Robo4 cooperates with Cxcr4 to specify hematopoietic stem cell localization to bone marrow niches

Cell Stem Cell

Volumn 8, Issue 1, 2011, Pages 72-83

  Smith Berdan, Stephanie ^a   Nguyen, Andrew ^a   Hassanein, Deena ^a   Zimmer, Matthew ^a   Ugarte, Fernando ^a   Ciriza, Jesús ^b   Li, Dean ^c   García Ojeda, Marcos E ^b   Hinck, Lindsay ^a   Forsberg, E Camilla ^a  

^a University of California Santa Cruz   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; MESSENGER RNA; PLERIXAFOR; PROTEIN ROBO4; ROUNDABOUT RECEPTOR; STROMAL CELL DERIVED FACTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CELL MIGRATION; CELLULAR DISTRIBUTION; HEMATOPOIETIC STEM CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; STEM CELL MOBILIZATION; UPREGULATION;

ANIMALS; BONE MARROW CELLS; HEMATOPOIETIC STEM CELLS; MICE; MICE, CONGENIC; MICE, INBRED STRAINS; NERVE TISSUE PROTEINS; RECEPTORS, CXCR4; RECEPTORS, IMMUNOLOGIC; SIGNAL TRANSDUCTION; STEM CELL NICHE;

EID: 78650974913     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2010.11.030     Document Type: Article

References (44)

