Aryl hydrocarbon receptor-null allele mice have hematopoietic stem/progenitor cells with abnormal characteristics and functions

Stem Cells and Development

Volumn 20, Issue 5, 2011, Pages 769-784

  Singh, Kameshwar P ^a   Garrett, Russell W ^b   Casado, Fanny L ^a   Gasiewicz, Thomas A ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b HAVERFORD COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER F1; ALPHA CHEMOKINE; AROMATIC HYDROCARBON RECEPTOR; ATAXIN 1; C REACTIVE PROTEIN; CCL1 CHEMOKINE; CHEMOKINE RECEPTOR CCR10; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR8; CHEMOKINE RECEPTOR CXCR5; CXCL11 CHEMOKINE; CXCL15 CHEMOKINE; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 11; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 20; INTERLEUKIN 3; INTERLEUKIN 4; MACROPHAGE INFLAMMATORY PROTEIN 3ALPHA; STEM CELL FACTOR; THYMUS AND ACTIVATION REGULATED CHEMOKINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL FUNCTION; CELL GROWTH; CELL LINEAGE; CELL POPULATION; CELL PROLIFERATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; CYTOKINE PRODUCTION; EOSINOPHIL; ERYTHROCYTE; FEMALE; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; LEUKOCYTE; LYMPHOCYTE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; RECEPTOR GENE; SPLEEN CELL; SPLENOMEGALY;

ALLELES; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BONE MARROW; BROMODEOXYURIDINE; CCAAT-ENHANCER-BINDING PROTEINS; CELL COUNT; CELL CYCLE; CELL PROLIFERATION; CIRCADIAN RHYTHM; ERYTHROCYTES; FEMALE; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; LEUKOCYTES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, ARYL HYDROCARBON; UP-REGULATION;

MUS;

EID: 79955749457     PISSN: 15473287     EISSN: 15578534     Source Type: Journal    
DOI: 10.1089/scd.2010.0333     Document Type: Article

References (65)

