Hematopoiesis in steady-state versus stress: Self-renewal, lineage fate choice, and the conversion of danger signals into cytokine signals in hematopoietic stem cells

Journal of Immunology

Volumn 193, Issue 5, 2014, Pages 2053-2058

  Borghesi, Lisa ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CYTOKINE; HISTONE; SPECIAL AT RICH BINDING PROTEIN 1; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; MATRIX ATTACHMENT REGION BINDING PROTEIN; SATB1 PROTEIN, HUMAN;

CELL FATE; CELL LINEAGE; CELL RENEWAL; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DNA METHYLATION; EPIGENETICS; GENETIC TRANSCRIPTION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; IMMUNE RESPONSE; INFECTION; INFLAMMATION; LONG TERM HEMATOPOIETIC STEM CELL; NONHUMAN; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; STEADY STATE; STRESS; TRANSCRIPTION REGULATION; ANIMAL; CYTOLOGY; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

ANIMALS; CYTOKINES; DNA METHYLATION; GENE EXPRESSION REGULATION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HISTONES; HUMANS; MATRIX ATTACHMENT REGION BINDING PROTEINS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84907033653     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1400936     Document Type: Review

References (79)

1. Kharas, M. G., C. J. Lengner, F. Al-Shahrour, L. Bullinger, B. Ball, S. Zaidi, K. Morgan, W. Tam, M. Paktinat, R. Okabe, et al. 2010. Musashi-2 regulates normal hematopoiesis and promotes aggressive myeloid leukemia. Nat. Med. 16: 903-908.
2. Laslo, P., C. J. Spooner, A. Warmflash, D. W. Lancki, H. J. Lee, R. Sciammas, B. N. Gantner, A. R. Dinner, and H. Singh. 2006. Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell 126: 755-766.
3. Wu, M., H. Y. Kwon, F. Rattis, J. Blum, C. Zhao, R. Ashkenazi, T. L. Jackson, N. Gaiano, T. Oliver, and T. Reya. 2007. Imaging hematopoietic precursor division in real time. Cell Stem Cell 1: 541-554.
4. Georgescu, C., W. J. Longabaugh, D. D. Scripture-Adams, E. S. David-Fung, M. A. Yui, M. A. Zarnegar, H. Bolouri, and E. V. Rothenberg. 2008. A gene regulatory network armature for T lymphocyte specification. Proc. Natl. Acad. Sci. USA 105: 20100-20105.
5. Lin, Y. C., C. Benner, R. Mansson, S. Heinz, K. Miyazaki, M. Miyazaki, V. Chandra, C. Bossen, C. K. Glass, and C. Murre. 2012. Global changes in the nuclear positioning of genes and intra- and interdomain genomic interactions that orchestrate B cell fate. Nat. Immunol. 13: 1196-1204.
6. Mansson, R., E. Welinder, J. Åhsberg, Y. C. Lin, C. Benner, C. K. Glass, J. S. Lucas, M. Sigvardsson, and C. Murre. 2012. Positive intergenic feedback circuitry, involving EBF1 and FOXO1, orchestrates B-cell fate. Proc. Natl. Acad. Sci. USA 109: 21028-21033.
7. Spooner, C. J., J. X. Cheng, E. Pujadas, P. Laslo, and H. Singh. 2009. A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates. Immunity 31: 576-586.
8. Rothenberg, E. V. 2014. Transcriptional control of early T and B cell developmental choices. Annu. Rev. Immunol. 32: 283-321.
9. Bernstein, B. E., T. S. Mikkelsen, X. Xie, M. Kamal, D. J. Huebert, J. Cuff, B. Fry, A. Meissner, M. Wernig, K. Plath, et al. 2006. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125: 315-326.
10. Bröske, A. M., L. Vockentanz, S. Kharazi, M. R. Huska, E. Mancini, M. Scheller, C. Kuhl, A. Enns, M. Prinz, R. Jaenisch, et al. 2009. DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction. Nat. Genet. 41: 1207-1215.
11. Spivakov, M., and A. G. Fisher. 2007. Epigenetic signatures of stem-cell identity. Nat. Rev. Genet. 8: 263-271.
12. Weishaupt, H., M. Sigvardsson, and J. L. Attema. 2010. Epigenetic chromatin states uniquely define the developmental plasticity of murine hematopoietic stem cells. Blood 115: 247-256.