1. A. Aiuti, I.J. Webb, C. Bleul, T. Springer, and J.C. Gutierrez-Ramos The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood J. Exp. Med. 185 1997 111 120
2. H. Bonig, D. Chudziak, G. Priestley, and T. Papayannopoulou Insights into the biology of mobilized hematopoietic stem/progenitor cells through innovative treatment schedules of the CXCR4 antagonist AMD3100 Exp. Hematol. 37 2009 402 415 e1
3. H.E. Broxmeyer, C.M. Orschell, D.W. Clapp, G. Hangoc, S. Cooper, P.A. Plett, W.C. Liles, X. Li, B. Graham-Evans, and T.B. Campbell Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist J. Exp. Med. 201 2005 1307 1318
4. A. Dallol, E. Forgacs, A. Martinez, Y. Sekido, R. Walker, T. Kishida, P. Rabbitts, E.R. Maher, J.D. Minna, and F. Latif Tumour specific promoter region methylation of the human homologue of the Drosophila Roundabout gene DUTT1 (ROBO1) in human cancers Oncogene 21 2002 3020 3028
5. N. Flomenberg, J. DiPersio, and G. Calandra Role of CXCR4 chemokine receptor blockade using AMD3100 for mobilization of autologous hematopoietic progenitor cells Acta Haematol. 114 2005 198 205
6. E.C. Forsberg, and S. Smith-Berdan Parsing the niche code: The molecular mechanisms governing hematopoietic stem cell adhesion and differentiation Haematologica 94 2009 1477 1481
7. E.C. Forsberg, S.S. Prohaska, S. Katzman, G.C. Heffner, J.M. Stuart, and I.L. Weissman Differential expression of novel potential regulators in hematopoietic stem cells PLoS Genet. 1 2005 e28
8. E.C. Forsberg, T. Serwold, S. Kogan, I.L. Weissman, and E. Passegué New evidence supporting megakaryocyte-erythrocyte potential of flk2/flt3+ multipotent hematopoietic progenitors Cell 126 2006 415 426
9. E.C. Forsberg, E. Passegué, S.S. Prohaska, A.J. Wagers, M. Koeva, J.M. Stuart, and I.L. Weissman Molecular signatures of quiescent, mobilized and leukemia-initiating hematopoietic stem cells PLoS ONE 5 2010 e8785
10. A.T. Hooper, J.M. Butler, D.J. Nolan, A. Kranz, K. Iida, M. Kobayashi, H.G. Kopp, K. Shido, I. Petit, and K. Yanger Engraftment and reconstitution of hematopoiesis is dependent on VEGFR2-mediated regeneration of sinusoidal endothelial cells Cell Stem Cell 4 2009 263 274
11. H. Hu Cell-surface heparan sulfate is involved in the repulsive guidance activities of Slit2 protein Nat. Neurosci. 4 2001 695 701
12. L. Huminiecki, M. Gorn, S. Suchting, R. Poulsom, and R. Bicknell Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis Genomics 79 2002 547 552
13. K.G. Johnson, A. Ghose, E. Epstein, J. Lincecum, M.B. O'Connor, and D. Van Vactor Axonal heparan sulfate proteoglycans regulate the distribution and efficiency of the repellent slit during midline axon guidance Curr. Biol. 14 2004 499 504
14. C.A. Jones, N.R. London, H. Chen, K.W. Park, D. Sauvaget, R.A. Stockton, J.D. Wythe, W. Suh, F. Larrieu-Lahargue, and Y.S. Mukouyama Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability Nat. Med. 14 2008 448 453
15. S. Kaur, M.D. Castellone, V.M. Bedell, M. Konar, J.S. Gutkind, and R. Ramchandran Robo4 signaling in endothelial cells implies attraction guidance mechanisms J. Biol. Chem. 281 2006 11347 11356
16. T. Kikuta, C. Shimazaki, E. Ashihara, Y. Sudo, H. Hirai, T. Sumikuma, N. Yamagata, T. Inaba, N. Fujita, T. Kina, and M. Nakagawa Mobilization of hematopoietic primitive and committed progenitor cells into blood in mice by anti-vascular adhesion molecule-1 antibody alone or in combination with granulocyte colony-stimulating factor Exp. Hematol. 28 2000 311 317
17. T. Lapidot Mechanism of human stem cell migration and repopulation of NOD/SCID and B2mnull NOD/SCID mice. The role of SDF-1/CXCR4 interactions Ann. N Y Acad. Sci. 938 2001 83 95
18. J.A. Legg, J.M. Herbert, P. Clissold, and R. Bicknell Slits and Roundabouts in cancer, tumour angiogenesis and endothelial cell migration Angiogenesis 11 2008 13 21
19. W.C. Liles, H.E. Broxmeyer, E. Rodger, B. Wood, K. Hübel, S. Cooper, G. Hangoc, G.J. Bridger, G.W. Henson, G. Calandra, and D.C. Dale Mobilization of hematopoietic progenitor cells in healthy volunteers by AMD3100, a CXCR4 antagonist Blood 102 2003 2728 2730
20. N.R. London, W. Zhu, F.A. Bozza, M.C. Smith, D.M. Greif, L.K. Sorensen, L. Chen, Y. Kaminoh, A.C. Chan, and S.F. Passi Targeting Robo4-dependent Slit signaling to survive the cytokine storm in sepsis and influenza Sci. Transl. Med. 2 2010 ra19
21. R. Marlow, P. Strickland, J.S. Lee, X. Wu, M. Pebenito, M. Binnewies, E.K. Le, A. Moran, H. Macias, and R.D. Cardiff SLITs suppress tumor growth in vivo by silencing Sdf1/Cxcr4 within breast epithelium Cancer Res. 68 2008 7819 7827
22. R. Marlow, M. Binnewies, L.K. Sorensen, S.D. Monica, P. Strickland, E.C. Forsberg, D.Y. Li, and L. Hinck Vascular Robo4 restricts proangiogenic VEGF signaling in breast Proc. Natl. Acad. Sci. USA 107 2010 10520 10525