1. Gu YZ, JB Hogenesch and CA Bradfield. (2000). The PAS superfamily: sensors of environmental and developmental signals. Annu Rev Pharmacol Toxicol 40:519-561. (Pubitemid 30340692)
2. Hankinson O. (2005). Role of coactivators in transcriptional activation by the aryl hydrocarbon receptor. Arch Biochem Biophys 433:379-386. (Pubitemid 39592792)
3. Puga A, SJ Barnes, TP Dalton, C Chang, ES Knudsen and MA Maier. (2000). Aromatic hydrocarbon receptor interaction with the retinoblastoma protein potentiates repression of E2F-dependent transcription and cell cycle arrest. J Biol Chem 275:2943-2950. (Pubitemid 30082071)
4. Vogel CF and F Matsumura. (2009). A new cross-talk between the aryl hydrocarbon receptor and RelB, a member of the NF-kappaB family. Biochem Pharmacol 77:734-745.
5. Whitlock JP Jr. (1999). Induction of cytochrome P4501A1. Annu Rev Pharmacol Toxicol 39:103-125. (Pubitemid 29222553)
6. Thomsen JS, S Kietz, A Strom and JA Gustafsson. (2004). HES-1, a novel target gene for the aryl hydrocarbon receptor. Mol Pharmacol 65:165-171. (Pubitemid 38113897)
7. Chiaro CR, RD Patel and GH Perdew. (2008). 12(R)-Hydroxy- 5(Z),8(Z),10(E),14(Z)-eicosatetraenoic acid [12(R)-HETE], an arachidonic acid derivative, is an activator of the aryl hydrocarbon receptor. Mol Pharmacol 74:1649-1656.
8. Chowdhury G, M Dostalek, EL Hsu, LP Nguyen, DF Stec, CA Bradfield and FP Guengerich. (2009). Structural identification of Diindole agonists of the aryl hydrocarbon receptor derived from degradation of indole-3-pyruvic acid. Chem Res Toxicol 22:1905-1912.
9. DiNatale BC, IA Murray, JC Schroeder, CA Flaveny, TS Lahoti, EM Laurenzana, CJ Omiecinski and GH Perdew. (2010). Kynurenic acid is a potent endogenous aryl hydrocarbon receptor ligand that synergistically induces interleukin-6 in the presence of inflammatory signaling. Toxicol Sci 115:89-97.
10. Kerkvliet NI. (2009). AHR-mediated immunomodulation: the role of altered gene transcription. Biochem Pharmacol 77:746-760.
11. Bertazzi PA, AC Pesatori, I Bernucci, MT Landi and D Consonni. (1999). Dioxin exposure and human leukemias and lymphomas. Lessons from the Seveso accident and studies on industrial workers. Leukemia 13 (Suppl. 1):S72-S74.
12. Baccarelli A, P Mocarelli, DG Patterson Jr., M Bonzini, AC Pesatori, N Caporaso and MT Landi. (2002). Immunologic effects of dioxin: new results from Seveso and comparison with other studies. Environ Health Perspect 110:1169-1173. (Pubitemid 36024299)
13. Kimura A, T Naka, K Nohara, Y Fujii-Kuriyama and T Kishimoto. (2008). Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc Natl Acad Sci U S A 105:9721-9726. (Pubitemid 352031367)
14. Quintana FJ, AS Basso, AH Iglesias, T Korn, MF Farez, E Bettelli, M Caccamo, M Oukka and HL Weiner. (2008). Control of T(reg) and T(H)17 cell differentiation by the aryl hydrocarbon receptor. Nature 453:65-71. (Pubitemid 351630328)
15. Thurmond TS and TA Gasiewicz. (2000). A single dose of 2,3,7,8-tetrachlorodibenzo-p-dioxin produces a time- and dose-dependent alteration in the murine bone marrow Blymphocyte maturation profile. Toxicol Sci 58:88-95.
16. Fine JS, AE Silverstone and TA Gasiewicz. (1990). Impairment of prothymocyte activity by 2,3,7,8-tetrachlorodibenzop- dioxin. J Immunol 144:1169-1176. (Pubitemid 20072879)
17. Murante FG and TA Gasiewicz. (2000). Hemopoietic progenitor cells are sensitive targets of 2,3,7,8-tetrachlorodibenzop- dioxin in C57BL/6J mice. Toxicol Sci 54:374-383. (Pubitemid 30185959)
18. Singh KP, A Wyman, FL Casado, RW Garrett and TA Gasiewicz. (2009). Treatment of mice with the Ah receptor agonist and human carcinogen dioxin results in altered numbers and function of hematopoietic stem cells. Carcinogenesis 30:11-19.
19. Staples JE, FG Murante, NC Fiore, TA Gasiewicz and AE Silverstone. (1998). Thymic alterations induced by 2,3,7,8- tetrachlorodibenzo-p-dioxin are strictly dependent on aryl hydrocarbon receptor activation in hemopoietic cells. J Immunol 160:3844-3854. (Pubitemid 28176089)
20. Sakai R, T Kajiume, H Inoue, R Kanno, M Miyazaki, Y Ninomiya and M Kanno. (2003). TCDD treatment eliminates the long-term reconstitution activity of hematopoietic stem cells. Toxicol Sci 72:84-91. (Pubitemid 36336437)
21. Fernandez-Salguero P, T Pineau, DM Hilbert, T McPhail, SS Lee, S Kimura, DW Nebert, S Rudikoff, JM Ward and FJ Gonzalez. (1995). Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268:722-726.
22. Schmidt JV, GH Su, JK Reddy, MC Simon and CA Bradfield. (1996). Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc Natl Acad Sci U S A 93:6731-6736. (Pubitemid 26230378)
