Molecular mechanisms underlying adhesion and migration of hematopoietic stem cells

References

• Xia L, McDaniel JM, Yago T, Doeden A, McEver RP. Surface fucosylation of human cord blood cells augments binding to P-selectin and E-selectin and enhances engraftment in bone marrow. Blood 2004; 104:3091 - 6; http://dx.doi.org/10.1182/blood-2004-02-0650; PMID: 15280192
   PubMed Web of Science ®Google Scholar
• Mazo IB, Gutierrez-Ramos JC, Frenette PS, Hynes RO, Wagner DD, von Andrian UH. Hematopoietic progenitor cell rolling in bone marrow microvessels: parallel contributions by endothelial selectins and vascular cell adhesion molecule 1. J Exp Med 1998; 188:465 - 74; http://dx.doi.org/10.1084/jem.188.3.465; PMID: 9687524
   PubMed Web of Science ®Google Scholar
• Naiyer AJ, Jo DY, Ahn J, Mohle R, Peichev M, Lam G, et al. Stromal derived factor-1-induced chemokinesis of cord blood CD34(+) cells (long-term culture-initiating cells) through endothelial cells is mediated by E-selectin. Blood 1999; 94:4011 - 9; PMID: 10590044
   PubMed Web of Science ®Google Scholar
• Voermans C, Rood PM, Hordijk PL, Gerritsen WR, van der Schoot CE. Adhesion molecules involved in transendothelial migration of human hematopoietic progenitor cells. Stem Cells 2000; 18:435 - 43; http://dx.doi.org/10.1634/stemcells.18-6-435; PMID: 11072032
   PubMed Web of Science ®Google Scholar
• Frenette PS, Subbarao S, Mazo IB, von Andrian UH, Wagner DD. Endothelial selectins and vascular cell adhesion molecule-1 promote hematopoietic progenitor homing to bone marrow. Proc Natl Acad Sci USA 1998; 95:14423 - 8; http://dx.doi.org/10.1073/pnas.95.24.14423; PMID: 9826716
   PubMed Web of Science ®Google Scholar
• Merzaban JS, Burdick MM, Gadhoum SZ, Dagia NM, Chu JT, Fuhlbrigge RC, et al. Analysis of glycoprotein E-selectin ligands on human and mouse marrow cells enriched for hematopoietic stem/progenitor cells. Blood 2011; 118:1774 - 83; http://dx.doi.org/10.1182/blood-2010-11-320705; PMID: 21659548
   PubMed Web of Science ®Google Scholar
• Dimitroff CJ, Lee JY, Rafii S, Fuhlbrigge RC, Sackstein R. CD44 is a major E-selectin ligand on human hematopoietic progenitor cells. J Cell Biol 2001; 153:1277 - 86; http://dx.doi.org/10.1083/jcb.153.6.1277; PMID: 11402070
   PubMed Web of Science ®Google Scholar
• Vermeulen M, Le Pesteur F, Gagnerault MC, Mary JY, Sainteny F, Lepault F. Role of adhesion molecules in the homing and mobilization of murine hematopoietic stem and progenitor cells. Blood 1998; 92:894 - 900; PMID: 9680357
   PubMed Web of Science ®Google Scholar
• Imai K, Kobayashi M, Wang J, Ohiro Y, Hamada J, Cho Y, et al. Selective transendothelial migration of hematopoietic progenitor cells: a role in homing of progenitor cells. Blood 1999; 93:149 - 56; PMID: 9864156
   PubMed Web of Science ®Google Scholar
• Peled A, Kollet O, Ponomaryov T, Petit I, Franitza S, Grabovsky V, et al. The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34(+) cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice. Blood 2000; 95:3289 - 96; PMID: 10828007
   PubMed Web of Science ®Google Scholar
• Carstanjen D, Gross A, Kosova N, Fichtner I, Salama A. The alpha4beta1 and alpha5beta1 integrins mediate engraftment of granulocyte-colony-stimulating factor-mobilized human hematopoietic progenitor cells. Transfusion 2005; 45:1192 - 200; http://dx.doi.org/10.1111/j.1537-2995.2005.00172.x; PMID: 15987366
   PubMed Web of Science ®Google Scholar
• Wierenga PK, Weersing E, Dontje B, de Haan G, van Os R. Differential role for very late antigen-5 in mobilization and homing of hematopoietic stem cells. Bone Marrow Transplant 2006; 38:789 - 97; http://dx.doi.org/10.1038/sj.bmt.1705534; PMID: 17086206
   PubMed Web of Science ®Google Scholar
• Scott LM, Priestley GV, Papayannopoulou T. Deletion of alpha4 integrins from adult hematopoietic cells reveals roles in homeostasis, regeneration, and homing. Mol Cell Biol 2003; 23:9349 - 60; http://dx.doi.org/10.1128/MCB.23.24.9349-9360.2003; PMID: 14645544
   PubMed Web of Science ®Google Scholar
