Hematogenous Metastasis: Roles of CD44v and Alternative Sialofucosylated Selectin Ligands

Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 705)

Abstract

P-selectin, expressed on activated endothelial cells and platelets, is a transmembrane glycoprotein (GP) that mediates, among others, host cell–tumor cell adhesion relevant to the process of hematogenous metastasis. The most compelling evidence for a direct role of P-selectin in the metastatic process is the pronounced inhibition of metastasis in P-selectin-deficient mice compared to wild-type controls in a colon carcinoma cell model [1–3]. Along these lines, enzymatic removal of P-selectin ligands from the colon carcinoma cell surface results in a pronounced reduction of experimental metastasis [1]. Although molecules that bind P-selectin have previously been identified in tumor cell lines [4–6], their functional roles and biological significance have not been substantiated. As has been appropriately argued in the literature [7], distinctions must be made between molecules that can bind to P-selectin under static conditions in vitro, and functional ligands that do interact with P-selectin under fluid dynamic conditions in vivo. By identifying the functional P-selectin ligand(s) on colon carcinoma cells, using an integrated approach consisting of bioengineering tools and contemporary biochemistry and molecular biology techniques, we provide guidelines for engineering novel therapeutic agents that selectively block tumor cell ligand binding function and thus interfere with metastatic spread. Such a strategy may offer specific antimetastatic efficacy without impairing other important P-selectin-mediated physiological processes [8, 9]. Alternatively, these molecules could be utilized in a targeted drug-delivery approach, which would aim at selectively or preferentially eradicating colon carcinoma cells from the vasculature.

Keywords

Metastasis Colon carcinoma cells Selectin CD44 Shear flow 

References

  1. 1.
    Borsig L, Wong R, Feramisco J, Nadeau DR, Varki NM, Varki A (2001) Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis. Proc Natl Acad Sci USA 98:3352–3357PubMedCrossRefGoogle Scholar
  2. 2.
    Borsig L, Wong R, Hynes RO, Varki NM, Varki A (2002) Synergistic effects of L- and P-selectin in facilitating tumor metastasis can involve non-mucin ligands and implicate leukocytes as enhancers of metastasis. Proc Natl Acad Sci USA 99:2193–2198PubMedCrossRefGoogle Scholar
  3. 3.
    Kim YJ, Borsig L, Varki NM, Varki A (1998) P-selectin deficiency attenuates tumor growth and metastasis. Proc Natl Acad Sci USA 95:9325–9330PubMedCrossRefGoogle Scholar
  4. 4.
    Kaytes PS, Geng JG (1998) P-selectin mediates adhesion of the human melanoma cell line NKI-4: identification of glycoprotein ligands. Biochemistry 37:10514–10521PubMedCrossRefGoogle Scholar
  5. 5.
    Kim YJ, Borsig L, Han HL, Varki NM, Varki A (1999) Distinct selectin ligands on colon carcinoma mucins can mediate pathological interactions among platelets, leukocytes, and endothelium. Am J Pathol 155:461–472PubMedCrossRefGoogle Scholar
  6. 6.
    Li L, Short HJ, Qian KX, Elhammer AP, Geng JG (2001) Characterization of glycoprotein ligands for P-selectin on a human small cell lung cancer cell line NCI-H345. Biochem Biophys Res Commun 288:637–644PubMedCrossRefGoogle Scholar
  7. 7.
    Varki A (1997) Selectin ligands: will the real ones please stand up? J Clin Invest 100:S31–S35PubMedGoogle Scholar
  8. 8.
    Konstantopoulos K, Neelamegham S, Burns AR, Kansas GS, Snapp KR, Berg E, Hellums JD, Smith CW, McIntire LV, Simon SI (1998) Venous levels of shear induce neutrophil–platelet adhesion and neutrophil aggregation mediated by P-selectin and β2-integrins. Circulation 98:873–882PubMedGoogle Scholar
  9. 9.
    Lowe JB, Ward PA (1997) Therapeutic inhibition of carbohydrate–protein interactions in vivo. J Clin Invest 99:822–826PubMedCrossRefGoogle Scholar
  10. 10.
    Kansas GS (1996) Selectins and their ligands: current concepts and controversies. Blood 88:3259–3287PubMedGoogle Scholar
  11. 11.
