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(American Journal of Pathology. 1999;155:739-752.)
© 1999 American Society for Investigative Pathology

Regular Articles

Vascular Channel Formation by Human Melanoma Cells in Vivo and in Vitro: Vasculogenic Mimicry

Andrew J. Maniotis*{dagger}, Robert Folberg{dagger}{ddagger}§, Angela Hess*, Elisabeth A. Seftor*{dagger}, Lynn M.G. Gardner{ddagger}, Jacob Pe'er, Jeffrey M. Trent||, Paul S. Meltzer|| and Mary J. C. Hendrix*{dagger}

From the Departments of Anatomy and Cell Biology,*
University of Iowa Cancer Center,{dagger}
and the Departments of Ophthalmology and Visual Sciences{ddagger}
and Pathology,§
University of Iowa College of Medicine, Iowa City, Iowa; the Department of Ophthalmology,
Hadassah University Hospital, Jerusalem, Israel; and the Cancer Genetics Branch, National Human Genome Research Institute, National Institutes of Health, Bethesda, Maryland||

Tissue sections from aggressive human intraocular (uveal) and metastatic cutaneous melanomas generally lack evidence of significant necrosis and contain patterned networks of interconnected loops of extracellular matrix. The matrix that forms these loops or networks may be solid or hollow. Red blood cells have been detected within the hollow channel components of this patterned matrix histologically, and these vascular channel networks have been detected in human tumors angiographically. Endothelial cells were not identified within these matrix-embedded channels by light microscopy, by transmission electron microscopy, or by using an immunohistochemical panel of endothelial cell markers (Factor VIII-related antigen, Ulex, CD31, CD34, and KDR[Flk-1]). Highly invasive primary and metastatic human melanoma cells formed patterned solid and hollow matrix channels (seen in tissue sections of aggressive primary and metastatic human melanomas) in three-dimensional cultures containing Matrigel or dilute Type I collagen, without endothelial cells or fibroblasts. These tumor cell-generated patterned channels conducted dye, highlighting looping patterns visualized angiographically in human tumors. Neither normal melanocytes nor poorly invasive melanoma cells generated these patterned channels in vitro under identical culture conditions, even after the addition of conditioned medium from metastatic pattern-forming melanoma cells, soluble growth factors, or regimes of hypoxia. Highly invasive and metastatic human melanoma cells, but not poorly invasive melanoma cells, contracted and remodeled floating hydrated gels, providing a biomechanical explanation for the generation of microvessels in vitro. cDNA microarray analysis of highly invasive versus poorly invasive melanoma tumor cells confirmed a genetic reversion to a pluripotent embryonic-like genotype in the highly aggressive melanoma cells. These observations strongly suggest that aggressive melanoma cells may generate vascular channels that facilitate tumor perfusion independent of tumor angiogenesis.




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M. Herlyn, M. Padarathsingh, L. Chin, M. Hendrix, D. Becker, M. Nelson, Y. DeClerck, J. McCarthy, and S. Mohla
New Approaches to the Biology of Melanoma: A Workshop of the National Institutes of Health Pathology B Study Section
Am. J. Pathol., November 1, 2002; 161(5): 1949 - 1957.
[Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
R. E. B. Seftor, E. A. Seftor, D. A. Kirschmann, and M. J. C. Hendrix
Targeting the Tumor Microenvironment with Chemically Modified Tetracyclines: Inhibition of Laminin 5 {gamma}2 Chain Promigratory Fragments and Vasculogenic Mimicry
Mol. Cancer Ther., November 1, 2002; 1(13): 1173 - 1179.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
C. Liu, H. Huang, F. Donate, C. Dickinson, R. Santucci, A. El-Sheikh, R. Vessella, and T. S. Edgington
Prostate-specific Membrane Antigen Directed Selective Thrombotic Infarction of Tumors
Cancer Res., October 1, 2002; 62(19): 5470 - 5475.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
J. Favier, P.-F. Plouin, P. Corvol, and J.-M. Gasc
Angiogenesis and Vascular Architecture in Pheochromocytomas : Distinctive Traits in Malignant Tumors
Am. J. Pathol., October 1, 2002; 161(4): 1235 - 1246.
[Abstract] [Full Text] [PDF]

