Why is melanoma so metastatic?

Malignant melanoma is one of the most aggressive cancers and can disseminate from a relatively small primary tumor and metastasize to multiple sites, including the lung, liver, brain, bone, and lymph nodes. Elucidating the molecular and genetic changes that take place during the metastatic process has led to a better understanding of why melanoma is so metastatic. Herein, we describe the unique features that distinguish melanoma from other solid tumors and contribute to the malignant phenotype of melanoma cells. For example, although melanoma cells are highly antigenic, they are extremely efficient at evading host immune response. Melanoma cells share numerous cell surface molecules with vascular cells, are highly angiogenic, are mesenchymal in nature, and possess a higher degree of ‘stemness’ than do other solid tumors. Finally, analysis of melanoma mutations has revealed that the gene expression profile of malignant melanoma is different from that of other cancers. Elucidating these molecular and genetic processes in highly metastatic melanoma can lead to the development of improved treatment and individualized therapy options.

[1]  G. Stamp,et al.  Genome sequencing of mucosal melanomas reveals that they are driven by distinct mechanisms from cutaneous melanoma , 2013, The Journal of pathology.

[2]  K. Kinzler,et al.  Cancer Genome Landscapes , 2013, Science.

[3]  A. Weeraratna,et al.  A Wnt-er Migration: The Confusing Role of β-Catenin in Melanoma Metastasis , 2013, Science Signaling.

[4]  Dean Y. Li,et al.  The Small GTPase ARF6 Stimulates β-Catenin Transcriptional Activity During WNT5A-Mediated Melanoma Invasion and Metastasis , 2013, Science Signaling.

[5]  Oshin Vartanian,et al.  Lesions to right prefrontal cortex impair real-world planning through prematurecommitments , 2013, Neuropsychologia.

[6]  K. Flaherty,et al.  Elucidating distinct roles for NF1 in melanomagenesis. , 2013, Cancer discovery.

[7]  L. Chin,et al.  HOXA1 drives melanoma tumor growth and metastasis and elicits an invasion gene expression signature that prognosticates clinical outcome , 2013, Oncogene.

[8]  M. Aurrand-Lions,et al.  Soluble Melanoma Cell Adhesion Molecule (sMCAM/sCD146) Promotes Angiogenic Effects on Endothelial Progenitor Cells through Angiomotin* , 2013, The Journal of Biological Chemistry.

[9]  R. Sullivan,et al.  BRAF Inhibition Is Associated with Enhanced Melanoma Antigen Expression and a More Favorable Tumor Microenvironment in Patients with Metastatic Melanoma , 2013, Clinical Cancer Research.

[10]  Matthew J. Davis,et al.  RAC1P29S is a spontaneously activating cancer-associated GTPase , 2013, Proceedings of the National Academy of Sciences.

[11]  M. Millward,et al.  Markers of circulating tumour cells in the peripheral blood of patients with melanoma correlate with disease recurrence and progression , 2013, The British journal of dermatology.

[12]  A. Jemal,et al.  Cancer statistics, 2013 , 2013, CA: a cancer journal for clinicians.

[13]  D. McConkey,et al.  Galectin-3 contributes to melanoma growth and metastasis via regulation of NFAT1 and autotaxin. , 2012, Cancer research.

[14]  S. Morrison,et al.  Human Melanoma Metastasis in NSG Mice Correlates with Clinical Outcome in Patients , 2012, Science Translational Medicine.

[15]  Peter J. Campbell,et al.  Evolution of the cancer genome , 2012, Nature Reviews Genetics.

[16]  A. Vartanian RETRACTED ARTICLE: Signaling pathways in tumor vasculogenic mimicry , 2012, Biochemistry (Moscow).

[17]  F. Passarelli,et al.  Expression of vascular endothelial growth factor‐C in primary cutaneous melanoma predicts sentinel lymph node positivity , 2012, Journal of cutaneous pathology.

[18]  M. Bar‐eli,et al.  The sweet and bitter sides of galectins in melanoma progression , 2012, Pigment cell & melanoma research.

[19]  P. Kulesa,et al.  Melanoma revives an embryonic migration program to promote plasticity and invasion , 2012, Pigment cell & melanoma research.

[20]  Qiao Li,et al.  Tumor cell-derived exosomes: a message in a bottle. , 2012, Biochimica et biophysica acta.

