Malignant melanoma: From cell kinetics to micrometastases

American Journal of Clinical Dermatology

Volumn 12, Issue 2, 2011, Pages 77-86

  Quatresooz, Pascale ^a   Piérard, Gérald E ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Malignant melanoma; Skin cancer

Indexed keywords

KI 67 ANTIGEN; TUMOR MARKER;

ARTICLE; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER INVASION; CANCER RELAPSE; CANCER STAGING; CANCER THERAPY; CARCINOMA CELL; CELL HOMING; CELL KINETICS; CELL MIGRATION; DERMIS; DISTANT METASTASIS; HUMAN; IMMUNOHISTOCHEMISTRY; LOCAL METASTASIS; MELANOMA; MICROMETASTASIS; OCCULT CANCER; OVERALL SURVIVAL; PATIENT CARE; PRIORITY JOURNAL; STROMA;

HUMANS; IMMUNOHISTOCHEMISTRY; MELANOMA; MICROSATELLITE REPEATS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASM STAGING; PROGNOSIS; SKIN NEOPLASMS; SURVIVAL;

EID: 79952178477     PISSN: 11750561     EISSN: 11791888     Source Type: Journal    
DOI: 10.2165/11318380-000000000-00000     Document Type: Article

References (107)

1. Helmbach H, Sinha P, Schadendorf D. Human melanoma: drug resistance. Recent results. Cancer Res 2003; 161: 93-110
2. Chin L, Garraway LA, Fisher DE. Malignant melanoma: genetics and therapeutics in the genomic era. Genet Dev 2006; 20: 2149-82
3. Beddingfield FC. Themelanoma epidemic: res ipsa loquitur. Oncologist 2003; 8: 459-65
4. Thompson JF, Scolyer RA, Kefford RF. Cutaneous melanoma. Lancet 2005; 365: 687-701 (Pubitemid 40260892)
5. Jemal A, Devesa SS, Hartge P, et al. Recent trends in cutaneous melanoma incidence among Whites in the United States. J Natl Cancer Inst 2001; 93: 678-83 (Pubitemid 32492808)
6. Balch CM, Soong SJ, Gerschenwald JE, et al. Prognostic factors analysis of 17,600 melanoma patients: validation of the American Joint Committee on Cancer melanoma staging system. J Clin Oncol 2001; 15: 3622-34 (Pubitemid 32786275)
7. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275-84 (Pubitemid 40488633)
8. Fang D, Nguyen TK, Leishear K, et al. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 2005; 65: 9328-37 (Pubitemid 41508000)
9. Grichnik JM. Genomic instability and tumor stem cells. J Invest Dermatol 2006; 126: 1214-6 (Pubitemid 43997898)
10. Topczewska JM, Postovit LM, Margaryan NV, et al. Embryonic and tumorigenic pathways converge via nodal signalling: role in melanoma aggressiveness. Nat Med 2006; 12: 925-32 (Pubitemid 44175144)
11. Wang E, Voiculescu S, Le Poole IC, et al. Clonal persistence and evolution during a decade of recurrent melanoma. J Invest Dermatol 2006; 126: 1372-7 (Pubitemid 43997921)
12. Monzani E, Facchetti F, Galmozzi E, et al. Melanoma contains CD133 and ABCG2 positive cells with enhanced tumorigenic potential. Eur J Cancer 2007; 43: 935-46 (Pubitemid 46366698)
13. Reya T, Morrison SJ, Clarke MF, et al. Stem cells, cancer, and cancer stem cells. Nature 2001; 414: 105-11 (Pubitemid 33041634)
14. Schatton T, Frank MH. Cancer stem cells and human malignant melanoma. Pigm Cell Mel Res 2008; 21: 39-55 (Pubitemid 351421465)
15. Schatton T, Murphy GF, Frank NY, et al. Identification of cells initiating human melanomas. Nature 2008; 451: 345-9
16. Wong CE, Paratore C, Dours-Zimmermann MT, et al. Neural crest derived cells with stem cell features can be traced back to multiple lineages in the adult skin. J Cell Biol 2006; 175: 1005-15 (Pubitemid 44969205)