13. Esplin, B. L., T. Shimazu, R. S. Welner, K. P. Garrett, L. Nie, Q. Zhang, M. B. Humphrey, Q. Yang, L. A. Borghesi, and P. W. Kincade. 2011. Chronic exposure to a TLR ligand injures hematopoietic stem cells. J. Immunol. 186: 5367-5375.
14. Massberg, S., P. Schaerli, I. Knezevic-Maramica, M. Köllnberger, N. Tubo, E. A. Moseman, I. V. Huff, T. Junt, A. J. Wagers, I. B. Mazo, and U. H. von Andrian. 2007. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 131: 994-1008.
15. Nagai, Y., K. P. Garrett, S. Ohta, U. Bahrun, T. Kouro, S. Akira, K. Takatsu, and P. W. Kincade. 2006. Toll-like receptors on hematopoietic progenitor cells stimulate innate immune system replenishment. Immunity 24: 801-812.
16. Zhao, J. L., C. Ma, R. M. O'Connell, A. Mehta, R. DiLoreto, J. R. Heath, and D. Baltimore. 2014. Conversion of danger signals into cytokine signals by hematopoietic stem and progenitor cells for regulation of stress-induced hematopoiesis. Cell Stem Cell 14: 445-459.
17. Notta, F., S. Doulatov, E. Laurenti, A. Poeppl, I. Jurisica, and J. E. Dick. 2011. Isolation of single human hematopoietic stem cells capable of long-term multilineage engraftment. Science 333: 218-221.
18. Yamamoto, R., Y. Morita, J. Ooehara, S. Hamanaka, M. Onodera, K. L. Rudolph, H. Ema, and H. Nakauchi. 2013. Clonal analysis unveils self-renewing lineagerestricted progenitors generated directly from hematopoietic stem cells. Cell 154: 1112-1126.
19. Adolfsson, J., R. Månsson, N. Buza-Vidas, A. Hultquist, K. Liuba, C. T. Jensen, D. Bryder, L. Yang, O. J. Borge, L. A. Thoren, et al. 2005. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121: 295-306.
20. Forsberg, E. C., T. Serwold, S. Kogan, I. L. Weissman, and E. Passegué. 2006. New evidence supporting megakaryocyte-erythrocyte potential of flk2/flt3+ multipotent hematopoietic progenitors. Cell 126: 415-426.
21. Kohn, L. A., Q. L. Hao, R. Sasidharan, C. Parekh, S. Ge, Y. Zhu, H. K. Mikkola, and G. M. Crooks. 2012. Lymphoid priming in human bone marrow begins before expression of CD10 with upregulation of L-selectin. Nat. Immunol. 13: 963-971.
22. Igarashi, H., S. C. Gregory, T. Yokota, N. Sakaguchi, and P. W. Kincade. 2002. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 17: 117-130.
23. Kondo, M., I. L. Weissman, and K. Akashi. 1997. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91: 661-672.
24. Mansson, R., S. Zandi, E. Welinder, P. Tsapogas, N. Sakaguchi, D. Bryder, and M. Sigvardsson. 2010. Single-cell analysis of the common lymphoid progenitor compartment reveals functional and molecular heterogeneity. Blood 115: 2601-2609.
25. Bell, J. J., and A. Bhandoola. 2008. The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature 452: 764-767.
26. Akashi, K., D. Traver, T. Miyamoto, and I. L.Weissman. 2000. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404: 193-197.
27. Manz, M. G., T. Miyamoto, K. Akashi, and I. L. Weissman. 2002. Prospective isolation of human clonogenic common myeloid progenitors. Proc. Natl. Acad. Sci. USA 99: 11872-11877.
28. Zimdahl, B., T. Ito, A. Blevins, J. Bajaj, T. Konuma, J. Weeks, C. S. Koechlein, H. Y. Kwon, O. Arami, D. Rizzieri, et al. 2014. Lis1 regulates asymmetric division in hematopoietic stem cells and in leukemia. Nat. Genet. 46: 245-252.
29. Mathas, S., M. Janz, F. Hummel, M. Hummel, B. Wollert-Wulf, S. Lusatis, I. Anagnostopoulos, A. Lietz, M. Sigvardsson, F. Jundt, et al. 2006. Intrinsic inhibition of transcription factor E2A by HLH proteins ABF-1 and Id2 mediates reprogramming of neoplastic B cells in Hodgkin lymphoma. Nat. Immunol. 7: 207-215.
30. Mullighan, C. G., S. Goorha, I. Radtke, C. B. Miller, E. Coustan-Smith, J. D. Dalton, K. Girtman, S. Mathew, J. Ma, S. B. Pounds, et al. 2007. Genomewide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature 446: 758-764.
