Impaired functionality and homing of fancg-deficient hematopoietic stem cells

Human Molecular Genetics

Volumn 21, Issue 1, 2012, Pages 121-135

  Barroca, Vilma ^a,b,c,d,e   Mouthon, Marc André ^a,c,d,e   Lewandowski, Daniel ^a,c,d,e   Brunet de la grange, Philippe ^a,c,d,e   Gauthier, Laurent Robert ^a,c,d,e   Pflumio, Françoise ^a,c,d,e   Boussin, François Dominique ^a,c,d,e   Arwert, Fre ^b   Riou, Lydia ^a,c,d,e   Allemand, Isabelle ^a,c,d,e   Romeo, Paul Henri ^a,c,d,e   Fouchet, Pierre ^a,c,d,e  

^a INSTITUT DE RADIOBIOLOGIE CELLULAIRE ET MOLÉCULAIRE   (France)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c Universite Paris Sud   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

[No Author keywords available]

Indexed keywords

STROMAL CELL DERIVED FACTOR 1;

ANIMAL CELL; APLASTIC ANEMIA; ARTICLE; BONE MARROW DEPRESSION; CANCER SUSCEPTIBILITY; CELL COMPARTMENTALIZATION; CELL HOMING; CELL MIGRATION; CELL RENEWAL; CONTROLLED STUDY; FANCG GENE; FANCONI ANEMIA; GENE; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IN VITRO STUDY; LEUKEMIA; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; BONE MARROW; CELL MOVEMENT; CHEMOKINE CXCL12; FANCONI ANEMIA; FANCONI ANEMIA COMPLEMENTATION GROUP G PROTEIN; FEMALE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC;

EID: 83455213486     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddr447     Document Type: Article

References (53)