• Papayannopoulou T, Priestley GV, Nakamoto B, Zafiropoulos V, Scott LM. Molecular pathways in bone marrow homing: dominant role of alpha(4)beta(1) over beta(2)-integrins and selectins. Blood 2001; 98:2403 - 11; http://dx.doi.org/10.1182/blood.V98.8.2403; PMID: 11588037
   PubMed Web of Science ®Google Scholar
• Qian H, Tryggvason K, Jacobsen SE, Ekblom M. Contribution of alpha6 integrins to hematopoietic stem and progenitor cell homing to bone marrow and collaboration with alpha4 integrins. Blood 2006; 107:3503 - 10; http://dx.doi.org/10.1182/blood-2005-10-3932; PMID: 16439681
   PubMed Web of Science ®Google Scholar
• Katayama Y, Hidalgo A, Peired A, Frenette PS. Integrin alpha4beta7 and its counterreceptor MAdCAM-1 contribute to hematopoietic progenitor recruitment into bone marrow following transplantation. Blood 2004; 104:2020 - 6; http://dx.doi.org/10.1182/blood-2003-12-4157; PMID: 15161666
   PubMed Web of Science ®Google Scholar
• Qian H, Georges-Labouesse E, Nystrom A, Domogatskaya A, Tryggvason K, Jacobsen SE, et al. Distinct roles of integrins alpha6 and alpha4 in homing of fetal liver hematopoietic stem and progenitor cells. Blood 2007; 110:2399 - 407; http://dx.doi.org/10.1182/blood-2006-10-051276; PMID: 17586725
   PubMed Web of Science ®Google Scholar
• Bonig H, Priestley GV, Wohlfahrt M, Kiem HP, Papayannopoulou T. Blockade of alpha6-integrin reveals diversity in homing patterns among human, baboon, and murine cells. Stem Cells Dev 2009; 18:839 - 44; http://dx.doi.org/10.1089/scd.2008.0269; PMID: 18842099
   PubMed Web of Science ®Google Scholar
• van Buul JD, Voermans C, van den Berg V, Anthony EC, Mul FP, van Wetering S, et al. Migration of human hematopoietic progenitor cells across bone marrow endothelium is regulated by vascular endothelial cadherin. J Immunol 2002; 168:588 - 96; PMID: 11777950
   PubMed Web of Science ®Google Scholar
• Zhang J, Niu C, Ye L, Huang H, He X, Tong WG, et al. Identification of the haematopoietic stem cell niche and control of the niche size. Nature 2003; 425:836 - 41; http://dx.doi.org/10.1038/nature02041; PMID: 14574412
   PubMed Web of Science ®Google Scholar
• Li P, Zon LI. Resolving the controversy about N-cadherin and hematopoietic stem cells. Cell Stem Cell 2010; 6:199 - 202; http://dx.doi.org/10.1016/j.stem.2010.02.007; PMID: 20207222
   PubMed Web of Science ®Google Scholar
• Haug JS, He XC, Grindley JC, Wunderlich JP, Gaudenz K, Ross JT, et al. N-cadherin expression level distinguishes reserved versus primed states of hematopoietic stem cells. Cell Stem Cell 2008; 2:367 - 79; http://dx.doi.org/10.1016/j.stem.2008.01.017; PMID: 18397756
   PubMed Web of Science ®Google Scholar
• Hosokawa K, Arai F, Yoshihara H, Nakamura Y, Gomei Y, Iwasaki H, et al. Function of oxidative stress in the regulation of hematopoietic stem cell-niche interaction. Biochem Biophys Res Commun 2007; 363:578 - 83; http://dx.doi.org/10.1016/j.bbrc.2007.09.014; PMID: 17897629
   PubMed Web of Science ®Google Scholar
• Hosokawa K, Arai F, Yoshihara H, Iwasaki H, Hembree M, Yin T, et al. Cadherin-based adhesion is a potential target for niche manipulation to protect hematopoietic stem cells in adult bone marrow. Cell Stem Cell 2010; 6:194 - 8; http://dx.doi.org/10.1016/j.stem.2009.04.013; PMID: 20207221
   PubMed Web of Science ®Google Scholar
• Kiel MJ, Radice GL, Morrison SJ. Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. Cell Stem Cell 2007; 1:204 - 17; http://dx.doi.org/10.1016/j.stem.2007.06.001; PMID: 18371351
   PubMed Web of Science ®Google Scholar
• Tashiro K, Tada H, Heilker R, Shirozu M, Nakano T, Honjo T. Signal sequence trap: a cloning strategy for secreted proteins and type I membrane proteins. Science 1993; 261:600 - 3; http://dx.doi.org/10.1126/science.8342023; PMID: 8342023
   PubMed Web of Science ®Google Scholar
• Aiuti A, Webb IJ, Bleul C, Springer T, Gutierrez-Ramos JC. 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 1997; 185:111 - 20; http://dx.doi.org/10.1084/jem.185.1.111; PMID: 8996247