31. Rosenbauer, F., K. Wagner, J. L. Kutok, H. Iwasaki, M. M. Le Beau, Y. Okuno, K. Akashi, S. Fiering, and D. G. Tenen. 2004. Acute myeloid leukemia induced by graded reduction of a lineage-specific transcription factor, PU.1. Nat. Genet. 36: 624-630.
32. Back, J., A. Dierich, C. Bronn, P. Kastner, and S. Chan. 2004. PU.1 determines the self-renewal capacity of erythroid progenitor cells. Blood 103: 3615-3623.
33. DeKoter, R. P., and H. Singh. 2000. Regulation of B lymphocyte and macrophage development by graded expression of PU.1. Science 288: 1439-1441.
34. Kim, H. G., C. G. de Guzman, C. S. Swindle, C. V. Cotta, L. Gartland, E. W. Scott, and C. A. Klug. 2004. The ETS family transcription factor PU.1 is necessary for the maintenance of fetal liver hematopoietic stem cells. Blood 104: 3894-3900.
35. Arinobu, Y., S. Mizuno, Y. Chong, H. Shigematsu, T. Iino, H. Iwasaki, T. Graf, R. Mayfield, S. Chan, P. Kastner, and K. Akashi. 2007. Reciprocal activation of GATA-1 and PU.1 marks initial specification of hematopoietic stem cells into myeloerythroid and myelolymphoid lineages. Cell Stem Cell 1: 416-427.
36. Medina, K. L., J. M. Pongubala, K. L. Reddy, D. W. Lancki, R. Dekoter, M. Kieslinger, R. Grosschedl, and H. Singh. 2004. Assembling a gene regulatory network for specification of the B cell fate. Dev. Cell 7: 607-617.
37. Heinz, S., C. Benner, N. Spann, E. Bertolino, Y. C. Lin, P. Laslo, J. X. Cheng, C. Murre, H. Singh, and C. K. Glass. 2010. Simple combinations of lineagedetermining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell 38: 576-589.
38. Dias, S., R. Månsson, S. Gurbuxani, M. Sigvardsson, and B. L. Kee. 2008. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 29: 217-227.
39. Georgopoulos, K., M. Bigby, J. H. Wang, A. Molnar, P. Wu, S. Winandy, and A. Sharpe. 1994. The Ikaros gene is required for the development of all lymphoid lineages. Cell 79: 143-156.
40. Semerad, C. L., E. M. Mercer, M. A. Inlay, I. L. Weissman, and C. Murre. 2009. E2A proteins maintain the hematopoietic stem cell pool and promote the maturation of myelolymphoid and myeloerythroid progenitors. Proc. Natl. Acad. Sci. USA 106: 1930-1935.
41. van Galen, P., A. Kreso, E. Wienholds, E. Laurenti, K. Eppert, E. R. Lechman, N. Mbong, K. Hermans, S. Dobson, C. April, et al. 2014. Reduced lymphoid lineage priming promotes human hematopoietic stem cell expansion. Cell Stem Cell 14: 94-106.
42. Yang, Q., B. Esplin, and L. Borghesi. 2011. E47 regulates hematopoietic stem cell proliferation and energetics but not myeloid lineage restriction. Blood 117: 3529-3538.
43. Yang, Q., L. Kardava, A. St Leger, K. Martincic, B. Varnum-Finney, I. D. Bernstein, C. Milcarek, and L. Borghesi. 2008. E47 controls the developmental integrity and cell cycle quiescence of multipotential hematopoietic progenitors. J. Immunol. 181: 5885-5894.
44. Santos, P. M., Y. Ding, and L. Borghesi. 2014. Cell-intrinsic in vivo requirement for the E47-p21 pathway in long-term hematopoietic stem cells. J. Immunol. 192: 160-168.
45. Papathanasiou, P., J. L. Attema, H. Karsunky, N. Hosen, Y. Sontani, G. F. Hoyne, R. Tunningley, S. T. Smale, and I. L. Weissman. 2009. Self-renewal of the longterm reconstituting subset of hematopoietic stem cells is regulated by Ikaros. Stem Cells 27: 3082-3092.
46. Winandy, S., P. Wu, and K. Georgopoulos. 1995. A dominant mutation in the Ikaros gene leads to rapid development of leukemia and lymphoma. Cell 83: 289-299.
