Rho GTPases in hematopoietic cells

Antioxidants and Redox Signaling

Volumn 7, Issue 11-12, 2005, Pages 1440-1455

  Van Hennik, Paula B ^a   Hordijk, Peter L ^a,b  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b SANQUIN RESEARCH   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; PROTEIN CDC42; RAC PROTEIN; RAC1 PROTEIN; RAC2 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; CHEMOTAXIS; CYTOSKELETON; GENE EXPRESSION REGULATION; GENE MUTATION; HEMATOLOGIC DISEASE; HEMATOPOIETIC STEM CELL; HUMAN; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL PHYSIOLOGY; HEMATOPOIETIC SYSTEM; HUMANS; REACTIVE OXYGEN SPECIES; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 28844472010     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2005.7.1440     Document Type: Review

References (149)

1. Abo A, Pick E, Hall A, Totty N, Teahan CG, and Segal AW. Activation of the NADPH oxidase involves the small GTP-binding protein p21rac1. Nature 353: 668-670, 1991.
2. Abramson S, Miller RG, and Phillips RA. The identification in adult bone marrow of pluripotent and restricted stem cells of the myeloid and lymphoid systems. J Exp Med 145: 1567-1579, 1977.
3. Albert MA, Danielson E, Rifai N, and Ridker PM. Effect of statin therapy on C-reactive protein levels: the pravastatin inflammation/CRP evaluation (PRINCE): a randomized trial and cohort study. JAMA 286: 64-70, 2001.
4. Aldrich RA, Steinberg AG, and Campbell DC. Pedigree demonstrating a sex-linked recessive condition characterised by draining ears, eczematoid dermatitis and bloody diarrhea. Pediatrics 13: 133-139, 1954.
5. Ambruso DR, Knall C, Abell AN, Panepinto J, Kurkchubasche A, Thurman G, Gonzalez-Aller C, Hiester A, deBoer M, Harbeck RJ, Oyer R, Johnson GL, and Roos D. Human neutrophil immunodeficiency syndrome is associated with an inhibitory Rac2 mutation. Proc Natl Acad Sci U S A 97: 4654-4659, 2000.
6. Aspenstrom P, Lindberg U, and Hall A. Two GTPases, Cdc42 and Rac, bind directly to a protein implicated in the immunodeficiency disorder Wiskott-Aldrich syndrome. Curr Bio 16: 70-75, 1996.
7. Babior BM, Lambeth JD, and Nauseef W. The neutrophil NADPH oxidase. Arch Biochem Biophys 397: 342-344, 2002.
8. Bandoh T, Sato EF, Mitani H, Nakashima A, Hoshi K, and Inoue M. Antioxidative potential of fluvastatin via the inhibition of nicotinamide adenine dinucleotide phosphate (NADPH) oxidase activity. Biol Pharm Bull 26: 818-822, 2003.
9. Ben Neriah Y, Daley GQ, Mes-Masson AM, Witte ON, and Baltimore D. The chronic myelogenous leukemia-specific P210 protein is the product of the bcr/abl hybrid gene. Science 233: 212-214, 1986.
10. Boettner B and Van Aelst L. The role of Rho GTPases in disease development. Gene 286: 155-174, 2002.
11. Borkhardt A, Bojesen S, Haas OA, Fuchs U, Bartelheimer D, Loncarevic IF, Bohle RM, Harbott J, Repp R, Jaeger U, Viehmann S, Henn T, Korth P, Scharr D, and Lampert F. The human GRAF gene is fused to MLL in a unique t(5;11) (q31;q23) and both alleles are disrupted in three cases of myelodysplastic syndrome/acute myeloid leukemia with a deletion 5q. Proc Natl Acad Sci U S A 97: 9168-9173, 2000.
12. Burns S, Cory GO, Vainchenker W, and Thrasher AJ. Mechanisms of WASp-mediated hematologic and immunologic disease. Blood 104: 3454-3462, 2004.
13. Cantrell D. Lymphocyte signalling: a coordinating role for Vav? Curr Biol 5: R535-R538, 1998.
14. Caron E. Cellular functions of the Rap1 GTP-binding protein: a pattern emerges. J Cell Sci 116: 435-440, 2003.
15. Chapman-Shimshoni D, Yuklea M, Radnay J, Shapiro H, and Lishner M. Simvastatin induces apoptosis of B-CLL cells by activation of mitochondrial caspase 9. Exp Hematol 31: 779-783, 2003.
16. Chen F, Ma L, Parrini MC; Mao X, Lopez M, Wu C, Marks PW, Davidson L, Kwiatkowski DJ, Kirchhausen T, Orkin SH, Rosen FS, Mayer BJ, Kirschner MW, and Alt FW. Cdc42 is required for PIP(2)-induced actin polymerization and early development but not for cell viability. Curr Biol 10: 758-765, 2000.
17. Cherry LK, Li X, Schwab P, Lim B, and Klickstein LB. RhoH is required to maintain the integrin LFA-1 in a non-adhesive state on lymphocytes. Nat Immunol 5: 961-967, 2004.