1. Stoepker, C., Hain, K., Schuster, B., Hilhorst-Hofstee, Y., Rooimans, M.A., Steltenpool, J., Oostra, A.B., Eirich, K., Korthof, E.T., Nieuwint, A.W. et al. (2011) SLX4, a coordinator of structure-specific endonucleases, is mutated in a new Fanconi anemia subtype. Nat. Genet., 43, 138-141.
2. Grompe, M. and van de Vrugt, H. (2007) The Fanconi family adds a fraternal twin. Dev. Cell, 12, 661-662.
3. Blom, E., van de Vrugt, H.J., de Vries, Y., de Winter, J.P., Arwert, F. and Joenje, H. (2004) Multiple TPR motifs characterize the Fanconi anemia FANCG protein. DNA Repair (Amst.), 3, 77-84.
4. Koomen, M., Cheng, N.C., van de Vrugt, H.J., Godthelp, B.C., van der Valk, M.A., Oostra, A.B., Zdzienicka, M.Z., Joenje, H. and Arwert, F. (2002) Reduced fertility and hypersensitivity to mitomycin C characterize Fancg/Xrcc9 null mice. Hum. Mol. Genet., 11, 273-281.
5. Carreau, M. (2004) Not-so-novel phenotypes in the Fanconi anemia group D2 mouse model. Blood, 103, 2430.
6. Wilson, A., Laurenti, E., Oser, G., van der Wath, R.C., Blanco-Bose, W., Jaworski, M., Offner, S., Dunant, C.F., Eshkind, L., Bockamp, E. et al. (2008) Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell, 135, 1118-1129.
7. Rossi, D.J., Bryder, D., Seita, J., Nussenzweig, A., Hoeijmakers, J. and Weissman, I.L. (2007) Deficiencies in DNA damage repair limit the function of haematopoietic stem cells with age. Nature, 447, 725-729.
8. Park, Y. and Gerson, S.L. (2005) DNA repair defects in stem cell function and aging. Annu. Rev. Med., 56, 495-508.
9. Sii-Felice, K., Etienne, O., Hoffschir, F., Mathieu, C., Riou, L., Barroca, V., Haton, C., Arwert, F., Fouchet, P., Boussin, F.D. et al. (2008) Fanconi DNA repair pathway is required for survival and long-term maintenance of neural progenitors. EMBO J., 27, 770-781.
10. Pagano, G., Degan, P., d'Ischia, M., Kelly, F.J., Nobili, B., Pallardo, F.V., Youssoufian, H. and Zatterale, A. (2005) Oxidative stress as a multiple effector in Fanconi anaemia clinical phenotype. Eur. J. Haematol., 75, 93-100.
11. Zhang, X., Sejas, D.P., Qiu, Y., Williams, D.A. and Pang, Q. (2007) Inflammatory ROS promote and cooperate with the Fanconi anemia mutation for hematopoietic senescence. J. Cell Sci., 120, 1572-1583.
12. Briot, D., Mace-Aime, G., Subra, F. and Rosselli, F. (2008) Aberrant activation of stress-response pathways leads to TNF-alpha oversecretion in Fanconi anemia. Blood, 111, 1913-1923.
13. Bijangi-Vishehsaraei, K., Saadatzadeh, M.R., Werne, A., McKenzie, K.A., Kapur, R., Ichijo, H. and Haneline, L.S. (2005) Enhanced TNF-alpha-induced apoptosis in Fanconi anemia type C-deficient cells is dependent on apoptosis signal-regulating kinase 1. Blood, 106, 4124-4130.
14. Si, Y., Ciccone, S., Yang, F.C., Yuan, J., Zeng, D., Chen, S., van de Vrugt, H.J., Critser, J., Arwert, F., Haneline, L.S. et al. (2006) Continuous in vivo infusion of interferon-gamma (IFN-gamma) enhances engraftment of syngeneic wild-type cells in Fanca-/- and Fancg-/- mice. Blood, 108, 4283-4287.
15. Carreau, M., Gan, O.I., Liu, L., Doedens, M., McKerlie, C., Dick, J.E. and Buchwald, M. (1998) Bone marrow failure in the Fanconi anemia group C mouse model after DNA damage. Blood, 91, 2737-2744.
16. Carreau, M., Gan, O.I., Liu, L., Doedens, M., Dick, J.E. and Buchwald, M. (1999) Hematopoietic compartment of Fanconi anemia group C null mice contains fewer lineage-negative CD34+ primitive hematopoietic cells and shows reduced reconstruction ability. Exp. Hematol., 27, 1667-1674.
17. Haneline, L.S., Gobbett, T.A., Ramani, R., Carreau, M., Buchwald, M., Yoder, M.C. and Clapp, D.W. (1999) Loss of FancC function results in decreased hematopoietic stem cell repopulating ability. Blood, 94, 1-8.
18. Navarro, S., Meza, N.W., Quintana-Bustamante, O., Casado, J.A., Jacome, A., McAllister, K., Puerto, S., Surralles, J., Segovia, J.C. and Bueren, J.A. (2006) Hematopoietic dysfunction in a mouse model for Fanconi anemia group D1. Mol. Ther., 14, 525-535.
