Abstract
Orchestrated modulation of cell adhesion is essential for development and homeostasis in multicellular organisms. It optimizes embedding of the cell in its dynamic environment and facilitates appropriate cell responses and intercellular communication. Chronic disturbance of this delicate equilibrium causes defects in tissue architecture and sometimes cancer. In tumor cell biology, dynamic control of adhesion molecules is important to proceed through the metastatic cascade and to allow cell release from the primary tumor, invasion of the surrounding matrix, intravasation and adhesion to vascular endothelial cells to facilitate extravasation. Intertwined and multiple adhesive interactions rather than individual interactions presumably play critical roles in neoplastic development. Yet, knowledge of the contribution of each individual adhesion molecule is essential to unravel this network of interactions. This review will focus on activated leukocyte cell adhesion molecule (ALCAM/CD166) and its role in human melanoma progression. It is hypothesized that ALCAM may function as a cell surface sensor to register local growth saturation and to regulate cellular signaling and dynamic responses.
Similar content being viewed by others
References
Hsu MY, Meier F, Herlyn M: Melanoma development and progression: A conspiracy between tumor and host. Differentiation 70: 522–536, 2002
McGary EC, Lev DC, Bar-Eli M: Cellular adhesion pathways and metastatic potential of human melanoma. Cancer Biol Ther 1: 459–465, 2002
Kadmon G, Montgomery AM, Altevogt P: L1 makes immunological progress by expanding its relations. Dev Immunol 6: 205–213, 1998
Hendrix MJ, Seftor EA, Meltzer PS, Gardner LM, Hess AR, Kirschmann DA, Schatteman GC, Seftor RE: Expression and functional significance of VE-cadherin in aggressive human melanoma cells: Role in vasculogenic mimicry. Proc Natl Acad Sci USA 98: 8018–8023, 2001
Li G, Satyamoorthy K, Meier F, Berking C, Bogenrieder T, Herlyn M: Function and regulation of melanoma-stromal fibroblast interactions: When seeds meet soil. Oncogene 22: 3162–3171, 2003
Hanahan D, Weinberg RA: The hallmarks of cancer. Cell 100: 57–70, 2000
van Muijen GN, Cornelissen LM, Jansen CF, Figdor CG, Johnson JP, Brocker EB, Ruiter DJ: Antigen expression of metastasizing and non-metastasizing human melanoma cells xenografted into nude mice. Clin Exp Metastasis 9: 259–272, 1991
van Muijen GN, Jansen KF, Cornelissen IM, Smeets, DF, Beck JL, Ruiter DJ: Establishment and characterization of a human melanoma cell line (MV3) which is highly metastatic in nude mice. Int J Cancer 48: 85–91, 1991
Westphal JR, Van’t Hullenaar R, Peek R, Willems RW, Crickard K, Crickard U, Askaa J, Clemmensen I, Ruiter DJ, De Waal RM: Angiogenic balance in human melanoma: Expression of VEGF, bFGF, IL-8, PDGF and angiostatin in relation to vascular density of xenografts in vivo. Int J Cancer 86: 768–776, 2000
Albelda SM, Mette SA, Elder DE, Stewart R, Damjanovich L, Herlyn M, Buck CA: Integrin distribution in malignant melanoma: Association of the beta 3 subunit with tumor progression. Cancer Res 50: 6757–6764, 1990
