help button home button Am J Pathol R & D Systems
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS

This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Purchase Article
Right arrow View Shopping Cart
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrow reprints & permissions
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Folberg, R.
Right arrow Articles by Maniotis, A. J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Folberg, R.
Right arrow Articles by Maniotis, A. J.
(American Journal of Pathology. 2000;156:361-381.)
© 2000 American Society for Investigative Pathology

Review

Vasculogenic Mimicry and Tumor Angiogenesis

Robert Folberg*{dagger}, Mary J. C. Hendrix{ddagger}§ and Andrew J. Maniotis{ddagger}§

From the Departments of Pathology*
and Ophthalmology,{dagger}
the University of Illinois at Chicago, Chicago, Illinois; and the University of Iowa Cancer Center{ddagger}
and Department of Anatomy and Cell Biology,§
The University of Iowa College of Medicine, Iowa City, Iowa

Tumors require a blood supply for growth and hematogenous dissemination. Much attention has been focused on the role of angiogenesis—the recruitment of new vessels into a tumor from pre-existing vessels. However, angiogenesis may not be the only mechanism by which tumors acquire a microcirculation. Highly aggressive and metastatic melanoma cells are capable of forming highly patterned vascular channels in vitro that are composed of a basement membrane that stains positive with the periodic acid-Schiff (PAS) reagent in the absence of endothelial cells and fibroblasts. These channels formed in vitro are identical morphologically to PAS-positive channels in histological preparations from highly aggressive primary uveal melanomas, in the vertical growth phase of cutaneous melanomas, and in metastatic uveal and cutaneous melanoma. The generation of microvascular channels by genetically deregulated, aggressive tumor cells was termed "vasculogenic mimicry" to emphasize their de novo generation without participation by endothelial cells and independent of angiogenesis. Techniques designed to identify the tumor microcirculation by the staining of endothelial cells may not be applicable to tumors that express vasculogenic mimicry. Although it is not known if therapeutic strategies targeting endothelial cells will be effective in tumors whose blood supply is formed by tumor cells in the absence of angiogenesis, the biomechanical and molecular events that regulate vasculogenic mimicry provide opportunities for the development of novel forms of tumor-targeted treatments. The unique patterning characteristic of vasculogenic mimicry provides an opportunity to design noninvasive imaging techniques to detect highly aggressive neoplasms and their metastases.




This article has been cited by other articles:


Home page
 J. Immunol.Home page
K. Hallermalm, K. Seki, A. De Geer, B. Motyka, R. C. Bleackley, M. J. Jager, C. J. Froelich, R. Kiessling, V. Levitsky, and J. Levitskaya
Modulation of the Tumor Cell Phenotype by IFN-{gamma} Results in Resistance of Uveal Melanoma Cells to Granule-Mediated Lysis by Cytotoxic Lymphocytes
J. Immunol., March 15, 2008; 180(6): 3766 - 3774.
[Abstract] [Full Text] [PDF]

Home page
 Exp. Biol. Med.Home page
B. Sun, S. Zhang, D. Zhang, X. Yin, S. Wang, Y. Gu, and Y. Wang
Doxycycline Influences Microcirculation Patterns in B16 Melanoma
Experimental Biology and Medicine, November 1, 2007; 232(10): 1300 - 1307.
[Abstract] [Full Text] [PDF]

Home page
 Cancer Res.Home page
L. W. Horton, Y. Yu, S. Zaja-Milatovic, R. M. Strieter, and A. Richmond
Opposing Roles of Murine Duffy Antigen Receptor for Chemokine and Murine CXC Chemokine Receptor-2 Receptors in Murine Melanoma Tumor Growth
Cancer Res., October 15, 2007; 67(20): 9791 - 9799.
[Abstract] [Full Text] [PDF]

Home page
 IOVSHome page
T. Meir, M. Zeschnigk, L. Masshofer, J. Pe'er, and I. Chowers
The Spatial Distribution of Monosomy 3 and Network Vasculogenic Mimicry Patterns in Uveal Melanoma
Invest. Ophthalmol. Vis. Sci., May 1, 2007; 48(5): 1918 - 1922.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Pathol.Home page
G. P. Robertson
Mig-7 Linked to Vasculogenic Mimicry
Am. J. Pathol., May 1, 2007; 170(5): 1454 - 1456.
[Full Text] [PDF]

Home page
 Am. J. Pathol.Home page
A. P. Petty, K. L. Garman, V. D. Winn, C. M. Spidel, and J. S. Lindsey
Overexpression of Carcinoma and Embryonic Cytotrophoblast Cell-Specific Mig-7 Induces Invasion and Vessel-Like Structure Formation
Am. J. Pathol., May 1, 2007; 170(5): 1763 - 1780.
[Abstract] [Full Text] [PDF]

