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Cited by 289Hematopoietic Stem Cell TransplantationMesenchymal stem cell researchAcute Myeloid Leukemia Research

Inflammation as a regulator of hematopoietic stem cell function in disease, aging, and clonal selection

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Caiado, Francisco, Pietras, Eric M., Manz, Markus G.·2021·Journal of Experimental Medicine
DOI 10.1084/jem.20201541PMC PMC8210622
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Abstract

Inflammation is an evolutionarily selected defense response to infection or tissue damage that involves activation and consumption of immune cells in order to reestablish and maintain organismal integrity. In this process, hematopoietic stem cells (HSCs) are themselves exposed to inflammatory cues and via proliferation and differentiation, replace mature immune cells in a demand-adapted fashion. Here, we review how major sources of systemic inflammation act on and subsequently shape HSC fate and function. We highlight how lifelong inflammatory exposure contributes to HSC inflamm-aging and selection of premalignant HSC clones. Finally, we explore emerging areas of interest and open questions remaining in the field.

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  • PU.1's braking mechanism allows sufficient myeloid expansion for host defense while preventing aberrant expansion of progenitor pools.

    “allowing for sufficient myeloid expansion for host defense while preventing aberrant expansion of progenitor pools (Caiado et al., 2021).”

    From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Caiado et al., 2021

    The IL-1 section (page unavailable) describes PU.1 activation as a proliferation-limiting mechanism: PU.1-deficient HSCs instead show aberrant proliferation and pool expansion. It also says PU.1 facilitates myeloid differentiation, and the Introduction links myeloid cells to host defense. The paper does not establish that PU.1’s braking mechanism permits sufficient myeloid expansion for host defense. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • Emergency myelopoiesis is a critical response to physiological insults that supplies the host with enough innate immune cells to fight infections and/or contribute to repair and immunosurveillance of damaged tissues.

    ““Emergency” myelopoiesis is a critical response to physiological insults that supplies the host with enough innate immune cells to fight infections and/or contribute to the repair and immunosurveillance of damaged tissues (Caiado et al., 2021; Collins et al., 2021).”

    From PU.1 is required to restrain myelopoiesis during chronic inflammatory stress (2023) · cites this paper as Caiado et al., 2021

    The Introduction describes emergency hematopoiesis as increased blood-cell production in response to stress such as infection, and identifies leukocytes as serving host defense. It does not say that emergency myelopoiesis supplies cells for the repair or immunosurveillance of damaged tissues; its separate discussion of immune surveillance concerns elimination of mutated cell clones. (LLM, conf=0.84)

    Experimental — accuracy not yet measured

  • There is emerging evidence that clonal HSCs can become inflammation-adapted and by altering the response to inflammatory challenges, mutations can thus confer a fitness advantage to HSCs.

    “There is emerging evidence that clonal HSCs can become inflammation-adapted47–49 and by altering the response to inflammatory challenges, mutations can thus confer a fitness advantage to HSCs.”

    From Single-cell multi-omics identifies chronic inflammation as a driver of TP53-mutant leukemic evolution (2023) · cites this paper as [47]

  • Inflammation is a cardinal regulator of HSC function with many effects on HSC fate and function, including proliferation-induced DNA-damage and depletion of HSCs.

    “Inflammation is a cardinal regulator of HSC function with many effects on HSC fate and function47, including proliferation-induced DNA-damage and depletion of HSCs41.”

    From Single-cell multi-omics identifies chronic inflammation as a driver of TP53-mutant leukemic evolution (2023) · cites this paper as [47]

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Research works printed but not linked: 157