17. Yu H, Fang D, Kumar SM, et al. Isolation of a novel population of multipotent adult stem cells from human hair follicles. Am J Pathol 2006; 168: 1879-88 (Pubitemid 43825308)
18. Buac K, Pavan WJ. Stem cells of the melanocyte lineage. Cancer Biomark 2007; 3: 203-9 (Pubitemid 351492645)
19. Grichnik JM, Burch JA, Schulteis RD, et al. Melanoma, a tumor based on a mutant stem cell? J Invest Dermatol 2006; 126: 142-53
20. Klein WM, Wu BP, Zhao S, et al. Increased expression of stem cell markers in malignant melanoma. Modern Pathol 2007; 20: 102-7 (Pubitemid 44967955)
21. Toma JG, Akhavan M, Fernandes KJ, et al. Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat Cell Biol 2001; 3: 778-84 (Pubitemid 32842682)
22. Hendrix MJ, Seftor EA, Hess AR, et al. Vasculogenic mimicry and tumourcell plasticity: lessons from melanoma. Nat Rev Cancer 2003; 3: 411-21 (Pubitemid 37328845)
23. Alonso SR, Ortiz P, Pollan M, et al. Progression in cutaneous malignant melanoma is associated with distinct expression profiles: a tissuemicroarray- based study. Am J Pathol 2004; 164: 193-203 (Pubitemid 38364604)
24. Curtin JA, Fridlyand J, Kageshita T, et al. Distinct sets of genetic alterations in melanoma. N Engl J Med 2005; 353: 2135-47 (Pubitemid 41653105)
25. Hoek KS. DNA microarray analyses of melanoma gene expression: a decade in the mines. Pigment Cell Res 2007; 20: 466-84 (Pubitemid 47568833)
26. Jönsson G, Dahl C, Staaf J, et al. Genomic profiling of malignant melanoma using tiling-resolution array CGH. Oncogene 2007; 26: 4738-48 (Pubitemid 47067402)
27. Plaza JA, Suster D, Perez-Montiel D. Expression of immunohistochemical markers in primary and metastatic malignant melanoma, a comparative study in 70 patients using a tissue microarray technique. Appl Immunohistochem Mol Morph 2007; 15: 421-5 (Pubitemid 350307848)
28. Rothhammer T, Bosserhoff AK. Epigenetic events in malignant melanoma. Pigment Cell Res 2007; 20: 92-111 (Pubitemid 46439524)
29. Stark M, Hayward N. Genome-wide loss of heterozygosity and copy number analysis in melanoma using high-density single-nucleotide polymorphism arrays. Cancer Res 2007; 67: 2632-42 (Pubitemid 46548950)
30. Simpson AJ, Caballero OL, Jungbluth A, et al. Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer 2005; 5: 615-25 (Pubitemid 41081387)
31. Rothhammer T, Bataille F, Spruss T, et al. Functional implication of BMP4 expression on angiogenesis in malignantmelanoma. Oncogene 2007; 26: 4158-70 (Pubitemid 46920167)
32. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005; 434: 843-50 (Pubitemid 40558990)
33. Rappa G, Fodstad O, Lorico A. The stem cell-associated antigen CD133 (Prominin-1) is a molecular therapeutic target for metastatic melanoma. Stem Cells 2008; 26: 2008-3017
34. Quatresooz P, Piérard GE, Piérard-Franchimont C, et al. Molecular pathways supporting the proliferation staging of malignant melanoma. Int J Molec Med 2009; 24: 295-301
35. Piérard-Franchimont C, Henry F, Heymans O, et al. Vascular retardation in dormant growth-stuntedmalignantmelanomas. Int J Mol Med 1999; 4: 403-6
36. Barnhill RL. The biology of melanoma micrometastases. In: Reinhold U, Tilgen W, editors. Minimal residual disease in melanoma: biology, detection and clinical relevance. Berlin: Springer, 2001: 3-13
