Harmacological manipulation of the RAR/RXR signaling pathway maintains the repopulating capacity of hematopoietic stem cells in culture

Molecular Endocrinology

Volumn 23, Issue 2, 2009, Pages 188-201

  Safi, Rachid ^a   Muramoto, Garrett G ^a   Salter, Alice B ^a   Meadows, Sarah ^a   Himburg, Heather ^a   Russell, Lauren ^a   Daher, Pamela ^a   Doan, Phuong ^a   Leibowitz, Mark D ^b   Chao, Nelson J ^a   McDonnell, Donald P ^a   Chute, John P ^a,c  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b LIGAND PHARMACEUTICALS INC   (United States)

^c DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LG 1506; RETINOID X RECEPTOR; RO 415253; UNCLASSIFIED DRUG; 7 (2 (2,2 DIFLUOROETHOXY) 3,5 DI TERT BUTYLBENZENE) 3 METHYLOCTA 2,4,6 TRIENOIC ACID; 7-(2-(2,2-DIFLUOROETHOXY)-3,5-DI-TERT-BUTYLBENZENE)-3-METHYLOCTA-2,4,6-TRIENOIC ACID; BENZOIC ACID DERIVATIVE; BIOLOGICAL MARKER; CD38 ANTIGEN; CHROMAN DERIVATIVE; DIPHENYL ETHER DERIVATIVE; RETINOIC ACID RECEPTOR; RETINOID; RO 41 5253; RO 41-5253; UNSATURATED FATTY ACID;

ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL LOSS; CELL POPULATION; CELL RENEWAL; CONTROLLED STUDY; DRUG INHIBITION; DRUG MECHANISM; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; ANIMAL; CELL CYCLE; CELL LINEAGE; CHEMISTRY; CYTOLOGY; DIMERIZATION; DRUG EFFECT; GENETICS; METABOLISM; MOUSE; MOUSE MUTANT; NONOBESE DIABETIC MOUSE; PHYSIOLOGY; PROTEIN CONFORMATION; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, CD38; BENZOATES; BIOLOGICAL MARKERS; CELL CYCLE; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHROMANS; DIMERIZATION; FATTY ACIDS, UNSATURATED; HEMATOPOIETIC STEM CELLS; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; PHENYL ETHERS; PROTEIN CONFORMATION; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; RETINOIDS; SIGNAL TRANSDUCTION;

EID: 58849113213     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2008-0121     Document Type: Article

References (58)