19. Pulliam-Leath, A.C., Ciccone, S.L., Nalepa, G., Li, X., Si, Y., Miravalle, L., Smith, D., Yuan, J., Li, J., Anur, P. et al. (2010) Genetic disruption of both Fancc and Fancg in mice recapitulates the hematopoietic manifestations of Fanconi anemia. Blood, 116, 2915-2920.
20. Habi, O., Delisle, M.C., Messier, N. and Carreau, M. (2005) Lack of self-renewal capacity in Fancc-/- stem cells after ex vivo expansion. Stem Cells, 23, 1135-1141.
21. Zhang, X., Li, J., Sejas, D.P. and Pang, Q. (2005) Hypoxia-reoxygenation induces premature senescence in FA bone marrow hematopoietic cells. Blood, 106, 75-85.
22. Nijnik, A., Woodbine, L., Marchetti, C., Dawson, S., Lambe, T., Liu, C., Rodrigues, N.P., Crockford, T.L., Cabuy, E., Vindigni, A. et al. (2007) DNA repair is limiting for haematopoietic stem cells during ageing. Nature, 447, 686-690.
23. Ito, K., Hirao, A., Arai, F., Matsuoka, S., Takubo, K., Hamaguchi, I., Nomiyama, K., Hosokawa, K., Sakurada, K., Nakagata, N. et al. (2004) Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature, 431, 997-1002.
24. Tothova, Z., Kollipara, R., Huntly, B.J., Lee, B.H., Castrillon, D.H., Cullen, D.E., McDowell, E.P., Lazo-Kallanian, S., Williams, I.R., Sears, C. et al. (2007) FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell, 128, 325-339.
25. Ito, K., Hirao, A., Arai, F., Takubo, K., Matsuoka, S., Miyamoto, K., Ohmura, M., Naka, K., Hosokawa, K., Ikeda, Y. et al. (2006) Reactive oxygen species act through p38 MAPK to limit the lifespan of hematopoietic stem cells. Nat. Med., 12, 446-451.
26. Wright, D.E., Bowman, E.P., Wagers, A.J., Butcher, E.C. and Weissman, I.L. (2002) Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J. Exp. Med., 195, 1145-1154.
27. Lewandowski, D., Barroca, V., Duconge, F., Bayer, J., Van Nhieu, J.T., Pestourie, C., Fouchet, P., Tavitian, B. and Romeo, P.H. (2010) In vivo cellular imaging pinpoints the role of reactive oxygen species in the early steps of adult hematopoietic reconstitution. Blood, 115, 443-452.
28. Laird, D.J., von Andrian, U.H. and Wagers, A.J. (2008) Stem cell trafficking in tissue development, growth, and disease. Cell, 132, 612-630.
29. Tremblay, C.S., Huard, C.C., Huang, F.F., Habi, O., Bourdages, V., Levesque, G. and Carreau, M. (2009) The fanconi anemia core complex acts as a transcriptional co-regulator in hairy enhancer of split 1 signaling. J. Biol. Chem., 284, 13384-13395.
30. Tremblay, C.S., Huang, F.F., Habi, O., Huard, C.C., Godin, C., Levesque, G. and Carreau, M. (2008) HES1 is a novel interactor of the Fanconi anemia core complex. Blood, 112, 2062-2070.
31. Viale, A., De Franco, F., Orleth, A., Cambiaghi, V., Giuliani, V., Bossi, D., Ronchini, C., Ronzoni, S., Muradore, I., Monestiroli, S. et al. (2009) Cell-cycle restriction limits DNA damage and maintains self-renewal of leukaemia stem cells. Nature, 457, 51-56.
32. Yang, L., Wang, L., Geiger, H., Cancelas, J.A., Mo, J. and Zheng, Y. (2007) Rho GTPase Cdc42 coordinates hematopoietic stem cell quiescence and niche interaction in the bone marrow. Proc. Natl Acad. Sci. USA, 104, 5091-5096.
33. Cancelas, J.A., Lee, A.W., Prabhakar, R., Stringer, K.F., Zheng, Y. and Williams, D.A. (2005) Rac GTPases differentially integrate signals regulating hematopoietic stem cell localization. Nat. Med., 11, 886-891.
34. Sugiyama, T., Kohara, H., Noda, M. and Nagasawa, T. (2006) Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches. Immunity, 25, 977-988.
35. Min, I.M., Pietramaggiori, G., Kim, F.S., Passegue, E., Stevenson, K.E. and Wagers, A.J. (2008) The transcription factor EGR1 controls both the proliferation and localization of hematopoietic stem cells. Cell Stem Cell, 2, 380-391.
36. Zhang, Q.S., Marquez-Loza, L., Eaton, L., Duncan, A.W., Goldman, D.C., Anur, P., Watanabe-Smith, K., Rathbun, R.K., Fleming, W.H., Bagby, G.C. et al. (2010) Fancd2-/- mice have hematopoietic defects that can be partially corrected by resveratrol. Blood, 116, 5140-5148.
