Podocalyxin-like protein is an E-/L-selectin ligand on colon carcinoma cells: Comparative biochemical properties of selectin ligands in host and tumor cells

American Journal of Physiology - Cell Physiology

Volumn 296, Issue 3, 2009, Pages

  Thomas, Susan N ^a   Schnaar, Ronald L ^b   Konstantopoulos, Konstantinos ^a  

^a Johns Hopkins University   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Adhesion; Colon carcinoma cells; Fluid shear; Metastasis

Indexed keywords

ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; GLYCAN DERIVATIVE; HERMES ANTIGEN; L SELECTIN; LIGAND; PODOCALYXIN; CD44 PROTEIN, HUMAN; PADGEM PROTEIN; SIALOGLYCOPROTEIN;

ANIMAL CELL; ARTICLE; ASSAY; BINDING AFFINITY; BIOCHEMISTRY; CARCINOMA CELL; COLON CARCINOMA; COMPARATIVE STUDY; CONTROLLED STUDY; CORRELATIONAL STUDY; FEMALE; HOST CELL; HUMAN; HUMAN CELL; IMMUNOREACTIVITY; METASTASIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; WILD TYPE; AFFINITY CHROMATOGRAPHY; ANIMAL; CARCINOMA; CELL ADHESION; CHO CELL; COLORECTAL TUMOR; CRICETULUS; GENETIC TRANSFECTION; GENETICS; GLYCOSYLATION; HAMSTER; METABOLISM; PATHOLOGY; PEPTIDE MAPPING; PROTEIN BINDING; TANDEM MASS SPECTROMETRY; TUMOR CELL LINE; UPREGULATION;

ANIMALS; ANTIGENS, CD44; CARCINOMA; CELL ADHESION; CELL LINE, TUMOR; CHO CELLS; CHROMATOGRAPHY, AFFINITY; COLORECTAL NEOPLASMS; CRICETINAE; CRICETULUS; E-SELECTIN; GLYCOSYLATION; HUMANS; L-SELECTIN; LIGANDS; NEOPLASM METASTASIS; P-SELECTIN; PEPTIDE MAPPING; PROTEIN BINDING; SIALOGLYCOPROTEINS; TANDEM MASS SPECTROMETRY; TRANSFECTION; UP-REGULATION;

EID: 65249108221     PISSN: 03636143     EISSN: 15221563     Source Type: Journal    
DOI: 10.1152/ajpcell.00472.2008     Document Type: Article

References (55)