[21]  A. Sivachenko,et al.  A Landscape of Driver Mutations in Melanoma , 2012, Cell.

[22]  Matthew J. Davis,et al.  Exome sequencing identifies recurrent somatic RAC1 mutations in melanoma , 2012, Nature Genetics.

[23]  Timothy J. Lavelle,et al.  Understanding the Melanocyte Distribution in Human Epidermis: An Agent-Based Computational Model Approach , 2012, PloS one.

[24]  David C. Smith,et al.  Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. , 2012, The New England journal of medicine.

[25]  M. Bar‐eli,et al.  Driving transcriptional regulators in melanoma metastasis , 2012, Cancer and Metastasis Reviews.

[26]  Gema Moreno-Bueno,et al.  Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET , 2012, Nature Medicine.

[27]  J. Wolchok,et al.  Ipilimumab in patients with melanoma and brain metastases: an open-label, phase 2 trial. , 2012, The Lancet. Oncology.

[28]  G. Mills,et al.  Lysophosphatidic acid induces lymphangiogenesis and IL-8 production in vitro in human lymphatic endothelial cells. , 2012, The American journal of pathology.

[29]  H. Moch,et al.  Tumor Cell Plasticity and Angiogenesis in Human Melanomas , 2012, PloS one.

[30]  T. Fennell,et al.  Melanoma genome sequencing reveals frequent PREX2 mutations , 2012, Nature.

[31]  D. Morton,et al.  Surgery for distant melanoma metastasis. , 2012, Cancer journal.

[32]  J. Wolchok,et al.  Targeting immune checkpoints: releasing the restraints on anti-tumor immunity for patients with melanoma. , 2012, Cancer journal.

[33]  C. V. Jongeneel,et al.  Exome sequencing identifies recurrent somatic MAP2K1 and MAP2K2 mutations in melanoma , 2011, Nature Genetics.

[34]  J. Wilmott,et al.  Selective BRAF Inhibitors Induce Marked T-cell Infiltration into Human Metastatic Melanoma , 2011, Clinical Cancer Research.

[35]  R. Gibbs,et al.  Frequent somatic MAP3K5 and MAP3K9 mutations in metastatic melanoma identified by exome sequencing , 2011, Nature Genetics.

[36]  H. Woo,et al.  Cross-species hybridization of microarrays for studying tumor transcriptome of brain metastasis , 2011, Proceedings of the National Academy of Sciences.

[37]  E. Greanya,et al.  The role of hepatitis B immunoglobulin in hepatitis B related liver transplantation: Canadian Transplant Centre Position Paper. , 2011, Annals of hepatology.

[38]  Yibin Kang,et al.  Unravelling the complexity of metastasis — molecular understanding and targeted therapies , 2011, Nature Reviews Cancer.

[39]  Gerald C. Chu,et al.  Proinvasion metastasis drivers in early-stage melanoma are oncogenes. , 2011, Cancer cell.

[40]  Axel Hoos,et al.  Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. , 2011, The New England journal of medicine.

[41]  I. Fidler,et al.  The seed and soil hypothesis revisited—The role of tumor‐stroma interactions in metastasis to different organs , 2011, International journal of cancer.

[42]  S. Wickline,et al.  Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. , 2011, Cancer research.

[43]  M. Bar‐eli,et al.  Expression of Id-1 is regulated by MCAM/MUC18: a missing link in melanoma progression. , 2011, Cancer research.

[44]  S. Davis,et al.  Exome sequencing identifies GRIN2A as frequently mutated in melanoma , 2011, Nature Genetics.

[45]  H. Moch,et al.  Human CD271-positive melanoma stem cells associated with metastasis establish tumor heterogeneity and long-term growth. , 2011, Cancer research.

[46]  M. Bar‐eli,et al.  Transcriptional control of melanoma metastasis: the importance of the tumor microenvironment. , 2011, Seminars in cancer biology.

[47]  D. Lyden,et al.  The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. , 2011, Seminars in cancer biology.

[48]  T. van Hall,et al.  Strategies to counteract MHC-I defects in tumors. , 2011, Current opinion in immunology.

[49]  Kylie M. Price,et al.  Murine Melanoma-Infiltrating Dendritic Cells Are Defective in Antigen Presenting Function Regardless of the Presence of CD4+CD25+ Regulatory T Cells , 2011, PloS one.

[50]  Sean Davis,et al.  Interferon-γ links ultraviolet radiation to melanomagenesis in mice. , 2011, Nature.