37. Li, Y., Chen, S., Yuan, J., Yang, Y., Li, J., Ma, J., Wu, X., Freund, M., Pollok, K., Hanenberg, H. et al. (2009) Mesenchymal stem/progenitor cells promote the reconstitution of exogenous hematopoietic stem cells in Fancg-/- mice in vivo. Blood, 113, 2342-2351.
38. Arai, F., Hirao, A., Ohmura, M., Sato, H., Matsuoka, S., Takubo, K., Ito, K., Koh, G.Y. and Suda, T. (2004) Tie2/angiopoietin-1 signaling regulates hematopoietic stem cell quiescence in the bone marrow niche. Cell, 118, 149-161.
39. Li, X., Plett, P.A., Yang, Y., Hong, P., Freie, B., Srour, E.F., Orschell, C.M., Clapp, D.W. and Haneline, L.S. (2003) Fanconi anemia type C-deficient hematopoietic stem/progenitor cells exhibit aberrant cell cycle control. Blood, 102, 2081-2084.
40. Sang, L., Coller, H.A. and Roberts, J.M. (2008) Control of the reversibility of cellular quiescence by the transcriptional repressor HES1. Science, 321, 1095-1100.
41. Yu, X., Alder, J.K., Chun, J.H., Friedman, A.D., Heimfeld, S., Cheng, L. and Civin, C.I. (2006) HES1 inhibits cycling of hematopoietic progenitor cells via DNA binding. Stem Cells, 24, 876-888.
42. Fagerlie, S.R., Diaz, J., Christianson, T.A., McCartan, K., Keeble, W., Faulkner, G.R. and Bagby, G.C. (2001) Functional correction of FA-C cells with FANCC suppresses the expression of interferon gamma-inducible genes. Blood, 97, 3017-3024.
43. van Os, R., Kamminga, L.M., Ausema, A., Bystrykh, L.V., Draijer, D.P., van Pelt, K., Dontje, B. and de Haan, G. (2007) A Limited role for p21Cip1/Waf1 in maintaining normal hematopoietic stem cell functioning. Stem Cells, 25, 836-843.
44. Choudhury, A.R., Ju, Z., Djojosubroto, M.W., Schienke, A., Lechel, A., Schaetzlein, S., Jiang, H., Stepczynska, A., Wang, C., Buer, J. et al. (2007) Cdkn1a deletion improves stem cell function and lifespan of mice with dysfunctional telomeres without accelerating cancer formation. Nat. Genet., 39, 99-105.
45. Mukhopadhyay, S.S., Leung, K.S., Hicks, M.J., Hastings, P.J., Youssoufian, H. and Plon, S.E. (2006) Defective mitochondrial peroxiredoxin-3 results in sensitivity to oxidative stress in Fanconi anemia. J. Cell Biol., 175, 225-235.
46. Zhang, X., Shang, X., Guo, F., Murphy, K., Kirby, M., Kelly, P., Reeves, L., Smith, F.O., Williams, D.A., Zheng, Y. et al. (2008) Defective homing is associated with altered Cdc42 activity in cells from patients with Fanconi anemia group A. Blood, 112, 1683-1686.
47. Nie, Y., Han, Y.C. and Zou, Y.R. (2008) CXCR4 is required for the quiescence of primitive hematopoietic cells. J. Exp. Med., 205, 777-783.
48. Wang, Z., Li, G., Tse, W. and Bunting, K.D. (2009) Conditional deletion of STAT5 in adult mouse hematopoietic stem cells causes loss of quiescence and permits efficient non-ablative stem cell replacement. Blood., 113, 4856-4865.
49. Qian, H., Buza-Vidas, N., Hyland, C.D., Jensen, C.T., Antonchuk, J., Mansson, R., Thoren, L.A., Ekblom, M., Alexander, W.S. and Jacobsen, S.E. (2007) Critical role of thrombopoietin in maintaining adult quiescent hematopoietic stem cells. Cell Stem Cell, 1, 671-684.
50. Umemoto, T., Yamato, M., Nishida, K., Yang, J., Tano, Y. and Okano, T. (2005) p57Kip2 is expressed in quiescent mouse bone marrow side population cells. Biochem. Biophys. Res. Commun., 337, 14-21.
51. Yamazaki, S., Iwama, A., Takayanagi, S., Morita, Y., Eto, K., Ema, H. and Nakauchi, H. (2006) Cytokine signals modulated via lipid rafts mimic niche signals and induce hibernation in hematopoietic stem cells. EMBO J., 25, 3515-3523.
52. Skinner, A.M., O'Neill, S.L., Grompe, M. and Kurre, P. (2008) CXCR4 induction in hematopoietic progenitor cells from Fanca(-/-), -c(-/-), and -d2(-/-) mice. Exp. Hematol., 36, 273-282.
53. Okabe, M., Ikawa, M., Kominami, K., Nakanishi, T. and Nishimune, Y. (1997) 'Green mice' as a source of ubiquitous green cells. FEBS Lett., 407, 313-319.