23. Fernandez-Salguero PM, JM Ward, JP Sundberg and FJ Gonzalez. (1997). Lesions of aryl-hydrocarbon receptordeficient mice. Vet Pathol 34:605-614.
24. Thurmond TS, JE Staples, AE Silverstone and TA Gasiewicz. (2000). The aryl hydrocarbon receptor has a role in the in vivo maturation of murine bone marrow B lymphocytes and their response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 165:227-236. (Pubitemid 30429906)
25. Fernandez-Salguero PM, DM Hilbert, S Rudikoff, JM Ward and FJ Gonzalez. (1996). Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxininduced toxicity. Toxicol Appl Pharmacol 140:173-179. (Pubitemid 26329475)
26. Vorderstrasse BA, LB Steppan, AE Silverstone and NI Kerkvliet. (2001). Aryl hydrocarbon receptor-deficient mice generate normal immune responses to model antigens and are resistant to TCDD-induced immune suppression. Toxicol Appl Pharmacol 171:157-164. (Pubitemid 32217666)
27. Uchida N, HL Aguila, WH Fleming, L Jerabek and IL Weissman. (1994). Rapid and sustained hematopoietic re- covery in lethally irradiated mice transplanted with purified Thy-1.1lo Lin-Sca-1+hematopoietic stem cells. Blood 83: 3758-3779.
28. Taswell C. (1981). Limiting dilution assays for the determination of immunocompetent cell frequencies. I. Data analysis. J Immunol 126:1614-1619. (Pubitemid 11149274)
29. Cacalano G, J Lee, K Kikly, AM Ryan, S Pitts-Meek, B Hultgren, WI Wood and MW Moore. (1994). Neutrophil and B cell expansion in mice that lack the murine IL-8 receptor homolog. Science 265:682-684. (Pubitemid 24268283)
30. Flaishon L, G Hart, E Zelman, C Moussion, V Grabovsky, G Lapidot Tal, S Feigelson, R Margalit, A Harmelin, T Avin- Wittenberg, D Shoseyov, R Alon, JP Girard and I Shachar. (2008). Anti-inflammatory effects of an inflammatory chemokine: CCL2 inhibits lymphocyte homing by modulation of CCL21-triggered integrin-mediated adhesions. Blood 112: 5016-5025.
31. Benevides L, CM Milanezi, LM Yamauchi, CF Benjamim, JS Silva and NM Silva. (2008). CCR2 receptor is essential to activate microbicidal mechanisms to control Toxoplasma gondii infection in the central nervous system. Am J Pathol 173:741-751.
32. Sanchez Y, D Rosado Jde, L Vega, G Elizondo, E Estrada- Muniz, R Saavedra, I Juarez and M Rodriguez-Sosa. (2010). The unexpected role for the aryl hydrocarbon receptor on susceptibility to experimental toxoplasmosis. J Biomed Biotechnol 2010:505694.
33. Si Y, CL Tsou, K Croft and IF Charo. (2010). CCR2 mediates hematopoietic stem and progenitor cell trafficking to sites of inflammation in mice. J Clin Invest 120:1192-1203.
34. Ito T, F Tajima and M Ogawa. (2000). Developmental changes of CD34 expression by murine hematopoietic stem cells. Exp Hematol 28:1269-1273.
35. Peters R, S Leyvraz and L Perey. (1998). Apoptotic regulation in primitive hematopoietic precursors. Blood 92:2041-2052. (Pubitemid 28446694)
36. Spangrude GJ, DM Brooks and DB Tumas. (1995). Longterm repopulation of irradiated mice with limiting numbers of purified hematopoietic stem cells: in vivo expansion of stem cell phenotype but not function. Blood 85:1006-1016.
37. Ema H, H Takano, K Sudo and H Nakauchi. (2000). In vitro self-renewal division of hematopoietic stem cells. J Exp Med 192:1281-1288.
38. Halene S, P Gaines, H Sun, T Zibello, S Lin, A Khanna- Gupta, SC Williams, A Perkins, D Krause and N Berliner. (2010). C/EBPepsilon directs granulocytic-vs-monocytic lineage determination and confers chemotactic function via Hlx. Exp Hematol 38:90-103.
39. Shtutman M, J Zhurinsky, I Simcha, C Albanese, M D'Amico, R Pestell and A Ben-Ze'ev. (1999). The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci U S A 96:5522-5527. (Pubitemid 29234650)
40. Reya T, M O'Riordan, R Okamura, E Devaney, K Willert, R Nusse and R Grosschedl. (2000). Wnt signaling regulates B lymphocyte proliferation through a LEF-1 dependent mechanism. Immunity 13:15-24.
41. Harper PA, DS Riddick and AB Okey. (2006). Regulating the regulator: factors that control levels and activity of the aryl hydrocarbon receptor. Biochem Pharmacol 72:267-279. (Pubitemid 43975077)
42. Cobaleda C, A Schebesta, A Delogu and M Busslinger. (2007). Pax5: the guardian of B cell identity and function. Nat Immunol 8:463-470. (Pubitemid 46605911)
43. Hirabayashi Y and T Inoue. (2009). Aryl hydrocarbon receptor biology and xenobiotic responses in hematopoietic progenitor cells. Biochem Pharmacol 77:521-535.
44. Hall MA, DJ Curtis, D Metcalf, AG Elefanty, K Sourris, L Robb, JR Gothert, SM Jane and CG Begley. (2003). The critical regulator of embryonic hematopoiesis, SCL, is vital in the adult for megakaryopoiesis, erythropoiesis, and lineage choice in CFU-S12. Proc Natl Acad Sci U S A 100: 992-997. (Pubitemid 36183943)
