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November 1995, Vol 121, No. 11 >
ARTICLE | November 1995

Adhesion of Head and Neck Squamous Cell Carcinoma to Endothelial Cells: Title and subTitle BreakThe Missing Links FREE

Christopher T. Wenzel, MD; Richard L. Scher, MD; William Richtsmeier, MD, PhD
Arch Otolaryngol Head Neck Surg. 1995;121(11):1279-1286. doi:10.1001/archotol.1995.01890110053010
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Objectives:  To examine the direct adhesion of head and neck squamous cell carcinoma (HNSCC) cells to basal and cytokine-activated human endothelial cells and to determine the cell adhesion molecules (CAMs) that mediate binding under these two conditions.

Design:  Using an established model of tumor metastasis, the adhesion of four HNSCC cell lines to human umbilical vein endothelial cell (HUVEC) monolayers was examined, with and without pretreatment of HUVEC with tumor necrosis factor α (TNF-α). Surface CAM expression of HNSCC and HUVEC was determined by flow cytometry, and the results were used to direct studies of adhesion blocking using monoclonal antibodies. The contribution of various CAM to HNSCC binding of basal and cytokine-activated human endothelial cells in vitro was established.

Main Outcome Measures:  Adhesion of HNSCC to HUVEC monolayers was determined by a sodium chromate Cr 51-labeling assay in the presence or absence of monoclonal antibodies directed against specific CAMs.

Results:  Four HNSCC cell lines were shown by flow cytometry to constitutively express the following CAMs: intercellular CAM-1, CD44, lymphocyte function-associated antigen-3, integrin chains α6 and β1, and sialyl Lewisx. No cell lines expressed lymphocyte function-associated antigen-1 or the integrin subunit α4. Adhesion of JHU-011-SCC to TNF-α-activated HUVEC was enhanced above the untreated level in a time-dependent manner, with maximal adhesion at 12 hours. This increase correlated with endothelial-selectin expression by HUVEC and HNSCC expression of its ligand sialyl Lewisx. Monoclonal antibody to sialyl Lewisx blocked the increased adhesion to TNF-α-activated HUVEC in two of four HNSCC cell lines. Monoclonal antibody to the α6 integrin reduced binding to TNF-α-activated and nonactivated HUVEC and to subendothelial matrix, but not to fibronectin.

Conclusions:  Studies of four HNSCC cell lines disclosed a consistent and distinctive pattern of adhesion molecule expression. The α6 integrin subunit may be involved in direct adhesion to nonactivated and cytokine-activated endothelial cells or to laminin present on the endothelial surface. Sialyl Lewisx was more specifically involved in the increased adhesion to cytokine-activated HUVEC. This suggests that the sialyl Lewisx-endothelial-selectin ligand interaction may be important in facilitating HNSCC adhesion during metastasis to sites of active or chronic inflammation in vivo.(Arch Otolaryngol Head Neck Surg. 1995;121:1279-1286)