[51]  M. Bar‐eli,et al.  Protease activated receptor-1 inhibits the Maspin tumor-suppressor gene to determine the melanoma metastatic phenotype , 2010, Proceedings of the National Academy of Sciences.

[52]  A. Bowcock,et al.  Frequent Mutation of BAP1 in Metastasizing Uveal Melanomas , 2010, Science.

[53]  K. Hoek,et al.  Cancer stem cells versus phenotype‐switching in melanoma , 2010, Pigment cell & melanoma research.

[54]  J. O'Brien,et al.  Mutations in GNA11 in uveal melanoma. , 2010, The New England journal of medicine.

[55]  P. Courtoy,et al.  A galectin-3 ligand corrects the impaired function of human CD4 and CD8 tumor-infiltrating lymphocytes and favors tumor rejection in mice. , 2010, Cancer research.

[56]  K. Aldape,et al.  Reactive astrocytes protect melanoma cells from chemotherapy by sequestering intracellular calcium through gap junction communication channels. , 2010, Neoplasia.

[57]  M. Bar‐eli,et al.  CREB Inhibits AP-2α Expression to Regulate the Malignant Phenotype of Melanoma , 2010, PloS one.

[58]  V. Engelhard,et al.  Tumor masses support naive T cell infiltration, activation, and differentiation into effectors , 2010, The Journal of experimental medicine.

[59]  A. Dalgleish,et al.  T regulatory cells, the evolution of targeted immunotherapy. , 2010, Biochimica et biophysica acta.

[60]  F. Garrido,et al.  “Hard” and “soft” lesions underlying the HLA class I alterations in cancer cells: Implications for immunotherapy , 2010, International journal of cancer.

[61]  D. Fisher,et al.  How Sunlight Causes Melanoma , 2010, Current oncology reports.

[62]  K. Flaherty,et al.  Selective BRAFV600E inhibition enhances T-cell recognition of melanoma without affecting lymphocyte function. , 2010, Cancer research.

[63]  Gary D Bader,et al.  International network of cancer genome projects , 2010, Nature.

[64]  D. Roberts,et al.  Autotaxin Signaling via Lysophosphatidic Acid Receptors Contributes to Vascular Endothelial Growth Factor–Induced Endothelial Cell Migration , 2010, Molecular Cancer Research.

[65]  Djuro Josic,et al.  Microvesicle entry into marrow cells mediates tissue-specific changes in mRNA by direct delivery of mRNA and induction of transcription. , 2010, Experimental hematology.

[66]  Jeffrey E Gershenwald,et al.  Final version of 2009 AJCC melanoma staging and classification. , 2009, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[67]  W. Sellers,et al.  MEK1 mutations confer resistance to MEK and B-RAF inhibition , 2009, Proceedings of the National Academy of Sciences.

[68]  D. Schadendorf,et al.  Skin Melanoma Development in ret Transgenic Mice Despite the Depletion of CD25+Foxp3+ Regulatory T Cells in Lymphoid Organs1 , 2009, The Journal of Immunology.

[69]  M. Hung,et al.  Crosstalk between Protease-activated Receptor 1 and Platelet-activating Factor Receptor Regulates Melanoma Cell Adhesion Molecule (MCAM/MUC18) Expression and Melanoma Metastasis* , 2009, The Journal of Biological Chemistry.

[70]  M. Bar‐eli,et al.  Overexpression of protease-activated receptor-1 contributes to melanoma metastasis via regulation of connexin 43. , 2009, Cancer research.

[71]  M. Bar‐eli,et al.  Silencing cAMP-response Element-binding Protein (CREB) Identifies CYR61 as a Tumor Suppressor Gene in Melanoma* , 2009, The Journal of Biological Chemistry.

[72]  M. Bar‐eli,et al.  Inflammation and melanoma metastasis , 2009, Pigment cell & melanoma research.

[73]  J. Pollard,et al.  Microenvironmental regulation of metastasis , 2009, Nature Reviews Cancer.

[74]  Jacopo Meldolesi,et al.  Shedding microvesicles: artefacts no more. , 2009, Trends in cell biology.

[75]  Rakesh K. Singh,et al.  Host CXCR2-dependent regulation of melanoma growth, angiogenesis, and experimental lung metastasis. , 2009, Cancer research.