37. Ralph SJ. An update on malignant melanoma vaccine research: insight into mechanisms for improving the design and potency of melanoma therapeutic vaccines. Am J Clin Dermatol 2007; 8: 123-41 (Pubitemid 46998541)
38. Terando AM, Faries MB, Morton DL. Vaccine therapy for melanoma: current status and future directions. Vaccine 2007; 25: 4-16
39. Lorigan P, Eisen T, Hauschild A. Systemic therapy for metastatic malignant melanoma: from deeply disappointing to bright future? Exp Dermatol 2008; 17: 383-94
40. Boni R, Doguoglu A, Burg G, et al. MIB-1 immunoreactivity correlates with metastatic dissemination in primary thick cutaneous melanoma. J Am Acad Dermatol 1996; 35: 416-8
41. Sparrow LE, English DR, Taran JM, et al. Prognostic significance of MIB-1 proliferative activity in thinmelanomas and immunohistochemical analysis of MIB-1 proliferative activity in melanocytic tumors. Am J Dermatopathol 1998; 20: 12-6 (Pubitemid 28092700)
42. Niezabitowski A, Czajecki K, Rys J, et al. Prognostic evaluation of cutaneous malignant melanoma: a clinicopathologic and immunohistochemical study. J Surg Oncol 1999; 70: 150-60 (Pubitemid 29147163)
43. Straume O, Sviland L, Akslen LA. Loss of nuclear p16 protein expression correlates with increased tumor cell proliferation (Ki-67) and poor prognosis in patients with vertical growth phase melanoma.Clin Cancer Res 2000; 6: 1845-53
44. Frahm SO, Schubert C, Parwaresch R, et al. High proliferative activity may predict early metastasis of thin melanomas. Hum Pathol 2001; 32: 1376-81 (Pubitemid 34038673)
45. Quatresooz P,Arrese JE, Piérard-Franchimont C, et al. Immunohistochemical aid at risk stratification of melanocytic neoplasms. Int J Oncol 2004; 24: 211-6
46. Smoller BR. Histologic criteria for diagnosing primary cutaneous malignant melanoma. Modern Pathol 2006; 19: 34-40
47. Ohsie SJ, Sarantopoulos GP, Cochran AJ, et al. Immunohistochemical characteristics of melanoma. J Cutan Pathol 2008; 35: 433-44 (Pubitemid 351519417)
48. Quatresooz P, Piérard-Franchimont C, Piérard GE. Highlighting the immunohistochemical profile of melanocytomas. Oncol Rep 2008; 19: 1367-72
49. Quatresooz P, Piérard-Franchimont C, Paquet P, et al.Angiogenic fast-growing melanomas and their micrometastases. Eur J Dermatol 2010; 20: 302-7
50. Quatresooz P, Piérard-Franchimont C, Piérard GE, et al. Molecular histology on the diagnostic cutting edge between malignantmelanomas and cutaneous melanocytomas. Oncol Rep 2009; 22: 1263-7
51. Piérard GE, Piérard-Franchimont C, Henry C, et al. The proliferative activity of cells of malignant melanomas. Am J Dermatopathol 1984; 6: S317-24
52. Claessens N, Piérard GE, Piérard-Franchimont C, et al. Immunohistochemical detection of incipient melanoma micrometastases: relationship with sentinel lymph node involvement. Melanoma Res 2005; 15: 107-10 (Pubitemid 40637988)
53. Lipsker D. Growth rate, early detection and prevention of melanoma: melanoma epidemiology revisited and future challenges. Arch Dermatol 2006; 142: 1638-40 (Pubitemid 44969222)
54. Liu W, Dowling JP, Murray WK, et al. Rate of growth in melanomas: characteristics and associations of rapidly growing melanoma. Arch Dermatol 2006; 142: 1551-8 (Pubitemid 44969210)