  1. Abegunde, S.O., R. Buckstein, R.A. Wells, and M.J. Rauh. 2018. An inflammatory environment containing TNFα favors Tet2-mutant clonal hematopoiesis. Exp. Hematol. 59: 60– 65. 10.1016/j.exphem.2017.11.002 29195897 · DOI · Paper page
  2. Arandjelovic, S., and K.S. Ravichandran. 2015. Phagocytosis of apoptotic cells in homeostasis. Nat. Immunol. 16: 907– 917. 10.1038/ni.3253 26287597 PMC4826466 · DOI · Paper page
  3. Arranz, L., A. Sánchez-Aguilera, D. Martín-Pérez, J. Isern, X. Langa, A. Tzankov, P. Lundberg, S. Muntión, Y.S. Tzeng, D.M. Lai,. 2014. Neuropathy of haematopoietic stem cell niche is essential for myeloproliferative neoplasms. Nature. 512: 78– 81. 10.1038/nature13383 25043017 · DOI · Paper page
  4. 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-γ in response to chronic infection. Nature. 465: 793– 797. 10.1038/nature09135 20535209 PMC2935898 · DOI · Paper page
  5. Balmer, M.L., C.M. Schürch, Y. Saito, M.B. Geuking, H. Li, M. Cuenca, L.V. Kovtonyuk, K.D. McCoy, S. Hapfelmeier, A.F. Ochsenbein,. 2014. Microbiota-derived compounds drive steady-state granulopoiesis via MyD88/TICAM signaling. J. Immunol. 193: 5273– 5283. 10.4049/jimmunol.1400762 25305320 · DOI
  6. Baylis, D., D.B. Bartlett, H.P. Patel, and H.C. Roberts. 2013. Understanding how we age: insights into inflammaging. Longev. Healthspan. 2: 8. 10.1186/2046-2395-2-8 24472098 PMC3922951 · DOI
  7. Beerman, I., J. Seita, M.A. Inlay, I.L. Weissman, and D.J. Rossi. 2014. Quiescent hematopoietic stem cells accumulate DNA damage during aging that is repaired upon entry into cell cycle. Cell Stem Cell. 15: 37– 50. 10.1016/j.stem.2014.04.016 24813857 PMC4082747 · DOI · Paper page
  8. Bernitz, J.M., H.S. Kim, B. MacArthur, H. Sieburg, and K. Moore. 2016. Hematopoietic stem cells count and remember self-renewal divisions. Cell. 167: 1296– 1309.e10. 10.1016/j.cell.2016.10.022 27839867 PMC5115957 · DOI · Paper page
  9. Bernitz, J.M., M.G. Daniel, Y.S. Fstkchyan, and K. Moore. 2017. Granulocyte colony-stimulating factor mobilizes dormant hematopoietic stem cells without proliferation in mice. Blood. 129: 1901– 1912. 10.1182/blood-2016-11-752923 28179275 PMC5383874 · DOI
  10. Binder, D., J. Fehr, H. Hengartner, and R.M. Zinkernagel. 1997. Virus-induced transient bone marrow aplasia: major role of interferon-α/β during acute infection with the noncytopathic lymphocytic choriomeningitis virus. J. Exp. Med. 185: 517– 530. 10.1084/jem.185.3.517 9053452 PMC2196026 · DOI
  11. Binder, S., M. Luciano, and J. Horejs-Hoeck. 2018. The cytokine network in acute myeloid leukemia (AML): A focus on pro- and anti-inflammatory mediators. Cytokine Growth Factor Rev. 43: 8– 15. 10.1016/j.cytogfr.2018.08.004 30181021 · DOI · Paper page
  12. Boettcher, S., and B.L. Ebert. 2019. Clonal hematopoiesis of indeterminate potential. J. Clin. Oncol. 37: 419– 422. 10.1200/JCO.2018.79.3588 30589599 · DOI
  13. Bordoni, V., D. Viola, A. Sacchi, C. Pinnetti, R. Casetti, E. Cimini, N. Tumino, A. Antinori, A. Ammassari, and C. Agrati. 2018. IL-18 and Stem Cell Factor affect hematopoietic progenitor cells in HIV-infected patients treated during primary HIV infection. Cytokine. 103: 34– 37. 10.1016/j.cyto.2017.12.033 29324258 · DOI
  14. Brunner, S.F., N.D. Roberts, L.A. Wylie, L. Moore, S.J. Aitken, S.E. Davies, M.A. Sanders, P. Ellis, C. Alder, Y. Hooks,. 2019. Somatic mutations and clonal dynamics in healthy and cirrhotic human liver. Nature. 574: 538– 542. 10.1038/s41586-019-1670-9 31645727 PMC6837891 · DOI · Paper page
  15. Bujanover, N., O. Goldstein, Y. Greenshpan, H. Turgeman, A. Klainberger, Y. Scharff, and R. Gazit. 2018. Identification of immune-activated hematopoietic stem cells. Leukemia. 32: 2016– 2020. 10.1038/s41375-018-0220-z 30042413 PMC6127088 · DOI
  16. Burberry, A., M.Y. Zeng, L. Ding, I. Wicks, N. Inohara, S.J. Morrison, and G. Núñez. 2014. Infection mobilizes hematopoietic stem cells through cooperative NOD-like receptor and Toll-like receptor signaling. Cell Host Microbe. 15: 779– 791. 10.1016/j.chom.2014.05.004 24882704 PMC4085166 · DOI
  17. Cai, Z., J.J. Kotzin, B. Ramdas, S. Chen, S. Nelanuthala, L.R. Palam, R. Pandey, R.S. Mali, Y. Liu, M.R. Kelley,. 2018. Inhibition of inflammatory signaling in Tet2 mutant preleukemic cells mitigates stress-induced abnormalities and clonal hematopoiesis. Cell Stem Cell. 23: 833– 849.e5. 10.1016/j.stem.2018.10.013 30526882 PMC6317370 · DOI · Paper page
  18. Cain, D.W., P.B. Snowden, G.D. Sempowski, and G. Kelsoe. 2011. Inflammation triggers emergency granulopoiesis through a density-dependent feedback mechanism. PLoS One. 6: e19957. 10.1371/journal.pone.0019957 21655273 PMC3104996 · DOI · Paper page
  19. Chalayer, E., N. Costedoat-Chalumeau, O. Beyne-Rauzy, J. Ninet, S. Durupt, J. Tebib, B. Asli, O. Lambotte, M. Ffrench, C. Vasselon, and P. Cathébras. 2017. Bone marrow involvement in systemic lupus erythematosus. QJM. 110: 701– 711. 10.1093/qjmed/hcx102 28525589 · DOI
  20. Challen, G.A., D. Sun, M. Jeong, M. Luo, J. Jelinek, J.S. Berg, C. Bock, A. Vasanthakumar, H. Gu, Y. Xi,. 2012. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat. Genet. 44: 23– 31. 10.1038/ng.1009 PMC3637952 22138693 · DOI · Paper page
  21. Challen, G.A., D. Sun, A. Mayle, M. Jeong, M. Luo, B. Rodriguez, C. Mallaney, H. Celik, L. Yang, Z. Xia,. 2014. Dnmt3a and Dnmt3b have overlapping and distinct functions in hematopoietic stem cells. Cell Stem Cell. 15: 350– 364. 10.1016/j.stem.2014.06.018 25130491 PMC4163922 · DOI · Paper page
  22. Chen, J., X. Feng, M.J. Desierto, K. Keyvanfar, and N.S. Young. 2015. IFN-γ-mediated hematopoietic cell destruction in murine models of immune-mediated bone marrow failure. Blood. 126: 2621– 2631. 10.1182/blood-2015-06-652453 26491068 PMC4671109 · DOI · Paper page
  23. Choi, H.H., K.K. Kim, K.D. Kim, H.J. Kim, E.K. Jo, and C.H. Song. 2011. Effects of mycobacterial infection on proliferation of hematopoietic precursor cells. Microbes Infect. 13: 1252– 1260. 10.1016/j.micinf.2011.08.001 21864704 · DOI
  24. Citrin, D.E., and J.B. Mitchell. 2017. Mechanisms of normal tissue injury from irradiation. Semin. Radiat. Oncol. 27: 316– 324. 10.1016/j.semradonc.2017.04.001 28865514 PMC5653270 · DOI
  25. Colmegna, I., and C.M. Weyand. 2011. Haematopoietic stem and progenitor cells in rheumatoid arthritis. Rheumatology (Oxford). 50: 252– 260. 10.1093/rheumatology/keq298 20837497 PMC3021951 · DOI · Paper page
  26. Colmegna, I., A. Diaz-Borjon, H. Fujii, L. Schaefer, J.J. Goronzy, and C.M. Weyand. 2008. Defective proliferative capacity and accelerated telomeric loss of hematopoietic progenitor cells in rheumatoid arthritis. Arthritis Rheum. 58: 990– 1000. 10.1002/art.23287 18383391 PMC2820283 · DOI · Paper page
  27. Cook, E.K., T. Izukawa, S. Young, G. Rosen, M. Jamali, L. Zhang, D. Johnson, E. Bain, J. Hilland, C.K. Ferrone,. 2019. Comorbid and inflammatory characteristics of genetic subtypes of clonal hematopoiesis. Blood Adv. 3: 2482– 2486. 10.1182/bloodadvances.2018024729 31434682 PMC6712533 · DOI
  28. Cook, E.K., M. Luo, and M.J. Rauh. 2020. Clonal hematopoiesis and inflammation: Partners in leukemogenesis and comorbidity. Exp. Hematol. 83: 85– 94. 10.1016/j.exphem.2020.01.011 32001341 · DOI