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 JCOHome page
F. A. Scappaticci
Mechanisms and Future Directions for Angiogenesis-Based Cancer Therapies
J. Clin. Oncol., September 15, 2002; 20(18): 3906 - 3927.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
R. D. Braun, A. Abbas, S. O. Bukhari, and W. Wilson III
Hemodynamic Parameters in Blood Vessels in Choroidal Melanoma Xenografts and Rat Choroid
Invest. Ophthalmol. Vis. Sci., September 1, 2002; 43(9): 3045 - 3052.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
W. C. Zamboni, A. C. Gervais, M. J. Egorin, J. H. M. Schellens, D. R. Hamburger, B. J. Delauter, A. Grim, E. G. Zuhowski, E. Joseph, D. Pluim, et al.
Inter- and Intratumoral Disposition of Platinum in Solid Tumors after Administration of Cisplatin
Clin. Cancer Res., September 1, 2002; 8(9): 2992 - 2999.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
N. Jessani, Y. Liu, M. Humphrey, and B. F. Cravatt
Enzyme activity profiles of the secreted and membrane proteome that depict cancer cell invasiveness
PNAS, August 6, 2002; 99(16): 10335 - 10340.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
X. Chen, A. J. Maniotis, D. Majumdar, J. Pe'er, and R. Folberg
Uveal Melanoma Cell Staining for CD34 and Assessment of Tumor Vascularity
Invest. Ophthalmol. Vis. Sci., August 1, 2002; 43(8): 2533 - 2539.
[Abstract] [Full Text] [PDF]

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 JEMHome page
H. Y. Wang, J. Zhou, K. Zhu, A. I. Riker, F. M. Marincola, and R.-F. Wang
Identification of a Mutated Fibronectin As a Tumor Antigen Recognized by CD4+T Cells: Its Role in Extracellular Matrix Formation and Tumor Metastasis
J. Exp. Med., June 3, 2002; 195(11): 1397 - 1406.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
J. K. L. Woodward, C. E. Nichols, I. G. Rennie, M. A. Parsons, A. K. Murray, and K. Sisley
An In Vitro Assay to Assess Uveal Melanoma Invasion across Endothelial and Basement Membrane Barriers
Invest. Ophthalmol. Vis. Sci., June 1, 2002; 43(6): 1708 - 1714.
[Abstract] [Full Text] [PDF]

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 JCOHome page
A. Thies, I. Moll, J. Berger, C. Wagener, J. Brummer, H.-J. Schulze, G. Brunner, and U. Schumacher
CEACAM1 Expression in Cutaneous Malignant Melanoma Predicts the Development of Metastatic Disease
J. Clin. Oncol., May 15, 2002; 20(10): 2530 - 2536.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
K. Carles-Kinch, K. E. Kilpatrick, J. C. Stewart, and M. S. Kinch
Antibody Targeting of the EphA2 Tyrosine Kinase Inhibits Malignant Cell Behavior
Cancer Res., May 1, 2002; 62(10): 2840 - 2847.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
R. Clarijs, I. Otte-Holler, D. J. Ruiter, and R. M. W. de Waal
Presence of a Fluid-Conducting Meshwork in Xenografted Cutaneous and Primary Human Uveal Melanoma
Invest. Ophthalmol. Vis. Sci., April 1, 2002; 43(4): 912 - 918.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
O. Straume and L. A. Akslen
Importance of Vascular Phenotype by Basic Fibroblast Growth Factor, and Influence of the Angiogenic Factors Basic Fibroblast Growth Factor/Fibroblast Growth Factor Receptor-1 and Ephrin-A1/EphA2 on Melanoma Progression
Am. J. Pathol., March 1, 2002; 160(3): 1009 - 1019.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
M. J. C. Hendrix, R. E. B. Seftor, E. A. Seftor, L. M. Gruman, L. M. L. Lee, B. J. Nickoloff, L. Miele, D. D. Sheriff, and G. C. Schatteman
Transendothelial Function of Human Metastatic Melanoma Cells: Role of the Microenvironment in Cell-Fate Determination
Cancer Res., February 1, 2002; 62(3): 665 - 668.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H. Kobayashi, K. Shirakawa, S. Kawamoto, T. Saga, N. Sato, A. Hiraga, I. Watanabe, Y. Heike, K. Togashi, J. Konishi, et al.
Rapid Accumulation and Internalization of Radiolabeled Herceptin in an Inflammatory Breast Cancer Xenograft with Vasculogenic Mimicry Predicted by the Contrast-enhanced Dynamic MRI with the Macromolecular Contrast Agent G6-(1B4M-Gd)256
Cancer Res., February 1, 2002; 62(3): 860 - 866.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
D. Dai, D. M. Wolf, E. S. Litman, M. J. White, and K. K. Leslie
Progesterone Inhibits Human Endometrial Cancer Cell Growth and Invasiveness: Down-Regulation of Cellular Adhesion Molecules through Progesterone B Receptors
Cancer Res., February 1, 2002; 62(3): 881 - 886.
[Abstract] [Full Text] [PDF]