   PubMed Web of Science ®Google Scholar
• Glass TJ, Lund TC, Patrinostro X, Tolar J, Bowman TV, Zon LI, et al. Stromal cell-derived factor-1 and hematopoietic cell homing in an adult zebrafish model of hematopoietic cell transplantation. Blood 2011; 118:766 - 74; http://dx.doi.org/10.1182/blood-2011-01-328476; PMID: 21622651
   PubMed Web of Science ®Google Scholar
• Wright DE, Bowman EP, Wagers AJ, Butcher EC, Weissman IL. Hematopoietic stem cells are uniquely selective in their migratory response to chemokines. J Exp Med 2002; 195:1145 - 54; http://dx.doi.org/10.1084/jem.20011284; PMID: 11994419
   PubMed Web of Science ®Google Scholar
• Liesveld JL, Rosell K, Panoskaltsis N, Belanger T, Harbol A, Abboud CN. Response of human CD34+ cells to CXC, CC, and CX3C chemokines: implications for cell migration and activation. J Hematother Stem Cell Res 2001; 10:643 - 55; http://dx.doi.org/10.1089/152581601753193850; PMID: 11672510
   PubMedGoogle Scholar
• Boehmler AM, Drost A, Jaggy L, Seitz G, Wiesner T, Denzlinger C, et al. The CysLT1 ligand leukotriene D4 supports alpha4beta1- and alpha5beta1-mediated adhesion and proliferation of CD34+ hematopoietic progenitor cells. J Immunol 2009; 182:6789 - 98; http://dx.doi.org/10.4049/jimmunol.0801525; PMID: 19454674
   PubMed Web of Science ®Google Scholar
• Bautz F, Denzlinger C, Kanz L, Mohle R. Chemotaxis and transendothelial migration of CD34(+) hematopoietic progenitor cells induced by the inflammatory mediator leukotriene D4 are mediated by the 7-transmembrane receptor CysLT1. Blood 2001; 97:3433 - 40; http://dx.doi.org/10.1182/blood.V97.11.3433; PMID: 11369634
   PubMed Web of Science ®Google Scholar
• Kim CH, Wu W, Wysoczynski M, Abdel-Latif A, Sunkara M, Morris A, et al. Conditioning for hematopoietic transplantation activates the complement cascade and induces a proteolytic environment in bone marrow: a novel role for bioactive lipids and soluble C5b-C9 as homing factors. Leukemia 2012; 26:106 - 16; http://dx.doi.org/10.1038/leu.2011.185; PMID: 21769103
   PubMed Web of Science ®Google Scholar
• Peled A, Grabovsky V, Habler L, Sandbank J, Arenzana-Seisdedos F, Petit I, et al. The chemokine SDF-1 stimulates integrin-mediated arrest of CD34(+) cells on vascular endothelium under shear flow. J Clin Invest 1999; 104:1199 - 211; http://dx.doi.org/10.1172/JCI7615; PMID: 10545519
   PubMed Web of Science ®Google Scholar
• Ponomaryov T, Peled A, Petit I, Taichman RS, Habler L, Sandbank J, et al. Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest 2000; 106:1331 - 9; http://dx.doi.org/10.1172/JCI10329; PMID: 11104786
   PubMed Web of Science ®Google Scholar
• Maekawa T, Ishii T. Chemokine/receptor dynamics in the regulation of hematopoiesis. Intern Med 2000; 39:90 - 100; http://dx.doi.org/10.2169/internalmedicine.39.90; PMID: 10732823
   PubMed Web of Science ®Google Scholar
• Janowski M. Functional diversity of SDF-1 splicing variants. Cell Adh Migr 2009; 3:243 - 9; http://dx.doi.org/10.4161/cam.3.3.8260; PMID: 19287206
   PubMed Web of Science ®Google Scholar
• Yu L, Cecil J, Peng SB, Schrementi J, Kovacevic S, Paul D, et al. Identification and expression of novel isoforms of human stromal cell-derived factor 1. Gene 2006; 374:174 - 9; http://dx.doi.org/10.1016/j.gene.2006.02.001; PMID: 16626895
   PubMed Web of Science ®Google Scholar
• Pillarisetti K, Gupta SK. Cloning and relative expression analysis of rat stromal cell derived factor-1 (SDF-1)1: SDF-1 alpha mRNA is selectively induced in rat model of myocardial infarction. Inflammation 2001; 25:293 - 300; http://dx.doi.org/10.1023/A:1012808525370; PMID: 11820456
   PubMed Web of Science ®Google Scholar
• Crump MP, Gong JH, Loetscher P, Rajarathnam K, Amara A, Arenzana-Seisdedos F, et al. Solution structure and basis for functional activity of stromal cell-derived factor-1; dissociation of CXCR4 activation from binding and inhibition of HIV-1. EMBO J 1997; 16:6996 - 7007; http://dx.doi.org/10.1093/emboj/16.23.6996; PMID: 9384579
   PubMed Web of Science ®Google Scholar
