Home LiteratureArticle Details
PMID: 16682494 Published · ppublish English Comparative Study Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

RARgamma is critical for maintaining a balance between hematopoietic stem cell self-renewal and differentiation.

The Journal of experimental medicine ·Vol. 203 ·No. 5 ·2006-05-15 ·Pages 1283-93

Purton LE, Dworkin S, Olsen GH, Walkley CR, Fabb SA, Collins SJ, Chambon P

Abstract

Hematopoietic stem cells (HSCs) sustain lifelong production of all blood cell types through finely balanced divisions leading to self-renewal and differentiation. Although several genes influencing HSC self-renewal have been identified, to date no gene has been described that, when activated, enhances HSC self-renewal and, when inactivated [corrected] promotes HSC differentiation. We observe that the retinoic acid receptor (RAR)gamma is selectively expressed in primitive hematopoietic precursors and that the bone marrow of RARgamma knockout mice exhibit markedly reduced numbers of HSCs associated with increased numbers of more mature progenitor cells compared with wild-type mice. In contrast, RARalpha is widely expressed in hematopoietic cells, but RARalpha knockout mice do not exhibit any HSC or progenitor abnormalities. Primitive hematopoietic precursors overexpressing RARalpha differentiate predominantly to granulocytes in short-term culture, whereas those overexpressing RARgamma exhibit a much more undifferentiated phenotype. Furthermore, loss of RARgamma abrogated the potentiating effects of all-trans retinoic acid on the maintenance of HSCs in ex vivo culture. Finally, pharmacological activation of RARgamma ex vivo promotes HSC self-renewal, as demonstrated by serial transplant studies. We conclude that the RARs have distinct roles in hematopoiesis and that RARgamma is a critical physiological and pharmacological regulator of the balance between HSC self-renewal and differentiation.