Danen EH, van Kraats AA, Cornelissen IM, Ruiter DJ, van Muijen GN: Integrin beta 3 cDNA transfection into a highly metastatic alpha v beta 3-negative human melanoma cell line inhibits invasion and experimental metastasis. Biochem Biophys Res Commun 226: 75–81, 1996
Shih IM: The role of CD146 (Mel-CAM) in biology and pathology. J Pathol 189: 4–11, 1999
Lehmann JM, Riethmuller G, Johnson JP: MUC18, a marker of tumor progression in human melanoma, shows sequence similarity to the neural cell adhesion molecules of the immunoglobulin superfamily. Proc Natl Acad Sci USA 86: 9891–9895, 1989
van Kempen LC, van den Oord JJ, van Muijen GN, Weidle UH, Bloemers HP, Swart GW: Activated leukocyte cell adhesion molecule/CD166, a marker of tumor progression in primary malignant melanoma of the skin. Am J Pathol 156: 769–774, 2000
Fogel M, Mechtersheimer S, Huszar M, Smirnov A, Abu-Dahi A, Tilgen W, Reichrath J, Georg T, Altevogt P, Gutwein P: L1 adhesion molecule (CD 171) in development and progression of human malignant melanoma. Cancer Lett 189: 237–247, 2003
Thies A, Schachner M, Moll I, Berger J, Schulze HJ, Brunner G, Schumacher U: Overexpression of the cell adhesion molecule L1 is associated with metastasis in cutaneous malignant melanoma. Eur J Cancer 38: 1708–1716, 2002
Hieken TJ, Ronan SG, Farolan M, Shilkaitis AL, Das Gupta TK: Molecular prognostic markers in intermediate-thickness cutaneous malignant melanoma. Cancer 85: 375–382, 1999
Felding-Habermann B, Fransvea E, O’Toole TE, Manzuk L, Faha B, Hensler M: Involvement of tumor cell integrin alpha v beta 3 in hematogenous metastasis of human melanoma cells. Clin Exp Metastasis 19: 427–436, 2002
Seftor EA, Meltzer PS, Schatteman GC, Gruman LM, Hess AR, Kirschmann DA, Seftor RE, Hendrix MJ: Expression of multiple molecular phenotypes by aggressive melanoma tumor cells: Role in vasculogenic mimicry. Crit Rev Oncol Hematol 44: 17–27, 2002
Danen EH, de Vries TJ, Morandini R, Ghanem GG, Ruiter DJ, van Muijen GN: E-cadherin expression in human melanoma. Melanoma Res 6: 127–131, 1996
Weeraratna AT, Becker D, Carr KM, Duray PH, Rosenblatt KP, Yang S, Chen Y, Bittner M, Strausberg RL, Riggins GJ, Wagner U, Kallioniemi OP, Trent JM, Morin PJ, Meltzer PS: Generation and analysis of melanoma SAGE libraries: SAGE advice on the melanoma transcriptome. Oncogene 23: 2264–2274, 2004
Albelda SM, Smith CW, Ward PA: Adhesion molecules and inflammatory injury. Faseb J 8: 504–512, 1994
Giavazzi R, Foppolo M, Dossi R, Remuzzi A: Rolling and adhesion of human tumor cells on vascular endothelium under physiological flow conditions. J Clin Invest 92: 3038–3044, 1993
Voura EB, Sandig M, Kalnins VI, Siu C: Cell shape changes and cytoskeleton reorganization during transendothelial migration of human melanoma cells. Cell Tissue Res 293: 375–387, 1998
Sandig M, Voura EB, Kalnins VI, Siu CH: Role of cadherins in the transendothelial migration of melanoma cells in culture. Cell Motil Cytoskeleton 38: 351–364, 1997
Voura EB, Ramjeesingh RA, Montgomery AM, Siu CH: Involvement of integrin alpha(v)beta(3) and cell adhesion molecule L1 in transendothelial migration of melanoma cells. Mol Biol Cell 12: 2699–2710, 2001
King JA, Al-Mehdi AB, Ofori-Acquah S, Stevens T: Role of ALCAM in interaction of breast cancer metastases and the endothelium of the lung (Abstract). FASEB J 18: A330, 2004
