Could pericytic mimicry represent another type of melanoma cell plasticity with embryonic properties?

Pigment Cell and Melanoma Research

Volumn 26, Issue 5, 2013, Pages 746-754

  Lugassy, Claire ^a   Péault, Bruno ^b,c   Wadehra, Madhuri ^a   Kleinman, Hynda K ^d   Barnhill, Raymond L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UCLA MEDICAL CENTER   (United States)

^d NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

Abluminal vascular surface; Angiotropism; Extravascular migratory metastasis (EVMM); Pericyticmimicry; Stem cell embryonic migration

Indexed keywords

CADHERIN;

ANGIOGENESIS; ARTICLE; BASEMENT MEMBRANE; CAPILLARY; CELL CONTACT; CELL INTERACTION; CELL MIGRATION; CELL TYPE; COCULTURE; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; ENDOTHELIUM CELL; GASTRULATION; GLIOBLASTOMA; GLIOMA; HUMAN; MELANOMA CELL; METASTATIC MELANOMA; NEURAL CREST CELL; NEURAL TUBE; NONHUMAN; PANCREAS CANCER; PERICYTE; TUMOR CELL; VASCULAR ENDOTHELIUM;

ABLUMINAL VASCULAR SURFACE; ANGIOTROPISM; EXTRAVASCULAR MIGRATORY METASTASIS (EVMM); PERICYTICMIMICRY; STEM CELL/EMBRYONIC MIGRATION;

ANIMALS; CELL MOVEMENT; HUMANS; MELANOMA; MOLECULAR MIMICRY; NEOVASCULARIZATION, PATHOLOGIC; NEURAL CREST; PERICYTES; SKIN NEOPLASMS;

EID: 84882862225     PISSN: 17551471     EISSN: 1755148X     Source Type: Journal    
DOI: 10.1111/pcmr.12120     Document Type: Article

References (82)