  29. Corces-Zimmerman, M.R., and R. Majeti. 2014. Pre-leukemic evolution of hematopoietic stem cells: the importance of early mutations in leukemogenesis. Leukemia. 28: 2276– 2282. 10.1038/leu.2014.211 25005245 PMC4262622 · DOI
  30. Cordua, S., L. Kjaer, V. Skov, N. Pallisgaard, H.C. Hasselbalch, and C. Ellervik. 2019. Prevalence and phenotypes of JAK2 V617F and calreticulin mutations in a Danish general population. Blood. 134: 469– 479. 10.1182/blood.2019001113 31217187 · DOI
  31. Craver, B.M., K. El Alaoui, R.M. Scherber, and A.G. Fleischman. 2018. The Critical role of inflammation in the pathogenesis and progression of myeloid malignancies. Cancers (Basel). 10: 104. 10.3390/cancers10040104 PMC5923359 29614027 · DOI
  32. Cyprus, G.N., J.W. Overlin, K.M. Hotchkiss, S. Kandalam, and R. Olivares-Navarrete. 2018. Cigarette smoke increases pro-inflammatory markers and inhibits osteogenic differentiation in experimental exposure model. Acta Biomater. 76: 308– 318. 10.1016/j.actbio.2018.06.018 29902595 · DOI
  33. Damia, G., K.L. Komschlies, H. Futami, T. Back, M.E. Gruys, D.L. Longo, J.R. Keller, F.W. Ruscetti, and R.H. Wiltrout. 1992. Prevention of acute chemotherapy-induced death in mice by recombinant human interleukin 1: protection from hematological and nonhematological toxicities. Cancer Res. 52: 4082– 4089. 1638519
  34. Dawoud, A.A.Z., W.J. Tapper, and N.C.P. Cross. 2020. Clonal myelopoiesis in the UK Biobank cohort: ASXL1 mutations are strongly associated with smoking. Leukemia. 34: 2660– 2672. 10.1038/s41375-020-0896-8 32518416 · DOI
  35. de Bruin, A.M., Ö. Demirel, B. Hooibrink, C.H. Brandts, and M.A. Nolte. 2013. Interferon-γ impairs proliferation of hematopoietic stem cells in mice. Blood. 121: 3578– 3585. 10.1182/blood-2012-05-432906 23487025 · DOI
  36. Deshmukh, H.S., Y. Liu, O.R. Menkiti, J. Mei, N. Dai, C.E. O’Leary, P.M. Oliver, J.K. Kolls, J.N. Weiser, and G.S. Worthen. 2014. The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice. Nat. Med. 20: 524– 530. 10.1038/nm.3542 24747744 PMC4016187 · DOI · Paper page
  37. Ehninger, A., T. Boch, H. Uckelmann, M.A. Essers, K. Müdder, B.P. Sleckman, and A. Trumpp. 2014. Posttranscriptional regulation of c-Myc expression in adult murine HSCs during homeostasis and interferon-α-induced stress response. Blood. 123: 3909– 3913. 10.1182/blood-2013-10-531038 24795346 · DOI
  38. Ergen, A.V., N.C. Boles, and M.A. Goodell. 2012. Rantes/Ccl5 influences hematopoietic stem cell subtypes and causes myeloid skewing. Blood. 119: 2500– 2509. 10.1182/blood-2011-11-391730 22289892 PMC3311273 · DOI · Paper page
  39. Essers, M.A.G., S. Offner, W.E. Blanco-Bose, Z. Waibler, U. Kalinke, M.A. Duchosal, and A. Trumpp. 2009. IFNalpha activates dormant haematopoietic stem cells in vivo. Nature. 458: 904– 908. 10.1038/nature07815 19212321 · DOI · Paper page
  40. Fleischman, A.G., K.J. Aichberger, S.B. Luty, T.G. Bumm, C.L. Petersen, S. Doratotaj, K.B. Vasudevan, D.H. LaTocha, F. Yang, R.D. Press,. 2011. TNFα facilitates clonal expansion of JAK2V617F positive cells in myeloproliferative neoplasms. Blood. 118: 6392– 6398. 10.1182/blood-2011-04-348144 21860020 PMC3236121 · DOI
  41. Florez, M.A., K.A. Matatall, Y. Jeong, L. Ortinau, P.W. Shafer, A.M. Lynch, R. Jaksik, M. Kimmel, D. Park, and K.Y. King. 2020. Interferon gamma mediates hematopoietic stem cell activation and niche relocalization through BST2. Cell Rep. 33: 108530. 10.1016/j.celrep.2020.108530 33357430 PMC7816211 · DOI
  42. Frisch, B.J., C.M. Hoffman, S.E. Latchney, M.W. LaMere, J. Myers, J. Ashton, A.J. Li, J. Saunders II, J. Palis, A.S. Perkins,. 2019. Aged marrow macrophages expand platelet-biased hematopoietic stem cells via Interleukin1B. JCI Insight. 5: e124213. 10.1172/jci.insight.124213 PMC6542605 30998506 · DOI · Paper page
  43. Fulop, T., A. Larbi, G. Dupuis, A. Le Page, E.H. Frost, A.A. Cohen, J.M. Witkowski, and C. Franceschi. 2018. Immunosenescence and inflamm-aging as two sides of the same coin: friends or foes? Front. Immunol. 8: 1960. 10.3389/fimmu.2017.01960 29375577 PMC5767595 · DOI · Paper page
  44. Fuster, J.J., S. MacLauchlan, M.A. Zuriaga, M.N. Polackal, A.C. Ostriker, R. Chakraborty, C.L. Wu, S. Sano, S. Muralidharan, C. Rius,. 2017. Clonal hematopoiesis associated with TET2 deficiency accelerates atherosclerosis development in mice. Science. 355: 842– 847. 10.1126/science.aag1381 28104796 PMC5542057 · DOI · Paper page
  45. Gasche, C., M.C.E. Lomer, I. Cavill, and G. Weiss. 2004. Iron, anaemia, and inflammatory bowel diseases. Gut. 53: 1190– 1197. 10.1136/gut.2003.035758 15247190 PMC1774131 · DOI
  46. Geiger, H., G. de Haan, and M.C. Florian. 2013. The ageing haematopoietic stem cell compartment. Nat. Rev. Immunol. 13: 376– 389. 10.1038/nri3433 23584423 · DOI · Paper page
  47. Genovese, G., A.K. Kähler, R.E. Handsaker, J. Lindberg, S.A. Rose, S.F. Bakhoum, K. Chambert, E. Mick, B.M. Neale, M. Fromer,. 2014. Clonal hematopoiesis and blood-cancer risk inferred from blood DNA sequence. N. Engl. J. Med. 371: 2477– 2487. 10.1056/NEJMoa1409405 25426838 PMC4290021 · DOI · Paper page
  48. Gerloff, D., R. Grundler, A.A. Wurm, D. Bräuer-Hartmann, C. Katzerke, J.U. Hartmann, V. Madan, C. Müller-Tidow, J. Duyster, D.G. Tenen,. 2015. NF-κB/STAT5/miR-155 network targets PU.1 in FLT3-ITD-driven acute myeloid leukemia. Leukemia. 29: 535– 547. 10.1038/leu.2014.231 25092144 PMC4490787 · DOI · Paper page
  49. Grassinger, J., B. Williams, G.H. Olsen, D.N. Haylock, and S.K. Nilsson. 2012. Granulocyte colony stimulating factor expands hematopoietic stem cells within the central but not endosteal bone marrow region. Cytokine. 58: 218– 225. 10.1016/j.cyto.2012.01.014 22341722 · DOI
  50. Griseri, T., B.S. McKenzie, C. Schiering, and F. Powrie. 2012. Dysregulated hematopoietic stem and progenitor cell activity promotes interleukin-23-driven chronic intestinal inflammation. Immunity. 37: 1116– 1129. 10.1016/j.immuni.2012.08.025 23200826 PMC3664922 · DOI
  51. Haltalli, M.L.R., S. Watcham, N.K. Wilson, K. Eilers, A. Lipien, H. Ang, F. Birch, S.G. Anton, C. Pirillo, N. Ruivo,. 2020. Manipulating niche composition limits damage to haematopoietic stem cells during Plasmodium infection. Nat. Cell Biol. 22: 1399– 1410. 10.1038/s41556-020-00601-w 33230302 PMC7611033 · DOI
  52. Hara, T., K. Ando, H. Tsurumi, and H. Moriwaki. 2004. Excessive production of tumor necrosis factor-alpha by bone marrow T lymphocytes is essential in causing bone marrow failure in patients with aplastic anemia. Eur. J. Haematol. 73: 10– 16. 10.1111/j.1600-0609.2004.00259.x 15182332 · DOI
  53. Hasan, S., C. Lacout, C. Marty, M. Cuingnet, E. Solary, W. Vainchenker, and J.L. Villeval. 2013. JAK2V617F expression in mice amplifies early hematopoietic cells and gives them a competitive advantage that is hampered by IFNα. Blood. 122: 1464– 1477. 10.1182/blood-2013-04-498956 23863895 · DOI
  54. Heaton, W.L., A.V. Senina, A.D. Pomicter, M.E. Salama, P.M. Clair, D. Yan, R.N. Bell, J.M. Gililland, J.T. Prchal, T. O’Hare, and M.W. Deininger. 2018. Autocrine Tnf signaling favors malignant cells in myelofibrosis in a Tnfr2-dependent fashion. Leukemia. 32: 2399– 2411. 10.1038/s41375-018-0131-z 29749399 PMC6224399 · DOI
  55. Helbling, P.M., E. Piñeiro-Yáñez, R. Gerosa, S. Boettcher, F. Al-Shahrour, M.G. Manz, and C. Nombela-Arrieta. 2019. Global transcriptomic profiling of the bone marrow stromal microenvironment during postnatal development, aging, and inflammation. Cell Rep. 29: 3313– 3330.e4. 10.1016/j.celrep.2019.11.004 31801092 · DOI · Paper page