[76]  E. Simpson,et al.  Frequent somatic mutations of GNAQ in uveal melanoma and blue nevi , 2008, Nature.

[77]  M. Bar‐eli,et al.  Tumorigenesis and Neoplastic Progression Expression Profiling of Galectin-3-Depleted Melanoma Cells Reveals Its Major Role in Melanoma Cell Plasticity and Vasculogenic Mimicry , 2010 .

[78]  R. Moon,et al.  CTLA-4 is a direct target of Wnt/beta-catenin signaling and is expressed in human melanoma tumors. , 2008, The Journal of investigative dermatology.

[79]  A. Sood,et al.  Targeting melanoma growth and metastasis with systemic delivery of liposome-incorporated protease-activated receptor-1 small interfering RNA. , 2008, Cancer research.

[80]  S. Morrison,et al.  Efficient tumor formation by single human melanoma cells , 2008, Nature.

[81]  L. Ellis,et al.  VEGF-targeted therapy: mechanisms of anti-tumour activity , 2008, Nature Reviews Cancer.

[82]  George Poste,et al.  The "seed and soil" hypothesis revisited. , 2008, The Lancet. Oncology.

[83]  J. Kirkwood,et al.  Next generation of immunotherapy for melanoma. , 2008, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[84]  M. Bar‐eli,et al.  Transcriptional control of the melanoma malignant phenotype , 2008, Cancer biology & therapy.

[85]  F. Garrido,et al.  Analysis of HLA class I expression in progressing and regressing metastatic melanoma lesions after immunotherapy , 2008, Immunogenetics.

[86]  T. Nomura,et al.  Regulatory T Cells and Immune Tolerance , 2008, Cell.

[87]  J. Schalkwijk,et al.  Attenuation of melanoma invasion by a secreted variant of activated leukocyte cell adhesion molecule. , 2008, Cancer research.

[88]  G. Zhu,et al.  B7-H1 is a ubiquitous antiapoptotic receptor on cancer cells. , 2008, Blood.

[89]  Kylie M. Price,et al.  Inefficient presentation of tumor-derived antigen by tumor-infiltrating dendritic cells , 2008, Cancer Immunology, Immunotherapy.

[90]  S. Ofori-Acquah,et al.  Activated leukocyte cell adhesion molecule: a new paradox in cancer. , 2008, Translational research : the journal of laboratory and clinical medicine.

[91]  C. Hess,et al.  Polymorphonuclear Neutrophil-Derived Ectosomes Interfere with the Maturation of Monocyte-Derived Dendritic Cells1 , 2008, The Journal of Immunology.

[92]  M. Bar‐eli,et al.  Inflammation and melanoma growth and metastasis: The role of platelet-activating factor (PAF) and its receptor , 2007, Cancer and Metastasis Reviews.

[93]  Kenneth P. Roos,et al.  Autocrine VEGF Signaling Is Required for Vascular Homeostasis , 2007, Cell.

[94]  J. McNamara Cancer Stem Cells , 2007, Methods in Molecular Biology.

[95]  A. Rudensky,et al.  TGFβ signalling in control of T-cell-mediated self-reactivity , 2007, Nature Reviews Immunology.

[96]  Arie Perry,et al.  Transcriptomic versus Chromosomal Prognostic Markers and Clinical Outcome in Uveal Melanoma , 2007, Clinical Cancer Research.

[97]  J. Gershenwald,et al.  Galectin-3 Expression Is Associated with Tumor Progression and Pattern of Sun Exposure in Melanoma , 2006, Clinical Cancer Research.

[98]  M. Bar‐eli,et al.  Bioimmunotherapy for melanoma using fully human antibodies targeting MCAM/MUC18 and IL-8. , 2006, Pigment cell research.

[99]  Z. Trajanoski,et al.  Type, Density, and Location of Immune Cells Within Human Colorectal Tumors Predict Clinical Outcome , 2006, Science.

[100]  J Ratajczak,et al.  Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication , 2006, Leukemia.

[101]  Y. Kawakami,et al.  The BRAF–MAPK signaling pathway is essential for cancer-immune evasion in human melanoma cells , 2006, The Journal of experimental medicine.

[102]  Colgan P. Sean Cell-Cell Interactions , 2006, Methods in Molecular Biology™.

[103]  Richard A Flavell,et al.  Transforming growth factor-beta regulation of immune responses. , 2006, Annual review of immunology.