1. Aigner S, Ramos CL, Hafezi-Moghadam A, Lawrence MB, Friederichs J, Altevogt P, Ley K. CD24 mediates rolling of breast carcinoma cells on P-selectin. FASEB J 12: 1241-1251, 1998. (Pubitemid 28418954)
2. Aigner S, Sthoeger ZM, Fogel M, Weber E, Zarn J, Ruppert M, Zeller Y, Vestweber D, Stahel R, Sammar M, Altevogt P. CD24, a mucin-type glycoprotein, is a ligand for P-selectin on human tumor cells. Blood 89: 3385-3395, 1997. (Pubitemid 27229826)
3. Alves CS, Burdick MM, Thomas SN, Pawar P, KK. The dual role of CD44 as a functional P-selectin and fibrin ligand in colon carcinoma cell adhesion. Am J Physiol Cell Physiol 294: C907-C916, 2008.
4. Borsig L, Wong R, Feramisco J, Nadeau DR, Varki NM, Varki A. Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis. Proc Natl Acad Sci USA 98: 3352-3357, 2001. (Pubitemid 32220849)
5. Borsig L, Wong R, Hynes RO, Varki NM, Varki A. 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: 2193-2198, 2002. (Pubitemid 34169037)
6. Brodt P, Fallavollita L, Bresalier RS, Meterissian S, Norton CR, Wolitzky BA. Liver endothelial E-selectin mediates carcinoma cell adhesion and promotes liver metastasis. Int J Cancer 71: 612-619, 1997. (Pubitemid 27239372)
7. Burdick MM, Konstantopoulos K. 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-C547, 2004. (Pubitemid 38955245)
8. Burdick MM, McCaffery JM, Kim YS, Bochner BS, Konstantopoulos K. Colon carcinoma cell glycolipids, integrins, and other glycoproteins mediate adhesion to HUVECs under flow. Am J Physiol Cell Physiol 284: C977-C987, 2003. (Pubitemid 36336954)
9. Burdick MM, McCarty OJT, Jadhav S, Konstantopoulos K. Cell-cell interactions in inflammation and cancer metastasis. IEEE Eng Med Biol 20: 86-91, 2001.
10. Casey G, Neville PJ, Liu X, Plummer SJ, Cicek MS, Krumroy LM, Curran AP, McGreevy MR, Catalona WJ, Klein EA, Witte JS. Podocalyxin variants and risk of prostate cancer and tumor aggressiveness. Hum Mol Genet 15: 735-741, 2006. (Pubitemid 43264698)
11. Dimitroff CJ, Lee JY, Fuhlbrigge RC, Sackstein R. A distinct glycoform of CD44 is an L-selectin ligand on human hematopoietic cells. Proc Natl Acad Sci USA 97: 13841-13846, 2000.
12. Dimitroff CJ, Lee JY, Rafii S, Fuhlbrigge RC, Sackstein R. CD44 is a major Eselectin ligand on human hematopoietic progenitor cells. J Cell Biol 153: 1277-1286, 2001. (Pubitemid 34289265)
13. Dimitroff CJ, Lee JY, Schor KS, Sandmaier BM, Sackstein R. Differential L-selectin binding activities of human hematopoietic cell L-selectin ligands, HCELL and PSGL-1. J Biol Chem 276: 47623-47631, 2001. (Pubitemid 33647076)
14. Doyonnas R, Kershaw DB, Duhme C, Merkens H, Chelliah S, Graf T, McNagny KM. Anuria, omphalocele, and perinatal lethality in mice lacking the CD34-related protein podocalyxin. J Exp Med 194: 13-27, 2001. (Pubitemid 32660434)
15. Fuhlbrigge RC, King SL, Dimitroff C, Kupper TS, Sackstein R. Direct real-time observation of E- and P-selectin-mediated rolling on cutaneous lymphocyte-associated antigen immobilized on western blots. J Immunol 168: 5645-5651, 2002. (Pubitemid 34556146)
16. Hanley WD, Burdick MM, Konstantopoulos K, Sackstein R. CD44 on LS174T colon carcinoma cells possesses E-selectin ligand activity. Cancer Res 65: 5812-5817, 2005. (Pubitemid 40911185)
17. Hanley WD, Napier SL, Burdick MM, Schnaar RL, Sackstein R, Konstantopoulos K. Variant isoforms of CD44 are P- and L-selectin ligands on colon carcinoma cells. FASEB J 20: 337-339, 2006. (Pubitemid 46671163)
18. Hanley WD, Wirtz D, Konstantopoulos K. Distinct kinetic and mechanical properties govern selectin-leukocyte interactions. J Cell Sci 117: 2503-2511, 2004. (Pubitemid 38877846)