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 Reproductive SciencesHome page
A. K. Sood, M. S. Fletcher, and M. J. C. Hendrix
The Embryonic-Like Properties of Aggressive Human Tumor Cells
Reproductive Sciences, January 1, 2002; 9(1): 2 - 9.
[Abstract] [PDF]

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 Cancer Res.Home page
K. Shirakawa, H. Kobayashi, Y. Heike, S. Kawamoto, M. W. Brechbiel, F. Kasumi, T. Iwanaga, F. Konishi, M. Terada, and H. Wakasugi
Hemodynamics in Vasculogenic Mimicry and Angiogenesis of Inflammatory Breast Cancer Xenograft
Cancer Res., January 1, 2002; 62(2): 560 - 566.
[Abstract] [Full Text] [PDF]

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 BloodHome page
N. Longo, M. Yanez-Mo, M. Mittelbrunn, G. de la Rosa, M.-L. Munoz, F. Sanchez-Madrid, and P. Sanchez-Mateos
Regulatory role of tetraspanin CD9 in tumor-endothelial cell interaction during transendothelial invasion of melanoma cells
Blood, December 15, 2001; 98(13): 3717 - 3726.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
N. D. Zantek, J. Walker-Daniels, J. Stewart, R. K. Hansen, D. Robinson, H. Miao, B. Wang, H.-J. Kung, M. J. Bissell, and M. S. Kinch
MCF-10A-NeoST: A New Cell System for Studying Cell-ECM and Cell-Cell Interactions in Breast Cancer
Clin. Cancer Res., November 1, 2001; 7(11): 3640 - 3648.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
T. Makitie, O. Carpen, A. Vaheri, and T. Kivela
Ezrin as a Prognostic Indicator and Its Relationship to Tumor Characteristics in Uveal Malignant Melanoma
Invest. Ophthalmol. Vis. Sci., October 1, 2001; 42(11): 2442 - 2449.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
A. G. M. Scholes, T. Liloglou, P. Maloney, S. Hagan, J. Nunn, P. Hiscott, B. E. Damato, I. Grierson, and J. K. Field
Loss of Heterozygosity on Chromosomes 3, 9, 13, and 17, Including the Retinoblastoma Locus, in Uveal Melanoma
Invest. Ophthalmol. Vis. Sci., October 1, 2001; 42(11): 2472 - 2477.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
U. Graeven, U. Rodeck, S. Karpinski, M. Jost, S. Philippou, and W. Schmiegel
Modulation of Angiogenesis and Tumorigenicity of Human Melanocytic Cells by Vascular Endothelial Growth Factor and Basic Fibroblast Growth Factor
Cancer Res., October 1, 2001; 61(19): 7282 - 7290.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
R. E. B. Seftor, E. A. Seftor, N. Koshikawa, P. S. Meltzer, L. M. G. Gardner, M. Bilban, W. G. Stetler-Stevenson, V. Quaranta, and M. J. C. Hendrix
Cooperative Interactions of Laminin 5 {gamma}2 Chain, Matrix Metalloproteinase-2, and Membrane Type-1-Matrix/Metalloproteinase Are Required for Mimicry of Embryonic Vasculogenesis by Aggressive Melanoma
Cancer Res., September 1, 2001; 61(17): 6322 - 6327.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. W. Nam, T. Clair, Y.-S. Kim, A. McMarlin, E. Schiffmann, L. A. Liotta, and M. L. Stracke
Autotaxin (NPP-2), a Metastasis-enhancing Motogen, Is an Angiogenic Factor
Cancer Res., September 1, 2001; 61(18): 6938 - 6944.
[Abstract] [Full Text] [PDF]