47. DeKoter, R. P., H. J. Lee, and H. Singh. 2002. PU.1 regulates expression of the interleukin-7 receptor in lymphoid progenitors. Immunity 16: 297-309.
48. Borghesi, L., J. Aites, S. Nelson, P. Lefterov, P. James, and R. Gerstein. 2005. E47 is required for V(D)J recombinase activity in common lymphoid progenitors. J. Exp. Med. 202: 1669-1677.
49. Treiber, T., E. M. Mandel, S. Pott, I. Györy, S. Firner, E. T. Liu, and R. Grosschedl. 2010. Early B cell factor 1 regulates B cell gene networks by activation, repression, and transcription-independent poising of chromatin. Immunity 32: 714-725.
50. Boos, M. D., Y. Yokota, G. Eberl, and B. L. Kee. 2007. Mature natural killer cell and lymphoid tissue-inducing cell development requires Id2-mediated suppression of E protein activity. J. Exp. Med. 204: 1119-1130.
51. Dickinson, L. A., T. Joh, Y. Kohwi, and T. Kohwi-Shigematsu. 1992. A tissuespecific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell 70: 631-645.
52. Dickinson, L. A., C. D. Dickinson, and T. Kohwi-Shigematsu. 1997. An atypical homeodomain in SATB1 promotes specific recognition of the key structural element in a matrix attachment region. J. Biol. Chem. 272: 11463-11470.
53. Kirillov, A., B. Kistler, R. Mostoslavsky, H. Cedar, T. Wirth, and Y. Bergman. 1996. A role for nuclear NF-kappaB in B-cell-specific demethylation of the Igkappa locus. Nat. Genet. 13: 435-441.
54. Cai, S., H. J. Han, and T. Kohwi-Shigematsu. 2003. Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat. Genet. 34: 42-51.
55. Notani, D., K. P. Gottimukkala, R. S. Jayani, A. S. Limaye, M. V. Damle, S. Mehta, P. K. Purbey, J. Joseph, and S. Galande. 2010. Global regulator SATB1 recruits beta-catenin and regulates T(H)2 differentiation in Wnt-dependent manner. PLoS Biol. 8: e1000296.
56. Alvarez, J. D., D. H. Yasui, H. Niida, T. Joh, D. Y. Loh, and T. Kohwi-Shigematsu. 2000. The MAR-binding protein SATB1 orchestrates temporal and spatial expression of multiple genes during T-cell development. Genes Dev. 14: 521-535.
57. Yasui, D., M. Miyano, S. Cai, P. Varga-Weisz, and T. Kohwi-Shigematsu. 2002. SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419: 641-645.
58. Wen, J., S. Huang, H. Rogers, L. A. Dickinson, T. Kohwi-Shigematsu, and C. T. Noguchi. 2005. SATB1 family protein expressed during early erythroid differentiation modifies globin gene expression. Blood 105: 3330-3339.
59. Savarese, F., A. Dávila, R. Nechanitzky, I. De La Rosa-Velazquez, C. F. Pereira, R. Engelke, K. Takahashi, T. Jenuwein, T. Kohwi-Shigematsu, A. G. Fisher, and R. Grosschedl. 2009. Satb1 and Satb2 regulate embryonic stem cell differentiation and Nanog expression. Genes Dev. 23: 2625-2638.
60. Will, B., T. O. Vogler, B. Bartholdy, F. Garrett-Bakelman, J. Mayer, L. Barreyro, A. Pandolfi, T. I. Todorova, U. C. Okoye-Okafor, R. F. Stanley, et al. 2013. Satb1 regulates the self-renewal of hematopoietic stem cells by promoting quiescence and repressing differentiation commitment. Nat. Immunol. 14: 437-445.
61. Satoh, Y., T. Yokota, T. Sudo, M. Kondo, A. Lai, P. W. Kincade, T. Kouro, R. Iida, K. Kokame, T. Miyata, et al. 2013. The Satb1 protein directs hematopoietic stem cell differentiation toward lymphoid lineages. Immunity 38: 1105-1115.
62. Rosenbauer, F., B. M. Owens, L. Yu, J. R. Tumang, U. Steidl, J. L. Kutok, L. K. Clayton, K. Wagner, M. Scheller, H. Iwasaki, et al. 2006. Lymphoid cell growth and transformation are suppressed by a key regulatory element of the gene encoding PU.1. Nat. Genet. 38: 27-37.