• Heesen M, Berman MA, Hopken UE, Gerard NP, Dorf ME. Alternate splicing of mouse fusin/CXC chemokine receptor-4: stromal cell-derived factor-1alpha is a ligand for both CXC chemokine receptor-4 isoforms. J Immunol 1997; 158:3561 - 4; PMID: 9103415
   PubMed Web of Science ®Google Scholar
• Loetscher M, Geiser T, O'Reilly T, Zwahlen R, Baggiolini M, Moser B. Cloning of a human seven-transmembrane domain receptor, LESTR, that is highly expressed in leukocytes. J Biol Chem 1994; 269:232 - 7; PMID: 8276799
   PubMed Web of Science ®Google Scholar
• Peled A, Petit I, Kollet O, Magid M, Ponomaryov T, Byk T, et al. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 1999; 283:845 - 8; http://dx.doi.org/10.1126/science.283.5403.845; PMID: 9933168
   PubMed Web of Science ®Google Scholar
• Brenner S, Whiting-Theobald N, Kawai T, Linton GF, Rudikoff AG, Choi U, et al. CXCR4-transgene expression significantly improves marrow engraftment of cultured hematopoietic stem cells. Stem Cells 2004; 22:1128 - 33; http://dx.doi.org/10.1634/stemcells.2003-0196; PMID: 15579633
   PubMed Web of Science ®Google Scholar
• Kahn J, Byk T, Jansson-Sjostrand L, Petit I, Shivtiel S, Nagler A, et al. Overexpression of CXCR4 on human CD34+ progenitors increases their proliferation, migration, and NOD/SCID repopulation. Blood 2004; 103:2942 - 9; http://dx.doi.org/10.1182/blood-2003-07-2607; PMID: 15070669
   PubMed Web of Science ®Google Scholar
• Kollet O, Spiegel A, Peled A, Petit I, Byk T, Hershkoviz R, et al. 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 2001; 97:3283 - 91; http://dx.doi.org/10.1182/blood.V97.10.3283; PMID: 11342460
   PubMed Web of Science ®Google Scholar
• Kollet O, Petit I, Kahn J, Samira S, Dar A, Peled A, et al. Human CD34(+)CXCR4(-) sorted cells harbor intracellular CXCR4, which can be functionally expressed and provide NOD/SCID repopulation. Blood 2002; 100:2778 - 86; http://dx.doi.org/10.1182/blood-2002-02-0564; PMID: 12351385
   PubMed Web of Science ®Google Scholar
• Oberlin E, Amara A, Bachelerie F, Bessia C, Virelizier JL, Arenzana-Seisdedos F, et al. The CXC chemokine SDF-1 is the ligand for LESTR/fusin and prevents infection by T-cell-line-adapted HIV-1. Nature 1996; 382:833 - 5; http://dx.doi.org/10.1038/382833a0; PMID: 8752281
   PubMed Web of Science ®Google Scholar
• Ma Q, Jones D, Borghesani PR, Segal RA, Nagasawa T, Kishimoto T, et al. Impaired B-lymphopoiesis, myelopoiesis, and derailed cerebellar neuron migration in CXCR4- and SDF-1-deficient mice. Proc Natl Acad Sci USA 1998; 95:9448 - 53; http://dx.doi.org/10.1073/pnas.95.16.9448; PMID: 9689100
   PubMed Web of Science ®Google Scholar
• Hattori K, Heissig B, Tashiro K, Honjo T, Tateno M, Shieh JH, et al. Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood 2001; 97:3354 - 60; http://dx.doi.org/10.1182/blood.V97.11.3354; PMID: 11369624
   PubMed Web of Science ®Google Scholar
• Sweeney EA, Priestley GV, Nakamoto B, Collins RG, Beaudet AL, Papayannopoulou T. Mobilization of stem/progenitor cells by sulfated polysaccharides does not require selectin presence. Proc Natl Acad Sci USA 2000; 97:6544 - 9; http://dx.doi.org/10.1073/pnas.97.12.6544; PMID: 10841555
   PubMed Web of Science ®Google Scholar
• Sweeney EA, Lortat-Jacob H, Priestley GV, Nakamoto B, Papayannopoulou T. Sulfated polysaccharides increase plasma levels of SDF-1 in monkeys and mice: involvement in mobilization of stem/progenitor cells. Blood 2002; 99:44 - 51; http://dx.doi.org/10.1182/blood.V99.1.44; PMID: 11756151
   PubMed Web of Science ®Google Scholar
• Broxmeyer HE, Orschell CM, Clapp DW, Hangoc G, Cooper S, Plett PA, et al. Rapid mobilization of murine and human hematopoietic stem and progenitor cells with AMD3100, a CXCR4 antagonist. J Exp Med 2005; 201:1307 - 18; http://dx.doi.org/10.1084/jem.20041385; PMID: 15837815
   PubMed Web of Science ®Google Scholar
• Möhle R, Bautz F, Rafii S, Moore MA, Brugger W, Kanz L. The chemokine receptor CXCR-4 is expressed on CD34+ hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1. Blood 1998; 91:4523 - 30; PMID: 9616148