MeSH Terms
Animals Antineoplastic Agents/pharmacology Bone Marrow/physiology Cell Differentiation/drug effects,physiology Cell Proliferation Cells, Cultured Gene Expression Regulation/drug effects,physiology Granulocytes/cytology,physiology Hematopoiesis/drug effects,physiology Hematopoietic Stem Cell Transplantation Hematopoietic Stem Cells/cytology,metabolism Mice Receptors, Retinoic Acid/genetics,metabolism Tretinoin/pharmacology
Chemicals
Antineoplastic Agents Receptors, Retinoic Acid retinoic acid receptor gamma Tretinoin
Authors & Affiliations
7 authors, click to expand affiliations / ORCID
Purton Louise E
Trescowthick Research Laboratories, Peter MacCallum Cancer Centre, East Melbourne, Victoria 3002, Australia. lpurton@partners.org
Dworkin Sebastian
Olsen Gemma Haines
Walkley Carl R
Fabb Stewart A
Collins Steven J
Chambon Pierre
References (45)
45 references, click to expand
  1. Identification of a retinoic acid response element upstream of the murine Hox-4.2 gene.
    Mol Cell Biol. 1993 Jan;13(1):257-65 PMID: 8093325
  2. Retinoids and Hox genes.
    FASEB J. 1996 Jul;10(9):969-78 PMID: 8801179
  3. Molecular pathogenesis of acute promyelocytic leukaemia and APL variants.
    Best Pract Res Clin Haematol. 2003 Sep;16(3):387-408 PMID: 12935958
  4. Beta-catenin is dispensable for hematopoiesis and lymphopoiesis.
    J Exp Med. 2004 Jan 19;199(2):221-9 PMID: 14718516
  5. Jagged1-dependent Notch signaling is dispensable for hematopoietic stem cell self-renewal and differentiation.
    Blood. 2005 Mar 15;105(6):2340-2 PMID: 15550486
  6. Hoxb4-deficient mice undergo normal hematopoietic development but exhibit a mild proliferation defect in hematopoietic stem cells.
    Blood. 2004 Jun 1;103(11):4126-33 PMID: 14962901
  7. Retinoic acid-induced proliferation of lung alveolar epithelial cells is linked to p21(CIP1) downregulation.
    Am J Physiol Lung Cell Mol Physiol. 2000 Jan;278(1):L42-50 PMID: 10645889
  8. Identification of the molecular requirements for an RAR alpha-mediated cell cycle arrest during granulocytic differentiation.
    Blood. 2004 Feb 15;103(4):1286-95 PMID: 14576045
  9. Identification of Lin(-)Sca1(+)kit(+)CD34(+)Flt3- short-term hematopoietic stem cells capable of rapidly reconstituting and rescuing myeloablated transplant recipients.
    Blood. 2005 Apr 1;105(7):2717-23 PMID: 15572596
  10. Expression of Notch 1, 2 and 3 is regulated by epithelial-mesenchymal interactions and retinoic acid in the developing mouse tooth and associated with determination of ameloblast cell fate.
    J Cell Biol. 1995 Jul;130(2):407-18 PMID: 7615640
  11. Impaired granulocytic differentiation in vitro in hematopoietic cells lacking retinoic acid receptors alpha1 and gamma.
    Blood. 1998 Jul 15;92(2):607-15 PMID: 9657762
  12. All-trans retinoic acid as a differentiation therapy for acute promyelocytic leukemia. I. Clinical results.
    Blood. 1990 Nov 1;76(9):1704-9 PMID: 2224119
  13. Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance.
    Nat Immunol. 2005 Mar;6(3):314-22 PMID: 15665828
  14. Multiple members of the retinoic acid receptor family are capable of mediating the granulocytic differentiation of HL-60 cells.
    Mol Cell Biol. 1992 Sep;12(9):3743-9 PMID: 1324405
  15. Identification of clonogenic common lymphoid progenitors in mouse bone marrow.
    Cell. 1997 Nov 28;91(5):661-72 PMID: 9393859
  16. Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling.
    Nat Med. 2000 Nov;6(11):1278-81 PMID: 11062542
  17. HOXB4-induced expansion of adult hematopoietic stem cells ex vivo.
    Cell. 2002 Apr 5;109(1):39-45 PMID: 11955445
  18. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages.
    Nature. 2000 Mar 9;404(6774):193-7 PMID: 10724173
  19. Differentiation therapy of acute promyelocytic leukemia with tretinoin (all-trans-retinoic acid).
    N Engl J Med. 1991 May 16;324(20):1385-93 PMID: 1850498
  20. Ex vivo expansion of hematopoietic cells. Part II: control of proliferation and differentiation of hematopoietic stem cells.
    Exp Hematol. 2004 Aug;32(8):692 PMID: 15308316
  21. Negative cell-cycle regulators cooperatively control self-renewal and differentiation of haematopoietic stem cells.
    Nat Cell Biol. 2005 Feb;7(2):172-8 PMID: 15654333
  22. Primitive hemopoietic stem cells: direct assay of most productive populations by competitive repopulation with simple binomial, correlation and covariance calculations.
    Exp Hematol. 1993 Feb;21(2):206-19 PMID: 8425559
  23. High postnatal lethality and testis degeneration in retinoic acid receptor alpha mutant mice.
    Proc Natl Acad Sci U S A. 1993 Aug 1;90(15):7225-9 PMID: 8394014
  24. All-trans retinoic acid enhances the long-term repopulating activity of cultured hematopoietic stem cells.
    Blood. 2000 Jan 15;95(2):470-7 PMID: 10627451
  25. Cell division and hematopoietic stem cells: not always exhausting.
    Cell Cycle. 2005 Jul;4(7):893-6 PMID: 15970708
  26. All-trans retinoic acid delays the differentiation of primitive hematopoietic precursors (lin-c-kit+Sca-1(+)) while enhancing the terminal maturation of committed granulocyte/monocyte progenitors.
    Blood. 1999 Jul 15;94(2):483-95 PMID: 10397716
  27. Use of all-trans retinoic acid in the treatment of acute promyelocytic leukemia.
    Blood. 1988 Aug;72(2):567-72 PMID: 3165295
  28. Organization of haemopoietic stem cells: the generation-age hypothesis.
    Cell Tissue Kinet. 1979 Jan;12(1):17-29 PMID: 33767
  29. Stem cell repopulation efficiency but not pool size is governed by p27(kip1).
    Nat Med. 2000 Nov;6(11):1235-40 PMID: 11062534
  30. A role for Wnt signalling in self-renewal of haematopoietic stem cells.
    Nature. 2003 May 22;423(6938):409-14 PMID: 12717450
  31. Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo.
    Genes Dev. 1995 Jul 15;9(14):1753-65 PMID: 7622039
  32. Developmental changes of CD34 expression by murine hematopoietic stem cells.
    Exp Hematol. 2000 Nov;28(11):1269-73 PMID: 11063875
  33. Quantitative assay for totipotent reconstituting hematopoietic stem cells by a competitive repopulation strategy.
    Proc Natl Acad Sci U S A. 1990 Nov;87(22):8736-40 PMID: 2247442
  34. Transcriptional activation of the human p21(WAF1/CIP1) gene by retinoic acid receptor. Correlation with retinoid induction of U937 cell differentiation.
    J Biol Chem. 1996 Dec 6;271(49):31723-8 PMID: 8940196
  35. Mice lacking all isoforms of retinoic acid receptor beta develop normally and are susceptible to the teratogenic effects of retinoic acid.
    Mech Dev. 1995 Sep;53(1):61-71 PMID: 8555112
  36. CD34 expression by murine hematopoietic stem cells mobilized by granulocyte colony-stimulating factor.
    Blood. 2000 Sep 1;96(5):1989-93 PMID: 10961905
  37. Function of RARalpha during the maturation of neutrophils.
    Oncogene. 2001 Oct 29;20(49):7178-85 PMID: 11704846
  38. HOXB4 overexpression mediates very rapid stem cell regeneration and competitive hematopoietic repopulation.
    Exp Hematol. 2001 Sep;29(9):1125-34 PMID: 11532354
  39. Function of retinoic acid receptor gamma in the mouse.
    Cell. 1993 May 21;73(4):643-58 PMID: 8388780
  40. An oxysterol-binding protein family identified in the mouse.
    DNA Cell Biol. 2002 Aug;21(8):571-80 PMID: 12215260
  41. All-trans retinoic acid (ATRA) enhances maintenance of primitive human hematopoietic progenitors and skews them towards myeloid differentiation in a stroma-noncontact culture system.
    Exp Hematol. 2005 Apr;33(4):422-7 PMID: 15781332
  42. In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells.
    Blood. 1992 Dec 15;80(12):3044-50 PMID: 1281687
  43. CD34 expression on long-term repopulating hematopoietic stem cells changes during developmental stages.
    Blood. 2001 Jan 15;97(2):419-25 PMID: 11154218
  44. Hematopoietic stem cell quiescence maintained by p21cip1/waf1.
    Science. 2000 Mar 10;287(5459):1804-8 PMID: 10710306
  45. Signalling downstream of activated mammalian Notch.
    Nature. 1995 Sep 28;377(6547):355-8 PMID: 7566092
Article Info
Journal
The Journal of experimental medicine
Abbr.
J Exp Med
ISSN
0022-1007
Published
2006-05-15
Epub
2006-00-08
Pages
1283-93
Language
English
Region
United States
NLM ID
2985109R
PMCID
PMC2121209
Subset
IM
Corrections
ErratumIn
-
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com