[104]  Rakesh K. Singh,et al.  Distinct expression of CXCL8 and its receptors CXCR1 and CXCR2 and their association with vessel density and aggressiveness in malignant melanoma. , 2006, American journal of clinical pathology.

[105]  S. Rafii,et al.  VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche , 2005, Nature.

[106]  Jean-Philippe Brunet,et al.  The melanocyte differentiation program predisposes to metastasis after neoplastic transformation , 2005, Nature Genetics.

[107]  N. Chen,et al.  Transendothelial migration of melanoma cells involves N-cadherin-mediated adhesion and activation of the beta-catenin signaling pathway. , 2005, Molecular biology of the cell.

[108]  M. Herlyn,et al.  Adhesion, migration and communication in melanocytes and melanoma. , 2005, Pigment cell research.

[109]  G. Swart,et al.  Activated leukocyte cell adhesion molecule (ALCAM/CD166): Signaling at the divide of melanoma cell clustering and cell migration? , 2005, Cancer and Metastasis Reviews.

[110]  Gerard C Blobe,et al.  Role of transforming growth factor Beta in human cancer. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[111]  G. Raposo,et al.  Exosomes: endosomal-derived vesicles shipping extracellular messages. , 2004, Current opinion in cell biology.

[112]  T. Utsugi,et al.  CD40 ligation releases immature dendritic cells from the control of regulatory CD4+CD25+ T cells. , 2003, Immunity.

[113]  M. Barbacid,et al.  RAS oncogenes: the first 30 years , 2003, Nature Reviews Cancer.

[114]  Michelle L. Varney,et al.  IL-8 Directly Enhanced Endothelial Cell Survival, Proliferation, and Matrix Metalloproteinases Production and Regulated Angiogenesis1 , 2003, The Journal of Immunology.

[115]  Hisataka Kobayashi,et al.  Inflammatory breast cancer: Vasculogenic mimicry and its hemodynamics of an inflammatory breast cancer xenograft model , 2003, Breast Cancer Research.

[116]  Kim-Anh Do,et al.  Steps toward mapping the human vasculature by phage display , 2002, Nature Medicine.

[117]  Suyun Huang,et al.  Fully human antibodies to MCAM/MUC18 inhibit tumor growth and metastasis of human melanoma. , 2002, Cancer research.

[118]  M. Schachner,et al.  Overexpression of the cell adhesion molecule L1 is associated with metastasis in cutaneous malignant melanoma. , 2002, European journal of cancer.

[119]  D. Lev,et al.  Cellular Adhesion Pathways and Metastatic Potential of Human Melanoma , 2002, Cancer biology & therapy.

[120]  Haidong Dong,et al.  Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion , 2002, Nature Medicine.

[121]  Laurence Zitvogel,et al.  Exosomes: composition, biogenesis and function , 2002, Nature Reviews Immunology.

[122]  S. Ullrich,et al.  Platelet-activating Factor, a Molecular Sensor for Cellular Damage, Activates Systemic Immune Suppression , 2002, The Journal of experimental medicine.

[123]  R. Tampé,et al.  Immune escape of melanoma: first evidence of structural alterations in two distinct components of the MHC class I antigen processing pathway. , 2001, Cancer research.

[124]  A. Montgomery,et al.  Involvement of integrin alpha(v)beta(3) and cell adhesion molecule L1 in transendothelial migration of melanoma cells. , 2001, Molecular biology of the cell.

[125]  Paul S. Meltzer,et al.  Expression and functional significance of VE-cadherin in aggressive human melanoma cells: Role in vasculogenic mimicry , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[126]  Jeffrey E Gershenwald,et al.  Dominant-negative transcription factor AP-2 augments SB-2 melanoma tumor growth in vivo , 2001, Oncogene.

[127]  K Satyamoorthy,et al.  N-cadherin-mediated intercellular interactions promote survival and migration of melanoma cells. , 2001, Cancer research.

[128]  Z. Ronai,et al.  Activating transcription factor 2-derived peptides alter resistance of human tumor cell lines to ultraviolet irradiation and chemical treatment. , 2001, Clinical cancer research : an official journal of the American Association for Cancer Research.

[129]  H. Hall,et al.  CD4+CD25+ regulatory T cells down‐regulate co‐stimulatory molecules on antigen‐presenting cells , 2000, European journal of immunology.