19. Harada N, Mizoi T, Kinouchi M, Hoshi K, Ishii S, Shiiba K, Sasaki I, Matsuno S. 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: 67-75, 2001.
20. Hayatsu N, Kaneko MK, Mishima K, Nishikawa R, Matsutani M, Price JE, Kato Y. Podocalyxin expression in malignant astrocytic tumors. Biochem Biophys Res Commun 374: 394-398, 2008.
21. Heukamp LC, Fischer HP, Schirmacher P, Chen X, Breuhahn K, Nicolay C, Buttner R, Gutgemann I. Podocalyxin-like protein 1 expression in primary hepatic tumours and tumour-like lesions. Histopathology 49: 242-247, 2006. (Pubitemid 44253613)
22. Hofmann M, Rudy W, Zoller M, Tolg C, Ponta H, Herrlich P, Gunthert U. CD44 splice variants confer metastatic behavior in rats: homologous sequences are expressed in human tumor cell lines. Cancer Res 51: 5292-5297, 1991.
23. Izumi Y, Taniuchi Y, Tsuji T, Smith CW, Nakamori S, Fidler IJ, Irimura T. Characterization of human colon carcinoma variant cells selected for sialyl Lex carbohydrate antigen: liver colonization and adhesion to vascular endothelial cells. Exp Cell Res 216: 215-221, 1995.
24. Jadhav S, Bochner BS, Konstantopoulos K. Hydrodynamic shear regulates the kinetics and receptor specificity of polymorphonuclear leukocyte: colon carcinoma cell adhesive interactions. J Immunol 167: 5986-5993, 2001. (Pubitemid 33062796)
25. Jadhav S, Eggleton CD, Konstantopoulos K. Mathematical modeling of cell adhesion in shear flow pertinent to inflammation and cancer metastasis. Curr Pharm Des 13: 1511-1526, 2007.
26. Jadhav S, Konstantopoulos K. Fluid shear- and time-dependent modulation of molecular interactions between polymorphonuclear leukocytes and colon carcinomas. Am J Physiol Cell Physiol 283: C1133-C1143, 2002.
27. Kannagi R, Izawa M, Koike T, Miyazaki K, Kimura N. Carbohydratemediated cell adhesion in cancer metastasis and angiogenesis. Cancer Sci 95: 377-384, 2004. (Pubitemid 38832679)
28. Kansas GS. Selectins and their ligands: current concepts and controversies. Blood 88: 3259-3287, 1996.
29. Kelley TWHD, McNagny KM, Roskelley CD, Hsi ED. Podocalyxin: a marker of blasts in acute leukemia. Am J Clin Pathol 124: 134-142, 2005.
30. Kerjaschki D. Epitopes and radicals: early events in glomerular injury in membranous nephropathy. Exp Nephrol 3: 1-8, 1995.
31. Kerosuo LJE, Alitalo R, Gylling M, Kerjaschki D, Miettinen A. Podocalyxin in human haematopoietic cells. Br J Haematol 124: 809-818, 2004. (Pubitemid 38365787)
32. Kim YJ, Borsig L, Varki NM, Varki A. P-selectin deficiency attenuates tumor growth and metastasis. Proc Natl Acad Sci USA 95: 9325-9330, 1998. (Pubitemid 28506230)
33. Kim YJ, Varki A. Perspectives on the significance of altered glycosylation of glycoproteins in cancer. Glycoconj J 14: 569-576, 1997. (Pubitemid 27353200)
34. Konstantopoulos K, Kukreti S, McIntire LV. Biomechanics of cell interactions in shear fields. Adv Drug Deliv Rev 33: 141-164, 1998. (Pubitemid 28403540)
35. Laubli H, Stevenson JL, Varki A, Varki NM, Borsig L. L-selectin facilitation of metastasis involves temporal induction of Fut7-dependent ligands at sites of tumor cell arrest. Cancer Res 66: 1536-1542, 2006. (Pubitemid 43259935)
36. Leppanen A, Yago T, Otto VI, McEver RP, Cummings RD. Model glycosulfopeptides from P-selectin glycoprotein ligand-1 require tyrosine sulfation and a core 2-branched O-glycan to bind to L-selectin. J Biol Chem 278: 26391-26400, 2003. (Pubitemid 36876778)
37. Li F, Wilkins PP, Crawley S, Weinstein J, Cummings RD, McEver RP. Posttranslational modifications of recombinant P-selectin glycoprotein ligand-1 required for binding to P- and E-selectin. J Biol Chem 271: 3255-3264, 1996. (Pubitemid 26055629)
38. Mannori G, Crottet P, Cecconi O, Hanasaki K, Aruffo A, Nelson RM, Varki A, Bevilacqua MP. Differential colon cancer cell adhesion to E-, P-, and L-selectin: role of mucintype glycoproteins. Cancer Res 55: 4425-4431, 1995.
