Lipid raft redistribution and morphological cell polarization are separable processes providing a basis for hematopoietic stem and progenitor cell migration

International Journal of Biochemistry and Cell Biology

Volumn 44, Issue 7, 2012, Pages 1121-1132

  Görgens, André ^a   Beckmann, Julia ^b   Ludwig, Anna Kristin ^a   Möllmann, Michael ^a   Dürig, Jan ^a   Horn, Peter A ^a   Rajendran, Lawrence ^c   Giebel, Bernd ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

CD34; Cell polarity; Hematopoietic stem cells; Homing; Migration

Indexed keywords

ACTIN; FLOTILLIN 1; FLOTILLIN 2; INTERCELLULAR ADHESION MOLECULE 3; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN POLYMERIZATION; ARTICLE; CELL MIGRATION; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOSKELETON; ENZYME ACTIVITY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LIPID RAFT; PROTEIN SYNTHESIS;

ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; CELL POLARITY; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNOBLOTTING; MEMBRANE MICRODOMAINS; MICE; MICE, INBRED NOD; STEM CELLS;

EID: 84861228341     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2012.03.020     Document Type: Article

References (52)

1. A.E. Adams, D.I. Johnson, R.M. Longnecker, B.F. Sloat, and J.R. Pringle CDC42 and CDC43 two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae J Cell Biol 111 1990 131 142
2. 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
3. J. Beckmann, S. Scheitza, P. Wernet, J.C. Fischer, and B. Giebel Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment: identification of asymmetrically segregating proteins Blood 109 2007 5494 5501
4. G. Bug, T. Rossmanith, R. Henschler, L.A. Kunz-Schughart, B. Schroder, and M. Kampfmann Rho family small GTPases control migration of hematopoietic progenitor cells into multicellular spheroids of bone marrow stroma cells J Leukoc Biol 72 2002 837 845
5. M.R. Campanero, P. Sanchez-Mateos, M.A. del Pozo, and F. Sanchez-Madrid ICAM-3 regulates lymphocyte morphology and integrin-mediated T cell interaction with endothelial cell and extracellular matrix ligands J Cell Biol 127 1994 867 878
6. J.F. Casella, M.D. Flanagan, and S. Lin Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change Nature 293 1981 302 305
7. J. Cau, and A. Hall Cdc42 controls the polarity of the actin and microtubule cytoskeletons through two distinct signal transduction pathways J Cell Sci 118 2005 2579 2587
8. T.D. Coates, R.G. Watts, R. Hartman, and T.H. Howard Relationship of F-actin distribution to development of polar shape in human polymorphonuclear neutrophils J Cell Biol 117 1992 765 774
9. M.J. De Brabander, R.M. Van de Veire, F.E. Aerts, M. Borgers, and P.A. Janssen The effects of methyl (5-(2-thienylcarbonyl)-1H-benzimidazol-2-yl) carbamate, (R 17934; NSC 238159), a new synthetic antitumoral drug interfering with microtubules on mammalian cells cultured in vitro Cancer Res 36 1976 905 916
10. S. Etienne-Manneville, and A. Hall Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity Nature 421 2003 753 756
11. N. Foger, R. Marhaba, and M. Zoller Involvement of CD44 in cytoskeleton rearrangement and raft reorganization in T cells J Cell Sci 114 2001 1169 1178
12. A.V. Fonseca, and D. Corbeil The hematopoietic stem cell polarization and migration: a dynamic link between RhoA signaling pathway, microtubule network and ganglioside-based membrane microdomains Commun Integr Biol 4 2011 201 204
13. A.V. Fonseca, D. Freund, M. Bornhauser, and D. Corbeil Polarization and migration of hematopoietic stem and progenitor cells rely on the RhoA/ROCK I pathway and an active reorganization of the microtubule network J Biol Chem 285 2010 31661 31671