REFERENCES

1 +
Rice GE, Gimbrone MA Jr, Bevilacqua MP.  Tumor cell-endothelial cell interactions: increased adhesion of human melanoma cells to activated vascular endothelium . Am J Pathol . 1989;;133:204-210.
2 +
Auerbach R, Lu WC, Pardon E, Gumkowski F, Kaminsko G, Kaminska M.  Specificity of adhesion between murine tumor cells and capillary endothelium: an in vitro correlate of preferential metastasis in vivo . Cancer Res . 1987;;47:1492-1496.
3 +
Varki NM, Viswanathan B, Vu T.  Endothelial cells enhance spontaneous metastasis of human lung carcinoma cells in athymic nude mice . Cancer Lett . 1990;;51:251-257.
4 +
Varani J, Lovett EJ, Elgebaly S, Lundy J, Ward PA.  In vitro and in vivo adherence of tumor cell variants correlated with tumor formation . Am J Pathol . 1980;; 101:345-352.
5 +
Van Roy F, Mareel M.  Tumor invasion: effects of cell adhesion and motility . Trends Cell Biol . 1992;;2:163-168.
6 +
Springer TA.  Adhesion receptors of the immune system . Nature . 1990;;346: 425-434.
7 +
Orr FW, Adamson YR, Young L.  Pulmonary inflammation generates chemotactic activity for tumor cells and promotes lung metastasis . Am Rev Respir Dis . 1985;;131:607-611.
8 +
Dejana E, Bertocchi F, Bortolami MC, et al.  Interleukin-1 promotes tumor cell adhesion to cultured human endothelial cells . J Clin Invest . 1988;;82:1466-1470.
9 +
Giavazzi R, Garofalo A, Bani MR, et al.  Interleukin-1-induced augmentation of experimental metastases from a human melanoma in nude mice . Cancer Res . 1990;;50:4771-4775.
10 +
Bevilacqua MP, Pober JS, Wheeler ME, Cotran RS, Gimbrone MA Jr.  Interleukin 1 acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes, and related leukocyte cell lines . J Clin Invest . 1985;;76:2003-2011.
11 +
Bevilacqua MP, Corless C, Lo SK.  Endothelial-leukocyte adhesion molecule-1 (ELAM-1): a vascular selectin that regulates inflammation . In: Cochrane CG, Gimbrone MA Jr, eds. Cellular and Molecular Mechanisms of Inflammation . Orlando, Fla: Academic Press Inc; 1991;;2:1-11.
12 +
Bevilacqua MP, Stengelin S, Gimbrone MA Jr, Seed B.  Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins . Science . 1989;;243:1160-1165.
13 +
Dustin ML, Springer TA.  Lymphocyte function-associated antigen (LFA-1) interaction with intercellular adhesion molecule (ICAM-1) is one of at least three mechanisms for lymphocyte adhesion to cultured endothelial cells . J Cell Biol 1988;;107:321-331.
14 +
Wawryk SO, Novotny JR, Wicks IP, et al.  The role of the LFA-1/ICAM-1 interaction in human leukocyte homing and adhesion . Immunol Rev . 1989;;108: 135-161.
15 +
Elices MJ, Osborn L, Takada Y, et al.  VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site . Cell . 1990;;60:577-584.
16 +
Osborn L, Hession C, Tizard R, et al.  Direct expression cloning of vascular cell adhesion molecule-1, a cytokine-induced endothelial protein that binds to lymphocytes . Cell . 1989;;59:1203-1211.
17 +
Bochner BS, Luscinskas FW, Gimbrone MA Jr, et al.  Adhesion of human basophils, eosinophils, and neutrophils to interleukin-1 activated human vascular endothelial cells: contribution of endothelial cell adhesion molecules . J Exp Med . 1991;;173:1553-1556.
18 +
Martin-Padura I, Mortarini R, Lauri D, et al.  Heterogeneity in human melanoma cell adhesion to cytokine activated endothelial cells correlates with VLA-4 expression . Cancer Res . 1991;;51:2249-2241.
19 +
Takada A, Ohmori K, Yoneda T, et al.  Contribution of carbohydrate antigens sialyl Lewisa and sialyl Lewisx to adhesion of human cancer cells to vascular endothelium . Cancer Res . 1993;;53:354-361.
20 +
Scher RL, Koch WM, Richtsmeier WJ.  Induction of the intercellular adhesion molecule (ICAM-1) on squamous cell carcinoma by interferon gamma . Arch Otolaryngol Head Neck Surg . 1993;;119:432-438.
21 +
Kramer RH, Gonzalez R, Nicolson GL.  Metastatic tumor cells adhere preferentially to the extracellular matrix underlying vascular endothelial cells . Int J Cancer . 1980;;26:639-645.
22 +
Springer TA, Lasky LA.  Sticky sugars for selectins . Nature . 1991;;349:196-197.
23 +
Hoff SD, Irimura Y, Matsushita DM, et al.  Metastatic potential of colon carcinoma: expression of ABO/Lewis-related antigens . Arch Surg . 1990;;125:206-209.
24 +
Matushita Y, Cleary KR, Ota DM, et al.  Sialyl-dimeric Lewis-X antigen expressed on mucin-like glycoproteins in colorectal cancer metastases . Lab Invest . 1990;;63:780-791.
25 +
Berg EL, Robinson MK, Mansson O, Butcher EC, Magnoni JL.  A carbohydrate domain common to both sialyl Lea and sialyl Lex is recognized by the endothelial cell leukocyte adhesion molecule ELAM-1 . J Biol Chem . 1991;;266:14869-14872.
26 +
Lauri D, Lindsey N, Marin-Padura.  Tumor cell adhesion to endothelial cells: endothelial leukocyte adhesion molecule-1 as inducible adhesive receptor for colon carcinoma cells . J Natl Cancer Inst . 1991;;83:1321-1323.
27 +
Cotran RS, Gimbrone MA Jr, Bevilacqua MP, Mendrick DL, Pober JS.  Induction and detection of a human endothelial antigen in vivo . J Exp Med . 1986;; 164:661-666.
28 +
Gasic GJ.  Role of plasma, platelets, and endothelial cells in tumor metastasis . Cancer Metastasis Rev . 1984;;3:99-116.
29 +
Kock A, Schwarz T, Urbanski A, et al.  Expression and release of interleukin-1 by different human melanoma cell lines . J Natl Cancer Inst . 1989;;81:36-42.
30 +
Bani MR, Garafalo A, Scanzion E, Giavazzi R.  Effect of interleukin-1-beta on metastasis formation in different tumor systems . J Natl Cancer Inst . 1991;;83: 119-123.
31 +
Larjava H.  Expression of β1 integrins in normal human keratinocytes . Am J Med Sci. 1991;;301:63-68.
32 +
Van Waes C, Carey TE.  Overexpression of the A9 antigen/alpha 6 beta 4 integrin in head and neck cancer . Otolaryngol Clin North Am . 1992;;25:1117-1139.
33 +
Wolf GT, Carey TE.  Tumor antigen phenotype, biologic staging, and prognosis in head and neck squamous carcinoma . Monogr Natl Cancer Inst . 1992;;13: 67-74.