18. Clark SS, McLaughlin J, Timmons M, Pendergast AM, Ben Neriah Y, Dow LW, Crist W, Rovera G, Smith SD, and Witte ON. Expression of a distinctive BCR-ABL oncogene in Ph1-positive acute lymphocytic leukemia (ALL). Science 239: 775-777, 1988.
19. Corre I, Gomez M, Vielkind S, and Cantrell DA. Analysis of thymocyte development reveals that the GTPase RhoA is a positive regulator of T cell receptor responses in vivo. J Exp Med 194: 903-914, 2001.
20. Croker BA, Tarlinton DM, Cluse LA, Tuxen AJ, Light A, Yang FC, Williams DA, and Roberts AW. The Rac2 guanosine triphosphatase regulates B lymphocyte antigen receptor responses and chemotaxis and is required for establishment of B-1a and marginal zone B lymphocytes. J Immunol 168: 3376-3386, 2002.
21. Delbosc S, Morena M, Djouad F, Ledoucen C, Descomps B, and Cristol JP. Statins, 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors, are able to reduce Superoxide anion production by NADPH oxidase in THP-1-derived monocytes. J Cardiovasc Pharmacol 40: 611-617, 2002.
22. del Pozo MA, Vicente-Manzanares M, Tejedor R, Serrador JM, and Sanchez-Madrid F. Rho GTPases control migration and polarization of adhesion molecules and cytoskeletal ERM components in T lymphocytes. Eur J Immunol 29: 3609-3620, 1999.
23. Dernbach E, Urbich C, Brandes RP, Hofmann WK, Zeiher AM, and Dimmeler S. Antioxidative stress-associated genes in circulating progenitor cells: evidence for enhanced resistance against oxidative stress. Blood 104: 3591-3597, 2004.
24. Derry JM, Ochs HD, and Francke U. Isolation of a novel gene mutated in Wiskott-Aldrich syndrome. Cell 79: following 922, 1994.
25. Devriendt K, Kim AS, Mathijs G, Prints SG, Schwartz M, Van Den Oord JJ, Verhoef GE, Boogaerts MA, Fryns JP, You D, Rosen MK, and Vandenberghe P. Constitutively activating mutation in WASP causes X-linked severe congenital neutropenia. Nat Genet 27: 313-317, 2001.
26. Dimitroulakos J, Nohynek D, Backway KL, Hedley DW, Yeger H, Freedman MH, Minden MD, and Perm LZ. Increased sensitivity of acute myeloid leukemias to lovastatin-induced apoptosis: a potential therapeutic approach. Blood 93: 1308-1318, 1999.
27. Eva A, Vecchio G, Rao CD, Tronick SR, and Aaronson SA. The predicted DBL oncogene product defines a distinct class of transforming proteins. Proc Natl Acad Sci U S A 85: 2061-2065, 1988.
28. Evans CA, Tonge R, Bunco D, Pierce A, Shaw J, Lu Y, Hamzah HG, Gray A, Downes CP, Gaskell SJ, Spooncer E, and Whetton AD. Comparative proteomics of primitive hematopoietic cell populations reveals differences in expression of proteins regulating motility. Blood 103: 3751-3759, 2004.
29. Fenteany G and Glogauer M. Cytoskeletal remodeling in leukocyte function. Curr Opin Hematol 11: 15-24, 2004.
30. Filippi MD, Harris CE, Meiler J, Gu Y, Zheng Y, and Williams DA. Localization of Rac2 via the C terminus and aspartic acid 150 specifies Superoxide generation, actin polarity and chemotaxis in neutrophils. Nat Immunol 5: 744-751, 2004.
31. Fischer KD, Zmuldzinas A, Gardner S, Barbacid M, Bernstein A, and Guidos C. Defective T-cell receptor signalling and positive selection of Vav-deficient CD4+ CD8+ thymocytes. Nature 374: 474-477, 1995.
32. Fujikawa K, Miletic AV, Alt FW, Faccio R, Brown T, Hoog J, Fredericks J, Nishi S, Mildiner S, Moores SL, Brugge J, Rosen FS, and Swat W. Vav1/2/3-null mice define an essential role for Vav family proteins in lymphocyte development and activation but a differential requirement in MAPK signaling in T and B cells. J Exp Med 198: 1595-1608, 2003.
33. Gardiner EM, Pestonjamasp KN, Bohl BP, Chamberlain C, Hahn KM, and Bokoch GM. Spatial and temporal analysis of Rac activation during live neutrophil chemotaxis. Curr Biol 12: 2029-2034, 2002.
34. Glassford J, Holman M, Banerji L, Clayton E, Klaus GG, Turner M, and Lam EW. Vav is required for cyclin D2 induction and proliferation of mouse B lymphocytes activated via the antigen receptor. J Biol Chem 276: 41040-41048, 2001.
35. Gomez M, Tybulewicz V, and Cantrell DA. Control of pre-T cell proliferation and differentiation by the GTPase Rac-I. Nat Immunol 1: 348-352, 2000.