Home page
 Cancer Res.Home page
G. C. Prendergast and E. M. Jaffee
Cancer Immunologists and Cancer Biologists: Why We Didn't Talk Then but Need to Now
Cancer Res., April 15, 2007; 67(8): 3500 - 3504.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Pathol.Home page
R. Folberg, Z. Arbieva, J. Moses, A. Hayee, T. Sandal, S. Kadkol, A. Y. Lin, K. Valyi-Nagy, S. Setty, L. Leach, et al.
Tumor Cell Plasticity in Uveal Melanoma: Microenvironment Directed Dampening of the Invasive and Metastatic Genotype and Phenotype Accompanies the Generation of Vasculogenic Mimicry Patterns
Am. J. Pathol., October 1, 2006; 169(4): 1376 - 1389.
[Abstract] [Full Text] [PDF]

Home page
 IOVSHome page
S. S. Kadkol, A. Y. Lin, V. Barak, I. Kalickman, L. Leach, K. Valyi-Nagy, D. Majumdar, S. Setty, A. J. Maniotis, R. Folberg, et al.
Osteopontin expression and serum levels in metastatic uveal melanoma: a pilot study.
Invest. Ophthalmol. Vis. Sci., March 1, 2006; 47(3): 802 - 806.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Pathol.Home page
M. Anghelina, P. Krishnan, L. Moldovan, and N. I. Moldovan
Monocytes/Macrophages Cooperate with Progenitor Cells during Neovascularization and Tissue Repair: Conversion of Cell Columns into Fibrovascular Bundles
Am. J. Pathol., February 1, 2006; 168(2): 529 - 541.
[Abstract] [Full Text] [PDF]

Home page
 IOVSHome page
R. D. Braun and A. Abbas
Orthotopic Human Choroidal Melanoma Xenografts in Nude Rats with Aggressive and Nonaggressive PAS Staining Patterns
Invest. Ophthalmol. Vis. Sci., January 1, 2006; 47(1): 7 - 16.
[Abstract] [Full Text] [PDF]

Home page
 Endocr Relat CancerHome page
A. Bagnato, F. Spinella, and L. Rosano
Emerging role of the endothelin axis in ovarian tumor progression
Endocr. Relat. Cancer, December 1, 2005; 12(4): 761 - 772.
[Abstract] [Full Text] [PDF]

Home page
 Arch OphthalmolHome page
M. R. Hussein, A. K. Haemel, D. M. Albert, and G. S. Wood
Microsatellite Instability and Alterations of Mismatch Repair Protein Expression in Choroidal Melanomas
Arch Ophthalmol, December 1, 2005; 123(12): 1705 - 1711.
[Abstract] [Full Text] [PDF]

Home page
 Cancer Res.Home page
A. R. Hess, L.-M. Postovit, N. V. Margaryan, E. A. Seftor, G. B. Schneider, R. E.B. Seftor, B. J. Nickoloff, and M. J.C. Hendrix
Focal Adhesion Kinase Promotes the Aggressive Melanoma Phenotype
Cancer Res., November 1, 2005; 65(21): 9851 - 9860.
[Abstract] [Full Text] [PDF]

Home page
 IOVSHome page
R. Clarijs, M. van Dijk, D. J. Ruiter, and R. M. W. de Waal
Functional and Morphologic Analysis of the Fluid-Conducting Meshwork in Xenografted Cutaneous and Primary Uveal Melanoma
Invest. Ophthalmol. Vis. Sci., September 1, 2005; 46(9): 3013 - 3020.
[Abstract] [Full Text] [PDF]

Home page
 J. Histochem. Cytochem.Home page
W.-Y. Yue and Z.-P. Chen
Does Vasculogenic Mimicry Exist in Astrocytoma?
J. Histochem. Cytochem., August 1, 2005; 53(8): 997 - 1002.
[Abstract] [Full Text] [PDF]

Home page
 Cancer Res.Home page
D. Ponti, A. Costa, N. Zaffaroni, G. Pratesi, G. Petrangolini, D. Coradini, S. Pilotti, M. A. Pierotti, and M. G. Daidone
Isolation and In vitro Propagation of Tumorigenic Breast Cancer Cells with Stem/Progenitor Cell Properties
Cancer Res., July 1, 2005; 65(13): 5506 - 5511.
[Abstract] [Full Text] [PDF]

Home page
 JCOHome page
B. P. Schneider and K. D. Miller
Angiogenesis of Breast Cancer
J. Clin. Oncol., March 10, 2005; 23(8): 1782 - 1790.
[Full Text] [PDF]

Home page
 BloodHome page
K. Podar and K. C. Anderson
The pathophysiologic role of VEGF in hematologic malignancies: therapeutic implications
Blood, February 15, 2005; 105(4): 1383 - 1395.
[Abstract] [Full Text] [PDF]

Home page
 J. Clin. Pathol.Home page
J Laitakari, V Nayha, and F Stenback
Size, shape, structure, and direction of angiogenesis in laryngeal tumour development
J. Clin. Pathol., April 1, 2004; 57(4): 394 - 401.
[Abstract] [Full Text] [PDF]