    McEver RP (2002) Selectins: lectins that initiate cell adhesion under flow. Curr Opin Cell Biol 14:581–586PubMedCrossRefGoogle Scholar
  12. 12.
    Guyer DA, Moore KL, Lynam EB, Schammel CMG, Rogelj S, McEver RP, Sklar LA (1996) P-selectin glycoprotein ligand-1 is a ligand for L-selectin in neutrophil aggregation. Blood 88:2415–2421PubMedGoogle Scholar
  13. 13.
    Hanley WD, Wirtz D, Konstantopoulos K (2004) Distinct kinetic and mechanical properties govern selectin–leukocyte interactions. J Cell Sci 117:2503–2511PubMedCrossRefGoogle Scholar
  14. 14.
    Sperandio M, Smith ML, Forlow SB, Olson TS, Xia L, McEver RP, Ley K (2003) P-selectin glycoprotein ligand-1 mediates L-selectin-dependent leukocyte rolling in venules. J Exp Med 197:1355–1363PubMedCrossRefGoogle Scholar
  15. 15.
    Walcheck B, Moore KL, McEver RP, Kishimoto TK (1996) Neutrophil–neutrophil interactions under hydrodynamic shear stress involve L-selectin and PSGL-1. A mechanism that amplifies initial leukocyte accumulation on P-selectin in vitro. J Clin Invest 98:1081–1087PubMedCrossRefGoogle Scholar
  16. 16.
    Jadhav S, Bochner BS, Konstantopoulos K (2001) Hydrodynamic shear regulates the kinetics and receptor specificity of polymorphonuclear leukocyte – colon carcinoma cell adhesive interactions. J Immunol 167:5986–5993PubMedGoogle Scholar
  17. 17.
    Jadhav S, Konstantopoulos K (2002) Fluid shear- and time-dependent modulation of molecular interactions between polymorphonuclear leukocytes and colon carcinomas. Am J Physiol Cell Physiol 283:C1133–C1143PubMedGoogle Scholar
  18. 18.
    Mannori G, Crottet P, Cecconi O, Hanasaki K, Aruffo A, Nelson RM, Varki A, Bevilacqua MP (1995) Differential colon cancer cell adhesion to E-, P-, and L-selectin: role of mucin-type glycoproteins. Cancer Res 55:4425–4431PubMedGoogle Scholar
  19. 19.
    Cotran RS, Gimbrone MA Jr, Bevilacqua MP, Mendrick DL, Pober JS (1986) Induction and detection of a human endothelial activation antigen in vivo. J Exp Med 164:661–666PubMedCrossRefGoogle Scholar
  20. 20.
    Yao L, Pan J, Setiadi H, Patel KD, McEver RP (1996) Interleukin 4 or oncostatin M induces a prolonged increase in P-selectin mRNA and protein in human endothelial cells. J Exp Med 184:81–92PubMedCrossRefGoogle Scholar
  21. 21.
    Lenter M, Levinovitz A, Isenmann S, Vestweber D (1994) Monospecific and common glycoprotein ligands for E- and P-selectin on myeloid cells. J Cell Biol 125:471–481PubMedCrossRefGoogle Scholar
  22. 22.
    Burdick MM, McCaffery JM, Kim YS, Bochner BS, Konstantopoulos K (2003) Colon carcinoma cell glycolipids, integrins, and other glycoproteins mediate adhesion to HUVECs under flow. Am J Physiol Cell Physiol 284:C977–C987PubMedGoogle Scholar
  23. 23.
    McCarty OJT, Jadhav S, Burdick MM, Bell WR, Konstantopoulos K (2002) Fluid shear regulates the kinetics and molecular mechanisms of activation-dependent platelet binding to colon carcinoma cells. Biophys J 83:836–848PubMedCrossRefGoogle Scholar
  24. 24.
    McCarty OJT, Mousa SA, Bray PF, Konstantopoulos K (2000) Immobilized platelets support human colon carcinoma cell tethering, rolling and firm adhesion under dynamic flow conditions. Blood 96:1789–1797PubMedGoogle Scholar
  25. 25.
    Stone JP, Wagner DD (1993) P-selectin mediates adhesion of platelets to neuroblastoma and small cell lung cancer. J Clin Invest 92:804–813PubMedCrossRefGoogle Scholar
  26. 26.