36. Gomez-Mouton C, Lacalle RA, Mira E, Jimenez-Baranda S, Barber DF, Carrera AC, Martinez A, and Manes S. Dynamic redistribution of raft domains as an organizing platform for signaling during cell chemotaxis. J Cell Biol 164: 759-768, 2004.
37. Gu Y, Jia B, Yang FC, D'Souza M, Harris CE, Derrow CW, Zheng Y, and Williams DA. Biochemical and biological characterization of a human Rac2 GTPase mutant associated with phagocytic immunodeficiency. J Biol Chem 276: 15929-15938, 2001.
38. Gu Y, Byrne MC, Paranavitana NC, Aronow B, Siefring JE, D'Souza M, Horton HF, Quilliam LA, and Williams DA. Rac2, a hematopoiesis-specific Rho GTPase, specifically regulates mast cell protease gene expression in bone marrow-derived mast cells. Mol Cell Biol 22: 7645-7657, 2002.
39. Gu Y, Filippi MD, Cancelas JA, Siefring JE, Williams EP, Jasti AC, Harris CE, Lee AW, Prabhakar R, Atkinson SJ, Kwiatkowski DJ, and Williams DA. Hematopoietic cell regulation by Rac1 and Rac2 guanosine triphosphatases. Science 302: 445-449, 2003.
40. Gu Y, Jasti AC, Jansen M, and Siefring JE. RhoH, a hematopoietic-specific Rho GTPase, regulates proliferation, survival, migration, and engraftment of hematopoietic progenitor cells. Blood 105: 1467-1475, 2005.
41. Haddad E, Zugaza JL, Louache F, Debili N, Crouin C, Schwarz K, Fischer A, Vainchenker W, and Bertoglio J. The interaction between Cdc42 and WASP is required for SDF-1-induced T-lymphocyte chemotaxis. Blood 97: 33-38, 2001.
42. Hara H and Ogawa M. Murine hemopoietic colonies in culture containing normoblasts, macrophages, and megakaryocytes. Am J Hematol 4: 23-34, 1978.
43. Harnois T, Constantin B, Rioux A, Grenioux E, Kitzis A, and Bourmeyster N. Differential interaction and activation of Rho family GTPases by p210bcr-abl and p190bcr-abl. Oncogene 22: 6445-6454, 2003.
44. Harrison DE, Astle CM, and Lerner C. Number and continuous proliferative pattern of transplanted primitive immunohematopoietic stem cells. Proc Natl Acad Sci U S A 85: 822-826, 1988.
45. Harrison DE, Astle CM, and Stone M. Numbers and functions of transplantable primitive immunohematopoietic stem cells. Effects of age. J Immunol 142: 3833-3840, 1989.
46. Harrison DE, Stone M, and Astle CM. Effects of transplantation on the primitive immunohematopoietic stem cell. J Exp Med 172: 431-437, 1990.
47. Hart MJ, Eva A, Evans T, Aaronson SA, and Cerione RA. Catalysis of guanine nucleotide exchange on the CDC42Hs protein by the dbl oncogene product. Nature 354: 311-314, 1991.
48. Heisterkamp N, Stam K, Groffen J, de Klein A, and Grosveld G. Structural organization of the bcr gene and its role in the Ph' translocation. Nature 315: 758-761, 1985.
49. Henning SW, Galandrini R, Hall A, and Cantrell DA. The GTPase Rho has a critical regulatory role in thymus development. EMBO J 16: 2397-2407, 1997.
50. Higgs HN and Pollard TD. Activation by Cdc42 and PIP(2) of Wiskott-Aldrich syndrome protein (WASp) stimulates actin nucleation by Arp2/3 complex. J Cell Biol 150: 1311-1320, 2000.
51. Hildebrand JD, Taylor JM, and Parsons JT. An SH3 domain-containing GTPase-activating protein for Rho and Cdc42 associates with focal adhesion kinase. Mol Cell Biol 16: 3169-3178, 1996.
52. Hirose K, Kawashima T, Iwamoto I, Nosaka T, and Kitamura T. MgcRacGAP is involved in cytokinesis through associating with mitotic spindle and midbody. J Biol Chem 276: 5821-5828, 2001.
53. Hodgson GS and Bradley TR. Properties of haematopoietic stem cells surviving 5-fluorouracil treatment: evidence for a pre-CFU-S cell? Nature 281: 381-382, 1979.
54. Ichiba T, Kuraishi Y, Sakai O, Nagata S, Groffen J, Kurata T, Hattori S, and Matsuda M. Enhancement of guanine-nucleotide exchange activity of C3G for Rap1 by the expression of Crk, CrkL, and Grb2. J Biol Chem 272: 22215-22220, 1997.
55. Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER, Sundaresan M, Finkel T, and Goldschmidt-Clermont PJ. Mitogenic signaling mediated by oxidants in Ras-transformed fibroblasts. Science 275: 1649-1652, 1997.
56. Ito K, Hirao A, Arai F, Matsuoka S, Takubo K, Hamaguchi I, Nomiyama K, Hosokawa K, Sakurada K, Nakagata N, Ikeda Y, Mak TW, and Suda T. Regulation of oxidative stress by ATM is required for self-renewal of haematopoietic stem cells. Nature 431: 997-1002, 2004.