1. Andjelkovic, A.V., Song, L., Dzenko, K.A., Cong, H., and Pachter, J.S. (2002). Functional expression of CCR2 by human fetal astrocytes. J. Neurosci. Res. 70, 219-231.
2. Armulik, A., Abramsson, A., and Betsholtz, C. (2005). Pericyte recruitment during angiogenesis. Circ. Res. 97, 512-523.
3. Bailey, C.M., Morrison, J.A., and Kulesa, P.M. (2012). Melanoma revives an embryonic migration program to promote plasticity and invasion. Pigment Cell Melanoma Res. 25, 573-583.
4. Barnhill, R.L., Dy, K., and Lugassy, C. (2002). Angiotropism in cutaneous melanoma: a prognostic factor strongly predicting risk for metastasis. J. Invest. Dermatol. 119, 705-706.
5. Barnhill, R.L., Busam, K.J., From, L., Bagot, M., Lugassy, C., and Berwick, M. (2011). Inter-observer concordance for the recognition of angiotropism in human melanoma. Pigment Cell Melanoma Res. 24, 582-583.
6. Bergers, G., and Song, S. (2005). The role of pericytes in blood-vessel formation and maintenance. Neuro Oncol. 7, 452-464. Review.
7. Cavalli, L.R., Noone, A.M., Makambi, K.H., Rone, J.D., and Kasid, U.N. (2011). Frequent loss of the BLID gene in early-onset breast cancer. Cytogenet Genome Res. 135, 19-24.
8. Chang, Y.S., di Tomaso, E., McDonald, D.M., Jones, R., Jain, R.K., and Munn, L.L. (2000). Mosaic blood vessels in tumors: frequency of cancer cells in contact with flowing blood. Proc. Natl. Acad. Sci. USA 97, 14608-14613.
9. Chang, Y., Paramasivam, M., Girgenti, M.J., Walikonis, R.S., and Bianchi, E. (2010). RanBPM regulates the progression of neuronal precursors through M-phase at the surface of the neocortical ventricular zone. Dev. Neurobiol 70, 1-15.
10. Chen, P.C., Lin, T.H., Cheng, H.C., and Tang, C.H. (2012). CCN3 increases cell motility and ICAM-1 expression in prostate cancer cells. Carcinogenesis 33, 937-945.
11. Cheng, L., Huang, Z., Zhou, W. et al. (2013). Glioblastoma stem cells generate vascular pericytes to support vessel function and tumor growth. Cell 153, 139-152.
12. Crisan, M., Yap, S., Casteilla, L. et al. (2008). A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3, 301-313.
13. Croucher, D.R., Saunders, D.N., Lobov, S., and Ranson, M. (2008). Revisiting the biological roles of PAI2 (SERPINB2) in cancer. Nat. Rev. Cancer 7, 535-545.
14. Dirks, P.B. (2001). Glioma migration: clues from the biology of neural progenitor cells and embryonic CNS cell migration. J. Neurooncol. 53, 203-212.
15. Drerup, C.M., Wiora, H.M., Topczewski, J., and Morris, J.A. (2009). Disc1 regulates foxd3 and sox10 expression, affecting neural crest migration and differentiation. Development 136, 2623-2632.
16. Fang, D., Nguyen, T.K., Leishear, K., Finko, R., Kulp, A.N., Hotz, S., Van Belle, P.A., Xu, X., Elder, D.E., and Herlyn, M. (2005). A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 65, 9328-9337.
17. Farin, A., Suzuki, S.O., Weiker, M., Goldman, J.E., Bruce, J.N., and Canoll, P. (2006). Transplanted glioma cells migrate and proliferate on host brain vasculature: a dynamic analysis. Glia 53, 799-808.
18. Fidler, I.J. (2002). The organ microenvironment and cancer metastasis. Differentiation 70, 498-505.
19. Friedl, P., and Wolf, K. (2003). Tumour-cell invasion and migration: diversity and escape mechanisms. Nat. Rev. Cancer 3, 362-374.
20. Fukunaga-Kalabis, M., Roesch, A., and Herlyn, M. (2011). From cancer stem cells to tumor maintenance in melanoma. J. Invest. Dermatol. 131, 1600-1604.
21. Giannelli, G., Falk-Marzillier, J., Schiraldi, O., Stetler-Stevenson, W.G., and Quaranta, V. (1997). Induction of cell migration by matrix metalloprotease-2 cleavage of laminin-5. Science 277, 225-228.
22. Girouard, S.D., and Murphy, G.F. (2011). Melanoma stem cells: not rare, but well done. Lab Invest. 91, 647-664.
23. Hendrix, M.J., Seftor, E.A., Seftor, R.E., Kasemeier-Kulesa, J., Kulesa, P.M., and Postovit, L.M. (2007). Reprogramming metastatic tumour cells with embryonic microenvironments. Nat. Rev. 7, 246-255.