1. Varnum-Finney B, Xu L, Brashem-Stein C, Nourigat C, Flowers D, Bakkour S, Pear W, Bernstein I 2000 Pluripotent, cytokine-dependent, hematopoietic stem cells are immortalized by constitutive Notch1 signaling. Nat Med 6:1278-1281
2. Krosl J, Austin P, Beslu N, Kroon, Humphries R, Sauvageau G 2003 In vitro expansion of hematopoietic stem cells by recombinant TAT-HOXB4 protein. Nat Med 9:1428-1432
3. Reya T, Duncan A, Ailles L, Domen J, Scherer D, Willert K, Hintz L, Nusse R, Weissman I 2003 A role for Wnt signalling in the self renewal of hematopoietic stem cells. Nature 423:409-414
4. Delaney C, Varnum-Finney B, Aoyama K, Brashem-Stein C, Bernstein I 2005 Dose-dependent effects of the Notch ligand A1 on ex vivo differentiation and in vivo marrow repopulating ability of cord blood cells. Blood 106:2693-2699
5. Delaney C, Bernstein I 2005 Culture of CD34+ umbilical cord blood progenitors with Notch ligand results in enhanced and more rapid human engraft-ment in a preclinical NOD/SCID mouse model. Blood 106:190 (Abstract)
6. Bhardwaj G, Murdoch B, Wu D, Baker D, Williams K, Chadwick K, Ling L, Karanu F, Bhatia M 2001 Sonic hedgehog induces the proliferation of primitive human hematopoietic cells via BMP regulation. Nat Immunol 2:172-180
7. Brun A, Bjornsson J, Magnusson, Larsson N, Leveen P, Ehinger M, Nillson E, Karlsson S 2004 Hoxb4-deficient mice undergo normal development but exhibit a mild proliferation defect in hematopoietic stem cells. Blood 4126-4133
8. Mancini S, Mantei N, Dumortier, Sutor U, MacDonald H, Radtke F 2005 Jagged-1 dependent Notch signaling is dispensable for hematopoietic stem cell self renewal and differentiation. Blood 105:2340-2342
9. Cobas M, Wilson A, Ernst B, Mancini S, MacDonald H, Kemler R, Radtke F 2004 B-catenin is dispensable for hematopoiesis and lymphopoiesis. J Exp Med 199:221-229
10. Bhatia M, Wang J, Kapp U, Bonnet D, Dick J 1997 Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci USA 94:5320-5325
11. + cells in non-obese diabetic/severe combined immune-deficient mice. Blood 92:2641-2649
12. - cells in ex vivo culture during retroviral transduction without a corresponding increase in SCID repopulating cell (SRC) frequency: dissociation of SRC phenotype and function. Blood 95:102-110
13. Chute J, Saini A, Chute D, Wells M, Clark W, Harlan D, Park J, Stull M, Civin C, Davis T 2002 Co-culture with human brain endothelial cells increases the SCID-repopulating capacity of adult human bone marrow. Blood 100:4433-4439
14. - cells and SCID-repopulating cells. Blood 105:576-583
15. Storms R, Green P, Safford K, Niedzwiecki D, Cogle C, Colvin O, Chao N, Rice H, Smith C 2005 Distinct hematopoietic progenitor compartments are delineated by the expression of aldehyde dehydrogenase and CD34. Blood 106:95-102
16. Hess D, Meyerosse T, Wirthlin L, Craft T, Herrbrich P, Creer M, Nolta J 2004 Functional characterization of highly purified hematopoietic repopulat-ing cells isolated according to aldehyde dehydrogenase activity. Blood 104:1648-1655
17. Chute J, Muramoto G, Whitesides J, Colvin M, Safi R, Chao N, McDonnell D 2006 Inhibition of aldehyde dehydrogenase and retinoid signaling induces the expansion of human hematopoietic stem cells. Proc Natl Acad Sci USA 103:11707-11712
18. Tocci A., Parolini I, Gabbianelli M, Testa U, Luchetti L, Samoggia P, Masella B, Russo G, Valtieri M, Peschle C 1996 Dual action of retinoic acid on human embryonic/fetalhematopoiesis: blockadeofprimitiveprogenitorproliferation and shift from multipotent/erythroid/ monocytic to granulocytic differentiation program. Blood 88:2878-2888
19. Sammons J, Ahmed N, Khokher M, Hassan H 2000 Mechanisms mediating the inhibitory effect of all-trans retinoic acid on primitive hematopoietic stem cells in long-term bone marrow culture. Stem Cells 18:214-219