57. Jordan CT and Lemischka IR. Clonal and systemic analysis of long-term hematopoiesis in the mouse. Genes Dev 4: 220-232, 1990.
58. Kawakami A, Tanaka A, Nakajima K, Shimokado K, and Yoshida M. Atorvastatin attenuates remnant lipoprotein-induced monocyte adhesion to vascular endothelium under flow conditions. Circ Res 91: 263-271, 2002.
59. Kawashima T, Hirose K, Satoh T, Kaneko A, Ikeda Y, Kaziro Y, Nosaka T, and Kitamura T. MgcRacGAP is involved in the control of growth and differentiation of hematopoietic cells. Blood 96: 2116-2124, 2000.
60. Keller G and Snodgrass R. Life span of multipotential hematopoietic stem cells in vivo. J Exp Med 171: 1407-1418, 1990.
61. Kim AS, Kakalis LT, Abdul-Manan N, Liu GA, and Rosen MK. Autoinhibition and activation mechanisms of the Wiskott-Aldrich syndrome protein. Nature 404: 151-158, 2000.
62. Klinger MB, Guilbault B, and Kay RJ. The RhoA- and CDC42-specific exchange factor Dbs promotes expansion of immature thymocytes and deletion of double-positive and single-positive thymocytes. Eur J Immunol 34: 806-816, 2004.
63. Knatterud GL, Rosenberg Y, Campeau L, Geller NL, Hunninghake DB, Forman SA, Forrester JS, Gobel FL, Herd JA, Hickey A, Hoogwerf BJ, Terrin ML, and White C. Long-term effects on clinical outcomes of aggressive lowering of low-density lipoprotein cholesterol levels and low-dose anticoagulation in the post coronary artery by-pass graft trial. Post CABG Investigators. Circulation 102: 157-165, 2000.
64. Kolluri R, Tolias KF, Carpenter CL, Rosen FS, and Kirchhausen T. Direct interaction of the Wiskott-Aldrich syndrome protein with the GTPase Cdc42. Proc Natl Acad Sci U S A 93: 5615-5618, 1996.
65. Kourlas PJ, Strout MP, Becknell B, Veronese ML, Croce CM, Theil KS, Krahe R, Ruutu T, Knuutila S, Bloomfield CD, and Caligiuri MA. Identification of a gene at 11q23 encoding a guanine nucleotide exchange factor: evidence for its fusion with MLL in acute myeloid leukemia. Proc Natl Acad Sci U S A 97: 2145-2150, 2000.
66. Lacout C, Haddad E, Sabri S, Svinarchouk F, Garcon L, Capron C, Foudi A, Mzali R, Snapper SB, Louache F, Vainchenker W, and Dumenil D. A defect in hematopoietic stem cell migration explains the nonrandom X-chromosome inactivation in carriers of Wiskott-Aldrich syndrome. Blood 102: 1282-1289, 2003.
67. Lambeth JD. NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4: 181-189, 2004.
68. Laufs U, Marra D, Node K, and Liao JK. 3-Hydroxy-3-methylglutaryl-CoA reductase inhibitors attenuate vascular smooth muscle proliferation by preventing rho GTPase-induced down-regulation of p27(Kip1). J Biol Chem 274: 21926-21931, 1999.
69. Leary AG, Hirai Y, Kishimoto T, Clark SC, and Ogawa M. Survival of hemopoietic progenitors in the GO period of the cell cycle does not require early hemopoietic regulators. Proc Natl Acad Sci U S A 86: 4535-4538, 1989.
70. Leary AG, Zeng HQ, Clark SC, and Ogawa M. Growth factor requirements for survival in GO and entry into the cell cycle of primitive human hemopoietic progenitors. Proc Natl Acad Sci U S A 89: 4013-4017, 1992.
71. Li B, Yu H, Zheng W, Voll R, Na S, Roberts AW, Williams DA, Davis RJ, Ghosh S, and Flavell RA. Role of the guanosine triphosphatase Rac2 in T helper 1 cell differentiation. Science 288: 2219-2222, 2000.
72. Li HY, Appelbaum FR, Willman CL, Zager RA, and Banker DE. Cholesterol-modulating agents kill acute myeloid leukemia cells and sensitize them to therapeutics by blocking adaptive cholesterol responses. Blood 101: 3628-3634, 2003.
73. Li S, Yamauchi A, Marchai CC, Molitoris JK, Quilliam LA, and Dinauer MC. Chemoattractant-stimulated Rac activation in wild-type and Rac2-deficient murine neutrophils: preferential activation of Rac2 and Rac2 gene dosage effect on neutrophil functions. J Immunol 169: 5043-5051, 2002.
74. Li X, Bu X, Lu B, Avraham H, Flavell RA, and Lim B. The hematopoiesis-specific GTP-binding protein RhoH is GTPase deficient and modulates activities of other Rho GTPases by an inhibitory function. Mol Cell Biol 22: 1158-1171, 2002.
