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Cited by 343Hematopoietic Stem Cell TransplantationPluripotent Stem Cells ResearchDevelopmental Biology and Gene Regulation

Lin28b Reprograms Adult Bone Marrow Hematopoietic Progenitors to Mediate Fetal-Like Lymphopoiesis

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Yuan, Joan, Nguyen, Cuong K., Liu, Xiuhuai, Kanellopoulou, Chrysi, Muljo, Stefan A.·2012·Science
DOI 10.1126/science.1216557PMC PMC3471381
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Abstract

Making Immune Cells Young Again: Hematopoiesis, the development of the immune system, occurs in distinct waves. The immune system is first populated by cells that arise from fetal hematopoietic stem cells (HSCs) and then later by cells derived from adult HSCs. Furthermore, fetal HSCs give rise to lymphocytes with innate immunelike properties, whereas adult HSCs give rise to classical T and B cells. Yuan et al. (p. 1195 , published online 16 February) now uncover the molecular mechanism behind these distinct waves of hematopoiesis. Expression of the RNA binding proteins Lin28 and Lin28b is enriched in fetal hematopoietic stem/progenitor cells (HSPCs) in mice and humans. Ectopic expression of Lin28 in mouse adult HSPCs was sufficient to induce the differentiation of both classical and innate-like lymphocyte lineages.

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  • This difference is now understood to be intrinsically programmed and due to an altered pathway of differentiation in the first-wave cells, which results in T-cell lineage commitment even before entry into the thymus.

    “This is now understood to be intrinsically programmed (136) and due to an altered pathway of differentiation in the first-wave cells, which results in T-cell lineage commitment even before entry into the thymus (137–139).”

    From Mechanisms of Action of Hematopoietic Transcription Factor PU.1 in Initiation of T-Cell Development (2019) · cites this paper as [136]