  56. Henry, C.J., M. Casás-Selves, J. Kim, V. Zaberezhnyy, L. Aghili, A.E. Daniel, L. Jimenez, T. Azam, E.N. McNamee, E.T. Clambey,. 2015. Aging-associated inflammation promotes selection for adaptive oncogenic events in B cell progenitors. J. Clin. Invest. 125: 4666– 4680. 10.1172/JCI83024 26551682 PMC4665776 · DOI · Paper page
  57. Hirche, C., T. Frenz, S.F. Haas, M. Döring, K. Borst, P.K. Tegtmeyer, I. Brizic, S. Jordan, K. Keyser, C. Chhatbar,. 2017. Systemic virus infections differentially modulate cell cycle state and functionality of long-term hematopoietic stem cells in vivo. Cell Rep. 19: 2345– 2356. 10.1016/j.celrep.2017.05.063 28614719 · DOI
  58. Hoermann, G., G. Greiner, and P. Valent. 2015. Cytokine regulation of microenvironmental cells in myeloproliferative neoplasms. Mediators Inflamm. 2015: 869242. 10.1155/2015/869242 26543328 PMC4620237 · DOI
  59. Isgrò, A., I. Mezzaroma, A. Aiuti, A. Fantauzzi, M. Pinti, A. Cossarizza, and F. Aiuti. 2004. Decreased apoptosis of bone marrow progenitor cells in HIV-1-infected patients during highly active antiretroviral therapy. AIDS. 18: 1335– 1337. 10.1097/00002030-200406180-00013 15362667 · DOI
  60. Isringhausen, S., L. Kovtonyuk, U. Suessbier, N.J. Kraeutler, A. Gomariz, P.M. Helbling, H.C. Wong, T. Nagasawa, M.G. Manz, A. Oxenius,. 2020. CD8 T cells induce destruction of bone marrow stromal niches and hematopoietic stem cell dysfunction in chronic viral infections. bioRxiv. (Preprint posted May 8, 2020) 10.1101/2020.05.07.076083 · DOI
  61. Ito, S., A.C. D’Alessio, O.V. Taranova, K. Hong, L.C. Sowers, and Y. Zhang. 2010. Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature. 466: 1129– 1133. 10.1038/nature09303 20639862 PMC3491567 · DOI
  62. Iwamura, C., N. Bouladoux, Y. Belkaid, A. Sher, and D. Jankovic. 2017. Sensing of the microbiota by NOD1 in mesenchymal stromal cells regulates murine hematopoiesis. Blood. 129: 171– 176. 10.1182/blood-2016-06-723742 27799160 PMC5234217 · DOI · Paper page
  63. Jeong, M., D. Sun, M. Luo, Y. Huang, G.A. Challen, B. Rodriguez, X. Zhang, L. Chavez, H. Wang, R. Hannah,. 2014. Large conserved domains of low DNA methylation maintained by Dnmt3a. Nat. Genet. 46: 17– 23. 10.1038/ng.2836 24270360 PMC3920905 · DOI · Paper page
  64. Kanayama, M., Y. Izumi, Y. Yamauchi, S. Kuroda, T. Shin, S. Ishikawa, T. Sato, M. Kajita, and T. Ohteki. 2020. CD86-based analysis enables observation of bona fide hematopoietic responses. Blood. 136: 1144– 1154. 10.1182/blood.2020004923 32438398 · DOI
  65. Kent, D.G., J. Li, H. Tanna, J. Fink, K. Kirschner, D.C. Pask, Y. Silber, T.L. Hamilton, R. Sneade, B.D. Simons, and A.R. Green. 2013. Self-renewal of single mouse hematopoietic stem cells is reduced by JAK2V617F without compromising progenitor cell expansion. PLoS Biol. 11: e1001576. 10.1371/journal.pbio.1001576 23750118 PMC3672217 · DOI
  66. Khaldoyanidi, S., L. Sikora, I. Orlovskaya, V. Matrosova, V. Kozlov, and P. Sriramarao. 2001. Correlation between nicotine-induced inhibition of hematopoiesis and decreased CD44 expression on bone marrow stromal cells. Blood. 98: 303– 312. 10.1182/blood.V98.2.303 11435297 · DOI
  67. Khan, N., J. Downey, J. Sanz, E. Kaufmann, B. Blankenhaus, A. Pacis, E. Pernet, E. Ahmed, S. Cardoso, A. Nijnik,. 2020. M. tuberculosis reprograms hematopoietic stem cells to limit myelopoiesis and impair trained immunity. Cell. 183: 752– 770.e22. 10.1016/j.cell.2020.09.062 33125891 PMC7599081 · DOI
  68. Khosravi, A., A. Yáñez, J.G. Price, A. Chow, M. Merad, H.S. Goodridge, and S.K. Mazmanian. 2014. Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe. 15: 374– 381. 10.1016/j.chom.2014.02.006 24629343 PMC4144825 · DOI
  69. King, K.Y., and M.A. Goodell. 2011. Inflammatory modulation of HSCs: viewing the HSC as a foundation for the immune response. Nat. Rev. Immunol. 11: 685– 692. 10.1038/nri3062 21904387 PMC4154310 · DOI
  70. King, K.Y., M.T. Baldridge, D.C. Weksberg, S.M. Chambers, G.L. Lukov, S. Wu, N.C. Boles, S.Y. Jung, J. Qin, D. Liu,. 2011. Irgm1 protects hematopoietic stem cells by negative regulation of IFN signaling. Blood. 118: 1525– 1533. 10.1182/blood-2011-01-328682 21633090 PMC3156044 · DOI
  71. Ko, M., H.S. Bandukwala, J. An, E.D. Lamperti, E.C. Thompson, R. Hastie, A. Tsangaratou, K. Rajewsky, S.B. Koralov, and A. Rao. 2011. Ten-Eleven-Translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice. Proc. Natl. Acad. Sci. USA. 108: 14566– 14571. 10.1073/pnas.1112317108 21873190 PMC3167529 · DOI · Paper page
  72. Kovtonyuk, L.V., K. Fritsch, X. Feng, M.G. Manz, and H. Takizawa. 2016 a. Inflamm-aging of hematopoiesis, hematopoietic stem cells, and the bone marrow microenvironment. Front. Immunol. 7: 502. 10.3389/fimmu.2016.00502 27895645 PMC5107568 · DOI · Paper page
  73. Kovtonyuk, L.V., M.G. Manz, and H. Takizawa. 2016 b. Enhanced thrombopoietin but not G-CSF receptor stimulation induces self-renewing hematopoietic stem cell divisions in vivo. Blood. 127: 3175– 3179. 10.1182/blood-2015-09-669929 27146433 · DOI
  74. Kuranda, K., J. Vargaftig, P. de la Rochere, C. Dosquet, D. Charron, F. Bardin, C. Tonnelle, D. Bonnet, and M. Goodhardt. 2011. Age-related changes in human hematopoietic stem/progenitor cells. Aging Cell. 10: 542– 546. 10.1111/j.1474-9726.2011.00675.x 21418508 · DOI
  75. Laurenti, E., B. Varnum-Finney, A. Wilson, I. Ferrero, W.E. Blanco-Bose, A. Ehninger, P.S. Knoepfler, P.F. Cheng, H.R. MacDonald, R.N. Eisenman,. 2008. Hematopoietic stem cell function and survival depend on c-Myc and N-Myc activity. Cell Stem Cell. 3: 611– 624. 10.1016/j.stem.2008.09.005 19041778 PMC2635113 · DOI · Paper page
  76. Lee, Y.K., J.S. Menezes, Y. Umesaki, and S.K. Mazmanian. 2011. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc. Natl. Acad. Sci. USA. 108(Suppl 1): 4615– 4622. 10.1073/pnas.1000082107 20660719 PMC3063590 · DOI · Paper page
  77. Lee, S., H. Kim, G. You, Y.M. Kim, S. Lee, V.H. Le, O. Kwon, S.H. Im, Y.M. Kim, K.S. Kim,. 2019. Bone marrow CX3CR1+ mononuclear cells relay a systemic microbiota signal to control hematopoietic progenitors in mice. Blood. 134: 1312– 1322. 10.1182/blood.2019000495 31387916 PMC6888141 · DOI
  78. Li, G., J. Zhao, L. Cheng, Q. Jiang, S. Kan, E. Qin, B. Tu, X. Zhang, L. Zhang, L. Su, and Z. Zhang. 2017. HIV-1 infection depletes human CD34+CD38- hematopoietic progenitor cells via pDC-dependent mechanisms. PLoS Pathog. 13: e1006505. 10.1371/journal.ppat.1006505 28759657 PMC5552321 · DOI
  79. Loberg, M.A., R.K. Bell, L.O. Goodwin, E. Eudy, L.A. Miles, J.M. SanMiguel, K. Young, D.E. Bergstrom, R.L. Levine, R.K. Schneider, and J.J. Trowbridge. 2019. Sequentially inducible mouse models reveal that Npm1 mutation causes malignant transformation of Dnmt3a-mutant clonal hematopoiesis. Leukemia. 33: 1635– 1649. 10.1038/s41375-018-0368-6 30692594 PMC6609470 · DOI
  80. Lussana, F., and A. Rambaldi. 2017. Inflammation and myeloproliferative neoplasms. J. Autoimmun. 85: 58– 63. 10.1016/j.jaut.2017.06.010 28669446 · DOI · Paper page
  81. MacNamara, K.C., M. Jones, O. Martin, and G.M. Winslow. 2011. Transient activation of hematopoietic stem and progenitor cells by IFNγ during acute bacterial infection. PLoS One. 6: e28669. 10.1371/journal.pone.0028669 22194881 PMC3237486 · DOI