14. J.E. Fox, and D.R. Phillips Inhibition of actin polymerization in blood platelets by cytochalasins Nature 292 1981 650 652
15. R.K. Ganju, S.A. Brubaker, J. Meyer, P. Dutt, Y. Yang, and S. Qin The alpha-chemokine, stromal cell-derived factor-1alpha, binds to the transmembrane G-protein-coupled CXCR-4 receptor and activates multiple signal transduction pathways J Biol Chem 273 1998 23169 23175
16. B. Giebel, D. Corbeil, J. Beckmann, J. Hohn, D. Freund, and K. Giesen Segregation of lipid raft markers including CD133 in polarized human hematopoietic stem and progenitor cells Blood 104 2004 2332 2338
17. B. Giebel, and M. Punzel Lineage development of hematopoietic stem and progenitor cells Biol Chem 389 2008 813 824
18. R.D. Goldman The role of three cytoplasmic fibers in BHK-21 cell motility. I. Microtubules and the effects of colchicine J Cell Biol 51 1971 752 762
19. C. Gomez-Mouton, J.L. Abad, E. Mira, R.A. Lacalle, E. Gallardo, and S. Jimenez-Baranda Segregation of leading-edge and uropod components into specific lipid rafts during T cell polarization Proc Natl Acad Sci U S A 98 2001 9642 9647
20. C. Gomez-Mouton, R.A. Lacalle, E. Mira, S. Jimenez-Baranda, D.F. Barber, and A.C. Carrera Dynamic redistribution of raft domains as an organizing platform for signaling during cell chemotaxis J Cell Biol 164 2004 759 768
21. P.A. Horn, and R. Blasczyk Severe combined immunodeficiency-repopulating cell assay may overestimate long-term repopulation ability Stem Cells 25 12 2007 3271 3272
22. P.A. Horn, B.M. Thomasson, B.L. Wood, R.G. Andrews, J.C. Morris, and H.P. Kiem Distinct hematopoietic stem/progenitor cell populations are responsible for repopulating NOD/SCID mice compared with nonhuman primates Blood 102 2003 4329 4335
23. G. Joberty, C. Petersen, L. Gao, and I.G. Macara The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42 Nat Cell Biol 2 2000 531 539
24. A. Johansson, M. Driessens, and P. Aspenstrom The mammalian homologue of the Caenorhabditis elegans polarity protein PAR-6 is a binding partner for the Rho GTPases Cdc42 and Rac1 J Cell Sci 113 Pt 18 2000 3267 3275
25. I. Just, J. Selzer, M. Wilm, C. von Eichel-Streiber, M. Mann, and K. Aktories Glucosylation of Rho proteins by Clostridium difficile toxin B Nature 375 1995 500 503
26. E.P. Kilsdonk, P.G. Yancey, G.W. Stoudt, F.W. Bangerter, W.J. Johnson, and M.C. Phillips Cellular cholesterol efflux mediated by cyclodextrins J Biol Chem 270 1995 17250 17256
27. O. Kollet, A. Spiegel, A. Peled, I. Petit, T. Byk, and R. Hershkoviz Rapid and efficient homing of human CD34(+)CD38(-/low)CXCR4(+) stem and progenitor cells to the bone marrow and spleen of NOD/SCID and NOD/SCID/B2m(null) mice Blood 97 2001 3283 3291
28. M.F. Langhorst, A. Reuter, G. Luxenhofer, E.M. Boneberg, D.F. Legler, and H. Plattner Preformed reggie/flotillin caps: stable priming platforms for macrodomain assembly in T cells FASEB J 20 2006 711 713
29. D.A. Lauffenburger, and A.F. Horwitz Cell migration: a physically integrated molecular process Cell 84 1996 359 369
30. J.A. Le Good, W.H. Ziegler, D.B. Parekh, D.R. Alessi, P. Cohen, and P.J. Parker Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1 Science 281 1998 2042 2045
31. H. Lecoeur, E. Ledru, M.C. Prevost, and M.L. Gougeon Strategies for phenotyping apoptotic peripheral human lymphocytes comparing ISNT annexin-V and 7-AAD cytofluorometric staining methods J Immunol Methods 209 1997 111 123
32. G. Liao, T. Nagasaki, and G.G. Gundersen Low concentrations of nocodazole interfere with fibroblast locomotion without significantly affecting microtubule level: implications for the role of dynamic microtubules in cell locomotion J Cell Sci 108 Pt 11 1995 3473 3483