23. S.J. Morrison, D.E. Wright, and I.L. Weissman Cyclophosphamide/ granulocyte colony-stimulating factor induces hematopoietic stem cells to proliferate prior to mobilization Proc. Natl. Acad. Sci. USA 94 1997 1908 1913
24. T. Nagasawa, S. Hirota, K. Tachibana, N. Takakura, S. Nishikawa, Y. Kitamura, N. Yoshida, H. Kikutani, and T. Kishimoto Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1 Nature 382 1996 635 638
25. Y. Nie, Y.C. Han, and Y.R. Zou CXCR4 is required for the quiescence of primitive hematopoietic cells J. Exp. Med. 205 2008 777 783
26. A.G. Ooi, H. Karsunky, R. Majeti, S. Butz, D. Vestweber, T. Ishida, T. Quertermous, I.L. Weissman, and E.C. Forsberg The adhesion molecule esam1 is a novel hematopoietic stem cell marker Stem Cells 27 2009 653 661
27. K.W. Park, C.M. Morrison, L.K. Sorensen, C.A. Jones, Y. Rao, C.B. Chien, J.Y. Wu, L.D. Urness, and D.Y. Li Robo4 is a vascular-specific receptor that inhibits endothelial migration Dev. Biol. 261 2003 251 267
28. E. Passegué, E.F. Wagner, and I.L. Weissman JunB deficiency leads to a myeloproliferative disorder arising from hematopoietic stem cells Cell 119 2004 431 443
29. E. Passegué, A.J. Wagers, S. Giuriato, W.C. Anderson, and I.L. Weissman Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates J. Exp. Med. 202 2005 1599 1611
30. A. Peled, I. Petit, O. Kollet, M. Magid, T. Ponomaryov, T. Byk, A. Nagler, H. Ben-Hur, A. Many, and L. Shultz Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4 Science 283 1999 845 848
31. A. Prasad, Z. Qamri, J. Wu, and R.K. Ganju Slit-2/Robo-1 modulates the CXCL12/CXCR4-induced chemotaxis of T cells J. Leukoc. Biol. 82 2007 465 476
32. E.A. Ross, S. Freeman, Y. Zhao, T.S. Dhanjal, E.J. Ross, S. Lax, Z. Ahmed, T.Z. Hou, N. Kalia, and S. Egginton A novel role for PECAM-1 (CD31) in regulating haematopoietic progenitor cell compartmentalization between the peripheral blood and bone marrow PLoS ONE 3 2008 e2338
33. Y. Sasaki, Y. Matsuoka, M. Hase, T. Toyohara, M. Murakami, M. Takahashi, R. Nakatsuka, Y. Uemura, and Y. Sonoda Marginal expression of CXCR4 on c-kit(+)Sca-1 (+)Lineage (-) hematopoietic stem/progenitor cells Int. J. Hematol. 90 2009 553 560
34. P. Seth, Y. Lin, J. Hanai, V. Shivalingappa, M.P. Duyao, and V.P. Sukhatme Magic roundabout, a tumor endothelial marker: Expression and signaling Biochem. Biophys. Res. Commun. 332 2005 533 541
35. H. Sheldon, M. Andre, J.A. Legg, P. Heal, J.M. Herbert, R. Sainson, A.S. Sharma, J.K. Kitajewski, V.L. Heath, and R. Bicknell Active involvement of Robo1 and Robo4 in filopodia formation and endothelial cell motility mediated via WASP and other actin nucleation-promoting factors FASEB J. 23 2009 513 522
36. F. Shibata, Y. Goto-Koshino, Y. Morikawa, T. Komori, M. Ito, Y. Fukuchi, J.P. Houchins, M. Tsang, D.Y. Li, T. Kitamura, and H. Nakajima Roundabout 4 is expressed on hematopoietic stem cells and potentially involved in the niche-mediated regulation of the side population phenotype Stem Cells 27 2009 183 190
37. P. Steigemann, A. Molitor, S. Fellert, H. Jäckle, and G. Vorbrüggen Heparan sulfate proteoglycan syndecan promotes axonal and myotube guidance by slit/robo signaling Curr. Biol. 14 2004 225 230
38. S. Suchting, P. Heal, K. Tahtis, L.M. Stewart, and R. Bicknell Soluble Robo4 receptor inhibits in vivo angiogenesis and endothelial cell migration FASEB J. 19 2005 121 123
39. T. Sugiyama, H. Kohara, M. Noda, and T. Nagasawa Maintenance of the hematopoietic stem cell pool by CXCL12-CXCR4 chemokine signaling in bone marrow stromal cell niches Immunity 25 2006 977 988
40. S.M. Watt, and S.P. Forde The central role of the chemokine receptor, CXCR4, in haemopoietic stem cell transplantation: Will CXCR4 antagonists contribute to the treatment of blood disorders? Vox Sang. 94 2008 18 32
41. D.E. Wright, S.H. Cheshier, A.J. Wagers, T.D. Randall, J.L. Christensen, and I.L. Weissman Cyclophosphamide/granulocyte colony-stimulating factor causes selective mobilization of bone marrow hematopoietic stem cells into the blood after M phase of the cell cycle Blood 97 2001 2278 2285
42. D.E. Wright, E.P. Bowman, A.J. Wagers, E.C. Butcher, and I.L. Weissman Hematopoietic stem cells are uniquely selective in their migratory response to chemokines J. Exp. Med. 195 2002 1145 1154
43. J.Y. Wu, L. Feng, H.T. Park, N. Havlioglu, L. Wen, H. Tang, K.B. Bacon, Zh Jiang, Xc Zhang, and Y. Rao The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors Nature 410 2001 948 952
44. Y.R. Zou, A.H. Kottmann, M. Kuroda, I. Taniuchi, and D.R. Littman Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development Nature 393 1998 595 599