    Romo GM, Dong JF, Schade AJ, Gardiner EE, Kansas GS, Li CQ, McIntire LV, Berndt MC, Lopez JA (1999) The glycoprotein Ib-IX-V complex is a platelet counterreceptor for P-selectin. J Exp Med 190:803–814PubMedCrossRefGoogle Scholar
  27. 27.
    Diacovo TG, Puri KD, Warnock RA, Springer TA, von Andrian UH (1996) Platelet-mediated lymphocyte delivery to high endothelial venules. Science 273:252–255PubMedCrossRefGoogle Scholar
  28. 28.
    Jadhav S, Eggleton CD, Konstantopoulos K (2007) Mathematical modeling of cell adhesion in shear flow pertinent to inflammation and cancer metastasis. Curr Pharm Des 13:1511–1526PubMedCrossRefGoogle Scholar
  29. 29.
    Malhotra R, Taylor NR, Bird MI (1996) Anionic phospholipids bind to L-selectin (but not E-selectin) at a site distinct from the carbohydrate-binding site. Biochem J 314:297–303PubMedGoogle Scholar
  30. 30.
    Moore KL, Stults NL, Diaz S, Smith DF, Cummings RD, Varki A, McEver RP (1992) Identification of a specific glycoprotein ligand for P-selectin (CD62) on myeloid cells. J Cell Biol 118:445–456PubMedCrossRefGoogle Scholar
  31. 31.
    Sako D, Chang XJ, Barone KM, Vachino G, White HM, Shaw G, Veldman GM, Bean KM, Ahern TJ, Furie B et al (1993) Expression cloning of a functional glycoprotein ligand for P-selectin. Cell 75:1179–1186PubMedCrossRefGoogle Scholar
  32. 32.
    McEver RP, Cummings RD (1997) Role of PSGL-1 binding to selectins in leukocyte recruitment. J Clin Invest 100:S97–S103PubMedCrossRefGoogle Scholar
  33. 33.
    Frenette PS, Denis CV, Weiss L, Jurk K, Subbarao S, Kehrel B, Hartwig JH, Vestweber D, Wagner DD (2000) P-Selectin glycoprotein ligand 1 (PSGL-1) is expressed on platelets and can mediate platelet–endothelial interactions in vivo. J Exp Med 191:1413–1422PubMedCrossRefGoogle Scholar
  34. 34.
    Leppanen A, Mehta P, Ouyang YB, Ju T, Helin J, Moore KL, van Die I, Canfield WM, McEver RP, Cummings RD (1999) A novel glycosulfopeptide binds to P-selectin and inhibits leukocyte adhesion to P-selectin. J Biol Chem 274:24838–24848PubMedCrossRefGoogle Scholar
  35. 35.
    Patel KD, Moore KL, Nollert MU, McEver RP (1995) Neutrophils use both shared and distinct mechanisms to adhere to selectins under static and flow conditions. J Clin Invest 96:1887–1896PubMedCrossRefGoogle Scholar
  36. 36.
    Afshar-Kharghan V, Diz-Kucukkaya R, Ludwig EH, Marian AJ, Lopez JA (2001) Human polymorphism of P-selectin glycoprotein ligand 1 attributable to variable numbers of tandem decameric repeats in the mucin like region. Blood 97:3306–3307PubMedCrossRefGoogle Scholar
  37. 37.
    Aigner S, Ramos CL, Hafezi-Moghadam A, Lawrence MB, Friederichs J, Altevogt P, Ley K (1998) CD24 mediates rolling of breast carcinoma cells on P-selectin. FASEB J 12:1241–1251PubMedGoogle Scholar
  38. 38.
    Aigner S, Sthoeger ZM, Fogel M, Weber E, Zarn J, Ruppert M, Zeller Y, Vestweber D, Stahel R, Sammar M, Altevogt P (1997) CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood 89:3385–3395PubMedGoogle Scholar
  39. 39.
    Friederichs J, Zeller Y, Hafezi-Moghadam A, Grone HJ, Ley K, Altevogt P (2000) The CD24/P-selectin binding pathway initiates lung arrest of human A125 adenocarcinoma cells. Cancer Res 60:6714–6722PubMedGoogle Scholar
  40. 40.
    Koenig A, Norgard-Sumnicht K, Linhardt R, Varki A (1998) Differential interactions of heparin and heparan sulfate glycosaminoglycans with the selectins. Implications for the use of unfractionated and low molecular weight heparins as therapeutic agents. J Clin Invest 101:877–889PubMedCrossRefGoogle Scholar
  41. 41.