75. Llevadot J, Murasawa S, Kureishi Y, Uchida S, Masuda H, Kawamoto A, Walsh K, Isner JM, and Asahara T. HMG-CoA reductase inhibitor mobilizes bone marrow-derived endothelial progenitor cells. J Clin Invest 108: 399-405, 2001.
76. Lugo TG, Pendergast AM, Muller AJ, and Witte ON. Tyrosine kinase activity and transformation potency of bcr-abl oncogene products. Science 247: 1079-1082, 1990.
77. McWhirter JR and Wang JY. Activation of tyrosinase kinase and micro filament-binding functions of c-abl by bcr sequences in bcr/abl fusion proteins. Mol Cell Biol 11: 1553-1565, 1991.
78. McWhirter JR and Wang JY. An actin-binding function contributes to transformation by the Bcr-Abl oncoprotein of Philadelphia chromosome-positive human leukemias. EMBO J 12: 1533-1546, 1993.
79. Meagher RC, Salvado AJ, and Wright DG. An analysis of the multilineage production of human hematopoietic progenitors in long-term bone marrow culture: evidence that reactive oxygen intermediates derived from mature phagocytic cells have a role in limiting progenitor cell self-renewal. Blood 12: 273-281, 1988.
80. Michaelson D, Silletti J, Murphy G, D'Eustachio P, Rush M, and Philips MR. Differential localization of Rho GTPases in live cells: regulation by hypervariable regions and RhoGD1 binding. J Cell Biol 152: 111-126, 2001.
81. Minoshima Y, Kawashima T, Hirose K, Tonozuka Y, Kawajiri A, Bao YC, Deng X, Tatsuka M, Narumiya S, May WS Jr, Nosaka T, Semba K, Inoue T, Satoh T, Inagaki M, and Kitamura T. Phosphorylation by Aurora B converts MgcRacGAP to a RhoGAP during cytokinesis. Dev Cell 4: 549-560, 2003.
82. Muller-Tidow C, Kiehl M, Sindermann JR, Probst M, Banger N, Zuhlsdorf M, Chou TC, Berdel WE, Serve H, and Koch OM. Synergistic growth inhibitory effects of interferon-alpha and lovastatin on bcr-abl positive leukemic cells. Int J Oncol 23: 151-158, 2003.
83. Musial J, Undas A, Gajewski P, Jankowski M, Sydor W, and Szczeklik A. Anti-inflammatory effects of simvastatin in subjects with hypercholesterolemia. Int J Cardiol 77: 247-253, 2001.
84. Nakata S, Matsumura I, Tanaka H, Ezoe S, Satoh Y, Ishikawa J, Era T, and Kanakura Y NF-{kappa}B family proteins participate in multiple steps of hematopoiesis through elimination of reactive oxygen species. J Biol Chem 279: 55578-55586, 2004.
85. Newman A, Clutterbuck RD, Powles RL, and Millar JL. Selective inhibition of primary acute myeloid leukaemia cell growth by simvastatin. Leukemia 8: 2023-2029, 1994.
86. Newman A, Clutterbuck RD, DeLord C, Powles RL, Catovsky D, and Millar JL. The sensitivity of leukemic bone marrow to simvastatin is lost at remission: a potential purging agent for autologous bone marrow transplantation. J Investig Med 43: 269-274, 1995.
87. Nijhara R, van Hennik PB, Gignac ML, Kruhlak MJ, Hordijk PL, Delon J, and Shaw S. Rac1 mediates collapse of microvilli on chemokine-activated T lymphocytes. J Immunol 173: 4985-4993, 2004.
88. Nishita M, Aizawa H, and Mizuno K. Stromal cell-derived factor 1alpha activates LIM kinase 1 and induces cofilin phosphorylation for T-cell chemotaxis. Mol Cell Biol 22: 774-783, 2002.
89. Olson MF, Ashworth A, and Hall A. An essential role for Rho, Rac, and Cdc42 GTPases in cell cycle progression through G1. Science 269: 1270-1272, 1995.
90. Olson MF, Paterson HF, and Marshall CJ. Signals from Ras and Rho GTPases interact to regulate expression of p21Waf1/Cip1. Ateure 394: 295-299, 1998.
91. Pasqualucci L, Neumeister P, Goossens T, Nanjangud G, Chaganti RS, Kuppers R, and Dalla-Favera R. Hypermutation of multiple proto-oncogenes in B-cell diffuse large-cell lymphomas. Nature 412: 341-346, 2001.
92. Pedersen TR, Wilhelmsen L, Faergeman O, Strandberg TE, Thorgeirsson G, Troedsson L, Kristianson J, Berg K, Cook TJ, Haghfelt T, Kjekshus J, Miettinen T, Olsson AG, Pyorala K, and Wedel H. Follow-up study of patients randomized in the Scandinavian simvastatin survival study (4S) of cholesterol lowering. Am J Cardiol 86: 257-262, 2000.