[130]  J. J. van den Oord,et al.  Activated leukocyte cell adhesion molecule/CD166, a marker of tumor progression in primary malignant melanoma of the skin. , 2000, The American journal of pathology.

[131]  G. Parmiani,et al.  T‐cell recognition of melanoma‐associated antigens , 2000 .

[132]  P. Meltzer,et al.  Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. , 1999, The American journal of pathology.

[133]  M. Herlyn,et al.  Immunohistochemical evidence of cytokine networks during progression of human melanocytic lesions , 1999, International journal of cancer.

[134]  M. Bar‐eli Role of Interleukin-8 in Tumor Growth and Metastasis of Human Melanoma , 1999, Pathobiology.

[135]  V. Kosma,et al.  Downregulation of transcription factor AP-2 predicts poor survival in stage I cutaneous malignant melanoma. , 1998, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[136]  E. Voura,et al.  Cell–cell interactions during transendothelial migration of tumor cells , 1998, Microscopy research and technique.

[137]  D. Williams,et al.  Activation of the epidermal platelet-activating factor receptor results in cytokine and cyclooxygenase-2 biosynthesis. , 1998, Journal of immunology.

[138]  R. Frade,et al.  Procathepsin-L, a proteinase that cleaves human C3 (the third component of complement), confers high tumorigenic and metastatic properties to human melanoma cells. , 1998, Cancer research.

[139]  P. Heikkilä,et al.  Enhanced expression of vascular endothelial growth factor in metastatic melanoma. , 1997, British Journal of Cancer.

[140]  D J Ruiter,et al.  Transition of horizontal to vertical growth phase melanoma is accompanied by induction of vascular endothelial growth factor expression and angiogenesis , 1997, Melanoma research.

[141]  J. Johnson,et al.  Expression of MCAM/MUC18 by human melanoma cells leads to increased tumor growth and metastasis. , 1997, Cancer research.

[142]  A. Vitiello,et al.  Expression and regulation of the neural cell adhesion molecule L1 on human cells of myelomonocytic and lymphoid origin. , 1997, Journal of immunology.

[143]  M. Schachner,et al.  L1/HNK‐1 Carbohydrate‐ and β1 Integrin‐Dependent Neural Cell Adhesion to Laminin‐1 , 1997, Journal of neurochemistry.

[144]  M. Hortsch,et al.  The L1 Family of Neural Cell Adhesion Molecules: Old Proteins Performing New Tricks , 1996, Neuron.

[145]  M. Herlyn,et al.  Shifts in cadherin profiles between human normal melanocytes and melanomas. , 1996, The journal of investigative dermatology. Symposium proceedings.

[146]  M. Mihm,et al.  Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma , 1996, Cancer.

[147]  J. Becker,et al.  Human neural cell adhesion molecule L1 and rat homologue NILE are ligands for integrin alpha v beta 3 , 1996, The Journal of cell biology.

[148]  R. Frade,et al.  A cysteine proteinase, which cleaves human C3, the third component of complement, is involved in tumorigenicity and metastasis of human melanoma. , 1996, Cancer research.

[149]  M. Lipkind,et al.  Isolation of Yucaipa virus , 1995, Veterinary Record.

[150]  R. Dermietzel,et al.  Immunolocalization of the neural cell adhesion molecule L1 in non-proliferating epithelial cells of the male urogenital tract , 1995, Histochemistry and Cell Biology.

[151]  D. Elder,et al.  Regulation of Mel-CAM/MUC18 expression on melanocytes of different stages of tumor progression by normal keratinocytes. , 1994, The American journal of pathology.

[152]  R. Folberg,et al.  Microcirculation architecture of melanocytic nevi and malignant melanomas of the ciliary body and choroid. A comparative histopathologic and ultrastructural study. , 1994, Ophthalmology.

[153]  W. Westerhof,et al.  Organotypic culture of human skin to study melanocyte migration. , 1994, Pigment cell research.

[154]  N. S. Mcnutt,et al.  Differential expression of basic fibroblast growth factor (bFGF) in melanocytic lesions demonstrated by in situ hybridization. Implications for tumor progression. , 1994, The American journal of pathology.

[155]  H. Tsou,et al.  Cultured human melanocytes express the intermediate filament vimentin. , 1993, The Journal of investigative dermatology.

