruns, I., Kunisaki, Y., and Frenette, P. S. (2013) PDGFRα and CD51 mark human nestin+ sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion. J. Exp. Med. 210, 1351-1367
48. Bretz, N. P., Ridinger, J., Rupp, A. K., Rimbach, K., Keller, S., Rupp, C., Marmé, F., Umansky, L., Umansky, V., Eigenbrod, T., Sammar, M., and Altevogt, P. (2013) Body fluid exosomes promote secretion of inflammatory cytokines in monocytic cells via Toll-like receptor signaling. J. Biol. Chem. 288, 36691-36702
49. Kaulen, D. R., Sanin, A. V., Khorobrykh, V. V., Malikov, V. E., and Dranovskaia, E. A. (1983) [Stimulating action of Brucella melitensis lipopolysaccharide on hemopoiesis in mice]. Zh. Mikrobiol. Epidemiol. Immunobiol. 84-87
50. Nielsen, E., Severin, F., Backer, J. M., Hyman, A. A., and Zerial, M. (1999) Rab5 regulates motility of early endosomes on microtubules. Nat. Cell Biol. 1, 376-382
51. Vanlandingham, P. A., and Ceresa, B. P. (2009) Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J. Biol. Chem. 284, 12110-12124
52. Simon, N. C., and Barbieri, J. T. (2014) Exoenzyme S ADP-ribosylates Rab5 effector sites to uncouple intracellular trafficking. Infect. Immun. 82, 21-28
53. Sahoo, S., and Losordo, D. W. (2014) Exosomes and cardiac repair after myocardial infarction. Circ. Res. 114, 333-344
54. Borggrefe, T., and Oswald, F. (2009) The Notch signaling pathway: transcriptional regulation at Notch target genes. Cell. Mol. Life Sci. 66, 1631-1646
55. Wilson, A. A., Kwok, L. W., Porter, E. L., Payne, J. G., McElroy, G. S., Ohle, S. J., Greenhill, S. R., Blahna, M. T., Yamamoto, K., Jean, J. C., Mizgerd, J. P., and Kotton, D. N. (2013) Lentiviral delivery of RNAi for in vivo lineagespecific modulation of gene expression in mouse lung macrophages. Mol. Ther. 21, 825-833
56. Ciuculescu, M. F., Brendel, C., Harris, C. E., and Williams, D. A. (2014) Retroviral transduction of murine and human hematopoietic progenitors and stem cells. Methods Mol. Biol. 1185, 287-309
57. Nagamoto-Combs, K., Kulas, J., and Combs, C. K. (2014) A novel cell line from spontaneously immortalized murine microglia. J. Neurosci. Methods 233, 187-198
58. Matsunaga, N., Tsuchimori, N., Matsumoto, T., and Ii, M. (2011) TAK-242 (resatorvid), a small-molecule inhibitor of Toll-like receptor (TLR) 4 signaling, binds selectively to TLR4 and interferes with interactions between TLR4 and its adaptor molecules. Mol. Pharmacol. 79, 34-41