    Needham LK, Schnaar RL (1993) The HNK-1 reactive sulfoglucuronyl glycolipids are ligands for L-selectin and P-selectin but not E-selectin. Proc Natl Acad Sci USA 90:1359–1363PubMedCrossRefGoogle Scholar
  42. 42.
    Gasic GJ, Gasic TB, Stewart CC (1968) Antimetastatic effects associated with platelet reduction. Proc Natl Acad Sci USA 61:46–52PubMedCrossRefGoogle Scholar
  43. 43.
    Martin TA, Harrison G, Mansel RE, Jiang WG (2003) The role of the CD44/ezrin complex in cancer metastasis. Crit Rev Oncol Hematol 46:165–186PubMedCrossRefGoogle Scholar
  44. 44.
    Ponta H, Wainwright D, Herrlich P (1998) The CD44 protein family. Int J Biochem Cell Biol 30:299–305PubMedCrossRefGoogle Scholar
  45. 45.
    Ponta H, Sherman L, Herrlich PA (2003) CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 4:33–45PubMedCrossRefGoogle Scholar
  46. 46.
    Borland G, Ross JA, Guy K (1998) Forms and functions of CD44. Immunology 93:139–148PubMedCrossRefGoogle Scholar
  47. 47.
    Peach RJ, Hollenbaugh D, Stamenkovic I, Aruffo A (1993) Identification of hyaluronic acid binding sites in the extracellular domain of CD44. J Cell Biol 122:257–264PubMedCrossRefGoogle Scholar
  48. 48.
    Culty M, Miyake K, Kincade PW, Sikorski E, Butcher EC, Underhill C (1990) The hyaluronate receptor is a member of the CD44 (H-CAM) family of cell surface glycoproteins. J Cell Biol 111:2765–2774PubMedCrossRefGoogle Scholar
  49. 49.
    Jalkanen S, Jalkanen M (1992) Lymphocyte CD44 binds the COOH-terminal heparin-binding domain of fibronectin. J Cell Biol 116:817–825PubMedCrossRefGoogle Scholar
  50. 50.
    Harada N, Mizoi T, Kinouchi M, Hoshi K, Ishii S, Shiiba K, Sasaki I, Matsuno S (2001) Introduction of antisense CD44S CDNA down-regulates expression of overall CD44 isoforms and inhibits tumor growth and metastasis in highly metastatic colon carcinoma cells. Int J Cancer 91:67–75PubMedCrossRefGoogle Scholar
  51. 51.
    Labarriere N, Piau JP, Otry C, Denis M, Lustenberger P, Meflah K, Le Pendu J (1994) H blood group antigen carried by CD44V modulates tumorigenicity of rat colon carcinoma cells. Cancer Res 54:6275–6281PubMedGoogle Scholar
  52. 52.
    Reeder JA, Gotley DC, Walsh MD, Fawcett J, Antalis TM (1998) Expression of antisense CD44 variant 6 inhibits colorectal tumor metastasis and tumor growth in a wound environment. Cancer Res 58:3719–3726PubMedGoogle Scholar
  53. 53.
    Wielenga VJ, Heider KH, Offerhaus GJ, Adolf GR, van den Berg FM, Ponta H, Herrlich P, Pals ST (1993) Expression of CD44 variant proteins in human colorectal cancer is related to tumor progression. Cancer Res 53:4754–4756PubMedGoogle Scholar
  54. 54.
    Kim H, Yang XL, Rosada C, Hamilton SR, August JT (1994) CD44 expression in colorectal adenomas is an early event occurring prior to K-ras and p53 gene mutation. Arch Biochem Biophys 310:504–507PubMedCrossRefGoogle Scholar
  55. 55.
    Wielenga VJ, Smits R, Korinek V, Smit L, Kielman M, Fodde R, Clevers H, Pals ST (1999) Expression of CD44 in Apc and Tcf mutant mice implies regulation by the WNT pathway. Am J Pathol 154:515–523PubMedCrossRefGoogle Scholar
  56. 56.
    Kim HR, Wheeler MA, Wilson CM, Iida J, Eng D, Simpson MA, McCarthy JB, Bullard KM (2004) Hyaluronan facilitates invasion of colon carcinoma cells in vitro via interaction with CD44. Cancer Res 64:4569–4576PubMedCrossRefGoogle Scholar
  57. 57.