55. Lipsker D, Engel F, Cribier B, et al. Trends in melanoma epidemiology suggest three different types of melanoma. Br J Dermatol 2007; 157: 328-43
56. Zalaudek I, Marghoob AA, Scope A, et al. Three roots of melanoma. Arch Dermatol 2008; 144: 1375-9
57. Piérard GE, Piérard-Franchimont C. Stochastic relationship between the growth fraction and vascularity of thin malignant melanomas. Eur J Cancer 1997; 33: 1888-92 (Pubitemid 28129222)
58. Gebhardt C, Averbeck M, Veirtel A, et al. Ultraviolet-B irradiation enhances melanoma cell motility via induction of autocrine interleukin 8 secretion. Exp Dermatol 2007; 16: 636-43 (Pubitemid 47079593)
59. Quatresooz P, Piérard-Franchimont C, Piérard GE. Diagnostic challenge of desmoplastic melanoma. Trends Cancer Res 2007; 3: 27-34
60. Shea CP, Kline MA, Lugo J, et al. Angiotropic metastatic malignant melanoma. Am J Dermatopathol 1995; 17: 58-62
61. Engbring JA, Kelinman HK. The basement membrane matrix in malignancy. J Pathol 2003; 200: 465-70 (Pubitemid 36818246)
62. Wernert N. The multiple roles of tumour stroma. Virchows Arch 1997; 430: 433-43 (Pubitemid 27322961)
63. Danen EHJ, Sonnenberg A. Integrins in regulation of tissue development and function. J Pathol 2003; 200: 471-80 (Pubitemid 36818247)
64. Wehrle-Haller B, Imhof BA. Integrin-dependent pathologies. J Pathol 2003; 200: 481-7 (Pubitemid 36818248)
65. Friedl P, Wolf K. Tumour-cell invasion and migration: diversity and escape mechanisms. Nat Rev Cancer 2003; 3: 362-74 (Pubitemid 37328856)
66. Piérard GE, Quatresooz P, Rorive A, et al. Malignant melanoma: conceptual and therapeutic innovations based on translational research. Rev Med Liège 2008; 63: 579-84
67. Fecher LA, Cummings SD, Keefe MJ, et al. Toward a molecular classification of melanoma. J Clin Oncol 2007; 25: 1606-20 (Pubitemid 46733089)
68. Bennet DC. How to make a melanoma: what do we know of the primary clonal events? Pigment Cell Melanoma Res 2008; 21: 27-38
69. Hoek KS, Schlegel NC, Brafford P, et al. Metastatic potential of melanomas defined by specific gene expression profiles with no BRAF signature. Pigment Cell Res 2006; 19: 290-302 (Pubitemid 44015592)
70. Liu W, Kelly JW, Trivett M, et al. Distinct clinical and pathological features are associated with BRAF mutation in primary melanoma. J Invest Dermatol 2007; 127: 900-5 (Pubitemid 46434654)
71. Yap AS, Brieher WM, Gumbiner BM. Molecular and functional analysis of cadherin-based adherens junctions. Annu Rev Cell Dev Biol 1997; 13: 119-46 (Pubitemid 28034522)
72. Tang A, Eller MS, Hara M, et al. E-cadherin is the major mediator of human melanocyte adhesion to keratinocytes in vitro. J Cell Sci 1994; 107: 983-92 (Pubitemid 24119356)
73. Haass NK, Smalley KS, Herlyn M. The role of altered cell-cell communication in melanoma progression. J Mol Histol 2004; 35: 309-18 (Pubitemid 40585316)
74. Li G, Satyamoorthy K, Herlyn M. N-cadherin-mediated intercellular interactions promote survival and migration of melanoma cells. Cancer Res 2001; 61: 3819-25 (Pubitemid 32694999)
75. Hsu MY, Meier FE, Nesbit M, et al. E-cadherin expression in melanoma cells restores keratinocyte-mediated growth control and down-regulates expression of invasion-related adhesion receptors. Am J Pathol 2000; 156: 1515-25 (Pubitemid 30646691)