  82. Manz, M.G., and S. Boettcher. 2014. Emergency granulopoiesis. Nat. Rev. Immunol. 14: 302– 314. 10.1038/nri3660 24751955 · DOI · Paper page
  83. Marandin, A., A. Katz, E. Oksenhendler, M. Tulliez, F. Picard, W. Vainchenker, and F. Louache. 1996. Loss of primitive hematopoietic progenitors in patients with human immunodeficiency virus infection. Blood. 88: 4568– 4578. 10.1182/blood.V88.12.4568.bloodjournal88124568 8977248 · DOI
  84. Martincorena, I., A. Roshan, M. Gerstung, P. Ellis, P. Van Loo, S. McLaren, D.C. Wedge, A. Fullam, L.B. Alexandrov, J.M. Tubio,. 2015. Tumor evolution. High burden and pervasive positive selection of somatic mutations in normal human skin. Science. 348: 880– 886. 10.1126/science.aaa6806 25999502 PMC4471149 · DOI · Paper page
  85. Martínez, A., C. Bono, J. Megías, A. Yáñez, D. Gozalbo, and M.L. Gil. 2018. Systemic candidiasis and TLR2 agonist exposure impact the antifungal response of hematopoietic stem and progenitor cells. Front. Cell. Infect. Microbiol. 8: 309. 10.3389/fcimb.2018.00309 30234030 PMC6130230 · DOI
  86. Matatall, K.A., C.-C. Shen, G.A. Challen, and K.Y. King. 2014. Type II interferon promotes differentiation of myeloid-biased hematopoietic stem cells. Stem Cells. 32: 3023– 3030. 10.1002/stem.1799 25078851 PMC4198460 · DOI
  87. Matatall, K.A., M. Jeong, S. Chen, D. Sun, F. Chen, Q. Mo, M. Kimmel, and K.Y. King. 2016. Chronic infection depletes hematopoietic stem cells through stress-induced terminal differentiation. Cell Rep. 17: 2584– 2595. 10.1016/j.celrep.2016.11.031 27926863 PMC5161248 · DOI · Paper page
  88. McKelvey, K.J., A.L. Hudson, M. Back, T. Eade, and C.I. Diakos. 2018. Radiation, inflammation and the immune response in cancer. Mamm. Genome. 29: 843– 865. 10.1007/s00335-018-9777-0 30178305 PMC6267675 · DOI
  89. McKenzie, M.D., M. Ghisi, E.P. Oxley, S. Ngo, L. Cimmino, C. Esnault, R. Liu, J.M. Salmon, C.C. Bell, N. Ahmed,. 2019. Interconversion between tumorigenic and differentiated states in acute myeloid leukemia. Cell Stem Cell. 25: 258– 272.e9. 10.1016/j.stem.2019.07.001 31374198 · DOI · Paper page
  90. Meisel, M., R. Hinterleitner, A. Pacis, L. Chen, Z.M. Earley, T. Mayassi, J.F. Pierre, J.D. Ernest, H.J. Galipeau, N. Thuille,. 2018. Microbial signals drive pre-leukaemic myeloproliferation in a Tet2-deficient host. Nature. 557: 580– 584. 10.1038/s41586-018-0125-z 29769727 PMC6238954 · DOI · Paper page
  91. Mohrin, M., E. Bourke, D. Alexander, M.R. Warr, K. Barry-Holson, M.M. Le Beau, C.G. Morrison, and E. Passegué. 2010. Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis. Cell Stem Cell. 7: 174– 185. 10.1016/j.stem.2010.06.014 20619762 PMC2924905 · DOI · Paper page
  92. Moran-Crusio, K., L. Reavie, A. Shih, O. Abdel-Wahab, D. Ndiaye-Lobry, C. Lobry, M.E. Figueroa, A. Vasanthakumar, J. Patel, X. Zhao,. 2011. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell. 20: 11– 24. 10.1016/j.ccr.2011.06.001 21723200 PMC3194039 · DOI · Paper page
  93. Mullally, A., S.W. Lane, B. Ball, C. Megerdichian, R. Okabe, F. Al-Shahrour, M. Paktinat, J.E. Haydu, E. Housman, A.M. Lord,. 2010. Physiological Jak2V617F expression causes a lethal myeloproliferative neoplasm with differential effects on hematopoietic stem and progenitor cells. Cancer Cell. 17: 584– 596. 10.1016/j.ccr.2010.05.015 20541703 PMC2909585 · DOI
  94. Mullally, A., C. Bruedigam, L. Poveromo, F.H. Heidel, A. Purdon, T. Vu, R. Austin, D. Heckl, L.J. Breyfogle, C.P. Kuhn,. 2013. Depletion of Jak2V617F myeloproliferative neoplasm-propagating stem cells by interferon-α in a murine model of polycythemia vera. Blood. 121: 3692– 3702. 10.1182/blood-2012-05-432989 23487027 PMC3643767 · DOI
  95. Niu, H., G. Fang, Y. Tang, L. Xie, H. Yang, L. Morel, B. Diamond, and Y.R. Zou. 2013. The function of hematopoietic stem cells is altered by both genetic and inflammatory factors in lupus mice. Blood. 121: 1986– 1994. 10.1182/blood-2012-05-433755 23315165 PMC3596961 · DOI
  96. Noguera, N.I., M.L. Piredda, R. Taulli, G. Catalano, G. Angelini, G. Gaur, C. Nervi, M.T. Voso, A. Lunardi, P.P. Pandolfi, and F. Lo-Coco. 2016. PML/RARa inhibits PTEN expression in hematopoietic cells by competing with PU.1 transcriptional activity. Oncotarget. 7: 66386– 66397. 10.18632/oncotarget.11964 27626703 PMC5341808 · DOI
  97. Nombela-Arrieta, C., and M.G. Manz. 2017. Quantification and three-dimensional microanatomical organization of the bone marrow. Blood Adv. 1: 407– 416. 10.1182/bloodadvances.2016003194 29296956 PMC5738992 · DOI
  98. Oduro, K.A. Jr., F. Liu, Q. Tan, C.K. Kim, O. Lubman, D. Fremont, J.C. Mills, and K. Choi. 2012. Myeloid skewing in murine autoimmune arthritis occurs in hematopoietic stem and primitive progenitor cells. Blood. 120: 2203– 2213. 10.1182/blood-2011-11-391342 22855602 PMC3447779 · DOI
  99. Okano, M., D.W. Bell, D.A. Haber, and E. Li. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell. 99: 247– 257. 10.1016/S0092-8674(00)81656-6 10555141 · DOI · Paper page
  100. Pandit, T.S., L. Sikora, G. Muralidhar, S.P. Rao, and P. Sriramarao. 2006. Sustained exposure to nicotine leads to extramedullary hematopoiesis in the spleen. Stem Cells. 24: 2373– 2381. 10.1634/stemcells.2005-0447 16825610 · DOI
  101. Papadaki, H.A., D.T. Boumpas, F.M. Gibson, D.R. Jayne, J.S. Axford, E.C. Gordon-Smith, J.C.W. Marsh, and G.D. Eliopoulos. 2001. Increased apoptosis of bone marrow CD34(+) cells and impaired function of bone marrow stromal cells in patients with systemic lupus erythematosus. Br. J. Haematol. 115: 167– 174. 10.1046/j.1365-2141.2001.03076.x 11722430 · DOI
  102. Papadaki, H.A., H.D. Kritikos, V. Valatas, D.T. Boumpas, and G.D. Eliopoulos. 2002. Anemia of chronic disease in rheumatoid arthritis is associated with increased apoptosis of bone marrow erythroid cells: improvement following anti-tumor necrosis factor-α antibody therapy. Blood. 100: 474– 482. 10.1182/blood-2002-01-0136 12091338 · DOI
  103. Pascual, V., F. Allantaz, E. Arce, M. Punaro, and J. Banchereau. 2005. Role of interleukin-1 (IL-1) in the pathogenesis of systemic onset juvenile idiopathic arthritis and clinical response to IL-1 blockade. J. Exp. Med. 201: 1479– 1486. 10.1084/jem.20050473 15851489 PMC2213182 · DOI
  104. Pietras, E.M., R. Lakshminarasimhan, J.M. Techner, S. Fong, J. Flach, M. Binnewies, and E. Passegué. 2014. Re-entry into quiescence protects hematopoietic stem cells from the killing effect of chronic exposure to type I interferons. J. Exp. Med. 211: 245– 262. 10.1084/jem.20131043 24493802 PMC3920566 · DOI · Paper page
  105. Pietras, E.M., C. Mirantes-Barbeito, S. Fong, D. Loeffler, L.V. Kovtonyuk, S. Zhang, R. Lakshminarasimhan, C.P. Chin, J.M. Techner, B. Will,. 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. 10.1038/ncb3346 27111842 PMC4884136 · DOI · Paper page
  106. Pioli, P.D., D. Casero, E. Montecino-Rodriguez, S.L. Morrison, and K. Dorshkind. 2019. Plasma cells are obligate effectors of enhanced myelopoiesis in aging bone marrow. Immunity. 51: 351– 366.e6. 10.1016/j.immuni.2019.06.006 31303400 PMC6703913 · DOI · Paper page
  107. Porta, C., R. Caporali, O. Epis, I. Ramaioli, R. Invernizzi, B. Rovati, G. Comolli, M. Danova, and C. Montecucco. 2004. Impaired bone marrow hematopoietic progenitor cell function in rheumatoid arthritis patients candidated to autologous hematopoietic stem cell transplantation. Bone Marrow Transplant. 33: 721– 728. 10.1038/sj.bmt.1704407 14743200 · DOI