    Ropponen K, Tammi M, Parkkinen J, Eskelinen M, Tammi R, Lipponen P, Agren U, Alhava E, Kosma VM (1998) Tumor cell-associated hyaluronan as an unfavorable prognostic factor in colorectal cancer. Cancer Res 58:342–347PubMedGoogle Scholar
  58. 58.
    Gao AC, Lou W, Dong JT, Isaacs JT (1997) CD44 is a metastasis suppressor gene for prostatic cancer located on human chromosome 11p13. Cancer Res 57:846–849PubMedGoogle Scholar
  59. 59.
    Shtivelman E, Bishop JM (1991) Expression of CD44 is repressed in neuroblastoma cells. Mol Cell Biol 11:5446–5453PubMedGoogle Scholar
  60. 60.
    Burdick MM, McCarty OJT, Jadhav S, Konstantopoulos K (2001) Cell–cell interactions in inflammation and cancer metastasis. IEEE Eng Med Biol Mag 20:86–91PubMedCrossRefGoogle Scholar
  61. 61.
    Krause T, Turner GA (1998) Are selectins involved in metastasis? Clin Exp Metastasis 17:183–192CrossRefGoogle Scholar
  62. 62.
    Sass PM (1998) The involvement of selectins in cell adhesion, tumor progression, and metastasis. Cancer Invest 16:322–328PubMedCrossRefGoogle Scholar
  63. 63.
    Kannagi R, Izawa M, Koike T, Miyazaki K, Kimura N (2004) Carbohydrate-mediated cell adhesion in cancer metastasis and angiogenesis. Cancer Sci 95:377–384PubMedCrossRefGoogle Scholar
  64. 64.
    Nakamori S, Kameyama M, Imaoka S, Furukawa H, Ishikawa O, Sasaki Y, Kabuto T, Iwanaga T, Matsushita Y, Irimura T (1993) Increased expression of sialyl Lewisx antigen correlates with poor survival in patients with colorectal carcinoma: clinicopathological and immunohistochemical study. Cancer Res 53:3632–3637PubMedGoogle Scholar
  65. 65.
    Nakayama T, Watanabe M, Katsumata T, Teramoto T, Kitajima M (1995) Expression of sialyl Lewis(a) as a new prognostic factor for patients with advanced colorectal carcinoma. Cancer 75:2051–2056PubMedCrossRefGoogle Scholar
  66. 66.
    Sato M, Narita T, Kimura N, Zenita K, Hashimoto T, Manabe T, Kannagi R (1997) The association of sialyl Lewis(a) antigen with the metastatic potential of human colon cancer cells. Anticancer Res 17:3505–3511PubMedGoogle Scholar
  67. 67.
    Karpatkin S, Pearlstein E, Ambrogio C, Coller BS (1988) Role of adhesive proteins in platelet tumor interaction in vitro and metastasis formation in vivo. J Clin Invest 81:1012–1019PubMedCrossRefGoogle Scholar
  68. 68.
    Camerer E, Qazi AA, Duong DN, Cornelissen I, Advincula R, Coughlin SR (2004) Platelets, protease-activated receptors, and fibrinogen in hematogenous metastasis. Blood 104:397–401PubMedCrossRefGoogle Scholar
  69. 69.
    Nieswandt B, Hafner M, Echtenacher B, Mannel DN (1999) Lysis of tumor cells by natural killer cells in mice is impeded by platelets. Cancer Res 59:1295–1300PubMedGoogle Scholar
  70. 70.
    Burdick MM, Konstantopoulos K (2004) Platelet-induced enhancement of LS174T colon carcinoma and THP-1 monocytoid cell adhesion to vascular endothelium under flow. Am J Physiol Cell Physiol 287:C539–C547PubMedCrossRefGoogle Scholar
  71. 71.
    Felding-Habermann B, Habermann R, Salvidar E, Ruggeri ZM (1996) Role of β3 integrins in melanoma cell adhesion to activated platelets under flow. J Biol Chem 271:5892–5900PubMedCrossRefGoogle Scholar
  72. 72.
    Hanley W, McCarty O, Jadhav S, Tseng Y, Wirtz D, Konstantopoulos K (2003) Single molecule characterization of P-selectin/ligand binding. J Biol Chem 278:10556–10561PubMedCrossRefGoogle Scholar
  73. 73.