   PubMed Web of Science ®Google Scholar
• Tarnowski M, Liu R, Wysoczynski M, Ratajczak J, Kucia M, Ratajczak MZ. CXCR7: a new SDF-1-binding receptor in contrast to normal CD34(+) progenitors is functional and is expressed at higher level in human malignant hematopoietic cells. Eur J Haematol 2010; 85:472 - 83; http://dx.doi.org/10.1111/j.1600-0609.2010.01531.x; PMID: 20887389
   PubMed Web of Science ®Google Scholar
• Heissig B, Hattori K, Dias S, Friedrich M, Ferris B, Hackett NR, et al. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand. Cell 2002; 109:625 - 37; http://dx.doi.org/10.1016/S0092-8674(02)00754-7; PMID: 12062105
   PubMed Web of Science ®Google Scholar
• Kollet O, Dar A, Shivtiel S, Kalinkovich A, Lapid K, Sztainberg Y, et al. Osteoclasts degrade endosteal components and promote mobilization of hematopoietic progenitor cells. Nat Med 2006; 12:657 - 64; http://dx.doi.org/10.1038/nm1417; PMID: 16715089
   PubMed Web of Science ®Google Scholar
• McQuibban GA, Butler GS, Gong JH, Bendall L, Power C, Clark-Lewis I, et al. Matrix metalloproteinase activity inactivates the CXC chemokine stromal cell-derived factor-1. J Biol Chem 2001; 276:43503 - 8; http://dx.doi.org/10.1074/jbc.M107736200; PMID: 11571304
   PubMed Web of Science ®Google Scholar
• Cho SY, Xu M, Roboz J, Lu M, Mascarenhas J, Hoffman R. The effect of CXCL12 processing on CD34+ cell migration in myeloproliferative neoplasms. Cancer Res 2010; 70:3402 - 10; http://dx.doi.org/10.1158/0008-5472.CAN-09-3977; PMID: 20388788
   PubMed Web of Science ®Google Scholar
• Marquez-Curtis L, Jalili A, Deiteren K, Shirvaikar N, Lambeir AM, Janowska-Wieczorek A. Carboxypeptidase M expressed by human bone marrow cells cleaves the C-terminal lysine of stromal cell-derived factor-1alpha: another player in hematopoietic stem/progenitor cell mobilization?. Stem Cells 2008; 26:1211 - 20; http://dx.doi.org/10.1634/stemcells.2007-0725; PMID: 18292211
   PubMed Web of Science ®Google Scholar
• Davis DA, Singer KE, De La Luz Sierra M, Narazaki M, Yang F, Fales HM, et al. Identification of carboxypeptidase N as an enzyme responsible for C-terminal cleavage of stromal cell-derived factor-1alpha in the circulation. Blood 2005; 105:4561 - 8; http://dx.doi.org/10.1182/blood-2004-12-4618; PMID: 15718415
   PubMed Web of Science ®Google Scholar
• Skidgel RA, Erdos EG. Cellular carboxypeptidases. Immunol Rev 1998; 161:129 - 41; http://dx.doi.org/10.1111/j.1600-065X.1998.tb01577.x; PMID: 9553770
   PubMed Web of Science ®Google Scholar
• Christopherson KW 2nd, Hangoc G, Broxmeyer HE. Cell surface peptidase CD26/dipeptidylpeptidase IV regulates CXCL12/stromal cell-derived factor-1 alpha-mediated chemotaxis of human cord blood CD34+ progenitor cells. J Immunol 2002; 169:7000 - 8; PMID: 12471135
   PubMed Web of Science ®Google Scholar
• De La Luz Sierra M, Yang F, Narazaki M, Salvucci O, Davis D, Yarchoan R, et al. Differential processing of stromal-derived factor-1alpha and stromal-derived factor-1beta explains functional diversity. Blood 2004; 103:2452 - 9; http://dx.doi.org/10.1182/blood-2003-08-2857; PMID: 14525775
   PubMed Web of Science ®Google Scholar
• Christopherson KW 2nd, Cooper S, Broxmeyer HE. Cell surface peptidase CD26/DPPIV mediates G-CSF mobilization of mouse progenitor cells. Blood 2003; 101:4680 - 6; http://dx.doi.org/10.1182/blood-2002-12-3893; PMID: 12576320
   PubMed Web of Science ®Google Scholar
• Christopherson KW 2nd, Uralil SE, Porecha NK, Zabriskie RC, Kidd SM, Ramin SM. G-CSF- and GM-CSF-induced upregulation of CD26 peptidase downregulates the functional chemotactic response of CD34+CD38- human cord blood hematopoietic cells. Exp Hematol 2006; 34:1060 - 8; http://dx.doi.org/10.1016/j.exphem.2006.03.012; PMID: 16863912
   PubMed Web of Science ®Google Scholar
• Christopherson KW 2nd, Hangoc G, Mantel CR, Broxmeyer HE. Modulation of hematopoietic stem cell homing and engraftment by CD26. Science 2004; 305:1000 - 3; http://dx.doi.org/10.1126/science.1097071; PMID: 15310902