76. Hendrix M, Maniotics A, Folberg R. Vascular channel formation by human melanoma cells in vivo and in vitro: vasculogenic mimicry. Am J Pathol 1999; 155: 739-52 (Pubitemid 29426820)
77. Pellegrini A. Regressed primary malignant melanoma with regional metastasis. Arch Dermatol 1980; 116: 585-6 (Pubitemid 10101720)
78. Anbari KK, Schuchter LM, Bucky LM, et al. Melanoma of unknown primary site: presentation, treatment and prognosis. A single institution study. Cancer 1997; 79: 1816-21 (Pubitemid 27176366)
79. Vijuk G, Coates AS. Survival of patients with visceral metastatic melanoma from an occult primary lesion: a retrospective matched cohort study. Ann Oncol 1998; 9: 419-22 (Pubitemid 28273035)
80. Henry F, Piérard-Franchimont C, Arrese JE, et al. How I explore y an orphan metastasis from melanoma. Rev Med Liège 2002; 57: 405-7
81. Day Jr CL, Harrist TJ, Gorstein F, et al. Malignant melanoma: prognostic significance of "microscopic satellites" in the reticular dermis and subcutaneous fat. Ann Surg 1981; 194: 108-12
82. Shaikh L, Sagebiel RW, Ferreira CM, et al. The role of microsatellites as a pronostic factor in primary malignant melanoma. Arch Dermatol 2008; 14: 739-42
83. Harrist JT, Rigel DS, Day Jr CL, et al. "Microscopic satellites" are more highly associated with regional lymph node metastases than is primary melanoma thickness. Cancer 1984; 53: 2183-7
84. Leon P, Daly JM, Synnestved M, et al. The prognostic implications of microscopic satellites in patients with clinical stage I melanoma. Arch Surg 1991; 126: 1461-8
85. Balch CM, Buzaid AC, Soong SJ, et al. Final version of the American Joint Committee on Cancer staging system for cutaneous melanoma. J Clin Oncol 2001; 19: 3635-48 (Pubitemid 32786276)
86. Crowley N, Seigler H. Relationship between disease-free interval and survival in patients with recurrent melanoma. Arch Surg 1992; 127: 1303-8
87. Holmgren L, O'Reilly MS, Folkman J. Dormancy of micrometastases: balanced proliferation and apoptosis in the presence of angiogenesis suppression. Nat Med 1995; 1: 149-53
88. Piepkorn M, Barnhill RL. A factual, not arbitrary, basis for choice of resection margins in melanoma. Arch Dermatol 1996; 132: 811-4
89. Piepkorn M, Weinstock MA, Barnhill RL. Theoretical and empirical arguments in relation to elective lymph node dissection for melanoma. Arch Dermatol 1997; 133: 995-1007
90. Piérard-Franchimont C, Piérard GE. The wide and deep excision of primary malignant melanoma: a dogma on the decline. Acta Clin Belgica 1998; 53: 98-9 (Pubitemid 28273079)
91. Piérard GE, Henry C, Franchimont C, et al. Immunotherapy by dinitrochloro-benzene of melanomas of the skin: II. Histology of the cytotoxic effect. In: Ackerman AB, editor. Pathology of malignant melanoma. New York: Masson, 1981: 373-85
92. Fildler IJ. The biology of melanoma metastasis. In: Balch CM, Houghton AN, Milton GW, et al., editors. Cut melanoma. 2nd ed. Philadelphia (PA): JB Lippincott, 1992: 112-29
93. Reinhold U, Lüdtke-Handjery HC, Schnautz S, et al. The analysis of tyrosinase-specific mRNA in blood samples of melanoma patients by RT-PCR is not a useful test for metastatic tumor progression. J Invest Dermatol 1997; 108: 166-9 (Pubitemid 27061027)