24. Hirschi, K.K., Rohovsky, S.A., and D'Amore, P.A. (1998). PDGF, TGF-beta, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J. Cell Biol. 141, 805-814.
25. Ito, Y., Zhang, Y., Dangaria, S., Luan, X., and Diekwisch, T.G. (2011). NF-Y and USF1 transcription factor binding to CCAAT-box and E-box elements activates the CP27 promoter. Gene 473, 92-99.
26. Jiang, Y., Boije, M., Westermark, B., and Uhrbom, L. (2011). PDGF-B Can sustain self-renewal and tumorigenicity of experimental glioma-derived cancer-initiating cells by preventing oligodendrocyte differentiation. Neoplasia 6, 492-503.
27. Kalisz, M., Winzi, M., Bisgaard, H.C., and Serup, P. (2012). EVEN-SKIPPED HOMEOBOX 1 controls human ES cell differentiation by directly repressing GOOSECOID expression. Dev. Biol. 362, 94-103.
28. Kirchhofer, D., and Vucic, D. (2012). Protease activity of MALT1: a mystery unravelled. Biochem. J. 444, e3-e5.
29. Kubota, Y., Kleinman, H.K., Martin, G.R., and Lawley, T.J. (1988). Role of laminin and basement membrane in the morphological differentiation of human endothelial cells into capillary-like structures. J. Cell Biol. 107, 1589-1598.
30. Kulesa, P.M., Kasemeier-Kulesa, J.C., Teddy, J.M., Margaryan, N.V., Seftor, E.A., Seftor, R.E., and Hendrix, M.J. (2006). Reprogramming metastatic melanoma cells to assume a neural crest cell-like phenotype in an embryonic microenvironment. Proc. Natl Acad. Sci. USA 103, 3752-3757.
31. Kuramitsu, Y., Hayashi, E., Okada, F., Tanaka, T., and Zhang, X. (2010). Proteomic analysis for nuclear proteins related to tumour malignant progression: a comparative proteomic study between malignant progressive cells and regressive cells. Anticancer Res. 30, 2093-2099.
32. Le Douarin, N.M., Creuzet, S., Couly, G., and Dupin, E. (2004). Neural crest cell plasticity and its limits. Development 131, 4637-4650.
33. Levy, M.J., Gleeson, F.C., and Zhang, L. (2009). Endoscopic ultrasound fine-needle aspiration detection of extravascular migratory metastasis from a remotely located pancreatic cancer. Clin. Gastroenterol. Hepatol. 7, 246-248.
34. Li, A., Ma, Y., Yu, X. et al. (2011). Rac1 drives melanoblast organization during mouse development by orchestrating pseudopod-driven motility and cell-cycle progression. Dev. Cell 21, 722-734.
35. Loberg, R.D., Day, L.L., Harwood, J., Ying, C., St John, L.N., Giles, R., Neeley, C.K., and Pienta, K.J. (2006). CCL2 is a potent regulator of prostate cancer cell migration and proliferation. Neoplasia 8, 578-586.
36. Lugassy, C., and Barnhill, R.L. (2007). Angiotropic malignant melanoma and extravascular migratory metastasis: A review. Adv. Anat. Pathol. 14, 195-201.
37. Lugassy, C., Eyden, B.P., Christensen, L., and Escande, J.P. (1997). Angio-tumoral complex in human malignant melanoma characterised by free laminin: ultrastructural and immunohistochemical observations. J. Submicrosc. Cytol. Pathol. 29, 19-28.
38. Lugassy, C., Haroun, R.I., Brem, H., Guarnieri, M., De Girolami, U., and Barnhill, R.L. (2002a). Pericytic-like angiotropism of glioma and melanoma cells. Am. J. Dermatopathol. 24, 473-478.
39. Lugassy, C., Kleinman, H.K., Fernandez, P.M., Patierno, S.R., Webber, M.M., Ghanem, G., Spatz, A., and Barnhill, R.L. (2002b). Human melanoma cell migration along capillary-like structures in vitro: a new dynamic model for studying extravascular migratory metastasis. J. Invest. Dermatol. 119, 703-704.
40. Lugassy, C., Kleinman, H.K., Engbring, J.A., Welch, D.R., Harms, J.F., Rufner, R., Ghanem, G., Patierno, S.R., and Barnhill, R.L. (2004). Angiotropism and pericyte-like location of GFP melanoma cells: ex vivo and in vivo studies of extravascular migratory metastasis. Am. J. Pathol. 164, 11911198.
41. Lugassy, C., Kleinman, H.K., Vernon, S.E., Welch, D.R., and Barnhill, R.L. (2007). C16 laminin peptide increases angiotropic extravascular migration of human melanoma cells in a shell-less chick chorioallantoic membrane assay. Br. J. Dermatol. 157, 780-782.6