King J, Ofori-Acquah S, Stevens T, Al-Mehdi AB: Potential role for activated leukocyte cell adhesion molecule and neural cadherin in metastasis to the lung microcirculation (Abstract). Chest 125: 150S–151S, 2004
Patel DD, Wee SF, Whichard LP, Bowen MA, Pesando JM, Aruffo A, Haynes BF: Identification and characterization of a 100-kD ligand for CD6 on human thymic epithelial cells. J Exp Med 181: 1563–1568, 1995
Uchida N, Yang Z, Combs J, Pourquie O, Nguyen M, Ramanathan R, Fu J, Welply A, Chen S, Weddell G, Sharma AK, Leiby KR, Karagogeos D, Hill B, Humeau L, Stallcup WB, Hoffman R, Tsukamoto AS, Gearing DP, Peault B: The characterization, molecular cloning, and expression of a novel hematopoietic cell antigen from CD34+ human bone marrow cells. Blood 89: 2706–2716, 1997
Bruder SP, Ricalton NS, Boynton RE, Connolly TJ, Jaiswal N, Zaia J, Barry FP: Mesenchymal stem cell surface antigen SB-10 corresponds to activated leukocyte cell adhesion molecule and is involved in osteogenic differentiation. J Bone Miner Res 13: 655–663, 1998
Ohneda O, Ohneda K, Arai F, Lee J, Miyamoto T, Fukushima Y, Dowbenko D, Lasky LA, Suda T: ALCAM (CD166): Its role in hematopoietic and endothelial development. Blood 98: 2134–2142, 2001
Swart GW: Activated leukocyte cell adhesion molecule (CD166/ALCAM): Developmental and mechanistic aspects of cell clustering and cell migration. Eur J Cell Biol 81: 313–321, 2002
Zhang Y, Li C, Jiang X, Zhang S, Wu Y, Liu B, Tang P, Mao N: Human placenta-derived mesenchymal progenitor cells support culture expansion of long-term culture-initiating cells from cord blood CD34(+) cells. Exp Hematol 32: 657–664, 2004
Lee MW, Choi J, Yang MS, Moon YJ, Park JS, Kim HC, Kim YJ: Mesenchymal stem cells from cryopreserved human umbilical cord blood. Biochem Biophys Res Commun 320: 273–278, 2004
Sammons J, Ahmed N, El-Sheemy M, Hassan HT: he Role of BMP-6, IL-6, and BMP-4 in Mesenchymal Stem Cell-Dependent Bone Development: Effects on Osteoblastic Differentiation Induced by Parathyroid Hormone and Vitamin D(3). Stem Cells Dev 13: 273–280, 2004
Oswald J, Boxberger S, Jorgensen B, Feldmann S, Ehninger G, Bornhauser M, Werner C: Mesenchymal stem cells can be differentiated into endothelial cells in vitro. Stem Cells 22: 377-384, 2004
Alsalameh S, Amin R, Gemba T, Lotz M: Identification of mesenchymal progenitor cells in normal and osteoarthritic human articular cartilage. Arthritis Rheum 50: 1522–1532, 2004
Fickert S, Fiedler J, Brenner RE: Identification, quantification and isolation of mesenchymal progenitor cells from osteoarthritic synovium by fluorescence automated cell sorting. Osteoarthritis Cartilage 11: 790–800, 2003
in ‘t Anker PS, Noort WA, Scherjon SA, Kleijburg-van der Keur C, Kruisselbrink AB, van Bezooijen RL, Beekhuizen W, Willemze R, Kanhai HH, Fibbe WE: Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 88: 845–852, 2003
Kobune M, Kawano Y, Ito Y, Chiba H, Nakamura K, Tsuda H, Sasaki K, Dehari H, Uchida H, Honmou O, Takahashi S, Bizen A, Takimoto R, Matsunaga T, Kato J, Kato K, Houkin K, Niitsu Y, Hamada H: Telomerized human multipotent mesenchymal cells can differentiate into hematopoietic and cobblestone area-supporting cells. Exp Hematol 31: 715–722, 2003