94. Schittek B, Blaheta HJ, Ellwanger U, et al. Polymerase chain reaction in the detection of circulating tumour cells in peripheral blood of melanoma patients. In: Reinhold U, Tilgen W, editors. Minimal residual disease in melanoma: biology, detection and clinical relevance. Berlin: Springer, 2001: 93-104
95. Seiter S, Rappl G, Tilgen W, et al. Facts in pitfalls in the detection of tyrosinase mRNA in the blood of melanoma patients by RT-PCR. In: Reinhold U, Tilgen W, editors. Minimal residual disease in melanoma: biology, detection and clinical relevance. Berlin: Springer, 2001: 105-12
96. Benez A, Schiebel U, Fierlbeck G. Morphologically intact melanoma cells may be detected in peripheral blood of melanoma patients. In: Reinhold U, Tilgen W, editors. Minimal residual disease in melanoma: biology, detection and clinical relevance. Berlin: Springer, 2001: 113-7
97. Waldmann V, Wacker J, Deichmann M, et al. Prognosis of metastatic melanoma: no correlation of tyrosinase mRNA in bone marrow and survival time. In: Reinhold U, Tilgen W, editors. Minimal residual disease in melanoma: biology, detection and clinical relevance. Berlin: Springer, 2001: 118-25
98. Von Knebel Doeberitz M, Weitz J, Koch M, et al. Molecular tools in the detection of micrometastatic cancer cells: technical aspects and clinical relevance. In: Reinhold U, Tilgen W, editors. Minimal residual disease in melanoma: biology, detection and clinical relevance. Berlin: Springer, 2001: 181-6
99. Palmieri G, Pirastu M, Strazzullo M, et al. Clinical significance of PCRpositive mRNA markers in peripheral blood and regional nodes of malignant melanoma patients. In: Reinhold U, Tilgen W, editors. Minimal residual disease in melanoma: biology, detection and clinical relevance. Berlin: Springer, 2001: 200-3
100. Taback B, Morton DL, O'Day SJ, et al. The clinical utility of multimarker RT-PCR in the detection of occult metastasis in patients with melanoma. In: Reinhold U, Tilgen W, editors. Minimal residual disease in melanoma: biology, detection and clinical relevance. Berlin: Springer, 2001: 78-92
101. Pantel K, Otte M. Disseminated tumor cells: diagnosis, prognostic relevance, and phenotyping. In: Reinhold U, Tilgen W, editors. Minimal residual disease in melanoma: biology, detection and clinical relevance. Berlin: Springer, 2001: 14-24
102. Moreno A, Espanol I, Romagosa V. Angiotropic malignant melanoma: report of two cases. J Cutan Pathol 1992; 19: 325-9
103. Saluja A, Money N, Zivony DI, et al. Angiotropic malignant melanoma: a rare pattern of local metastases. J Am Acad Dermatol 2001; 44: 829-32 (Pubitemid 32391172)
104. Siegel DM, McClain SA. Angiotropic malignant melanoma: more common than we think? J Am Acad Dermatol 2001; 44: 870-1
105. Barnhill RL, Dy K, Lugassy C. Angiotropism in cutaneous melanoma: a prognostic factor strongly predicting risk formetastasis. J Invest Dermatol 2002; 119: 705-6
106. Lugassy C, Barnhill RL. Angiotropicmalignant melanoma and extravascular migratory metastasis: description of 26 cases with emphasis on a new mechanism of tumor spread. Pathology 2004; 36: 485-90 (Pubitemid 39273994)
107. Lugassy C, Barnhill RL. Angiotropic melanoma and extravascular migratory metastasis: a review. Adv Anat Pathol 2007; 14: 195-201 (Pubitemid 46659190)