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1 +
Rice GE, Gimbrone MA Jr, Bevilacqua MP.  Tumor cell-endothelial cell interactions: increased adhesion of human melanoma cells to activated vascular endothelium . Am J Pathol . 1989;;133:204-210.
2 +
Auerbach R, Lu WC, Pardon E, Gumkowski F, Kaminsko G, Kaminska M.  Specificity of adhesion between murine tumor cells and capillary endothelium: an in vitro correlate of preferential metastasis in vivo . Cancer Res . 1987;;47:1492-1496.
3 +
Varki NM, Viswanathan B, Vu T.  Endothelial cells enhance spontaneous metastasis of human lung carcinoma cells in athymic nude mice . Cancer Lett . 1990;;51:251-257.
4 +
Varani J, Lovett EJ, Elgebaly S, Lundy J, Ward PA.  In vitro and in vivo adherence of tumor cell variants correlated with tumor formation . Am J Pathol . 1980;; 101:345-352.
5 +
Van Roy F, Mareel M.  Tumor invasion: effects of cell adhesion and motility . Trends Cell Biol . 1992;;2:163-168.
6 +
Springer TA.  Adhesion receptors of the immune system . Nature . 1990;;346: 425-434.
7 +
Orr FW, Adamson YR, Young L.  Pulmonary inflammation generates chemotactic activity for tumor cells and promotes lung metastasis . Am Rev Respir Dis . 1985;;131:607-611.
8 +
Dejana E, Bertocchi F, Bortolami MC, et al.  Interleukin-1 promotes tumor cell adhesion to cultured human endothelial cells . J Clin Invest . 1988;;82:1466-1470.
9 +
Giavazzi R, Garofalo A, Bani MR, et al.  Interleukin-1-induced augmentation of experimental metastases from a human melanoma in nude mice . Cancer Res . 1990;;50:4771-4775.
10 +
Bevilacqua MP, Pober JS, Wheeler ME, Cotran RS, Gimbrone MA Jr.  Interleukin 1 acts on cultured human vascular endothelium to increase the adhesion of polymorphonuclear leukocytes, monocytes, and related leukocyte cell lines . J Clin Invest . 1985;;76:2003-2011.
11 +
Bevilacqua MP, Corless C, Lo SK.  Endothelial-leukocyte adhesion molecule-1 (ELAM-1): a vascular selectin that regulates inflammation . In: Cochrane CG, Gimbrone MA Jr, eds. Cellular and Molecular Mechanisms of Inflammation . Orlando, Fla: Academic Press Inc; 1991;;2:1-11.
12 +
Bevilacqua MP, Stengelin S, Gimbrone MA Jr, Seed B.  Endothelial leukocyte adhesion molecule 1: an inducible receptor for neutrophils related to complement regulatory proteins and lectins . Science . 1989;;243:1160-1165.
13 +
Dustin ML, Springer TA.  Lymphocyte function-associated antigen (LFA-1) interaction with intercellular adhesion molecule (ICAM-1) is one of at least three mechanisms for lymphocyte adhesion to cultured endothelial cells . J Cell Biol 1988;;107:321-331.
14 +
Wawryk SO, Novotny JR, Wicks IP, et al.  The role of the LFA-1/ICAM-1 interaction in human leukocyte homing and adhesion . Immunol Rev . 1989;;108: 135-161.
15 +
Elices MJ, Osborn L, Takada Y, et al.  VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site . Cell . 1990;;60:577-584.
16 +
Osborn L, Hession C, Tizard R, et al.  Direct expression cloning of vascular cell adhesion molecule-1, a cytokine-induced endothelial protein that binds to lymphocytes . Cell . 1989;;59:1203-1211.