  108. Pronk, C.J.H., O.P. Veiby, D. Bryder, and S.E.W. Jacobsen. 2011. Tumor necrosis factor restricts hematopoietic stem cell activity in mice: involvement of two distinct receptors. J. Exp. Med. 208: 1563– 1570. 10.1084/jem.20110752 21768269 PMC3149225 · DOI
  109. Pyrovolaki, K., I. Mavroudi, P. Sidiropoulos, A.G. Eliopoulos, D.T. Boumpas, and H.A. Papadaki. 2009. Increased expression of CD40 on bone marrow CD34+ hematopoietic progenitor cells in patients with systemic lupus erythematosus: contribution to Fas-mediated apoptosis. Arthritis Rheum. 60: 543– 552. 10.1002/art.24257 19180486 · DOI
  110. Rao, T.N., N. Hansen, J. Stetka, D. Luque Paz, M. Kalmer, J. Hilfiker, M. Endele, N. Ahmed, L. Kubovcakova, M. Rybarikova,. 2021. JAK2-V617F and interferon-α induce megakaryocyte-biased stem cells characterized by decreased long-term functionality. Blood. 137: 2139– 2151. 10.1182/blood.2020005563 33667305 PMC8103999 · DOI · Paper page
  111. Regan-Komito, D., J.W. Swann, P. Demetriou, E.S. Cohen, N.J. Horwood, S.N. Sansom, and T. Griseri. 2020. GM-CSF drives dysregulated hematopoietic stem cell activity and pathogenic extramedullary myelopoiesis in experimental spondyloarthritis. Nat. Commun. 11: 155. 10.1038/s41467-019-13853-4 31919358 PMC6952438 · DOI
  112. Rodrigues-Moreira, S., S.G. Moreno, G. Ghinatti, D. Lewandowski, F. Hoffschir, F. Ferri, A.S. Gallouet, D. Gay, H. Motohashi, M. Yamamoto,. 2017. Low-dose irradiation promotes persistent oxidative stress and decreases self-renewal in hematopoietic stem cells. Cell Rep. 20: 3199– 3211. 10.1016/j.celrep.2017.09.013 28954235 · DOI
  113. Rozhok, A.I., J.L. Salstrom, and J. DeGregori. 2014. Stochastic modeling indicates that aging and somatic evolution in the hematopoetic system are driven by non-cell-autonomous processes. Aging (Albany NY). 6: 1033– 1048. 10.18632/aging.100707 25564763 PMC4298364 · DOI
  114. Rozhok, A.I., J.L. Salstrom, and J. DeGregori. 2016. Stochastic modeling reveals an evolutionary mechanism underlying elevated rates of childhood leukemia. Proc. Natl. Acad. Sci. USA. 113: 1050– 1055. 10.1073/pnas.1509333113 26755588 PMC4743806 · DOI
  115. Rundberg Nilsson, A., S. Soneji, S. Adolfsson, D. Bryder, and C.J. Pronk. 2016. Human and murine hematopoietic stem cell aging is associated with functional impairments and intrinsic megakaryocytic/erythroid bias. PLoS One. 11: e0158369. 10.1371/journal.pone.0158369 27368054 PMC4930192 · DOI
  116. Sano, S., K. Oshima, Y. Wang, Y. Katanasaka, M. Sano, and K. Walsh. 2018a. CRISPR-mediated gene editing to assess the roles of TET2 and DNMT3A in clonal hematopoiesis and cardiovascular disease. Circ. Res. 123: 335– 341. 10.1161/CIRCRESAHA.118.313225 29728415 PMC6054544 · DOI · Paper page
  117. Sano, S., K. Oshima, Y. Wang, S. MacLauchlan, Y. Katanasaka, M. Sano, M.A. Zuriaga, M. Yoshiyama, D. Goukassian, M.A. Cooper,. 2018 b. Tet2-mediated clonal hematopoiesis accelerates heart failure through a mechanism involving the IL-1β/NLRP3 inflammasome. J. Am. Coll. Cardiol. 71: 875– 886. 10.1016/j.jacc.2017.12.037 29471939 PMC5828038 · DOI · Paper page
  118. Sato, T., N. Onai, H. Yoshihara, F. Arai, T. Suda, and T. Ohteki. 2009. Interferon regulatory factor-2 protects quiescent hematopoietic stem cells from type I interferon-dependent exhaustion. Nat. Med. 15: 696– 700. 10.1038/nm.1973 19483695 · DOI
  119. Schuettpelz, L.G., J.N. Borgerding, M.J. Christopher, P.K. Gopalan, M.P. Romine, A.C. Herman, J.R. Woloszynek, A.M. Greenbaum, and D.C. Link. 2014. G-CSF regulates hematopoietic stem cell activity, in part, through activation of Toll-like receptor signaling. Leukemia. 28: 1851– 1860. 10.1038/leu.2014.68 24518205 PMC4130805 · DOI
  120. Schürch, C.M., C. Riether, and A.F. Ochsenbein. 2014. Cytotoxic CD8+ T cells stimulate hematopoietic progenitors by promoting cytokine release from bone marrow mesenchymal stromal cells. Cell Stem Cell. 14: 460– 472. 10.1016/j.stem.2014.01.002 24561082 · DOI
  121. Scognamiglio, R., N. Cabezas-Wallscheid, M.C. Thier, S. Altamura, A. Reyes, Á.M. Prendergast, D. Baumgärtner, L.S. Carnevalli, A. Atzberger, S. Haas,. 2016. Myc depletion induces a pluripotent dormant state mimicking diapause. Cell. 164: 668– 680. 10.1016/j.cell.2015.12.033 26871632 PMC4752822 · DOI · Paper page
  122. Scumpia, P.O., K.M. Kelly-Scumpia, M.J. Delano, J.S. Weinstein, A.G. Cuenca, S. Al-Quran, I. Bovio, S. Akira, Y. Kumagai, and L.L. Moldawer. 2010. Cutting edge: bacterial infection induces hematopoietic stem and progenitor cell expansion in the absence of TLR signaling. J. Immunol. 184: 2247– 2251. 10.4049/jimmunol.0903652 20130216 PMC3837089 · DOI
  123. Shao, L., Y. Wang, J. Chang, Y. Luo, A. Meng, and D. Zhou. 2013. Hematopoietic stem cell senescence and cancer therapy-induced long-term bone marrow injury. Transl. Cancer Res. 2: 397– 411. 24605290 PMC3941916
  124. Shi, W., T. Vu, D. Boucher, A. Biernacka, J. Nde, R.K. Pandita, J. Straube, G.M. Boyle, F. Al-Ejeh, P. Nag,. 2017. Ssb1 and Ssb2 cooperate to regulate mouse hematopoietic stem and progenitor cells by resolving replicative stress. Blood. 129: 2479– 2492. 10.1182/blood-2016-06-725093 28270450 PMC5418634 · DOI
  125. Shi, X., S. Wei, K.J. Simms, D.N. Cumpston, T.J. Ewing, and P. Zhang. 2018. Sonic hedgehog signaling regulates hematopoietic stem/progenitor cell activation during the granulopoietic response to systemic bacterial infection. Front. Immunol. 9: 349. 10.3389/fimmu.2018.00349 29535725 PMC5834434 · DOI
  126. Siggins, R.W., F. Hossain, T. Rehman, J.N. Melvan, P. Zhang, and D.A. Welsh. 2014. Cigarette smoke alters the hematopoietic stem cell niche. Med. Sci. (Basel). 2: 37– 50. 10.3390/medsci2010037 28868162 PMC5576506 · DOI
  127. Skirecki, T., J. Kawiak, E. Machaj, Z. Pojda, D. Wasilewska, J. Czubak, and G. Hoser. 2015. Early severe impairment of hematopoietic stem and progenitor cells from the bone marrow caused by CLP sepsis and endotoxemia in a humanized mice model. Stem Cell Res. Ther. 6: 142. 10.1186/s13287-015-0135-9 26272069 PMC4536694 · DOI
  128. Skirecki, T., M. Mikaszewska-Sokolewicz, M. Godlewska, B. Dołęgowska, J. Czubak, G. Hoser, J. Kawiak, and U. Zielińska-Borkowska. 2019. Mobilization of stem and progenitor cells in septic shock patients. Sci. Rep. 9: 3289. 10.1038/s41598-019-39772-4 30824730 PMC6397313 · DOI
  129. Smith, J.N.P., Y. Zhang, J.J. Li, A. McCabe, H.J. Jo, J. Maloney, and K.C. MacNamara. 2018. Type I IFNs drive hematopoietic stem and progenitor cell collapse via impaired proliferation and increased RIPK1-dependent cell death during shock-like ehrlichial infection. PLoS Pathog. 14: e1007234. 10.1371/journal.ppat.1007234 30080899 PMC6095620 · DOI
  130. Staber, P.B., P. Zhang, M. Ye, R.S. Welner, C. Nombela-Arrieta, C. Bach, M. Kerenyi, B.A. Bartholdy, H. Zhang, M. Alberich-Jordà,. 2013. Sustained PU.1 levels balance cell-cycle regulators to prevent exhaustion of adult hematopoietic stem cells. Mol. Cell. 49: 934– 946. 10.1016/j.molcel.2013.01.007 23395001 PMC3644723 · DOI · Paper page
  131. Staffas, A., M. Burgos da Silva, A.E. Slingerland, A. Lazrak, C.J. Bare, C.D. Holman, M.D. Docampo, Y. Shono, B. Durham, A.J. Pickard,. 2018. Nutritional support from the intestinal microbiota improves hematopoietic reconstitution after bone marrow transplantation in mice. Cell Host Microbe. 23: 447– 457.e4. 10.1016/j.chom.2018.03.002 29576480 PMC5897172 · DOI