93. Preudhomme C, Roumier C, Hildebrand MP, Dallery-Prudhomme E, Lantoine D, Lai JL, Daudignon A, Adenis C, Bauters F, Fenaux P, Kerckaert JP, and Galiegue-Zouitina S. Nonrandom 4p13 rearrangements of the RhoH/TTF gene, encoding a GTP-binding protein, in non-Hodgkin's lymphoma and multiple myeloma. Oncogene 19: 2023-2032, 2000.
94. Puck JM, Siminovitch KA, Poncz M, Greenberg CR. Rottem M, and Conley ME. Atypical presentation of Wiskott-Aldrich syndrome: diagnosis in two unrelated males based on studies of maternal T cell X chromosome inactivation. Blood 75: 2369-2374, 1990.
95. Raftopoulou M and Hall A. Cell migration: Rho GTPases lead the way. Dev Biol 265: 23-32, 2004.
96. Reuther GW, Lambert QT, Booden MA, Wennerberg K, Becknell B, Marcucci G, Sondek J, Caligiuri MA, and Der CJ. Leukemia-associated Rho guanine nucleotide exchange factor, a Dbl family protein found mutated in leukemia, causes transformation by activation of RhoA. J Biol Chem 276: 27145-27151, 2001.
97. Ridley AJ. Rho GTPases and cell migration. J Cell Sci 114: 2713-2722, 2001.
98. Ridley AJ and Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70: 389-399, 1992.
99. Ridley AJ, Paterson HF, Johnston CL, Diekmann D, and Hall A. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70: 401-410, 1992.
100. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, and Horwitz AR. Cell migration: integrating signals from front to back. Science 302: 1704-1709, 2003.
101. Roberts AW, Kim C, Zhen L, Lowe JB, Kapur R, Petryniak B, Spaetti A, Pollock JD, Borneo JB, Bradford GB, Atkinson SJ, Dinauer MC, and Williams DA. Deficiency of the hematopoietic cell-specific Rho family GTPase Rac2 is characterized by abnormalities in neutrophil function and host defense. Immunity 10: 183-196, 1999.
102. Salgia R, Li JL, Ewaniuk DS, Pear W, Pisick E, Burky SA, Ernst T, Sattler M, Chen LB, and Griffin JD. BCR/ABL induces multiple abnormalities of cytoskeletal function. J Clin Invest 100: 46-57, 1997.
103. Sattler M, Winkler T, Verma S, Byrne CH, Shrikhande G, Salgia R, and Griffin JD. Hematopoietic growth factors signal through the formation of reactive oxygen species. Blood 93: 2928-2935, 1999.
104. Sattler M, Verma S, Shrikhande G, Byrne CH, Pride YB, Winkler T, Greenfield EA, Salgia R, and Griffin JD. The BCR/ABL tyrosine kinase induces production of reactive oxygen species in hematopoietic cells. J Biol Chem 275: 24273-24278, 2000.
105. Scalia R, Gooszen ME, Jones SP, Hoffmeyer M, Rimmer DM III, Trocha SD, Huang PL, Smith MB, Lefer AM, and Lefer DJ. Simvastatin exerts both anti-inflammatory and cardioprotective effects in apolipoprotein E-deficient mice. Circulation 103: 2598-2603, 2001.
106. Scheffold C, Schottker B, Lefterova P, Csipai M, Glasmacher A, Huhn D, Neubauer A, and Schmidt-Wolf IG. Increased sensitivity of myeloid leukemia cell lines: potential of lovastatin as bone-marrow-purging agent. Acta Haematol 104: 72-79, 2000.
107. Schror K, Lobel P, and Steinhagen-Thiessen E. Simvastatin reduces platelet thromboxane formation and restores normal platelet sensitivity against prostacyclin in type IIa hypercholesterolemia. Eicosanoids 2: 39-45, 1989.
108. Schwartz GG, Olsson AG, Ezekowitz MD, Ganz P, Oliver MF, Waters D, Zeiher A, Chaitman BR, Leslie S, and Stern T. Effects of atorvastatin on early recurrent ischemic events in acute coronary syndromes: the MIRACL study: a randomized controlled trial. JAMA 285: 1711-1718, 2001.
109. Sini P, Cannas A, Koleske AJ, Di Fiore PP, and Scita G. Abl-dependent tyrosine phosphorylation of Sos-1 mediates growth-factor-induced Rac activation. Nat Cell Biol 6: 268-274, 2004.
110. Sivalenka RR and Jessberger R. SWAP-70 regulates c-kit-induced mast cell activation, cell-cell adhesion, and migration. Mol Cell Biol 24: 10277-10288, 2004.
111. Skorski T, Wlodarski P, Daheron L, Salomoni P, Nieborowska-Skorska M, Majewski M, Wasik M, and Calabretta B. BCR/ABL-mediated leukemogenesis requires the activity of the small GTP-binding protein Rac. Proc Natl Acad Sci U S A 95: 11858-11862, 1998.
112. Skourides PA, Perera SA, and Ren R. Polarized distribution of Bcr-Abl in migrating myeloid cells and co-localization of Bcr-Abl and its target proteins. Oncogene 18: 1165-1176, 1999.