Home page
 Am. J. Pathol.Home page
C. Lugassy, H. K. Kleinman, J. A. Engbring, D. R. Welch, J. F. Harms, R. Rufner, G. Ghanem, S. R. Patierno, and R. L. Barnhill
Pericyte-Like Location of GFP-Tagged Melanoma Cells: Ex Vivo and In Vivo Studies of Extravascular Migratory Metastasis
Am. J. Pathol., April 1, 2004; 164(4): 1191 - 1198.
[Abstract] [Full Text] [PDF]

Home page
 BloodHome page
A. Vacca, R. Ria, F. Semeraro, F. Merchionne, M. Coluccia, A. Boccarelli, C. Scavelli, B. Nico, A. Gernone, F. Battelli, et al.
Endothelial cells in the bone marrow of patients with multiple myeloma
Blood, November 1, 2003; 102(9): 3340 - 3348.
[Abstract] [Full Text] [PDF]

Home page
 Cancer Res.Home page
W. Ruf, E. A. Seftor, R. J. Petrovan, R. M. Weiss, L. M. Gruman, N. V. Margaryan, R. E. B. Seftor, Y. Miyagi, and M. J. C. Hendrix
Differential Role of Tissue Factor Pathway Inhibitors 1 and 2 in Melanoma Vasculogenic Mimicry
Cancer Res., September 1, 2003; 63(17): 5381 - 5389.
[Abstract] [Full Text] [PDF]

Home page
 Toxicol PatholHome page
V. Nayha, J. Laitakari, and F. Stenback
Stage-Dependent Expression of an Angiogenic Agent and Vascular Organization in Experimental Skin Tumor Development
Toxicol Pathol, August 1, 2003; 31(5): 539 - 548.
[Abstract] [PDF]

Home page
 IOVSHome page
R.'a T. Al-Jamal, T. Makitie, and T. Kivela
Nucleolar Diameter and Microvascular Factors as Independent Predictors of Mortality from Malignant Melanoma of the Choroid and Ciliary Body
Invest. Ophthalmol. Vis. Sci., June 1, 2003; 44(6): 2381 - 2389.
[Abstract] [Full Text] [PDF]

Home page
 Ann OncolHome page
K. D. Miller, C. J. Sweeney, and G. W. Sledge
The Snark is a Boojum: the continuing problem of drug resistance in the antiangiogenic era
Ann. Onc., January 1, 2003; 14(1): 20 - 28.
[Abstract] [Full Text] [PDF]

Home page
 J. Histochem. Cytochem.Home page
Y.-J. Lee, N. Nagai, C.-H. Siar, K. Nakano, H. Nagatsuka, H. Tsujigiwa, C.-H. Roan, and M. Gunduz
Angioarchitecture of Primary Oral Malignant Melanomas
J. Histochem. Cytochem., November 1, 2002; 50(11): 1555 - 1562.
[Abstract] [Full Text] [PDF]

Home page
 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]

Home page
 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]

Home page
 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]

Home page
 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]

Home page
 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]

Home page
 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]

Home page
 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]

Home page
 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]

Home page
 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]

Home page
 Sci SignalHome page
T. Matsumoto and L. Claesson-Welsh
VEGF Receptor Signal Transduction
Sci. Signal., December 11, 2001; 2001(112): re21 - re21.
[Abstract] [Full Text] [PDF]

Home page
 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]

Home page
 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]

Home page
 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]

Home page
 JNCI J Natl Cancer InstHome page
H. K. Kleinman and G. Liau
Gene Therapy for Antiangiogenesis
J Natl Cancer Inst, July 4, 2001; 93(13): 965 - 967.
[Full Text] [PDF]

Home page
 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]

Home page
 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]

Home page
 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]

Home page
 Cancer Res.Home page
T. E. Konopka, J. E. Barker, T. L. Bamford, E. Guida, R. L. Anderson, and A. G. Stewart
Nitric Oxide Synthase II Gene Disruption: Implications for Tumor Growth and Vascular Endothelial Growth Factor Production
Cancer Res., April 1, 2001; 61(7): 3182 - 3187.
[Abstract] [Full Text]

Home page
 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]

Home page
 Clin. Cancer Res.Home page
M. A. Warso, A. J. Maniotis, X. Chen, D. Majumdar, M. K. Patel, A. Shilkaitis, T. K. Das Gupta, and R. Folberg
Prognostic Significance of Periodic Acid-Schiff-positive Patterns in Primary Cutaneous Melanoma
Clin. Cancer Res., March 1, 2001; 7(3): 473 - 477.
[Abstract] [Full Text]

Home page
 Cardiovasc ResHome page
E. M. Conway, D. Collen, and P. Carmeliet
Molecular mechanisms of blood vessel growth
Cardiovasc Res, February 16, 2001; 49(3): 507 - 521.
[Full Text] [PDF]

Home page
 Circ. Res.Home page
M. P. Bendeck
Mining the Myocardium With Macrophage Drills : A Novel Mechanism for Revascularization
Circ. Res., September 1, 2000; 87(5): 341 - 343.
[Full Text] [PDF]

Home page
 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, July 3, 2001; 98(14): 8018 - 8023.
[Abstract] [Full Text] [PDF]


HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
Copyright © 2000 by the American Society for Investigative Pathology.