  132. Stetka, J., P. Vyhlidalova, L. Lanikova, P. Koralkova, J. Gursky, A. Hlusi, P. Flodr, S. Hubackova, J. Bartek, Z. Hodny, and V. Divoky. 2019. Addiction to DUSP1 protects JAK2V617F-driven polycythemia vera progenitors against inflammatory stress and DNA damage, allowing chronic proliferation. Oncogene. 38: 5627– 5642. 10.1038/s41388-019-0813-7 30967632 PMC6756199 · DOI
  133. Sun, J., A. Ramos, B. Chapman, J.B. Johnnidis, L. Le, Y.J. Ho, A. Klein, O. Hofmann, and F.D. Camargo. 2014. Clonal dynamics of native haematopoiesis. Nature. 514: 322– 327. 10.1038/nature13824 25296256 PMC4408613 · DOI
  134. Tada, T., S. Yamamura, Y. Kuwano, and T. Abo. 1996. Level of myelopoiesis in the bone marrow is influenced by intestinal flora. Cell. Immunol. 173: 155– 161. 10.1006/cimm.1996.0261 8871611 · DOI
  135. Takizawa, H., R.R. Regoes, C.S. Boddupalli, S. Bonhoeffer, and M.G. Manz. 2011. Dynamic variation in cycling of hematopoietic stem cells in steady state and inflammation. J. Exp. Med. 208: 273– 284. 10.1084/jem.20101643 21300914 PMC3039863 · DOI
  136. Takizawa, H., S. Boettcher, and M.G. Manz. 2012. Demand-adapted regulation of early hematopoiesis in infection and inflammation. Blood. 119: 2991– 3002. 10.1182/blood-2011-12-380113 22246037 · DOI
  137. Takizawa, H., K. Fritsch, L.V. Kovtonyuk, Y. Saito, C. Yakkala, K. Jacobs, A.K. Ahuja, M. Lopes, A. Hausmann, W.D. Hardt,. 2017. Pathogen-induced TLR4-TRIF innate immune signaling in hematopoietic stem cells promotes proliferation but reduces competitive fitness. Cell Stem Cell. 21: 225– 240.e5. 10.1016/j.stem.2017.06.013 28736216 · DOI
  138. Talhout, R., T. Schulz, E. Florek, J. van Benthem, P. Wester, and A. Opperhuizen. 2011. Hazardous compounds in tobacco smoke. Int. J. Environ. Res. Public Health. 8: 613– 628. 10.3390/ijerph8020613 21556207 PMC3084482 · DOI
  139. Taraldsrud, E., H.K. Grøgaard, S. Solheim, K. Lunde, Y. Fløisand, H. Arnesen, I. Seljeflot, and T. Egeland. 2009. Age and stress related phenotypical changes in bone marrow CD34+ cells. Scand. J. Clin. Lab. Invest. 69: 79– 84. 10.1080/00365510802419447 18836945 · DOI
  140. Trumpp, A., M. Essers, and A. Wilson. 2010. Awakening dormant haematopoietic stem cells. Nat. Rev. Immunol. 10: 201– 209. 10.1038/nri2726 20182459 · DOI
  141. Vainieri, M.L., A.M. Blagborough, A.L. MacLean, M.L.R. Haltalli, N. Ruivo, H.A. Fletcher, M.P.H. Stumpf, R.E. Sinden, and C.L. Celso. 2016. Systematic tracking of altered haematopoiesis during sporozoite-mediated malaria development reveals multiple response points. Open Biol. 6: 160038. 10.1098/rsob.160038 27335321 PMC4929935 · DOI
  142. Valletta, S., A. Thomas, Y. Meng, X. Ren, R. Drissen, H. Sengül, C. Di Genua, and C. Nerlov. 2020. Micro-environmental sensing by bone marrow stroma identifies IL-6 and TGFβ1 as regulators of hematopoietic ageing. Nat. Commun. 11: 4075. 10.1038/s41467-020-17942-7 32796847 PMC7427787 · DOI · Paper page
  143. van der Meer, J.W.M., M. Barza, S.M. Wolff, and C.A. Dinarello. 1988. A low dose of recombinant interleukin 1 protects granulocytopenic mice from lethal gram-negative infection. Proc. Natl. Acad. Sci. USA. 85: 1620– 1623. 10.1073/pnas.85.5.1620 3125553 PMC279825 · DOI
  144. Vasto, S., G. Candore, C.R. Balistreri, M. Caruso, G. Colonna-Romano, M.P. Grimaldi, F. Listi, D. Nuzzo, D. Lio, and C. Caruso. 2007. Inflammatory networks in ageing, age-related diseases and longevity. Mech. Ageing Dev. 128: 83– 91. 10.1016/j.mad.2006.11.015 17118425 · DOI
  145. Vyas, D., G. Laput, and A.K. Vyas. 2014. Chemotherapy-enhanced inflammation may lead to the failure of therapy and metastasis. OncoTargets Ther. 7: 1015– 1023. 10.2147/OTT.S60114 PMC4061164 24959088 · DOI
  146. Walter, D., A. Lier, A. Geiselhart, F.B. Thalheimer, S. Huntscha, M.C. Sobotta, B. Moehrle, D. Brocks, I. Bayindir, P. Kaschutnig,. 2015. Exit from dormancy provokes DNA-damage-induced attrition in haematopoietic stem cells. Nature. 520: 549– 552. 10.1038/nature14131 25707806 · DOI · Paper page
  147. Wang, W., W. Liu, T. Fidler, Y. Wang, Y. Tang, B. Woods, C. Welch, B. Cai, C. Silvestre-Roig, D. Ai,. 2018. Macrophage inflammation, erythrophagocytosis, and accelerated atherosclerosis in JAK2V617F mice. Circ. Res. 123: e35– e47. 10.1161/CIRCRESAHA.118.313283 30571460 PMC6309796 · DOI · Paper page
  148. Wang, Y., S. Sano, Y. Yura, Z. Ke, M. Sano, K. Oshima, H. Ogawa, K. Horitani, K.D. Min, E. Miura-Yura,. 2020. Tet2-mediated clonal hematopoiesis in nonconditioned mice accelerates age-associated cardiac dysfunction. JCI Insight. 5: e135204. 10.1172/jci.insight.135204 PMC7213793 32154790 · DOI · Paper page
  149. Wang, P., J. Wang, Y.H. Li, L. Wang, H.C. Shang, and J.X. Wang. 2021. Phenotypical changes of hematopoietic stem and progenitor cells in sepsis patients: correlation with immune status? Front. Pharmacol. 11: 640203. 10.3389/fphar.2020.640203 33542693 PMC7850983 · DOI
  150. Weisser, M., U.M. Demel, S. Stein, L. Chen-Wichmann, F. Touzot, G. Santilli, S. Sujer, C. Brendel, U. Siler, M. Cavazzana,. 2016. Hyperinflammation in patients with chronic granulomatous disease leads to impairment of hematopoietic stem cell functions. J. Allergy Clin. Immunol. 138: 219– 228.e9. 10.1016/j.jaci.2015.11.028 26853280 · DOI · Paper page
  151. Wilson, A., M.J. Murphy, T. Oskarsson, K. Kaloulis, M.D. Bettess, G.M. Oser, A.C. Pasche, C. Knabenhans, H.R. Macdonald, and A. Trumpp. 2004. c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev. 18: 2747– 2763. 10.1101/gad.313104 15545632 PMC528895 · DOI · Paper page
  152. Woolthuis, C.M., N. Mariani, R.N. Verkaik-Schakel, A.Z. Brouwers-Vos, J.J. Schuringa, E. Vellenga, J.T.M. de Wolf, and G. Huls. 2014. Aging impairs long-term hematopoietic regeneration after autologous stem cell transplantation. Biol. Blood Marrow Transplant. 20: 865– 871. 10.1016/j.bbmt.2014.03.001 24607555 · DOI
  153. Yamashita, M., and E. Passegué. 2019. TNF-α Coordinates Hematopoietic Stem Cell Survival and Myeloid Regeneration. Cell Stem Cell. 25: 357– 372.e7. 10.1016/j.stem.2019.05.019 31230859 PMC6733032 · DOI · Paper page
  154. Yang, H., H. Liang, J.S. Yan, R. Tao, S.G. Hao, and L.Y. Ma. 2012. Down-regulation of hematopoiesis master regulator PU.1 via aberrant methylation in chronic myeloid leukemia. Int. J. Hematol. 96: 65– 73. 10.1007/s12185-012-1106-x 22674382 · DOI
  155. Zhang, X., D.P. Sejas, Y. Qiu, D.A. Williams, and Q. Pang. 2007. Inflammatory ROS promote and cooperate with the Fanconi anemia mutation for hematopoietic senescence. J. Cell Sci. 120: 1572– 1583. 10.1242/jcs.003152 17405815 PMC2857731 · DOI
  156. Zhang, M., L. Yin, K. Zhang, W. Sun, S. Yang, B. Zhang, P. Salzman, W. Wang, C. Liu, S. Vidyasagar,. 2012. Response patterns of cytokines/chemokines in two murine strains after irradiation. Cytokine. 58: 169– 177. 10.1016/j.cyto.2011.12.023 22277799 · DOI
  157. Zhao, M., F. Tao, A. Venkatraman, Z. Li, S.E. Smith, J. Unruh, S. Chen, C. Ward, P. Qian, J.M. Perry,. 2019. N-cadherin-expressing bone and marrow stromal progenitor cells maintain reserve hematopoietic stem cells. Cell Rep. 26: 652– 669.e6. 10.1016/j.celrep.2018.12.093 30650358 PMC6890378 · DOI · Paper page