42. Lugassy, C., Wadehra, M., Li, X. et al. (2013). Pilot study on "pericytic mimicry" and potential embryonic/stem cell properties of angiotropic melanoma cells interacting with the abluminal vascular surface. Cancer Microenviron. 6, 19-29.
43. Maniotis, A.J., Folberg, R., Hess, A., Seftor, E.A., Gardner, L.M., Pe'er, J., Trent, J.M., Meltzer, P.S., and Hendrix, M.J. (1999). Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am. J. Pathol. 155, 739-752.
44. McGary, E.C., Onn, A., Mills, L., Heimberger, A., Eton, O., Thomas, G.W., Shtivelband, M., and Bar-Eli, M. (2004). Imatinib mesylate inhibits platelet-derived growth factor receptor phosphorylation of melanoma cells but does not affect tumorigenicity in vivo. J. Invest. Dermatol. 122, 400-405.
45. Nagy, N., Mwizerwa, O., Yaniv, K., Carmel, L., Pieretti-Vanmarcke, R., Weinstein, B.M., and Goldstein, A.M., (2009). Endothelial cells promote migration and proliferation of enteric neural crest cells via beta1 integrin signaling. Dev. Biol. 330, 263-272.
46. Natali, P.G., Hamby, C.V., Felding-Habermann, B., Liang, B., Nicotra, M.R., Di Filippo, F., Giannarelli, D., Temponi, M., and Ferrone, S. (1997). Clinical significance of alpha(v) beta3 integrin and intercellular adhesion molecule-1 expression in cutaneous malignant melanoma lesions. Cancer Res. 57, 1554-1560.
47. Orgaz, J.L., and Sanz-Moreno, V. (2013). Emerging molecular targets in melanoma invasion and metastasis. Pigment Cell Melanoma Res. 26, 39-57.
48. Paget, S. (1889). The distribution of secondary growths in cancer of the breast. Lancet 133, 571-573.
49. Perris, R., and Perissinotto, D. (2000). Role of the extracellular matrix during neural crest cell migration. Mech. Dev. 95, 3-21.
50. Poste, G., and Fidler, I.J. (1980). The pathogenesis of cancer metastasis. Nature 283, 139-146.
51. Ribatti, D., Nico, B., and Crivellato, E. (2011). The role of pericytes in angiogenesis. Int. J. Dev. Biol. 55, 261-268.
52. Risau, W. (1997). Mechanisms of angiogenesis. Nature 386, 671-674.
53. Schwarz, Q., Maden, C.H., Vieira, J.M., and Ruhrberg, C. (2009). Neuropilin 1 signaling guides neural crest cells to coordinate pathway choice with cell specification. PNAS 106, 6164-6169.
54. Seftor, R.E., Hess, A.R., Seftor, E.A., Kirschmann, D.A., Hardy, K.M., Margaryan, N.V., and Hendrix, M.J. (2012). Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am. J. Pathol. 181, 1115-1125.
55. Shi, H., Kong, X., Ribas, A., and Lo, R.S. (2011). Combinatorial treatments that overcome PDGFRβ-driven resistance of melanoma cells to V600EB-RAF inhibition. Cancer Res. 71, 5067-5074.
56. Sitohy, B., Nagy, J.A., and Dvorak, H.F. (2012). Anti-VEGF/VEGFR therapy for cancer: reassessing the target. Cancer Res. 72, 1909-1914.
57. Sleeman, J.P., Cady, B., and Pantel, K. (2012). The connectivity of lymphogenous and hematogenous tumor cell dissemination: biological insights and clinical implications. Clin. Exp. Metastasis 29, 737-746.
58. Snyder, M., Huang, X.Y., and Zhang, J.J. (2011). Signal transducers and activators of transcription 3 (STAT3) directly regulates cytokine-induced fascin expression and is required for breast cancer cell migration. J. Biol. Chem. 286, 38886-38893.
59. Soria, G., and Ben-Baruch, A. (2008). The inflammatory chemokines CCL2 and CCL5 in breast cancer. Cancer Lett. 267, 271-285.
60. Soria, G., Ofri-Shahak, M., Haas, I., Yaal-Hahoshen, N., and Leider-Trejo, L. (2011). Inflammatory mediators in breast cancer: coordinated expression of TNFα and IL-1β with CCL2 & CCL5 and effects on epithelial-to-mesenchymal transition. BMC Cancer 11, 130.
61. Suresh, B., Ramakrishna, S., Kim, Y.S., Kim, S.M., Kim, M.S., and Baek, K.H. (2010). Stability and function of mammalian lethal giant larvae-1 oncoprotein are regulated by the scaffolding protein RanBPM. J. Biol. Chem. 285, 35340-35349.