39. Mannori G, Santoro D, Carter L, Corless C, Nelson RM, Bevilacqua MP. Inhibition of colon carcinoma cell lung colony formation by a soluble form of E-selectin. Am J Pathol 151: 233-243, 1997. (Pubitemid 27283974)
40. McCarty OJT, Jadhav S, Burdick MM, Bell WR, Konstantopoulos K. Fluid shear regulates the kinetics and molecular mechanisms of activationdependent platelet binding to colon carcinoma cells. Biophys J 83: 836-848, 2002.
41. McCarty OJT, Mousa SA, Bray PF, Konstantopoulos K. Immobilized platelets support human colon carcinoma cell tethering, rolling and firm adhesion under dynamic flow conditions. Blood 96: 1789-1797, 2000. (Pubitemid 30661063)
42. Nakamori S, Kameyama M, Imaoka S, Furukawa H, Ishikawa O, Sasaki Y, Kabuto T, Iwanaga T, Matsushita Y, Irimura T. Increased expression of sialyl Lewisx antigen correlates with poor survival in patients with colorectal carcinoma: clinicopathological and immunohistochemical study. Cancer Res 53: 3632-3637, 1993. (Pubitemid 23229648)
43. Nakayama T, Watanabe M, Katsumata T, Teramoto T, Kitajima M. Expression of sialyl Lewis(a) as a new prognostic factor for patients with advanced colorectal carcinoma. Cancer 75: 2051-2056, 1995.
44. Napier SL, Healy ZR, Schnaar RL, Konstantopoulos K. 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: 3433-3441, 2007. (Pubitemid 47084453)
45. Nieswandt B, Hafner M, Echtenacher B, Mannel DN. Lysis of tumor cells by natutal killer cells in mice is impeded by platelets. Cancer Res 59: 1295-1300, 1999. (Pubitemid 29136261)
46. Sackstein R, Dimitroff CJ. A hematopoietic cell L-selectin ligand that is distinct from PSGL-1 and displays N-glycan-dependent binding activity. Blood 96: 2765-2774, 2000.
47. Sassetti C, Tangemann K, Singer MS, Kershaw DB, Rosen SD. Identification of podocalyxin-like protein as a high endothelial venule ligand for L-selectin: parallels to CD34. J Exp Med 187: 1965-1975, 1998. (Pubitemid 28285566)
48. Sato M, Narita T, Kimura N, Zenita K, Hashimoto T, Manabe T, Kannagi R. The association of sialyl Lewis(a) antigen with the metastatic potential of human colon cancer cells. Anticancer Res 17: 3505-3511, 1997. (Pubitemid 27522317)
49. Simon SI, Green CE. Molecular mechanics and dynamics of leukocyte recruitment during inflammation. Annu Rev Biomed Eng 7: 151-185, 2005.
50. Somasiri A, Nielsen JS, Makretsov N, McCoy ML, Prentice L, Gilks CB, Chia SK, Gelmon KA, Kershaw DB, Huntsman DG, McNagny KM, Roskelley CD. Overexpression of the anti-adhesin podocalyxin is an independent predictor of breast cancer progression. Cancer Res 64: 5068-5073 2004. (Pubitemid 39006520)
51. Somers WS, Tang J, Shaw GD, Camphausen RT. Insights into the molecular basis of leukocyte tethering and rolling revealed by structures of P- and E-selectin bound to SLe(X) and PSGL-1. Cell 103: 467-479, 2000.
52. Stone JP, Wagner DD. P-selectin mediates adhesion of platelets to neuroblastoma and small cell lung cancer. J Clin Invest 92: 804-813, 1993.
53. Thomas SN, Zhu F, Schnaar RL, Alves CS, Konstantopoulos K. Carcinoembryonic antigen and CD44 variant isoforms cooperate to mediate colon carcinoma cell adhesion to E- and L-selectin in shear flow. J Biol Chem 283: 15647-15655, 2008.
54. Varki A. Selectin ligands: will the real ones please stand up? J Clin Invest 100: S31-35, 1997.
55. Zou X, Shinde Patil VR, Dagia NM, Smith LA, Wargo MJ, Interliggi KA, Lloyd CM, Tees DF, Walcheck B, Lawrence MB, Goetz DJ. PSGL-1 derived from human neutrophils is a high-efficiency ligand for endothelium-expressed E-selectin under flow. Am J Physiol Cell Physiol 289: C415-C424, 2005. (Pubitemid 41008888)