Cited by

Sorted by citations

Authors
Caiado, F., Pietras, E. M., & Manz, M. G.
Affiliations
  • University of Zurich (CH)
  • University of Colorado Anschutz (US)
Corresponding author
  • Pietras, Eric M.
  • Manz, Markus G.
ORCID
Venue
Journal of Experimental Medicine
Publisher
Rockefeller University Press
Published
2021-06-15
Volume
218
Issue
7
ISSN
  • 0022-1007 (ISSN-L)
  • 1540-9538
DOI
10.1084/jem.20201541
PMC
PMC8210622
OpenAlex
W3167469263
Cited by
289
References
35
Citations by year
2026: 51 · 2025: 71 · 2024: 64 · 2023: 52 · 2022: 44 · 2021: 7
FWCI
7.30
Type
journal article
Language
en
Open access
Licence
Locations
  • The Journal of Experimental Medicine (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion, cc-by-nc-sa)
  • PubMed (publishedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by-nc-sa)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by-nc-sa)
  • Zurich Open Repository and Archive (University of Zurich)
Funders
  • National Institutes of Health (R01 DK119394)
  • Cleo Meador and George Ryland Scott Endowed Chair in Hematology
  • Comprehensive Cancer Center Zurich
  • Swiss National Science Foundation (310030B_166673/1)
Topics
  • Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
  • Health Sciences › Medicine › Genetics › Mesenchymal stem cell research
  • Health Sciences › Medicine › Hematology › Acute Myeloid Leukemia Research
Keywords
inflammation, hematopoietic stem cells, inflammaging, clonal selection, systemic inflammation, aging
MeSH terms
Aging, Animals, Cell Differentiation, Clone Cells, Hematopoietic Stem Cells, Humans, Inflammation, Cell Proliferation

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