33. J. Millan, M.C. Montoya, D. Sancho, F. Sanchez-Madrid, and M.A. Alonso Lipid rafts mediate biosynthetic transport to the T lymphocyte uropod subdomain and are necessary for uropod integrity and function Blood 99 2002 978 984
34. H. Nakanishi, K.A. Brewer, and J.H. Exton Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate J Biol Chem 268 1993 13 16
35. V. Niggli, A.V. Meszaros, C. Oppliger, and S. Tornay Impact of cholesterol depletion on shape changes, actin reorganization and signal transduction in neutrophil-like HL-60 cells Exp Cell Res 296 2004 358 368
36. C.D. Nobes, and A. Hall Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia Cell 81 1995 53 62
37. A. Peled, I. Petit, O. Kollet, M. Magid, T. Ponomaryov, and T. Byk Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4 Science 283 1999 845 848
38. I. Petit, P. Goichberg, A. Spiegel, A. Peled, C. Brodie, and R. Seger Atypical PKC-zeta regulates SDF-1-mediated migration and development of human CD34+ progenitor cells J Clin Invest 115 2005 168 176
39. L.M. Pierini, R.J. Eddy, M. Fuortes, S. Seveau, C. Casulo, and F.R. Maxfield Membrane lipid organization is critical for human neutrophil polarization J Biol Chem 278 2003 10831 10841
40. L. Rajendran, J. Beckmann, A. Magenau, E.M. Boneberg, K. Gaus, and A. Viola Flotillins are involved in the polarization of primitive and mature hematopoietic cells PLoS ONE 4 2009 e8290
41. L. Rajendran, M. Masilamani, S. Solomon, R. Tikkanen, C.A. Stuermer, and H. Plattner Asymmetric localization of flotillins/reggies in preassembled platforms confers inherent polarity to hematopoietic cells Proc Natl Acad Sci U S A 100 2003 8241 8246
42. P. Sanchez-Mateos, M.R. Campanero, M.A. del Pozo, and F. Sanchez-Madrid Regulatory role of CD43 leukosialin on integrin-mediated T-cell adhesion to endothelial and extracellular matrix ligands and its polar redistribution to a cellular uropod Blood 86 1995 2228 2239
43. J.M. Serrador, M. Nieto, J.L. Alonso-Lebrero, M.A. del Pozo, J. Calvo, and H. Furthmayr CD43 interacts with moesin and ezrin and regulates its redistribution to the uropods of T lymphocytes at the cell-cell contacts Blood 91 1998 4632 4644
44. S. Seveau, H. Keller, F.R. Maxfield, F. Piller, and L. Halbwachs-Mecarelli Neutrophil polarity and locomotion are associated with surface redistribution of leukosialin (CD43) an antiadhesive membrane molecule Blood 95 2000 2462 2470
45. S. Seveau, S. Lopez, P. Lesavre, J. Guichard, E.M. Cramer, and L. Halbwachs-Mecarelli Leukosialin (CD43, sialophorin) redistribution in uropods of polarized neutrophils is induced by CD43 cross-linking by antibodies, by colchicine or by chemotactic peptides J Cell Sci 110 Pt 13 1997 1465 1475
46. M.R. Siegel, and H.D. Sisler Inhibition of protein synthesis in vitro by cycloheximide Nature 200 1963 675 676
47. S.E. Siegrist, and C.Q. Doe Microtubule-induced cortical cell polarity Genes Dev 21 2007 483 496
48. K. Simons, and M.J. Gerl Revitalizing membrane rafts: new tools and insights Nat Rev Mol Cell Biol 11 2010 688 699
49. J.A. Theriot, and T.J. Mitchison Actin microfilament dynamics in locomoting cells Nature 352 1991 126 131
50. J.M. Vasiliev, I.M. Gelfand, L.V. Domnina, O.Y. Ivanova, S.G. Komm, and L.V. Olshevskaja Effect of colcemid on the locomotory behaviour of fibroblasts J Embryol Exp Morphol 24 1970 625 640
51. A.J. Vila-Coro, J.M. Rodriguez-Frade, A. Martin De Ana, M.C. Moreno-Ortiz, A.C. Martinez, and M. Mellado The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway FASEB J 13 1999 1699 1710
52. J.F. Wang, I.W. Park, and J.E. Groopman Stromal cell-derived factor-1alpha stimulates tyrosine phosphorylation of multiple focal adhesion proteins and induces migration of hematopoietic progenitor cells: roles of phosphoinositide-3 kinase and protein kinase C Blood 95 2000 2505 2513