113. Suda T, Suda J, and Ogawa M. Proliferative kinetics and differentiation of murine blast cell colonies in culture: evidence for variable GO periods and constant doubling rates of early pluripotent hemopoietic progenitors. J Cell Physiol 117: 308-318, 1983.
114. Sugihara K, Nakatsuji N, Nakamura K, Nakao K, Hashimoto R, Otani H, Sakagami H, Kondo H, Nozawa S, Aiba A, and Katsuki M. Rac1 is required for the formation of three germ layers during gastrulation. Oncogene 17: 3427-3433, 1998.
115. Sullivan KE, Mullen CA, Blaese RM, and Winkelstein JA. A multiinstitutional survey of the Wiskott-Aldrich syndrome. J Pediatr 125: 876-885, 1994.
116. Symons M and Settleman J. Rho family GTPases: more than simple switches. Trends Cell Biol 10: 415-419, 2000.
117. Symons M, Derry JM, Karlak B, Jiang S, Lemahieu V, McCormick F, Francke U, and Abo A. Wiskott-Aldrich syndrome protein, a novel effector for the GTPase CDC42Hs, is implicated in actin polymerization. Cell 84: 723-734, 1996.
118. Takenawa T and Miki H. WASP and WAVE family proteins: key molecules for rapid rearrangement of cortical actin filaments and cell movement. J Cell Sci 114: 1801-1809, 2001.
119. Tarakhovsky A, Turner M, Schaal S, Mee PJ, Duddy LP, Rajewsky K, and Tybulewicz VL. Defective antigen receptor-mediated proliferation of B and T cells in the absence of Vav. Nature 374: 467-470, 1995.
120. Tedford K, Nitschke L, Girkontaite I, Charlesworth A, Chan G, Sakk V, Barbacid M, and Fischer KD. Compensation between Vav-1 and Vav-2 in B cell development and antigen receptor signaling. Nat Immunol 2: 548-555, 2001.
121. Timokhina I, Kissel H, Stella G, and Besmer P. Kit signaling through PI 3-kinase and Src kinase pathways: an essential role for Rac1 and JNK activation in mast cell proliferation. EMBO J 17: 6250-6262, 1998.
122. van Buul JD, Voermans C, van den Berg V, Anthony EC, Mul FP, van Wetering S, van der School CE, and Hordijk PL. Migration of human hematopoietic progenitor cells across bone marrow endothelium is regulated by vascular endothelial cadherin. J Immunol 168: 588-596, 2002.
123. Van Etten RA, Jackson PK, Baltimore D, Sanders MC, Matsudaira PT, and Janmey PA. The COOH terminus of the c-Abl tyrosine kinase contains distinct F- and G-actin binding domains with bundling activity. J Cell Biol 124: 325-340, 1994.
124. van Hennik PB, ten Klooster JP, Halstead JR, Voermans C, Anthony EC, Divecha N, and Hordijk PL. The C-terminal domain of Rac1 contains two motifs that control targeting and signaling specificity. J Biol Chem 278: 39166-3 9175, 2003.
125. Vasa M, Fichtischerer S, Adler K, Aicher A, Martin H, Zeiher AM, and Dimmeler S. Increase in circulating endothelial progenitor cells by statin therapy in patients with stable coronary artery disease. Circulation 103: 2885-2890, 2001.
126. Vicente-Manzanares M and Sanchez-Madrid F. Role of the cytoskeleton during leukocyte responses. Nat Rev Immunol 4: 110-122, 2004.
127. Villa A, Notarangelo L, Macchi P, Mantuano E, Cavagni G, Brugnoni D, Strina D, Patrosso MC, Ramenghi U, Sacco MG, Ugazio A, and Vezzoni P. X-linked thrombocytopenia and Wiskott-Aldrich syndrome are allelic diseases with mutations in the WASP gene. Nat Genet 9: 414-417, 1995.
128. Walker LC, Ganesan TS, Dhut S, Gibbons B, Lister TA, Rothbard J, and Young BD. Novel chimaeric protein expressed in Philadelphia positive acute lymphoblastic leukaemia. Nature 329: 851-853, 1987.
129. Walmsley MJ, Ooi SK, Reynolds LF, Smith SH, Ruf S, Mathiot A, Vanes L, Williams DA, Cancro MP, and Tybulewicz VL. Critical roles for Rac1 and Rac2 GTPases in B cell development and signaling. Science 302: 459-462, 2003.
130. Walter DH, Rittig K, Bahlmann FH, Kirchmair R, Silver M, Murayama T, Nishimura H, Losordo DW, Asahara T, and Isner JM. Statin therapy accelerates reendothelialization: a novel effect involving mobilization and incorporation of bone marrow-derived endothelial progenitor cells. Circulation 105: 3017-3024, 2002.
131. Wang B, Zou JX, Ek-Rylander B, and Ruoslahti E. R-Ras contains a proline-rich site that binds to SH3 domains and is required for integrin activation by R-Ras. J Biol Chem 275: 5222-5227, 2000.
132. Wells CM, Walmsley M, Ooi S, Tybulewicz V, and Ridley AJ. Rac1-deficient macrophages exhibit defects in cell spreading and membrane ruffling but not migration. J Cell Sci 117: 1259-1268, 2004.