17 +
Bochner BS, Luscinskas FW, Gimbrone MA Jr, et al.  Adhesion of human basophils, eosinophils, and neutrophils to interleukin-1 activated human vascular endothelial cells: contribution of endothelial cell adhesion molecules . J Exp Med . 1991;;173:1553-1556.
18 +
Martin-Padura I, Mortarini R, Lauri D, et al.  Heterogeneity in human melanoma cell adhesion to cytokine activated endothelial cells correlates with VLA-4 expression . Cancer Res . 1991;;51:2249-2241.
19 +
Takada A, Ohmori K, Yoneda T, et al.  Contribution of carbohydrate antigens sialyl Lewisa and sialyl Lewisx to adhesion of human cancer cells to vascular endothelium . Cancer Res . 1993;;53:354-361.
20 +
Scher RL, Koch WM, Richtsmeier WJ.  Induction of the intercellular adhesion molecule (ICAM-1) on squamous cell carcinoma by interferon gamma . Arch Otolaryngol Head Neck Surg . 1993;;119:432-438.
21 +
Kramer RH, Gonzalez R, Nicolson GL.  Metastatic tumor cells adhere preferentially to the extracellular matrix underlying vascular endothelial cells . Int J Cancer . 1980;;26:639-645.
22 +
Springer TA, Lasky LA.  Sticky sugars for selectins . Nature . 1991;;349:196-197.
23 +
Hoff SD, Irimura Y, Matsushita DM, et al.  Metastatic potential of colon carcinoma: expression of ABO/Lewis-related antigens . Arch Surg . 1990;;125:206-209.
24 +
Matushita Y, Cleary KR, Ota DM, et al.  Sialyl-dimeric Lewis-X antigen expressed on mucin-like glycoproteins in colorectal cancer metastases . Lab Invest . 1990;;63:780-791.
25 +
Berg EL, Robinson MK, Mansson O, Butcher EC, Magnoni JL.  A carbohydrate domain common to both sialyl Lea and sialyl Lex is recognized by the endothelial cell leukocyte adhesion molecule ELAM-1 . J Biol Chem . 1991;;266:14869-14872.
26 +
Lauri D, Lindsey N, Marin-Padura.  Tumor cell adhesion to endothelial cells: endothelial leukocyte adhesion molecule-1 as inducible adhesive receptor for colon carcinoma cells . J Natl Cancer Inst . 1991;;83:1321-1323.
27 +
Cotran RS, Gimbrone MA Jr, Bevilacqua MP, Mendrick DL, Pober JS.  Induction and detection of a human endothelial antigen in vivo . J Exp Med . 1986;; 164:661-666.
28 +
Gasic GJ.  Role of plasma, platelets, and endothelial cells in tumor metastasis . Cancer Metastasis Rev . 1984;;3:99-116.
29 +
Kock A, Schwarz T, Urbanski A, et al.  Expression and release of interleukin-1 by different human melanoma cell lines . J Natl Cancer Inst . 1989;;81:36-42.
30 +
Bani MR, Garafalo A, Scanzion E, Giavazzi R.  Effect of interleukin-1-beta on metastasis formation in different tumor systems . J Natl Cancer Inst . 1991;;83: 119-123.
31 +
Larjava H.  Expression of β1 integrins in normal human keratinocytes . Am J Med Sci. 1991;;301:63-68.
32 +
Van Waes C, Carey TE.  Overexpression of the A9 antigen/alpha 6 beta 4 integrin in head and neck cancer . Otolaryngol Clin North Am . 1992;;25:1117-1139.
33 +
Wolf GT, Carey TE.  Tumor antigen phenotype, biologic staging, and prognosis in head and neck squamous carcinoma . Monogr Natl Cancer Inst . 1992;;13: 67-74.

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