   PubMed Web of Science ®Google Scholar
• Campbell TB, Hangoc G, Liu Y, Pollok K, Broxmeyer HE. Inhibition of CD26 in human cord blood CD34+ cells enhances their engraftment of nonobese diabetic/severe combined immunodeficiency mice. Stem Cells Dev 2007; 16:347 - 54; http://dx.doi.org/10.1089/scd.2007.9995; PMID: 17610364
   PubMed Web of Science ®Google Scholar
• Christopherson KW 2nd, Paganessi LA, Napier S, Porecha NK. CD26 inhibition on CD34+ or lineage- human umbilical cord blood donor hematopoietic stem cells/hematopoietic progenitor cells improves long-term engraftment into NOD/SCID/Beta2null immunodeficient mice. Stem Cells Dev 2007; 16:355 - 60; http://dx.doi.org/10.1089/scd.2007.9996; PMID: 17610365
   PubMed Web of Science ®Google Scholar
• Kawai T, Choi U, Liu PC, Whiting-Theobald NL, Linton GF, Malech HL. Diprotin A infusion into nonobese diabetic/severe combined immunodeficiency mice markedly enhances engraftment of human mobilized CD34+ peripheral blood cells. Stem Cells Dev 2007; 16:361 - 70; http://dx.doi.org/10.1089/scd.2007.9997; PMID: 17610366
   PubMed Web of Science ®Google Scholar
• Broxmeyer HE, Hangoc G, Cooper S, Campbell T, Ito S, Mantel C. AMD3100 and CD26 modulate mobilization, engraftment, and survival of hematopoietic stem and progenitor cells mediated by the SDF-1/CXCL12-CXCR4 axis. Ann N Y Acad Sci 2007; 1106:1 - 19; http://dx.doi.org/10.1196/annals.1392.013; PMID: 17360804
   PubMed Web of Science ®Google Scholar
• Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, et al. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol 2002; 3:687 - 94; http://dx.doi.org/10.1038/ni813; PMID: 12068293
   PubMed Web of Science ®Google Scholar
• Le´vesque JP, Hendy J, Takamatsu Y, Williams B, Winkler IG, Simmons PJ. Mobilization by either cyclophosphamide or granulocyte colony-stimulating factor transforms the bone marrow into a highly proteolytic environment. Exp Hematol 2002; 30:440 - 9; http://dx.doi.org/10.1016/S0301-472X(02)00788-9; PMID: 12031650
   PubMed Web of Science ®Google Scholar
• Hidalgo A, Sanz-Rodriguez F, Rodriguez-Fernandez JL, Albella B, Blaya C, Wright N, et al. Chemokine stromal cell-derived factor-1alpha modulates VLA-4 integrin-dependent adhesion to fibronectin and VCAM-1 on bone marrow hematopoietic progenitor cells. Exp Hematol 2001; 29:345 - 55; http://dx.doi.org/10.1016/S0301-472X(00)00668-8; PMID: 11274763
   PubMed Web of Science ®Google Scholar
• Fuhler GM, Drayer AL, Olthof SG, Schuringa JJ, Coffer PJ, Vellenga E. Reduced activation of protein kinase B, Rac, and F-actin polymerization contributes to an impairment of stromal cell derived factor-1 induced migration of CD34+ cells from patients with myelodysplasia. Blood 2008; 111:359 - 68; http://dx.doi.org/10.1182/blood-2006-11-060632; PMID: 17898317
   PubMed Web of Science ®Google Scholar
• del Pozo MA, Vicente-Manzanares M, Tejedor R, Serrador JM, Sanchez-Madrid F. Rho GTPases control migration and polarization of adhesion molecules and cytoskeletal ERM components in T lymphocytes. Eur J Immunol 1999; 29:3609 - 20; http://dx.doi.org/10.1002/(SICI)1521-4141(199911)29:11<3609::AID-IMMU3609>3.0.CO;2-S; PMID: 10556816
   PubMed Web of Science ®Google Scholar
• Shirvaikar N, Marquez-Curtis LA, Ratajczak MZ, Janowska-Wieczorek A. Hyaluronic acid and thrombin upregulate MT1-MMP through PI3K and Rac-1 signaling and prime the homing-related responses of cord blood hematopoietic stem/progenitor cells. Stem Cells Dev 2011; 20:19 - 30; http://dx.doi.org/10.1089/scd.2010.0118; PMID: 20629539
   PubMed Web of Science ®Google Scholar
• Cancelas JA, Lee AW, Prabhakar R, Stringer KF, Zheng Y, Williams DA. Rac GTPases differentially integrate signals regulating hematopoietic stem cell localization. Nat Med 2005; 11:886 - 91; http://dx.doi.org/10.1038/nm1274; PMID: 16025125
   PubMed Web of Science ®Google Scholar
• Ghiaur G, Lee A, Bailey J, Cancelas JA, Zheng Y, Williams DA. Inhibition of RhoA GTPase activity enhances hematopoietic stem and progenitor cell proliferation and engraftment. Blood 2006; 108:2087 - 94; http://dx.doi.org/10.1182/blood-2006-02-001560; PMID: 16709932