133. Welsh CF, Roovers K, Villanueva J, Liu Y, Schwartz MA, and Assoian RK. Timing of cyclin D1 expression within Gl phase is controlled by Rho. Nat Cell Biol 3: 950-957, 2001.
134. Wengler GS, Notarangelo LD, Berardelli S, Pollonni G, Mella P, Fasth A, Ugazio AG, and Parolini O. High prevalence of nonsense, frame shift, and splice-site mutations in 16 patients with full-blown Wiskott-Aldrich syndrome. Blood 86: 3648-3654, 1995.
135. Werner N, Priller J, Laufs U, Endres M, Bohm M, Dirnagl U, and Nickenig G. Bone marrow-derived progenitor cells modulate vascular reendothelialization and neointimal formation: effect of 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibition. Arterioscler Thromb Vasc Biol 22: 1567-1572, 2002.
136. Weston VJ and Stankovic T. Rac1 and Rac2 GTPases in haematopoiesis. Bioessays 26: 221-224, 2004.
137. Wetzler M, Talpaz M, Van Etten RA, Hirsh-Ginsberg C, Beran M, and Kurzrock R. Subcellular localization of Bcr, Abl, and Bcr-Abl proteins in normal and leukemic cells and correlation of expression with myeloid differentiation. J Clin Invest 92: 1925-1939, 1993.
138. Whetton AD, Lu Y, Pierce A, Carney L, and Spooncer E. Lysophospholipids synergistically promote primitive hematopoietic cell chemotaxis via a mechanism involving Vav 1. Blood 102: 2798-2802, 2003.
139. Williams DA, Tao W, Yang F, Kim C, Gu Y, Mansfield P, Levine JE, Petryniak B, Derrow CW, Harris C, Jia B, Zheng Y, Ambruso DR, Lowe JB, Atkinson SJ, Dihauer MC, and Boxer L. Dominant negative mutation of the hematopoietic-specific Rho GTPase, Rac2, is associated with a human phagocyte immunodeficiency. Blood 96: 1646-1654, 2000.
140. Wiskott A. Familiarer, angeborener Morbus Werlhofii? Monatsschr Kinderheilkd 68: 212-216, 1937.
141. Wong WW, Dimitroulakos J, Minden MD, and Penn LZ. HMG-CoA reductase inhibitors and the malignant cell: the statin family of drugs as triggers of tumor-specific apoptosis. Leukemia 16: 508-519, 2002.
142. Wysoczynski M, Reca R, Ratajczak J, Kucia M, Shirvaikar N, Honczarenko M, Mills M, Wanzeck J, Janowska-Wieczorek A, and Ratajczak MZ. Incorporation of CXCR4 into membrane lipid rafts primes homing-related responses of hematopoietic stem/progenitor cells to an SDF-1 gradient. Blood 105: 40-48, 2005.
143. Xia Z, Tan MM, Wong WW, Dimitroulakos J, Minden MD, and Penn LZ. Blocking protein geranylgeranylation is essential for lovastatin-induced apoptosis of human acute myeloid leukemia cells. Leukemia 15: 1398-1407, 2001.
144. Yamauchi A, Marchal CC, Molitoris J, Pech N, Knaus U, Towe J, Atkinson SJ, and Dinauer MC. Rac GTPase isoform-specific regulation of NADPH oxidase and chemotaxis in murine neutrophils in vivo: role of the C-terminal polybasic domain. J Biol Chem 280: 953-964, 2005.
145. Yang FC, Kapur R, King AJ, Tao W, Kim C, Borneo J, Breese R, Marshall M, Dinauer MC, and Williams DA. Rac2 stimulates Akt activation affecting BAD/Bcl-XL expression while mediating survival and actin function in primary mast cells. Immunity 12: 557-568, 2000.
146. Yang FC, Atkinson SJ, Gu Y, Borneo JB, Roberts AW, Zheng Y, Pennington J, and Williams DA. Rac and Cdc42 GTPases control hematopoietic stem cell shape, adhesion, migration, and mobilization. Proc Natl Acad Sci U S A 98: 5614-5618, 2001.
147. Yoshida M, Sawada T, Ishii H, Gerszten RE, Rosenzweig A, Gimbrone MA Jr, Yasukochi Y, and Numano F. HMG-CoA reductase inhibitor modulates monocyte-endothelial cell interaction under physiological flow conditions in vitro: involvement of Rho GTPase-dependent mechanism. Arterioscler Thromb Vasc Biol 21: 1165-1171, 2001.
148. Zhang R, Alt FW, Davidson L, Orkin SH, and Swat W. Defective signalling through the T- and B-cell antigen receptors in lymphoid cells lacking the vav proto-oncogene. Nature 374: 470-473, 1995.
149. Zinovyeva M, Sveshnikova E, Visser J, and Belyavsky A. Molecular cloning, sequence and expression pattern analysis of the mouse orthologue of the leukemia-associated guanine nucleotide exchange factor. Gene 337: 181-188, 2004.