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  1. [1]Kikuchi K Kondo M Developmental switch of mouse hematopoietic stem cells from fetal to adult type occurs in bone marrow after birth Proc Natl Acad Sci U S A 103 17852 11 21 2006 17090683 PMC1693836
  2. [2]Bowie MB Identification of a new intrinsically timed developmental checkpoint that reprograms key hematopoietic stem cell properties Proc Natl Acad Sci U S A 104 5878 4 3 2007 17379664 PMC1829493
  3. [3]Herzenberg LA Toward a layered immune system Cell 59 953 12 22 1989 2688900
  4. [4]Ikuta K Weissman IL The junctional modifications of a T cell receptor gamma chain are determined at the level of thymic precursors J Exp Med 174 1279 11 1 1991 1834763 PMC2118991
  5. [6]Hardy RR Hayakawa K A developmental switch in B lymphopoiesis Proc Natl Acad Sci U S A 88 11550 12 15 1991 1722338 PMC53173
  6. [7]Kantor AB Stall AM Adams S Herzenberg LA Differential development of progenitor activity for three B-cell lineages Proc Natl Acad Sci U S A 89 3320 4 15 1992 1565622 PMC48858
  7. [8]Yoshimoto M Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential Proc Natl Acad Sci U S A 108 1468 1 25 2011 21209332 PMC3029764
  8. [9]Bendelac A Bonneville M Kearney J Autoreactivity by design: innate B and T lymphocytes Nature reviews Immunology 1 177 2001 11905826
  9. [10]Garman RD Doherty PJ Raulet DH Diversity, rearrangement, and expression of murine T cell gamma genes Cell 45 733 6 6 1986 3486721
  10. [11]Barber CL Montecino-Rodriguez E Dorshkind K Reduced production of B-1-specified common lymphoid progenitors results in diminished potential of adult marrow to generate B-1 cells Proc Natl Acad Sci U S A 108 13700 8 16 2011 21808010 PMC3158209
  11. [12]Kim I Saunders TL Morrison SJ Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells Cell 130 470 8 10 2007 17655922 PMC2577201
  12. [13]Kuchen S Regulation of microRNA expression and abundance during lymphopoiesis Immunity 32 828 6 25 2010 20605486 PMC2909788
  13. [14]Heo I TUT4 in concert with Lin28 suppresses microRNA biogenesis through pre-microRNA uridylation Cell 138 696 8 21 2009 19703396
  14. [15]Viswanathan SR Daley GQ Gregory RI Selective blockade of microRNA processing by Lin28 Science 320 97 4 4 2008 18292307 PMC3368499
  15. [16]Piskounova E Determinants of microRNA processing inhibition by the developmentally regulated RNA-binding protein Lin28 J Biol Chem 283 21310 8 1 2008 18550544
  16. [17]Piskounova E Lin28A and Lin28B inhibit let-7 microRNA biogenesis by distinct mechanisms Cell 147 1066 2011 22118463 PMC3227872
  17. [18]Jotereau F Heuze F Salomon-Vie V Gascan H Cell kinetics in the fetal mouse thymus: precursor cell input, proliferation, and emigration J Immunol 138 1026 2 15 1987 2879866
  18. [19]Ranganath S GATA-3-dependent enhancer activity in IL-4 gene regulation J Immunol 161 3822 10 15 1998 9780146
  19. [20]Lewis BP Burge CB Bartel DP Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets Cell 120 15 1 14 2005 15652477
  20. [21]Krek A Combinatorial microRNA target predictions Nat Genet 37 495 5 2005 15806104
  21. [22]Carvalho TL Mota-Santos T Cumano A Demengeot J Vieira P Arrested B lymphopoiesis and persistence of activated B cells in adult interleukin 7(−/)− mice J Exp Med 194 1141 10 15 2001 11602642 PMC2193519
  22. [23]Carey JB Moffatt-Blue CS Watson LC Gavin AL Feeney AJ Repertoire-based selection into the marginal zone compartment during B cell development J Exp Med 205 2043 9 1 2008 18710933 PMC2526199
  23. [24]Haas W Pereira P Tonegawa S Gamma/delta cells Annual review of immunology 11 637 1993 8476575
  24. [25]Grigoriadou K Boucontet L Pereira P Most IL-4-producing gamma delta thymocytes of adult mice originate from fetal precursors J Immunol 171 2413 9 1 2003 12928388
  25. [26]Lee YJ Generation of PLZF+ CD4+ T cells via MHC class II-dependent thymocyte-thymocyte interaction is a physiological process in humans J Exp Med 207 237 1 18 2010 20038602 PMC2812550
  26. [27]Benlagha K Kyin T Beavis A Teyton L Bendelac A A thymic precursor to the NK T cell lineage Science 296 553 4 19 2002 11968185
  27. [28]Gapin L Matsuda JL Surh CD Kronenberg M NKT cells derive from double-positive thymocytes that are positively selected by CD1d Nat Immunol 2 971 10 2001 11550008
  28. [29]Bendelac A CD1 recognition by mouse NK1+ T lymphocytes Science (New York, NY) 268 863 1995 7538697
  29. [30]Alonzo ES Sant’Angelo DB Development of PLZF-expressing innate T cells Curr Opin Immunol 23 220 4 2011 21257299 PMC3073746
  30. [31]Weinreich MA Odumade OA Jameson SC Hogquist KA T cells expressing the transcription factor PLZF regulate the development of memory-like CD8+ T cells Nat Immunol 11 709 8 2010 20601952 PMC3051359
  31. [32]Verykokakis M Boos MD Bendelac A Kee BL SAP protein-dependent natural killer T-like cells regulate the development of CD8(+) T cells with innate lymphocyte characteristics Immunity 33 203 8 27 2010 20674402 PMC2933745
  32. [33]Lai D KLF13 sustains thymic memory-like CD8(+) T cells in BALB/c mice by regulating IL-4-generating invariant natural killer T cells J Exp Med 208 1093 5 9 2011 21482696 PMC3092346
  33. [34]Weinreich MA KLF2 transcription-factor deficiency in T cells results in unrestrained cytokine production and upregulation of bystander chemokine receptors Immunity 31 122 7 17 2009 19592277 PMC2724594
  34. [35]Tajima F Deguchi T Laver J Zeng H Ogawa M Reciprocal expression of CD38 and CD34 by adult murine hematopoietic stem cells Blood 97 2618 2001 11313250
  35. [36]Randall T Weissman I Phenotypic and functional changes induced at the clonal level in hematopoietic stem cells after 5-fluorouracil treatment Blood 89 3596 1997 9160664
  36. [37]Rebel V A comparison of long-term repopulating hematopoietic stem cells in fetal liver and adult bone marrow from the mouse Experimental hematology 24 638 1996 8605969
  37. [39]Jordan C McKearn J Lemischka I Cellular and developmental properties of fetal hematopoietic stem cells Cell 61 953 1990 1972037
  38. [40]Ito T Tajima F Ogawa M Developmental changes of CD34 expression by murine hematopoietic stem cells Experimental hematology 28 1269 2000 11063875
  39. [41]Kiel M SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells Cell 121 1109 2005 15989959
  40. [42]Lacombe J Scl regulates the quiescence and the long-term competence of hematopoietic stem cells Blood 115 792 2010 19850742
  41. [43]Kataoka K Evi1 is essential for hematopoietic stem cell self-renewal, and its expression marks hematopoietic cells with long-term multilineage repopulating activity The Journal of experimental medicine 208 2403 2011 22084405 PMC3256960
  42. [44]Ikeda K Mason P Bessler M 3′UTR-truncated Hmga2 cDNA causes MPN-like hematopoiesis by conferring a clonal growth advantage at the level of HSC in mice Blood 117 5860 2011 21460244 PMC3112035
  43. [45]Mayr C Hemann M Bartel D Disrupting the pairing between let-7 and Hmga2 enhances oncogenic transformation Science (New York, NY) 315 1576 2007 PMC2556962 17322030
  44. [46]Polesskaya A Lin-28 binds IGF-2 mRNA and participates in skeletal myogenesis by increasing translation efficiency Genes & development 21 1125 2007 17473174 PMC1855237
  45. [47]Kiel M Iwashita T Yilmaz O Morrison S Spatial differences in hematopoiesis but not in stem cells indicate a lack of regional patterning in definitive hematopoietic stem cells Developmental biology 283 29 2005 15913595
  46. [48]Brown J Boussiotis V Umbilical cord blood transplantation: basic biology and clinical challenges to immune reconstitution Clinical immunology (Orlando, Fla) 127 286 2008 PMC2468219 18395491
  47. [49]Haas KM Poe JC Steeber DA Tedder TF B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae Immunity 23 7 7 2005 16039575
  48. [50]Rauch P Innate Response Activator B Cells Protect Against Microbial Sepsis Science (New York, NY) 2012 PMC3279743 22245738
  49. [51]Belles C Bias in the gamma delta T cell response to Listeria monocytogenes. V delta 6.3+ cells are a major component of the gamma delta T cell response to Listeria monocytogenes J Immunol 156 4280 6 1 1996 8666799
  50. [52]Godfrey DI Kronenberg M Going both ways: immune regulation via CD1d− dependent NKT cells J Clin Invest 114 1379 11 2004 15545985 PMC525753