Seshi B, Kumar S, Sellers D: Human bone marrow stromal cell: coexpression of markers specific for multiple mesenchymal cell lineages. Blood Cells Mol Dis 26: 234–246, 2000
Guo Z, Yang J, Liu X, Li X, Hou C, Tang PH, Mao N: Biological features of mesenchymal stem cells from human bone marrow. Chin Med J (Engl) 114: 950–953, 2001
Arai F, Ohneda O, Miyamoto T, Zhang XQ, Suda T: Mesenchymal stem cells in perichondrium express activated leukocyte cell adhesion molecule and participate in bone marrow formation. J Exp Med 195: 1549–1563, 2002
Gotherstrom C, Ringden O, Westgren M, Tammik C, Le Blanc K: Immunomodulatory effects of human foetal liver-derived mesenchymal stem cells Bone. Marrow Transplant 32: 265–272, 2003
Le Blanc K, Tammik L, Sundberg B, Haynesworth SE, Ringden O: Mesenchymal stem cells inhibit and stimulate mixed lymphocyte cultures and mitogenic responses independently of the major histocompatibility complex. Scand J Immunol 57: 11–20, 2003
Stewart K, Monk P, Walsh S, Jefferiss CM, Letchford J, Beresford JN: STRO-1, HOP-26 (CD63), CD49a and SB-10 (CD166) as markers of primitive human marrow stromal cells and their more differentiated progeny: a comparative investigation in vitro. Cell Tissue Res 313: 281–290, 2003
Fujiwara H, Tatsumi K, Kosaka K, Sato Y, Higuchi T, Yoshioka S, Maeda M, Ueda M, Fujii S: Human blastocysts and endometrial epithelial cells express activated leukocyte cell adhesion molecule (ALCAM/CD166). J Clin Endocrinol Metab 88: 3437–3443, 2003
Friedl P: Collective cell migration in morphogenesis and cancer. Int J Dev Biol 48: 2004 (in press)
Tomita K, van Bokhoven A, Jansen CF, Kiemeney LA, Karthaus HF, Vriesema J, Bussemakers MJ, Witjes A, Schalken JA: Activated Leukocyte Cell Adhesion Molecule (ALCAM) expression is associated with a poor prognosis for bladder cancer patients. UroOncology 3: 121–129, 2003
Ernst T, Hergenhahn M, Kenzelmann M, Cohen CD, Bonrouhi M, Weninger A, Klaren R, Grone EF, Wiesel M, Gudemann C, Kuster J, Schott W, Staehler G, Kretzler M, Hollstein M, Grone HJ: Decrease and gain of gene expression are equally discriminatory markers for prostate carcinoma: A gene expression analysis on total and microdissected prostate tissue. Am J Pathol 160: 2169–2180, 2002
Kristiansen G, Pilarsky C, Wissmann C, Stephan C, Weissbach L, Loy V, Loening S, Dietel M, Rosenthal A: ALCAM/CD166 is up-regulated in low-grade prostate cancer and progressively lost in high-grade lesions. Prostate 54: 34–43, 2003
Stamey TA, Warrington A, Caldwell MC, Chen Z, Fan Z, Mahadevappa M, McNeal JE, Nolley R, Zhang Z: Molecular genetic profiling of Gleason grade 4/5 prostate cancers compared to benign prostatic hyperplasia. J Urol 166: 2171–2177, 2001
King JA, Ofori-Acquah SF, Stevens T, Al-Mehdi AB, Fodstad O, Jiang WG: Activated leukocyte cell adhesion molecule in breast cancer: Prognostic indicator. Breast Cancer Res 6: R478–R487, 2004
Bowen MA, Aruffo AA, Bajorath J: Cell surface receptors and their ligands: in vitro analysis of CD6-CD166 interactions. Proteins 40: 420–428, 2000
Campbell IG, Foulkes WD, Senger G, Trowsdale J, Garin-Chesa P, Rettig WJ: Molecular cloning of the B-CAM cell surface glycoprotein of epithelial cancers: A novel member of the immunoglobulin superfamily. Cancer Res 54: 5761–5765, 1994