62. Suzuki, S.O., Kitai, R., Llena, J., Lee, S.C., Goldman, J.E., and Shafit-Zagardo, B. (2002). MAP-2e, a novel MAP-2 isoform, is expressed in gliomas and delineates tumor architecture and patterns of infiltration. J. Neuropathol. Exp. Neurol. 61, 403-412.
63. Talmadge, J.E., and Fidler, I.J. (2010). AACR centennial series: the biology of cancer metastasis: historical perspective. Cancer Res. 70, 5649-5669.
64. Tamura, Y., Matsumura, K., Sano, M., Tabata, H., and Kimura, K. (2011). Neural crest-derived stem cells migrate and differentiate into cardiomyocytes after myocardial infarction. Arterioscler. Thromb. Vasc. Biol. 31, 582-589.
65. Tang, C.H., and Tsai, C.C. (2012). CCL2 increases MMP-9 expression and cell motility in human chondrosarcoma cells via the Ras/Raf/MEK/ERK/NF-κB signaling pathway. Biochem. Pharmacol. 83, 335-344.
66. Thiery, J.P., Acloque, H., Huang, R.Y., and Nieto, M.A. (2009). Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890.
67. Tigges, U., Boroujerdi, A., Welser-Alves, J.V., and Milner, R. (2013). TNF-α promotes cerebral pericyte remodeling in vitro, via a switch from α1 to α2 integrins. J. Neuroinflammation 10, 33.
68. Tsuyada, A., Chow, A., Wu, J., Somlo, G., and Chu, P. (2012). CCL2 mediates crosstalk between cancer cells and stromal fibroblasts that regulates breast cancer. Stem Cells 72, 2768-2779.
69. Van Es, S.L., Colman, M., Thompson, J.F., McCarthy, S.W., and Scolyer, R.A. (2008). Angiotropism is an independent predictor of local recurrence and in-transit metastasis in primary cutaneous melanoma. Am. J. Surg. Pathol. 32, 1396-1403.
70. Verbeke, H., Struyf, S., Berghmans, N., Van Coillie, E., and Opdenakker, G. (2011). Isotypic neutralizing antibodies against mouse GCP-2/CXCL6 inhibit melanoma growth and metastasis. Cancer Lett. 302, 54-62.
71. Wai Wong, C., Dye, D.E., and Coombe, D.R. (2012). The role of immunoglobulin superfamily cell adhesion molecules in cancer metastasis. Int. J. Cell. Biol. 2012, 340296.
72. Wang, D., Zavadil, J., Martin, L., Parisi, F., and Friedman, E. (2011). Inhibition of nonsense-mediated RNA decay by the tumor microenvironment promotes tumorigenesis. Mol. Cell. Biol. 17, 3670-3680.
73. Weiss, L. (1986). Metastatic inefficiency: causes and consequences. Cancer Rev. 3, 1-24.
74. Wesseling, P., Ruiter, D.J., and Burger, P.C. (1997). Angiogenesis in brain tumors: pathobiological and clinical aspects. J. Neurooncol. 32, 253-265.
75. Wilmott, J., Haydu, L., Bagot, M., Zhang, Y., Jakrot, V., McCarthy, S., Lugassy, C., Thompson, J., Scolyer, R., and Barnhill, R. (2012). Angiotropism is an independent predictor of microscopic satellites in primary cutaneous melanoma. Histopathology 61, 889-898.
76. Witz, I.P. (2008). The selectin-selectin ligand axis in tumor progression. Cancer Metastasis Rev. 1, 19-30.
77. Yamaoka, T., Fujimoto, M., Ogawa, F. et al. (2011). The roles of P- and E-selectins and P-selectin glycoprotein ligand-1 in primary and metastatic mouse melanomas. J. Dermatol. Sci. 2, 99-107.
78. Yancopoulos, G.D., Davis, S., Gale, N.W., Rudge, J.S., Wiegand, S.J., and Holash, J. (2000). Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248.
79. Yang, L., Gu, L., Li, Z., and Zhou, M. (2010). Translation of TRAF1 is regulated by IRES-dependent mechanism and stimulated by vincristine. Nucleic Acids Res. 38, 4503-4513.
80. Yu, H.G., Nam, J.O., Miller, N.L. et al. (2011). p190RhoGEF (Rgnef) promotes colon carcinoma tumor progression via interaction with focal adhesion kinase. Cancer Res. 71, 360-370.
81. Yurchenco, P.D., and Patton, B.L. (2009). Developmental and pathogenic mechanisms of basement membrane assembly. Curr. Pharm. Des. 15, 1277-1294.
82. Zhang, F., Suarez, G., Sha, J., Sierra, J.C., and Peterson, J.W. (2009). Phospholipase A2-activating protein (PLAA) enhances cisplatin-induced apoptosis in HeLa cells. Cell. Signal. 7, 1085-1099.