63. De Luca, K., V. Frances-Duvert, M. J. Asensio, R. Ihsani, E. Debien, M. Taillardet, E. Verhoeyen, C. Bella, S. Lantheaume, L. Genestier, and T. Defrance. 2009. The TLR1/2 agonist PAM(3)CSK(4) instructs commitment of human hematopoietic stem cells to a myeloid cell fate. Leukemia 23: 2063-2074.
64. Reece, P., A. Thanendran, L. Crawford, M. K. Tulic, L. Thabane, S. L. Prescott, R. Sehmi, and J. A. Denburg. 2011. Maternal allergy modulates cord blood hematopoietic progenitor Toll-like receptor expression and function. J. Allergy Clin. Immunol. 127: 447-453.
65. Sioud, M., and Y. Fløisand. 2007. TLR agonists induce the differentiation of human bone marrow CD34+ progenitors into CD11c+ CD80/86+ DC capable of inducing a Th1-type response. Eur. J. Immunol. 37: 2834-2846.
66. Sioud, M., and Y. Fløisand. 2009. NOD2/CARD15 on bone marrow CD34+ hematopoietic cells mediates induction of cytokines and cell differentiation. J. Leukoc. Biol. 85: 939-946.
67. Sioud, M., Y. Fløisand, L. Forfang, and F. Lund-Johansen. 2006. Signaling through toll-like receptor 7/8 induces the differentiation of human bone marrow CD34+ progenitor cells along the myeloid lineage. J. Mol. Biol. 364: 945-954.
68. Takizawa, H., S. Boettcher, and M. G. Manz. 2012. Demand-adapted regulation of early hematopoiesis in infection and inflammation. Blood 119: 2991-3002.
69. Baldridge, M. T., K. Y. King, N. C. Boles, D. C. Weksberg, and M. A. Goodell. 2010. Quiescent haematopoietic stem cells are activated by IFN-gamma in response to chronic infection. Nature 465: 793-797.
70. Bernad, A., M. Kopf, R. Kulbacki, N. Weich, G. Koehler, and J. C. Gutierrez- Ramos. 1994. Interleukin-6 is required in vivo for the regulation of stem cells and committed progenitors of the hematopoietic system. Immunity 1: 725-731.
71. Pronk, C. J., O. P. Veiby, D. Bryder, and S. E. Jacobsen. 2011. Tumor necrosis factor restricts hematopoietic stem cell activity in mice: involvement of two distinct receptors. J. Exp. Med. 208: 1563-1570.
72. Rebel, V. I., S. Hartnett, G. R. Hill, S. B. Lazo-Kallanian, J. L. Ferrara, and C. A. Sieff. 1999. Essential role for the p55 tumor necrosis factor receptor in regulating hematopoiesis at a stem cell level. J. Exp. Med. 190: 1493-1504.
73. McKinstry, W. J., C. L. Li, J. E. Rasko, N. A. Nicola, G. R. Johnson, and D. Metcalf. 1997. Cytokine receptor expression on hematopoietic stem and progenitor cells. Blood 89: 65-71.
74. Pavan Kumar, P., P. K. Purbey, C. K. Sinha, D. Notani, A. Limaye, R. S. Jayani, and S. Galande. 2006. Phosphorylation of SATB1, a global gene regulator, acts as a molecular switch regulating its transcriptional activity in vivo. Mol. Cell 22: 231-243.
75. Tan, J. A., J. Song, Y. Chen, and L. K. Durrin. 2010. Phosphorylation-dependent interaction of SATB1 and PIAS1 directs SUMO-regulated caspase cleavage of SATB1. Mol. Cell. Biol. 30: 2823-2836.
76. Galande, S., L. A. Dickinson, I. S. Mian, M. Sikorska, and T. Kohwi-Shigematsu. 2001. SATB1 cleavage by caspase 6 disrupts PDZ domain-mediated dimerization, causing detachment from chromatin early in T-cell apoptosis. Mol. Cell. Biol. 21: 5591-5604.
77. Ng, S. Y., T. Yoshida, J. Zhang, and K. Georgopoulos. 2009. Genome-wide lineage-specific transcriptional networks underscore Ikaros-dependent lymphoid priming in hematopoietic stem cells. Immunity 30: 493-507.
78. Morrison, S. J., and D. T. Scadden. 2014. The bone marrow niche for haematopoietic stem cells. Nature 505: 327-334.
79. Naik, S. H., L. Perié, E. Swart, C. Gerlach, N. van Rooij, R. J. de Boer, and T. N. Schumacher. 2013. Diverse and heritable lineage imprinting of early haematopoietic progenitors. Nature 496: 229-232.