[156]  I. Shih,et al.  Undifferentiated keratinocytes control growth, morphology, and antigen expression of normal melanocytes through cell-cell contact. , 1993, Laboratory investigation; a journal of technical methods and pathology.

[157]  A. Harris,et al.  A study of adhesion molecules as markers of progression in malignant melanoma , 1992, The Journal of pathology.

[158]  P. Altevogt,et al.  Expression and function of the neural cell adhesion molecule L1 in mouse leukocytes , 1992, European journal of immunology.

[159]  L. Liotta,et al.  Identification, purification, and partial sequence analysis of autotaxin, a novel motility-stimulating protein. , 1992, The Journal of biological chemistry.

[160]  A. Haake,et al.  Keratinocytes regulate melanocyte number in human fetal and neonatal skin equivalents. , 1991, The Journal of investigative dermatology.

[161]  H. Soyer,et al.  Expression of Cytoskeletal Components in Melanocytic Skin Lesions An Immunohistochemical Study , 1991, The American Journal of dermatopathology.

[162]  N. Bornfeld,et al.  Nonrandom chromosomal abnormalities in primary uveal melanoma. , 1990, Journal of the National Cancer Institute.

[163]  R. Rees,et al.  Cytogenetic findings in six posterior uveal melanomas: Involvement of chromosomes 3, 6, and 8 , 1990, Genes, chromosomes & cancer.

[164]  J. Rootman,et al.  Monosomy 3 and isochromosome 8q in a uveal melanoma. , 1990, Cancer genetics and cytogenetics.

[165]  R. Meli,et al.  Isolation and identification of platelet-activating factor in UV-irradiated guinea pig skin. , 1988, Journal of pharmacological methods.

[166]  J. Lehmann,et al.  Discrimination between benign and malignant cells of melanocytic lineage by two novel antigens, a glycoprotein with a molecular weight of 113,000 and a protein with a molecular weight of 76,000. , 1987, Cancer research.

[167]  H. Dvorak Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. , 1986, The New England journal of medicine.

[168]  S Paget,et al.  THE DISTRIBUTION OF SECONDARY GROWTHS IN CANCER OF THE BREAST. , 1889 .

[169]  Matthew J. Davis,et al.  Exome sequencing identifies recurrent somatic RAC 1 mutations in melanoma , 2016 .

[170]  Sophia Kluge,et al.  Hard And Soft , 2016 .

[171]  C. Figdor,et al.  Regulatory T cells in melanoma: the final hurdle towards effective immunotherapy? , 2012, The Lancet. Oncology.

[172]  G. Barsh,et al.  Frequent somatic mutations of GNAQ in uveal melanoma and blue naevi , 2010 .

[173]  Mark Shackleton,et al.  Efficient tumour formation by single human melanoma cells , 2008 .

[174]  A. Rudensky,et al.  TGFbeta signalling in control of T-cell-mediated self-reactivity. , 2007, Nature reviews. Immunology.

[175]  Gabriel A. Rabinovich,et al.  Galectins as modulators of tumour progression , 2005, Nature Reviews Cancer.

[176]  K. Naresh,et al.  Altered melanoma cell surface glycosylation mediates organ specific adhesion and metastasis via lectin receptors on the lung vascular endothelium , 2005, Clinical & Experimental Metastasis.

[177]  Ridgway Pf Tumours : wounds that do not heal. , 2002 .

[178]  G. Zhu,et al.  Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion , 2002, Nature Medicine.

[179]  G. Parmiani,et al.  T-cell recognition of melanoma-associated antigens. , 2000, Journal of cellular physiology.

[180]  E. Voura,et al.  Role of cadherins in the transendothelial migration of melanoma cells in culture. , 1997, Cell motility and the cytoskeleton.

[181]  D. Adams,et al.  Cellular Adhesion , 1994, New Horizons in Therapeutics.

[182]  S. Ferrone,et al.  Lack of HLA class I antigen expression by cultured melanoma cells FO-1 due to a defect in B2m gene expression. , 1991, The Journal of clinical investigation.

[183]  M. Luck,et al.  Genome sequencing , 1987, Nature.

[184]  A. Haddow Molecular repair, wound healing, and carcinogenesis: tumor production a possible overhealing? , 1972, Advances in cancer research.

[185]  A. Vartanian Signaling Pathways in Tumor Vasculogenic Mimicry , 2022 .

[186]  Sozen,et al.  Mutations in GNA 11 in Uveal Melanoma , 2022 .