20. + hematopoietic progenitor cells: involvement of retinoic acid receptors and retinoid X receptors depends on lineage commitment of the hematopoietic progenitor cells. Exp Hematol 27:642-653
21. Kastner P, Chan S 2001 Function of RARα during the maturation of neutrophils. Oncogene 20:7178-7185
22. Tsai S, Bartelmez S, Heyman R, Damm K, Evans R, Collins S 1992 A mutated retinoic acid receptor-α exhibiting dominant-negative activity alters the lineage development of a multipotent hematopoietic cell line. Genes Dev 6:2258-2269
23. Zhang P, Nelson E, Radomska H, Iwasaki J, Akashi K, Friedman A, Tenen D 2002 Induction of granulocytic differentiation by 2 pathways. Blood 99:4406-4412
24. Purton L, Bernstein I, Collins S 2000 All-trans retinoic acid enhances the long-term repopulating activity of cultured hematopoietic stem cells. Blood 95:470-477
25. γ is critical for maintaining a balance between hematopoietic stem cell self-renewal and differentiation. J Exp Med 203:1283-1293
26. Sakashita A, Kizaki M, Pakkala S, Schiller G, Tsuruoka N, Tomasaki R, Cameron J, Dawson M, Koeffler H 1993 9-cis retinoic acid: effects on normal and leukemic hematopoiesis in vitro. Blood 81:1009-1016
27. + erythroid progenitor cells. Blood 87:1728-1736
28. Ricote M, Snyder C, Leung H, Chen J, Chien K, Glass C 2006 Normal hematopoiesis after conditional targeting of RXRa in murine hematopoietic stem/progenitor cells. J Leukoc Biol 80:850-861
29. Michellys P, Ardecky R, Chen J, Crombie D, Etgen G, Faul M, Faulkner A, Grese T, Heyman R, Karanewsky D, Klausing K, Leibowitz M, Liu S, Mais D, Mapes C, Marschke K, Reifel-Miller A, Ogilvie K, Runtka D, Thompson A, Tyhonas J, Boehm M 2003 Novel (2E,4E,6Z)-7-(2-alkoxy-3,5-dialkylben-zene)-3- methylocta-2,4,6-trienoic acid retinoid X receptor modulators are active in models of type 2 diabetes. J Med Chem 46:2683-2696
30. Leibowitz M, Ardecky R, Boehm M, Broderick C, Carfagna M, Crombie D, D'Arrigo J, Etgen G, Faul M, Grese T, Havel H, Hein N, Heyman R, Jolley D, Klausing K, Liu S, Mais D, Mapes C, Marschke K, Michellys P, Montrose-Rafizadeh C, Ogilvie K, Pascual B, Runtga D, Tyhonas J, Urcan M, Wardlow M, Yumibe N, Reifel-Miller A 2006 Biological characterization of a het-erodimer selective RXR modulator: potential benefits for the treatment of type 2 diabetes. Endocrinology 147:1044-1053
31. Wang J, Doedens M, Dick J 1997 Primitive human hematopoietic cells are enriched in cord blood compared with adult bone marrow or mobilized peripheral blood as measured by the quantitative in vivo SCID-repopulating cell assay. Blood 89:3919-3924
32. Nervi C, Grippo J, Sherman M, George M, Jetten A 1989 Identification and characterization of nuclear retinoic acid-binding activity in human myeloblas-tic leukemia HL-60 cells. Proc Natl Acad Sci USA 86:5854-5858
33. Kishimoto H, Hoshino S, Ohori M, Kontani K, Nishina H, Suzawa M, Kato S, Katada T 1998 Molecular mechanism of human CD38 gene expression by retinoic acid. Identification of retinoic acid response element in the first in-tron. J Biol Chem 273:15429-15434
34. Mehta K, McQueen T, Manshouri T, Andreeff M, Collins S, Albitar M 1997 Involvement of retinoic acid receptor-α-mediated signaling pathway in induction of CD38 cell-surface antigen. Blood 89:3607-3614
35. Doyonnas R, Labarge M, Sacco A, Charlton C, Blau H 2004 Hematopoietic contribution to skeletal muscle regeneration by myelomonocytic precursors. Proc Natl Acad Sci USA 101:13507-13512
36. Huang H, Norris J, McDonnell D 2002 Identification of a negative regulatory surface within estrogen receptor α provides evidence in support of a role for corepressors in regulating cellular responses to agonists and antagonists. Mol Endocrinol 16:1778-1792
37. Shulman A, Mangelsdorf D 2005 Retinoid X receptor heterodimers in the metabolic syndrome. N Engl JMed 353:604-615
38. Szanto A, Narkar V, Shen Q, Uray I, Davies P, Nagy L 2004 Retinoid X receptors: X-ploring their (patho)physiological functions. Cell Death Differ 11(Suppl 2):S126-S143