Cited by

Sorted by citations

Authors
Yuan, J., Nguyen, C. K., Liu, X., Kanellopoulou, C., & Muljo, S. A.
Affiliations
  • National Institutes of Health (US)
  • Laboratory of Immunology, National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health, Bethesda, MD 20892, USA.
Corresponding author
Muljo, Stefan A.
ORCID
Venue
Science
Publisher
American Association for the Advancement of Science (AAAS)
Published
2012-03-09
Volume
335
Issue
6073
Pages
1195-1200
ISSN
  • 0036-8075 (ISSN-L)
  • 1095-9203
DOI
10.1126/science.1216557
PMC
PMC3471381
OpenAlex
W2088907802
Cited by
343
References
3
Citations by year
2026: 14 · 2025: 20 · 2024: 20 · 2023: 25 · 2022: 24 · 2021: 20 · 2020: 21 · 2019: 29 · 2018: 24 · 2017: 26 · 2016: 27 · 2015: 27 · 2014: 20 · 2013: 36 · 2012: 10
FWCI
19.83
Type
journal article
Language
en
Open access
Locations
  • Science (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institutes of Health
  • National Institute of Allergy and Infectious Diseases (ZIAAI001131)
Topics
  • Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
LIN28B, hematopoietic stem and progenitor cells, bone marrow, hematopoietic reprogramming, multilineage reconstitution, B-1a cells, marginal zone B cells, γδ T cells, NKT cells, fetal liver, thymus
MeSH terms
Animals, B-Lymphocytes, Bone Marrow Cells, DNA-Binding Proteins, Fetal Blood, Fetus, Flow Cytometry, Hematopoietic Stem Cells, Humans, Liver, Mice, Inbred C57BL, T-Lymphocytes, Thymus Gland, Transduction, Genetic, B-Lymphocyte Subsets, T-Lymphocyte Subsets, RNA-Binding Proteins, Cell Lineage, Reverse Transcriptase Polymerase Chain Reaction, MicroRNAs, Lymphopoiesis, Mice, Adult Stem Cells, Natural Killer T-Cells

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