   PubMed Web of Science ®Google Scholar
• Göttig S, Mobest D, Ruster B, Grace B, Winter S, Seifried E, et al. Role of the monomeric GTPase Rho in hematopoietic progenitor cell migration and transplantation. Eur J Immunol 2006; 36:180 - 9; http://dx.doi.org/10.1002/eji.200525607; PMID: 16323242
   PubMed Web of Science ®Google Scholar
• Bug G, Rossmanith T, Henschler R, Kunz-Schughart LA, Schroder B, Kampfmann M, et al. Rho family small GTPases control migration of hematopoietic progenitor cells into multicellular spheroids of bone marrow stroma cells. J Leukoc Biol 2002; 72:837 - 45; PMID: 12377954
   PubMed Web of Science ®Google Scholar
• Henschler R, Piiper A, Bistrian R, Mobest D. SDF-1alpha-induced intracellular calcium transient involves Rho GTPase signalling and is required for migration of hematopoietic progenitor cells. Biochem Biophys Res Commun 2003; 311:1067 - 71; http://dx.doi.org/10.1016/j.bbrc.2003.10.112; PMID: 14623290
   PubMed Web of Science ®Google Scholar
• Sahai E, Marshall CJ. RHO-GTPases and cancer. Nat Rev Cancer 2002; 2:133 - 42; http://dx.doi.org/10.1038/nrc725; PMID: 12635176
   PubMed Web of Science ®Google Scholar
• Gu Y, Jasti AC, Jansen M, Siefring JE. RhoH, a hematopoietic-specific Rho GTPase, regulates proliferation, survival, migration, and engraftment of hematopoietic progenitor cells. Blood 2005; 105:1467 - 75; http://dx.doi.org/10.1182/blood-2004-04-1604; PMID: 15494435
   PubMed Web of Science ®Google Scholar
• Wysoczynski M, Reca R, Ratajczak J, Kucia M, Shirvaikar N, Honczarenko M, et al. Incorporation of CXCR4 into membrane lipid rafts primes homing-related responses of hematopoietic stem/progenitor cells to an SDF-1 gradient. Blood 2005; 105:40 - 8; http://dx.doi.org/10.1182/blood-2004-04-1430; PMID: 15328152
   PubMed Web of Science ®Google Scholar
• Yang FC, Atkinson SJ, Gu Y, Borneo JB, Roberts AW, Zheng Y, et al. Rac and Cdc42 GTPases control hematopoietic stem cell shape, adhesion, migration, and mobilization. Proc Natl Acad Sci USA 2001; 98:5614 - 8; http://dx.doi.org/10.1073/pnas.101546898; PMID: 11320224
   PubMed Web of Science ®Google Scholar
• Sanchez-Aguilera A, Lee YJ, Lo Celso C, Ferraro F, Brumme K, Mondal S, et al. Guanine nucleotide exchange factor Vav1 regulates perivascular homing and bone marrow retention of hematopoietic stem and progenitor cells. Proc Natl Acad Sci USA 2011; 108:9607 - 12; http://dx.doi.org/10.1073/pnas.1102018108; PMID: 21606370
   PubMed Web of Science ®Google Scholar
• Carmona G, Chavakis E, Koehl U, Zeiher AM, Dimmeler S. Activation of Epac stimulates integrin-dependent homing of progenitor cells. Blood 2008; 111:2640 - 6; http://dx.doi.org/10.1182/blood-2007-04-086231; PMID: 18032709
   PubMed Web of Science ®Google Scholar
• Chan JY, Lee-Prudhoe JE, Jorgensen B, Ihrke G, Doyonnas R, Zannettino AC, et al. Relationship between novel isoforms, functionally important domains, and subcellular distribution of CD164/endolyn. J Biol Chem 2001; 276:2139 - 52; http://dx.doi.org/10.1074/jbc.M007965200; PMID: 11027692
   PubMed Web of Science ®Google Scholar
• Zannettino AC, Buhring HJ, Niutta S, Watt SM, Benton MA, Simmons PJ. The sialomucin CD164 (MGC-24v) is an adhesive glycoprotein expressed by human hematopoietic progenitors and bone marrow stromal cells that serves as a potent negative regulator of hematopoiesis. Blood 1998; 92:2613 - 28; PMID: 9763543
   PubMed Web of Science ®Google Scholar
• Forde S, Tye BJ, Newey SE, Roubelakis M, Smythe J, McGuckin CP, et al. Endolyn (CD164) modulates the CXCL12-mediated migration of umbilical cord blood CD133+ cells. Blood 2007; 109:1825 - 33; http://dx.doi.org/10.1182/blood-2006-05-023028; PMID: 17077324
   PubMed Web of Science ®Google Scholar
• Petit I, Goichberg P, Spiegel A, Peled A, Brodie C, Seger R, et al. Atypical PKC-zeta regulates SDF-1-mediated migration and development of human CD34+ progenitor cells. J Clin Invest 2005; 115:168 - 76; PMID: 15630457