39. Johnson B, Chandraratna R, Heyman R, Allegretto E, Mueller L, Collins S 1999 Retinoid X receptor (RXR) agonist-induced activation of dominant-negative RXR-retinoic acid receptor α403 heterodimers is developmentally regulated during myeloid differentiation. Mol Cell Biol 19:3372-3382
40. Bhatia M, Bonnet D, Kapp U, Wang J, Murdoch B, Dick J 1997 Quantitative analysis reveals expansion of human hematopoietic repopulating cells after short-term ex vivo culture. J Exp Med 186:619-624
41. Glimm H, Eaves C 1999 Direct evidence for multiple self renewal divisions of human in vivo repopulating hematopoietic cells in short-term culture. Blood 94:2161-2168
42. Amsellem S, Pflumio F, Bardinet D, Izac B, Charneau P, Romeo P, Dubart-Kupperschmitt A, Fickelson S 2003 Ex vivo expansion of human hematopoi-etic stem cells by direct delivery of the HOXB4 homeoprotein. Nat Med 9:1423-1427
43. Hackney J, Charbord P, Brunk P, Stoeckert C, Lemischka I, Moore K 2002 A molecular profile of a hematopoietic stem cell niche. Proc Natl Acad Sci USA 99:13061-13066
44. - cord blood cells. J Clin Invest 110:1165-1174
45. Karanu F, Murdoch B, Gallacher L, Wu D, Koremoto M, Sakano S, Bhatia M 2000 The Notch ligand Jagged-1 represents a novel growth factor of human hematopoietic stem cells. J Exp Med 192:1365-1372
46. Thorsteindottir U, Sauvageau G, Humphries R 1999 Enhanced in vivo regenerative potential of HOXB4-transduced hematopoietic stem cells with regulation of their pool size. Blood 94:2605-2612
47. Mangelsdorf D, Evans R 1995 The RXR heterodimers and orphan receptors. Cell 83:841-850
48. YuV, Delsert C, Andersen B, Holloway J, Devary O, Naar A, Kim S, Boutin J, Glass C, Rosenfeld M 1991 RXRβ: a coregulator that enhances binding of retinoic acid, thyroid hormone and vitamin D receptors to their cognate response elements. Cell 67:1251-1266
49. Vivat-Hannah V, Bourguet W, Gottardis M, Gronemeyer H 2003 Separation of retinoid X receptor homo- and heterodimerization functions. Mol Cell Biol 23:7678-7688
50. Duncan A, Rattis F, DiMascio L, Congdon K, Pazianos G, Zhao C, Yoon K, Cook J, Willert K, Gaiano N, Reya T 2005 Integration of Notch and Wnt signaling in hematopoietic stem cell maintenance. Nat Immunol 6:314-322
51. Blank U, Karlsson G, Karlsson S 2008 Signaling pathways governing stem cell fate. Blood 111:492-503
52. Sorrentino B 2004 Clinical strategies for expansion of haematopoietic stem cells. Nat Immunol 4:878-888
53. Taswell C 1981 Limiting dilution assays for the determination of immuno-competent cell frequencies. I. Data analysis. J Immunol 126:1614-1619
54. Jordan CT, Yamasaki G, Minamoto D 1996 High-resolution cell cycle analysis of defined phenotypic subsets within primitive human hematopoietic cell populations. Exp Hematol 24:1347-1355
55. Muramoto G, Chen B, Cui X, Chao N, Chute JP 2006 Vascular endothelial cells produce soluble factors capable of rescuing human hematopoietic stem cells following radiation injury. Biol Blood Marrow Transplant 12:530-540
56. Safi R, Kovacic A, Gaillard S, Murata Y, Simpson E, McDonnell D, Clyne C 2005 Co-activation of liver receptor homologue-1 peroxisome proliferator-activated receptor γ coactivator-1α on aromatase promoter II and its inhibition by activated retinoid X receptor suggest a novel target for breast-specific anti-estrogen therapy. Cancer Res 65:11762-11770
57. Chang C, Norris J, Gron H, Paige L, Hamilton P, Kenan P, Kenan D, Fowlkes D, McDonnell D 1999 Dissection of the LXXLL NR-coactivator interaction motif using combinatorial peptide libraries: discovery of peptide antagonists of estrogen receptors α and β. Mol Cell Biol 19:8226-8239
58. Chang C, Abdo J, Hartney T, McDonnell D 2005 Development of peptide antagonists for the androgen receptor using combinatorial peptide phage display. Mol Endocrinol 19:2478 -2490