45. Matsuo T, S Yamaguchi, S Mitsui, A Emi, F Shimoda and H Okamura. (2003). Control mechanism of the circadian clock for timing of cell division in vivo. Science 302:255-259. (Pubitemid 37248750)
46. Venezia TA, AA Merchant, CA Ramos, NL Whitehouse, AS Young, CA Shaw and MA Goodell. (2004). Molecular signatures of proliferation and quiescence in hematopoietic stem cells. PLoS Biol 2:e301.
47. Garrett RW and TA Gasiewicz. (2006). The aryl hydrocarbon receptor agonist 2,3,7,8-tetrachlorodibenzo-p-dioxin alters the circadian rhythms, quiescence, and expression of clock genes in murine hematopoietic stem and progenitor cells. Mol Pharmacol 69:2076-2083. (Pubitemid 43894327)
48. Abrahamsen JF, R Smaaland, RB Sothern and OD Laerum. (1998). Variation in cell yield and proliferative activity of positive selected human CD34+ bone marrow cells along the circadian time scale. Eur J Haematol 60:7-15. (Pubitemid 28035754)
49. Scadden DT. (2008). Circadian rhythms: stem cells traffic in time. Nature 452:416-417. (Pubitemid 351450831)
50. Boitano AE, J Wang, R Romeo, LC Bouchez, AE Parker, SE Sutton, JR Walker, CA Flaveny, GH Perdew, MS Denison, PG Schultz and MP Cooke. (2010). Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 329:1345-1348.
51. Mulero-Navarro S, JM Carvajal-Gonzalez, M Herranz, E Ballestar, MF Fraga, S Ropero, M Esteller and PM Fernandez-Salguero. (2006). The dioxin receptor is silenced by promoter hypermethylation in human acute lymphoblastic leukemia through inhibition of Sp1 binding. Carcinogenesis 27:1099-1104.
52. de Haan G and G Van Zant. (1999). Dynamic changes in mouse hematopoietic stem cell numbers during aging. Blood 93:3294-3301. (Pubitemid 29220896)
53. de Haan G, W Nijhof and G Van Zant. (1997). Mouse straindependent changes in frequency and proliferation of hematopoietic stem cells during aging: correlation between lifespan and cycling activity. Blood 89:1543-1550. (Pubitemid 27097446)
54. Nebert DW, DD Brown, DW Towne and HJ Eisen. (1984). Association of fertility, fitness and longevity with the murine Ah locus among (C57BL/6N) (C3H/HeN) recombinant inbred lines. Biol Reprod 30:363-373. (Pubitemid 14144460)
55. Spindler SR, A Koizumi, RL Walford and PL Mote. (1989). P1-450 and P3-450 gene expression and maximum life span in mice. Mutat Res 219:89-94. (Pubitemid 19068475)
56. Gasiewicz TA, EC Henry and LL Collins. (2008). Expression and activity of aryl hydrocarbon receptors in development and cancer. Crit Rev Eukaryot Gene Expr 18:279-321. (Pubitemid 351991362)
57. Zaher H, PM Fernandez-Salguero, J Letterio, MS Sheikh, AJ Fornace Jr., AB Roberts and FJ Gonzalez. (1998). The involvement of aryl hydrocarbon receptor in the activation of transforming growth factor-beta and apoptosis. Mol Pharmacol 54:313-321. (Pubitemid 28368821)
58. Isufi I, M Seetharam, L Zhou, D Sohal, J Opalinska, P Pahanish and A Verma. (2007). Transforming growth factorbeta signaling in normal and malignant hematopoiesis. J Interferon Cytokine Res 27:543-552. (Pubitemid 47122713)
59. Andreola F, PM Fernandez-Salguero, MV Chiantore, MP Petkovich, FJ Gonzalez and LM De Luca. (1997). Aryl hydrocarbon receptor knockout mice (AHR-/-) exhibit liver retinoid accumulation and reduced retinoic acid metabolism. Cancer Res 57:2835-2838. (Pubitemid 27315022)
60. Collins SJ. (2008). Retinoic acid receptors, hematopoiesis and leukemogenesis. Curr Opin Hematol 15:346-351.
61. Ghaffari S. (2008). Oxidative stress in the regulation of normal and neoplastic hematopoiesis. Antioxid Redox Signal 10:1923-1940.
62. Ferrara N, HP Gerber and J LeCouter. (2003). The biology of VEGF and its receptors. Nat Med 9:669-676. (Pubitemid 36749215)
63. Lahvis GP, RW Pyzalski, E Glover, HC Pitot, MK McElwee and CA Bradfield. (2005). The aryl hydrocarbon receptor is required for developmental closure of the ductus venosus in the neonatal mouse. Mol Pharmacol 67:714-720. (Pubitemid 40365318)
64. Roman AC, JM Carvajal-Gonzalez, EM Rico-Leo and PM Fernandez-Salguero. (2009). Dioxin receptor deficiency impairs angiogenesis by a mechanism involving VEGF-A depletion in the endothelium and transforming growth factor-beta overexpression in the stroma. J Biol Chem 284: 25135-25148.
65. Loges S, B Fehse, MA Brockmann, K Lamszus, M Butzal, M Guckenbiehl, G Schuch, S Ergun, U Fischer, AR Zander, DK Hossfeld, W Fiedler and UM Gehling. (2004). Identification of the adult human hemangioblast. Stem Cells Dev 13: 229-242. (Pubitemid 38738365)