   PubMed Web of Science ®Google Scholar
• de la Vega M, Kelvin AA, Dunican DJ, McFarlane C, Burrows JF, Jaworski J, et al. The deubiquitinating enzyme USP17 is essential for GTPase subcellular localization and cell motility. Nat Commun 2011; 2:259; http://dx.doi.org/10.1038/ncomms1243; PMID: 21448158
   PubMed Web of Science ®Google Scholar
• Boucheix C, Benoit P, Frachet P, Billard M, Worthington RE, Gagnon J, et al. Molecular cloning of the CD9 antigen. A new family of cell surface proteins. J Biol Chem 1991; 266:117 - 22; PMID: 1840589
   PubMed Web of Science ®Google Scholar
• Leung KT, Chan KY, Ng PC, Lau TK, Chiu WM, Tsang KS, et al. The tetraspanin CD9 regulates migration, adhesion, and homing of human cord blood CD34+ hematopoietic stem and progenitor cells. Blood 2011; 117:1840 - 50; http://dx.doi.org/10.1182/blood-2010-04-281329; PMID: 21063023
   PubMed Web of Science ®Google Scholar
• Burgering BM, Coffer PJ. Protein kinase B (c-Akt) in phosphatidylinositol-3-OH kinase signal transduction. Nature 1995; 376:599 - 602; http://dx.doi.org/10.1038/376599a0; PMID: 7637810
   PubMed Web of Science ®Google Scholar
• Ganju RK, Brubaker SA, Meyer J, Dutt P, Yang Y, Qin S, et al. 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 1998; 273:23169 - 75; http://dx.doi.org/10.1074/jbc.273.36.23169; PMID: 9722546
   PubMed Web of Science ®Google Scholar
• Basu S, Ray NT, Atkinson SJ, Broxmeyer HE. Protein phosphatase 2A plays an important role in stromal cell-derived factor-1/CXC chemokine ligand 12-mediated migration and adhesion of CD34+ cells. J Immunol 2007; 179:3075 - 85; PMID: 17709522
   PubMed Web of Science ®Google Scholar
• Buitenhuis M, van der Linden E, Ulfman LH, Hofhuis FM, Bierings MB, Coffer PJ. Protein kinase B (PKB/c-akt) regulates homing of hematopoietic progenitors through modulation of their adhesive and migratory properties. Blood 2010; 116:2373 - 84; http://dx.doi.org/10.1182/blood-2009-10-250258; PMID: 20566894
   PubMed Web of Science ®Google Scholar
• Damen JE, Liu L, Rosten P, Humphries RK, Jefferson AB, Majerus PW, et al. The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Proc Natl Acad Sci USA 1996; 93:1689 - 93; http://dx.doi.org/10.1073/pnas.93.4.1689; PMID: 8643691
   PubMed Web of Science ®Google Scholar
• Desponts C, Hazen AL, Paraiso KH, Kerr WG. SHIP deficiency enhances HSC proliferation and survival but compromises homing and repopulation. Blood 2006; 107:4338 - 45; http://dx.doi.org/10.1182/blood-2005-12-5021; PMID: 16467196
   PubMed Web of Science ®Google Scholar
• Maehama T, Dixon JE. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 1998; 273:13375 - 8; http://dx.doi.org/10.1074/jbc.273.22.13375; PMID: 9593664
   PubMed Web of Science ®Google Scholar
• Zhang J, Grindley JC, Yin T, Jayasinghe S, He XC, Ross JT, et al. PTEN maintains haematopoietic stem cells and acts in lineage choice and leukaemia prevention. Nature 2006; 441:518 - 22; http://dx.doi.org/10.1038/nature04747; PMID: 16633340
   PubMed Web of Science ®Google Scholar
• Kharas MG, Okabe R, Ganis JJ, Gozo M, Khandan T, Paktinat M, et al. Constitutively active AKT depletes hematopoietic stem cells and induces leukemia in mice. Blood 2010; 115:1406 - 15; http://dx.doi.org/10.1182/blood-2009-06-229443; PMID: 20008787
   PubMed Web of Science ®Google Scholar
• Roberts MS, Woods AJ, Dale TC, Van Der Sluijs P, Norman JC. Protein kinase B/Akt acts via glycogen synthase kinase 3 to regulate recycling of alpha v beta 3 and alpha 5 beta 1 integrins. Mol Cell Biol 2004; 24:1505 - 15; http://dx.doi.org/10.1128/MCB.24.4.1505-1515.2004; PMID: 14749368
   PubMed Web of Science ®Google Scholar
• Brunstein CG, Barker JN, Weisdorf DJ, Defor TE, McKenna D, Chong SY, et al. Intra-BM injection to enhance engraftment after myeloablative umbilical cord blood transplantation with two partially HLA-matched units. Bone Marrow Transplant 2009; 43:935 - 40; http://dx.doi.org/10.1038/bmt.2008.417; PMID: 19139736
   PubMed Web of Science ®Google Scholar