Parsons SF, Spring FA, Chasis JA, Anstee DJ: Erythroid cell adhesion molecules Lutheran and LW in health and disease. Baillieres Best Pract Res Clin Haematol 12: 729–745, 1999
van Kempen LC, Nelissen JM, Degen WG, Torensma R, Weidle UH, Bloemers HP, Figdor CG, Swart GW: Molecular basis for the homophilic activated leukocyte cell adhesion molecule (ALCAM)-ALCAM interaction. J Biol Chem 276: 25783–25790, 2001
Hassan NJ, Barclay AN, Brown MH: Frontline: Optimal T cell activation requires the engagement of CD6 and CD166. Eur J Immunol 34: 930–940, 2004
Tomita K, van Bokhoven A, Jansen CF, Bussemakers MJ, Schalken JA: Coordinate recruitment of E-cadherin and ALCAM to cell-cell contacts by alpha-catenin. Biochem Biophys Res Commun 267: 870–874, 2000
Umbas R, Isaacs WB, Bringuier PP, Xue Y, Debruyne FM, Schalken JA: Relation between aberrant alpha-catenin expression and loss of E-cadherin function in prostate cancer. Int J Cancer 74: 374–377, 1997
Richmond PJ, Karayiannakis AJ, Nagafuchi A, Kaisary AV, Pignatelli M: Aberrant E-cadherin and alpha-catenin expression in prostate cancer: correlation with patient survival. Cancer Res 57: 3189–3193, 1997
Nelissen JM, Peters IM, de Grooth BG, van Kooyk Y, Figdor CG: Dynamic regulation of activated leukocyte cell adhesion molecule-mediated homotypic cell adhesion through the actin cytoskeleton. Mol Biol Cell 11: 2057–2068, 2000
Zimmerman, AW, Nelissen, JM, Van Emst-De Vries, SE, Willems, PH, De Lange, F, Collard JG, Van Leeuwen FN, Figdor CG: Cytoskeletal restraints regulate homotypic ALCAM-mediated adhesion through PKC{alpha} independently of Rho-like GTPases. J Cell Sci 117: 2841–2852, 2004
Oka M, Kageshita T, Ono T, Goto A, Kuroki T, Ichihashi M: Protein kinase C alpha associates with phospholipase D1 and enhances basal phospholipase D activity in a protein phosphorylation-independent manner in human melanoma cells. J Invest Dermatol 121: 69–76, 2003
Pollock PM, Cohen-Solal K, Sood R, Namkoong J, Martino JJ, Koganti A, Zhu H, Robbins C, Makalowska I, Shin SS, Marin Y, Roberts KG, Yudt LM, Chen A, Cheng J, Incao A, Pinkett HW, Graham CL, Dunn K, Crespo-Carbone SM, Mackason KR, Ryan, KB, Sinsimer D, Goydos J, Reuhl KR, Eckhaus M, Meltzer PS, Pavan WJ, Trent JM, Chen S: Melanoma mouse model implicates metabotropic glutamate signaling in melanocytic neoplasia. Nat Genet 34: 108–112, 2003
Weeraratna AT, Jiang Y, Hostetter G, Rosenblatt K, Duray P, Bittner M, Trent JM: Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1: 279–288, 2002
Guasch RM, Scambler P, Jones GE, Ridley AJ: RhoE regulates actin cytoskeleton organization and cell migration. Mol Cell Biol 18: 4761–4771, 1998
Aresta S, de Tand-Heim MF, Beranger F, de Gunzburg J: A novel Rho GTPase-activating-protein interacts with Gem, a member of the Ras superfamily of GTPases. Biochem J 367: 57–65, 2002
Olson MF: Gem GTPase: Between a ROCK and a hard place. Curr Biol 12: R496–498, 2002
Riento K, Guasch RM, Garg R, Jin B, Ridley AJ: RhoE binds to ROCK I and inhibits downstream signaling. Mol Cell Biol 23: 4219–4229, 2003
Wennerberg K, Forget MA, Ellerbroek SM, Arthur WT, Burridge K, Settleman J, Der CJ, Hansen SH: Rnd proteins function as RhoA antagonists by activating p190 RhoGAP. Curr Biol 13: 1106–1115, 2003