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 Arch DermatolHome page
M. Kashani-Sabet, R. W. Sagebiel, C. M. M. Ferreira, M. Nosrati, and J. R. Miller III
Vascular Involvement in the Prognosis of Primary Cutaneous Melanoma
Arch Dermatol, September 1, 2001; 137(9): 1169 - 1173.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
T. Kivela, S. Eskelin, T. Makitie, and P. Summanen
Exudative Retinal Detachment from Malignant Uveal Melanoma: Predictors and Prognostic Significance
Invest. Ophthalmol. Vis. Sci., August 1, 2001; 42(9): 2085 - 2093.
[Abstract] [Full Text] [PDF]

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 Stem CellsHome page
M. Harraz, C. Jiao, H. D. Hanlon, R. S. Hartley, and G. C. Schatteman
CD34- Blood-Derived Human Endothelial Cell Progenitors
Stem Cells, July 1, 2001; 19(4): 304 - 312.
[Abstract] [Full Text] [PDF]

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 Am. J. Pathol.Home page
O. Straume and L. A. Akslen
Expresson of Vascular Endothelial Growth Factor, Its Receptors (FLT-1, KDR) and TSP-1 Related to Microvessel Density and Patient Outcome in Vertical Growth Phase Melanomas
Am. J. Pathol., July 1, 2001; 159(1): 223 - 235.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
M. J. C. Hendrix, E. A. Seftor, P. S. Meltzer, L. M. G. Gardner, A. R. Hess, D. A. Kirschmann, G. C. Schatteman, and R. E. B. Seftor
Expression and functional significance of VE-cadherin in aggressive human melanoma cells: Role in vasculogenic mimicry
PNAS, June 12, 2001; (2001) 131209798.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
T. Mäkitie, P. Summanen, A. Tarkkanen, and T. Kivelä
Tumor-Infiltrating Macrophages (CD68+ Cells) and Prognosis in Malignant Uveal Melanoma
Invest. Ophthalmol. Vis. Sci., June 1, 2001; 42(7): 1414 - 1421.
[Abstract] [Full Text]

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 IOVSHome page
R. Clarijs, L. Schalkwijk, D. J. Ruiter, and R. M. W. de Waal
Lack of Lymphangiogenesis Despite Coexpression of VEGF-C and Its Receptor Flt-4 in Uveal Melanoma
Invest. Ophthalmol. Vis. Sci., June 1, 2001; 42(7): 1422 - 1428.
[Abstract] [Full Text]

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 Cancer Res.Home page
C. Khanna, J. Khan, P. Nguyen, J. Prehn, J. Caylor, C. Yeung, J. Trepel, P. Meltzer, and L. Helman
Metastasis-associated Differences in Gene Expression in a Murine Model of Osteosarcoma
Cancer Res., May 1, 2001; 61(9): 3750 - 3759.
[Abstract] [Full Text]

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 Arch OphthalmolHome page
The Collaborative Ocular Melanoma Study Group
Assessment of Metastatic Disease Status at Death in 435 Patients With Large Choroidal Melanoma in the Collaborative Ocular Melanoma Study (COMS): COMS Report No. 15
Arch Ophthalmol, May 1, 2001; 119(5): 670 - 676.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
A. R. Hess, E. A. Seftor, L. M. G. Gardner, K. Carles-Kinch, G. B. Schneider, R. E. B. Seftor, M. S. Kinch, and M. J. C. Hendrix
Molecular Regulation of Tumor Cell Vasculogenic Mimicry by Tyrosine Phosphorylation: Role of Epithelial Cell Kinase (Eck/EphA2)
Cancer Res., April 1, 2001; 61(8): 3250 - 3255.
[Abstract] [Full Text]

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 Am. J. Pathol.Home page
A. K. Sood, E. A. Seftor, M. S. Fletcher, L. M. G. Gardner, P. M. Heidger, R. E. Buller, R. E. B. Seftor, and M. J. C. Hendrix
Molecular Determinants of Ovarian Cancer Plasticity
Am. J. Pathol., April 1, 2001; 158(4): 1279 - 1288.
[Abstract] [Full Text] [PDF]

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 Arch OphthalmolHome page
A. G. M. Scholes, S. Hagan, P. Hiscott, B. E. Damato, and I. Grierson
Overexpression of Epidermal Growth Factor Receptor Restricted to Macrophages in Uveal Melanoma
Arch Ophthalmol, March 1, 2001; 119(3): 373 - 377.
[Abstract] [Full Text] [PDF]


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