    McCarty OJ, Tien N, Bochner BS, Konstantopoulos K (2003) Exogenous eosinophil activation converts PSGL-1-dependent binding to CD18-dependent stable adhesion to platelets in shear flow. Am J Physiol Cell Physiol 284:C1223–C1234PubMedGoogle Scholar
  74. 74.
    Ahn KC, Jun AJ, Pawar P, Jadhav S, Napier S, McCarty OJ, Konstantopoulos K (2005) Preferential binding of platelets to monocytes over neutrophils under flow. Biochem Biophys Res Commun 329:345–355PubMedCrossRefGoogle Scholar
  75. 75.
    Goetz DJ, Ding H, Atkinson WJ, Vachino G, Camphausen RT, Cumming DA, Luscinskas FW (1996) A human colon carcinoma cell line exhibits adhesive interactions with P-selectin under fluid flow via a PSGL-1-independent mechanism. Am J Pathol 149:1661–1673PubMedGoogle Scholar
  76. 76.
    Honn KV, Tang DG, Crissman JD (1992) Platelets and cancer metastasis. Cancer Metastasis Rev 11:325–351PubMedCrossRefGoogle Scholar
  77. 77.
    Oleksowicz L, Mrowiec Z, Schwartz E, Khorshidi M, Dutcher JP, Puszkin E (1995) Characterization of tumor-induced platelet aggregation: the role of immunorelated GPIb and GPIIb/IIIa expression by MCF-7 breast cancer cells. Thromb Res 79:261–274PubMedCrossRefGoogle Scholar
  78. 78.
    Abe A, Radin N, Shayman J, Wotring L, Zipkin R, Sivakumar R, Ruggieri J, Carson K, Ganem B (1995) Structural and stereochemical studies of potent inhibitors of glucosylceramide synthase and tumor cell growth. J Lipid Res 36:611–621PubMedGoogle Scholar
  79. 79.
    Kojima N, Handa K, Newman W, Hakomori S (1992) Inhibition of selectin-dependent tumor cell adhesion to endothelial cells and platelets by blocking O-glycosylation of these cells. Biochem Biophys Res Commun 182:1288–1295PubMedCrossRefGoogle Scholar
  80. 80.
    Kuan SF, Byrd JC, Basbaum C, Kim YS (1989) Inhibition of mucin glycosylation by aryl-N-acetyl-alpha-galactosaminides in human colon cancer cells. J Biol Chem 264:19271–19277PubMedGoogle Scholar
  81. 81.
    Hanley WD, Burdick MM, Konstantopoulos K, Sackstein R (2005) CD44 on LS174T colon carcinoma cells possesses E-selectin ligand activity. Cancer Res 65:5812–5817PubMedCrossRefGoogle Scholar
  82. 82.
    Hanley WD, Napier SL, Burdick MM, Schnaar RL, Sackstein R, Konstantopoulos K (2006) Variant isoforms of CD44 are P- and L-selectin ligands on colon carcinoma cells. FASEB J 20:337–339PubMedGoogle Scholar
  83. 83.
    Fuhlbrigge RC, King SL, Dimitroff C, Kupper TS, Sackstein R (2002) Direct real-time observation of E- and P-selectin-mediated rolling on cutaneous lymphocyte-associated antigen immobilized on western blots. J Immunol 168:5645–5651PubMedGoogle Scholar
  84. 84.
    Napier SL, Healy ZR, Schnaar RL, Konstantopoulos K (2007) Selectin ligand expression regulates the initial vascular interactions of colon carcinoma cells: the roles of CD44V and alternative sialofucosylated selectin ligands. J Biol Chem 282:3433–3441PubMedCrossRefGoogle Scholar
  85. 85.
    Dimitroff CJ, Lee JY, Fuhlbrigge RC, Sackstein R (2000) A distinct glycoform of CD44 is an L-selectin ligand on human hematopoietic cells. Proc Natl Acad Sci USA 97:13841–13846PubMedCrossRefGoogle Scholar
  86. 86.
    Dimitroff CJ, Lee JY, Rafii S, Fuhlbrigge RC, Sackstein R (2001) CD44 is a major E-selectin ligand on human hematopoietic progenitor cells. J Cell Biol 153:1277–1286PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Department of Chemical and Biomolecular EngineeringThe Johns Hopkins UniversityBaltimoreUSA

Personalised recommendations