van Kempen LC, Meier F, Egeblad M, Kersten-Niessen MJ, Garbe C, Weidle UH, Van Muijen GN, Herlyn M, Bloemers, HP, and Swart GW: Truncation of activated leukocyte cell adhesion molecule: A gateway to melanoma metastasis. J Invest Dermatol 122: 1293–1301, 2004
Degen WG, van Kempen LC, Gijzen EG, van Groningen JJ, van Kooyk Y, Bloemers HP, Swart GW: MEMD, a new cell adhesion molecule in metastasizing human melanoma cell lines, is identical to ALCAM (activated leukocyte cell adhesion molecule). Am J Pathol 152: 805–813, 1998
van Groningen JJ, Bloemers HP, Swart GW: Identification of melanoma inhibitory activity and other differentially expressed messenger RNAs in human melanoma cell lines with different metastatic capacity by messenger RNA differential display. Cancer Res 55: 6237–6243, 1995
Weterman MA, Stoopen GM, van Muijen GN, Kuznicki J, Ruiter DJ, Bloemers HP: Expression of calcyclin in human melanoma cell lines correlates with metastatic behavior in nude mice Cancer Res 52: 1291–1296, 1992
de Wit PE, Moretti S, Koenders PG, Weterman MA, van Muijen GN, Gianotti B, Ruiter DJ: Increasing epidermal growth factor receptor expression in human melanocytic tumor progression. J Invest Dermatol 99: 168–173, 1992
van Groningen JJ, Cornelissen TM, van Muijen GN, Bloemers HP, Swart GW: Simultaneous suppression of progression marker genes in the highly malignant human melanoma cell line BLM after transfection with the adenovirus-5 E1A gene. Biochem Biophys Res Commun 225: 808–816, 1996
Degen WG, Agterbos MA, Muyrers JP, Bloemers HP, Swart GW: MemA/DRS, a putative mediator of multiprotein complexes, is overexpressed in the metastasizing human melanoma cell lines BLM and MV3. Biochim Biophys Acta 1444: 384–394, 1999
Kunz M, Moeller S, Koczan D, Lorenz P, Wenger RH, Glocker MO, Thiesen HJ, Gross G, Ibrahim SM: Mechanisms of hypoxic gene regulation of angiogenesis factor Cyr61 in melanoma cells. J Biol Chem 278: 45651–45660, 2003
Quax PH, van Muijen GN, Weening-Verhoeff EJ, Lund LR, Dano K, Ruiter DJ, Verheijen JH: Metastatic behavior of human melanoma cell lines in nude mice correlates with urokinase-type plasminogen activator, its type-1 inhibitor, and urokinase-mediated matrix degradation. J Cell Biol 115: 191–199, 1991
de Vries TJ, Verheijen JH, de Bart AC, Weidle UH, Ruiter DJ, van Muijen GN: Decreased expression of both the low-density lipoprotein receptor-related protein/alpha(2)-macroglobulin receptor and its receptor-associated protein in late stages of cutaneous melanocytic tumor progression. Cancer Res 56: 1432–1439, 1996
van Groningen JJ, Klink SL, Bloemers HP, Swart GW: Expression of tissue-type transglutaminase correlates positively with metastatic properties of human melanoma cell lines. Int J Cancer 60: 383–387, 1995
Weterman MA, van Muijen GN, Ruiter DJ, Bloemers HP: Thymosin beta-10 expression in melanoma cell lines and melanocytic lesions: a new progression marker for human cutaneous melanoma. Int J Cancer 53: 278–284, 1993
Kunz M, Hartmann A, Flory E, Toksoy A, Koczan D, Thiesen HJ, Mukaida N, Neumann M, Rapp UR, Brocker EB, Gillitzer R: Anoxia-induced up-regulation of interleukin-8 in human malignant melanoma A potential mechanism for high tumor aggressiveness. Am J Pathol 155: 753–763, 1999
Kurschat P, Zigrino P, Nischt R, Breitkopf K, Steurer P, Klein CE, Krieg T, Mauch C: Tissue inhibitor of matrix metalloproteinase-2 regulates matrix metalloproteinase-2 activation by modulation of membrane-type 1 matrix metalloproteinase activity in high and low invasive melanoma cell lines. J Biol Chem 274: 21056–21062, 1999
Hofmann UB, Westphal JR, Waas ET, Zendman AJ, Cornelissen IM, Ruiter DJ, van Muijen GN: Matrix metalloproteinases in human melanoma cell lines and xenografts: increased expression of activated matrix metalloproteinase-2 (MMP-2) correlates with melanoma progression. Br J Cancer 81: 774–782, 1999
Zendman AJ, Cornelissen IM, Weidle UH, Ruiter DJ, van Muijen GN: CTp11, a novel member of the family of human cancer/testis antigens. Cancer Res 59: 6223–6229, 1999
Danen EH, van Muijen GN, van de Wiel-van Kemenade E, Jansen KF, Ruiter DJ, Figdor CG: Regulation of integrin-mediated adhesion to laminin and collagen in human melanocytes and in non-metastatic and highly metastatic human melanoma cells. Int J Cancer 54: 315–321, 1993
Manten-Horst E, Danen EH, Smit L, Snoek M, Le Poole IC, Van Muijen GN, Pals ST, Ruiter DJ: Expression of CD44 splice variants in human cutaneous melanoma and melanoma cell lines is related to tumor progression and metastatic potential. Int J Cancer 64: 182–188, 1995
Robledo MM, Bartolome RA, Longo N, Rodriguez-Frade JM, Mellado M, Longo I, van Muijen GN, Sanchez-Mateos P, Teixido J: Expression of functional chemokine receptors CXCR3 and CXCR4 on human melanoma cells. J Biol Chem 276: 45098–45105, 2001
Degen WG, Weterman MA, van Groningen JJ, Cornelissen IM, Lemmers JP, Agterbos MA, Geurts van Kessel A, Swart GW, Bloemers HP: Expression of nma, a novel gene, inversely correlates with the metastatic potential of human melanoma cell lines and xenografts. Int J Cancer 65: 460–465, 1996
Weterman MA, Ajubi N, van Dinter IM, Degen WG, van Muijen GN, Ruitter DJ, Bloemers HP: Nmb, a novel gene, is expressed in low-metastatic human melanoma cell lines and xenografts. Int J Cancer 60: 73–81, 1995
van Groningen JJ, Egmond MR, Bloemers HP, Swart GW: Nmd, a novel gene differentially expressed in human melanoma cell lines, encodes a new atypical member of the enzyme family of lipases. FEBS Lett 404: 82–86, 1997
Zendman AJ, Cornelissen IM, Weidle UH, Ruiter DJ, van Muijen GN: TM7XN1, a novel human EGF-TM7-like cDNA, detected with mRNA differential display using human melanoma cell lines with different metastatic potential. FEBS Lett 446: 292–298, 1999
Danen EH, Jansen KF, Van Kraats AA, Cornelissen IM, Ruiter DJ, Van Muijen GN: Alpha v-integrins in human melanoma: Gain of alpha v beta 3 and loss of alpha v beta 5 are related to tumor progression in situ but not to metastatic capacity of cell lines in nude mice. Int J Cancer 61: 491–496, 1995
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Swart, G.W.M., Lunter, P.C., Kilsdonk, J.W.J.v. et al. Activated leukocyte cell adhesion molecule (ALCAM/CD166): Signaling at the divide of melanoma cell clustering and cell migration?. Cancer Metastasis Rev 24, 223–236 (2005). https://doi.org/10.1007/s10555-005-1573-0
Issue Date:
DOI: https://doi.org/10.1007/s10555-005-1573-0